Published online April 3, 2006
PEDIATRICS Vol. 117 No. 4 April 2006, pp. e725-e732 (doi:10.1542/peds.2005-0779)
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Comparison of Techniques to Evaluate Adiposity in Stunted and Nonstunted Children

Daniel J. Hoffman, PhDa, Ana L. Sawaya, PhDb, Paula A. Martins, PhDb, Megan A. McCrory, PhDc and Susan B. Roberts, PhDd

a Department of Nutritional Sciences, Rutgers, the State University of New Jersey, New Brunswick, New Jersey
b Department of Endocrine Physiology, Federal University of São Paulo School of Medicine, São Paulo, Brazil
c School of Nutrition and Exercise Science, Bastyr University, Kenmore, Washington
d Energy Metabolism Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, Massachusetts


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
OBJECTIVE. The use of anthropometric measures (eg, skinfold thicknesses, BMI) to assess obesity is not without controversy and has not been explored with respect to the use among groups of children with growth retardation (ie, stunting). Therefore, the objective of this study was to determine whether growth retardation affects the accuracy of field methods for assessing body composition in children.

METHODS. A cross-sectional study was conducted in 30 stunted children and 30 nonstunted children who were matched for age- and weight-for-height z score and living in the shantytowns of São Paulo, Brazil. Body composition (fat mass, fat-free mass, and percentage of body fat [%BF]) was measured by H218O dilution (reference technique) using group-specific values for the hydration of fat-free mass and dual-energy x-ray absorptiometry. BMI and body composition that were calculated from 3 pediatric skinfold prediction equations were evaluated for accuracy of %BF in comparison with the reference technique.

RESULTS. Stunted children were shorter and weighed less than nonstunted children, but BMI did not differ significantly between groups. All 3 skinfold equations tested resulted in a calculated %BF that was significantly lower than that measured by H218O dilution for both stunted and nonstunted groups, and %BF as calculated by any of the skinfold equations tested did not significantly predict %BF by H218O dilution. In contrast, BMI significantly predicted %BF in both stunted and nonstunted children, and this relationship did not differ by growth status.

CONCLUSION. BMI but not skinfolds significantly predicted %BF measured by H218O dilution. The relationship between BMI and %BF did not differ between stunted and nonstunted children; this indicates that BMI can be used in field studies of obesity and stunting. However, the prediction of %BF by BMI is relatively poor in both groups of children, and continued investigation of more accurate field methods for measuring %BF is warranted.

Key Words: body composition • BMI • stunting • obesity • developing countries

Abbreviations: WHZ—weight-for-age z score • HAZ—height-for-age z score • DXA—dual-energy x-ray absorptiometry • TBW—total body water • FFM—fat-free mass • %BF—percentage of body fat • FM—fat-mass

The prevalence of childhood overweight is increasing worldwide,1–3 even in countries that have a high prevalence of growth retardation.3 Although it is common to use BMI to determine levels of overweight or obese in pediatric populations, the question of whether BMI is an accurate indicator of relative body fatness in all children, especially those who have growth retardation, has not been established.4–6 Moreover, other simple methods of determining body composition, such as skinfold prediction equations, have not been well validated in large cohorts of children from developing countries or among children who have growth retardation.

Linear growth retardation, or stunting, is a relatively widespread phenomenon in developing countries,7 with the prevalence of stunting ranging from 13% to 24% in Latin America8 to 48% in South Central Asia and East Africa. In the United States, 12% of children of low socioeconomic status have low height for age.9 On theoretical grounds, stunted children might be expected to be a group for which BMI would not be an accurate index of body fatness, because stunting results in a disproportionate lengthening of the torso (which has a higher ratio of weight to height than limbs) during growth relative to leg length.10 This is perhaps as a result of sparing of ponderal growth in favor of organ and visceral growth when growth retardation occurs.11 Consistent with this suggestion, Post et al12 reported that the weight-for-height underestimated wasting in a sample of poor children who had relatively low height and were living in urban areas of southern Brazil and was associated with a disproportionately large abdominal circumference. In addition, relatively low skinfold thickness in comparison with weight for height was reported in nutritionally stunted children.12,13 However, it is important to note that the potential for alterations in the ratio of limb to torso growth to influence the relationship between BMI and body fatness assumes that the composition of torso and limbs is different and/or that other body measurements, such as head size, are relatively unaffected by stunting.14,15 Combined, these observations and studies indicate the need for an evaluation of the accuracy of BMI as an index of body fatness in stunted children. We therefore conducted a study to examine whether stunting influences the ability of different field methods (BMI and skinfolds) to estimate body composition as determined by accurate methods.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Study Children
Children were identified as potential participants during population surveys of 3 shantytowns in the city of São Paulo, Brazil, in which >300 children aged 7 to 11 years were weighed and measured. Children from the survey who were found to be eligible on the basis of anthropometric criteria were invited to participate in the study. All participants had to have a normal weight-for-age z score (WHZ) of –2.0 to 1.5 according to National Center for Health Statistics standards.16 Children who were recruited for the stunted group (n = 30) had to have a height-for-age z score (HAZ) less than –1.5, and children who were recruited for the nonstunted group (n = 30) had to have an HAZ more than –1.5. Note that well-nourished Brazilian children grow adequately relative to National Center for Health Statistics standards in terms of both weight and height17 and that low HAZ is widely believed to be a result of chronic, moderate undernutrition.18 In addition, the 2 groups were matched for age and WHZ. The characteristics of the study children are shown in Table 1.


