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Estimating total body fat using a skinfold prediction equation in Brazilian


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Article in Annals of Human Biology · March 2012


DOI: 10.3109/03014460.2012.660989 · Source: PubMed

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Annals of Human Biology, March–April 2012; 39(2): 156–160
Copyright q Informa UK, Ltd.
ISSN 0301-4460 print/ISSN 1464-5033 online
DOI: 10.3109/03014460.2012.660989

RESEARCH PAPER

Estimating total body fat using a skinfold prediction equation


in Brazilian children
Daniel J. Hoffman1, Tatiana Toro-Ramos1, Ana Lydia Sawaya2, Susan B. Roberts3 & Patricia Rondo4
1
Department of Nutritional Sciences, Rutgers, the State University of New Jersey, 26 Nichol Avenue, New Brunswick, NJ 08901,
USA, 2Department of Endocrine Physiology, Federal University of São Paulo School of Medicine, Rua Botucatu, 862, São Paulo,
SP, Brazil 04023-900, 3Energy Metabolism Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts
University, 711 Washington St., Boston, MA 02111, USA, and 4