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  		TABLE 1 Physical Characteristics and Body Compositiona of Nonstunted and Stunted Children

 
Children who seemed to be eligible for the study on the basis of weight and height and who were willing to participate were given a screening examination. This included a medical history, physical examination, evaluation of Tanner stage,19 blood collection for glucose and iron concentrations, and fecal and urine screening for acute infections. Children were excluded from the study when they were taking any medication, when their Tanner stage criterion was >1, or when we identified any past medical problems that might influence current health status or metabolic condition (eg, hyperthyroidism, chronic anemia). Any child who had an acute health problem, such as an acute intestinal or urinary infection, was treated according to the usual procedures of the São Paulo Hospital and began the study only after successful completion of treatment. Ethical approval for the study was obtained from the Federal University of São Paulo Hospital and the Institutional Review Board of Tufts University/New England Medical Center when the data were collected in 1998, only, and not at the 2 institutions where 2 of the authors currently reside. Written informed assent and consent were obtained from the children and their parents, respectively, before the study began.

Study Protocol
Children were studied as part of a larger investigation on the relationship between nutritional stunting and metabolic risk factors for obesity.20 H218O dilution was conducted during the field phase of the study in which the children were living at home. Other measurements were made during an inpatient study that was conducted the weekend after the field phase, in which the children were admitted to the metabolic research unit of the Center for Nutritional Recovery and Education at the Federal University of São Paulo. The children were admitted in groups of 4 (2 stunted children and 2 nonstunted children were admitted together when possible) at 7:00 A.M. on study day 1 and were returned to their homes at 9:00 P.M. on day 3. Dual-energy x-ray absorptiometry (DXA) measurements were made on the afternoon of day 1, and anthropometric measurements were made in the morning of day 2 or 3. Continuous daytime supervision was provided by investigator D.J.H. and 2 assistants, and nighttime supervision was provided by a nurse.

H218O Dilution
Body composition was assessed using H218O dilution and was used as the more precise technique against which other methods were compared. Data were obtained from only 57 children (30 nonstunted and 27 stunted) because 1 child had a physiologically impossible total energy expenditure estimate and samples from 2 children were damaged during transport in preparation for analysis. The protocol for this measurement has been described in detail elsewhere.20 Briefly, a diluted dose of 0.20 18O g/kg body wt was given to each child after measurement of body weight on outpatient study day 1, and a baseline (predose) urine specimen was collected. Subsequent urine samples were collected 2, 3, 4, and 5 hours postdose and during the subsequent week. All samples were dispensed as aliquots into freezer tubes and kept refrigerated until frozen at –20°C at the end of each study day until transported for analysis. Analysis of the samples was done using standard methods.21,22 Total body water (TBW) was estimated from back-extrapolated time 0 enrichments and the isotopic abundance of the dose, assuming TBW = 2H2O dilution space/1.01. To calculate fat-free mass (FFM) from H218O dilution, we then used group-specific hydration values (0.721 for nonstunted and 0.744 for stunted, calculated as described below and in Results), and body fat was calculated as the difference between body weight and FFM.

DXA
Body fat and FFM were also measured with a Hologic QDR-4500A DXA (Hologic Inc, Bedford, MA) with an adult quick-scan software program version 8.26. Despite the potential problems with estimating percentage of body fat (%BF) in children using an adult scan with DXA, reports suggest that the repeatability for lean tissue estimation using DXA is high (coefficient of variation: 0.8%).23

Hydration of FFM
For the purpose of having an independent assessment of TBW from which FFM hydration could be calculated, TBW was determined by 2H2O dilution (TBW = 2H2O dilution space/1.04). The hydration of FFM then was calculated as TBW/FFM measured with DXA. A significant difference between stunted and nonstunted groups with respect to hydration of FFM was found, allowing us to calculate group-specific hydration factors in the calculation of %BF as described above.

Anthropometry
Anthropometric measurements were made in the mornings by the same investigator (P.A.M.) and with the children wearing shorts and t-shirts. Anthropometric data from 57 children are presented because 3 children (different from those who were not included in the isotope dilution protocol) withdrew from the study before measurements were obtained. Height was measured to the nearest 0.5 cm using a mounted measuring stick (Stadi-o-meter; Country Technologies, Green Bay, WI). Weight was measured using a digital electronic scale (Country Technologies) that was accurate to within 0.1 kg. Skinfold measurements were made on both sides of the body at the biceps, triceps, subscapular, suprailiac, thigh, and calf sites using a Harpenden skinfold caliper (Country Technologies) according to the protocol of Lohman.24 Measurements were made in triplicate by a single investigator (P.A.M.) using a standardized protocol, and the mean values were used in all analyses.

Three child-specific prediction equations were used to calculate fat mass (FM; in kg) and, subsequently, %BF from body weight (in kg) and skinfold thickness (in mm):

  1. Goran et al25 boys and girls: FM = 0.18 * weight + 0.23 * subscapular + 0.13 * triceps – 3.0
  2. Brook et al21 boys: FM = weight * ([4.95/1.1690 – 0.0788 * log sum of 4 skinfolds] – 4/5) girls: FM = weight * ([4.95/1.2063 – 0.0999 * log sum of 4 skinfolds] – 4/5), where the 4 skinfolds used are subscapular, triceps, biceps, and suprailiac
  3. Slaughter et al22 boys: FM = weight * [(1.21 * SUMTRSB – 0.008 * (SUMTRSB)2 – 1.7)/100] girls: FM = weight * [(1.33 * SUMTRSB – 0.013 * (SUMTRSB)2 – 2.5)/100], where SUMTRSB is the sum of the triceps and subscapular skinfolds.

Children were also grouped into normal or overweight on the basis of their BMI for age as recommended by Cole et al.26 The %BF (determined by H218O dilution) cutoff for normal weight and overweight was set at 25% as recommended by Ellis et al.27,28 This allowed for the assessment of the validity of BMI for determining excess adiposity in individual children.

Statistical Analysis
Values are expressed as means ± SD or SEM as noted. Statistical analyses were performed using SPSS Version 10.0 and SYSTAT 8.0 for WINDOWS (SPSS Inc, Chicago, IL). Differences in physical characteristics and mean body composition variables between stunted and nonstunted groups were tested using Student's unpaired t test. Whether the mean %BF from each test method differed from %BF as measured by H218O dilution according to stunting group was tested by using analysis of variance with method, group, and method x group interaction terms. The validity of the skinfold equations, BMI, and BMI percentile for predicting %BF was evaluated using multiple linear regression analysis. Whether the validity differed according to stunting group was determined by including an interaction term with group in the models. Therefore, each model included %BF measured by H218O dilution as the dependent variable and %BF by the test method (eg, skinfold prediction equation), stunting group (0 = nonstunted and 1 = stunted), and a test method x stunting group interaction term and was controlled for gender (0 = boys and 1 = girls). When the test method x stunting group interaction terms were not significant, the 2 groups were combined for additional linear regression analysis. Results were considered statistically significant at P < .05.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Physical Characteristics and Body Composition
The 2 groups of children studied were of similar age and body weight (Table 1), but the nonstunted children weighed more and were significantly taller compared with the nonstunted children. The nonstunted children also had significantly higher HAZ but not WHZ or BMI compared with the stunted children.

Body composition data are presented in Table 1. The FFM hydration was significantly higher in the stunted compared with the nonstunted group (P < .05). TBW was significantly higher in the control group compared with the stunted group when measured by either H218O or D2O dilution. However, %BF was not significantly different between the groups as measured by both H218O dilution (P = .319) and DXA (P = .07). Relationships between %BF from H218O dilution and %BF from DXA for stunted and nonstunted groups independently and for the 2 groups combined are illustrated in Fig 1. Linear regression analysis showed that there was no significant interaction effect of group by %BF from DXA, indicating that stunting did not affect the relationship between %BF from DXA and %BF from H218O dilution. Therefore, the regression line for both groups combined, also shown, did not differ from the line of identity (P = .022).


Figure 1
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  		FIGURE 1 Relationship between %BF as measured with H218O and DXA in nonstunted (• and solid line, R2 = 0.745) and stunted ({circ} and dashed line, R2 = 0.663) children. The R2 for both groups combined was 0.708 and is indicated by the thin dashed line; %BF by H218O dilution = 3.544 + 0.785 (%BF by DXA) – 2.096 (group) + 0.140 (group * %BF by DXA), with R2 = 0.714. The slope and the intercept for each group were not significantly different from 1 and 0, respectively.

 
Body Fatness Predicted by Skinfold Equations
Also shown in Table 1 are the predicted %BF values from skinfold thickness measurements. The %BF as predicted by the equations of Brook et al21 and Slaughter et al22 did not differ significantly between the 2 groups; however, the equation of Goran et al25 predicted a significantly lower %BF in the stunted group. In comparison with the reference technique, each equation predicted a significantly lower %BF in both groups. Furthermore, none of the associations between %BF as predicted by each of the 3 skinfold equations and %BF as measured by H218O dilution were statistically significant and the R2 values were very low, ranging from 0.000 to 0.089, indicating that none of the equations accurately predicted %BF in either the stunted or the nonstunted group. Similar results were obtained when the 2 groups were combined. Results from the linear regression analyses (Table 2) to test whether stunting significantly affected the ability of any of the skinfold equations to predict %BF indicated that this was not the case, even after controlling for gender.


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  		TABLE 2 Regression Models Predicting %BF by H218O Dilution From Group, Gender, and Skinfold Equations by Brook et al, Goran et al, and Slaughter et al

 
BMI as a Predictor of Fatness
The %BF measured by H218O dilution in relation to BMI and BMI percentile are shown in Fig 2A and B, respectively, and in Table 3. In models that controlled for gender, both analyses indicated that BMI and BMI percentile significantly predicted %BF as measured by H218O dilution and that these relationships did not differ by stunting group.


Figure 2
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  		FIGURE 2 A, Relationship between %BF as measured with H218O (%BF-18O) and BMI (kg/m2) in nonstunted (• and solid line, R2 = 0.201) and stunted ({circ} and dashed line, R2 = 0.125) children. The R2 for both groups combined was 0.157 and is indicated by the thin dashed line. B, Relationship between BMI percentile and %BF-H218O nonstunted (• and solid line, R2 = 0.168) and stunted ({circ} and dashed line, R2 = 0.052) children. The R2 for both groups combined was 0.125 and is indicated by the thin dashed line. C, Individual variations in %BF-H218O within each of the 2 BMI categories for nonstunted (•) and stunted ({circ}) children, specific to gender and age.26 Provisional healthy %BF cutoff value of 25% is indicated for all children.

 

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  		TABLE 3 Regression Models Predicting %BF as Measured by H218O Dilution From BMI (or BMI percentile) and Growth Retardation, Controlling for Gender

 
Figure 2C shows %BF as measured by H218O dilution in relation to international categories of normal weight and overweight according to Cole et al26 for both stunted and nonstunted children. A provisional cutoff for dividing children into normal and overfat according to %BF as suggested by Ellis et al28 is also shown.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
The prevalence of overweight and obesity is increasing throughout the world, including in many developing countries, most of which have a high prevalence of stunted children. However, differences in height for age may influence the ability to interpret results from simple tools that currently are used to assess overweight and obesity in children, such as BMI and anthropometric prediction equations. The results of this study suggest that growth retardation does not seem to influence the relationship between body fatness as measured using a H218O dilution and BMI. Therefore, BMI may be broadly valid for population studies on the prevalence of obesity, even in countries with a high prevalence of stunting. In addition, we found that existing prediction equations using skinfold measurements are not adequate for determining body fatness in the cohort studied.

In particular, we found that current prediction equations for estimating body composition from skinfold thicknesses in children did not correlate well with our more precise measure of body composition, H218O dilution. This was not an unexpected result because the accuracy of anthropometric prediction equations depends not only on the equations but also on measurements that are subject to substantial error, as a result of either investigator or instrument. However, the relationship between body fatness as measured with H218O dilution and the anthropometric prediction equations was even less accurate than for BMI and body fatness as measured with H218O dilution. Previous studies have reported a high correlation between predicted body fat from skinfold equations and other methods, such as an R2 of 0.7029 with TBW (measured with oxygen-18) or an R2 of 0.84 with bioelectrical impedance.30 However, not all previous studies reported such good correlations, especially in prepubertal children,22,31 which may help to explain the results of the present study. Therefore, the use of these equations, most of which were derived from either small samples or children who lived in developed regions, is not recommended for assessing overweight or obesity in pediatric cohorts who live in developing countries. In addition, these results raise the question of whether BMI, an index rather than a measure of adiposity, would be a better field tool to assess overweight or obesity in children who live in developing countries.

Regarding BMI, the use of BMI to determine the prevalence of overweight or obesity in pediatric groups throughout the world has gained acceptance4,26,32,33 despite several reports that suggest that BMI may not be a valid tool for assessing body composition in growing children.16,17 More important, though, given that obesity is increasing in countries with a high prevalence of stunting, it is necessary to determine whether growth retardation influences the relationship between BMI and body fatness to avoid the potential for stunted children to seem to be overweight when they are not.10 Even though BMI and %BF were found to be correlated significantly in both normal-height and stunted children, the R2 was low. This does not preclude investigators from using BMI to categorize children into normal-weight or overweight categories, especially when studying large populations or access to alternative methods is limited, but caution should be used if BMI is to be used as a predictor of %BF, regardless of whether one is studying normal-height or stunted children.

It should be noted that H218O dilution was used as the body composition technique for determining %BF using group-specific values for the hydration of FFM (determined independent of the assessment of TBW). Although H218O has been widely validated for measuring TBW in humans,34 the potential accuracy H218O for assessing %BF in any given population depends on the accuracy of the assumed hydration of FFM.35,36 Because several reports of FFM hydration vary between different populations37–39 and over time in childhood,40 we decided to assess FFM hydration in our nonstunted and stunted samples and used their mean values to calculate group-specific %BF. Our finding that the hydration of FFM was significantly higher in stunted compared with nonstunted children indicates that this component of the study was important because failure to account for the seemingly higher hydration of FFM in stunted children would result in false underestimation of FFM and overestimation of body fat. It is apparent that the higher hydration of the stunted children is particular to that group because the values that we obtained for the normal-height children, although lower than some, are consistent with the hydration values that have been reported for children in the same age range.25,38,41,42 Explanations for this difference are few, given the lack of published research on tissue hydration after recovery from chronic undernutrition. However, one potential explanation may be the delayed development of muscle tissue during the period of growth retardation. This essentially would mimic the gender differences observed during normal growth, resulting in girls' having less relative muscle mass and a smaller cell mass as boys of the same age, resulting in decreased total body protein and lower hydration values for the same tissue mass. In addition, it is widely known that undernutrition results in an increase in both intracellular and extracellular water, both of which would result in higher hydration values in the stunted compared with the control group.


   CONCLUSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
We have found that BMI as a continuous variable, although not an extremely accurate field method to assess adiposity, is a relatively valid and inexpensive tool for estimating overweight and obesity in populations that include stunted children. In addition, skinfold thickness measurements had a very poor correlation with %BF. More accurate and sensitive field methods for assessing body fatness in children who have normal height and growth retardation and live in developed regions of the world are needed.


   ACKNOWLEDGMENTS
 
This study was funded by the Nestlé International Foundation.

We thank Celia de Nascimento for work in recruiting and assisting in the measurements of these children and the staff at the Center for Nutritional Recovery and Education and the São Paulo Hospital, Federal University of São Paulo, Escola Paulista de Medicine for cooperation and assistance in this study. Finally, we are indebted to the families and parents of the children who participated in this study, without whose cooperation this work would not have been possible.


   FOOTNOTES
 
Accepted Oct 17, 2005.

Address correspondence to Daniel J. Hoffman, PhD, Department of Nutritional Science, Rutgers, the State University of New Jersey, 26 Nichol Ave 228B, New Brunswick, NJ 08901. E-mail: dhoffman{at}aesop.rutgers.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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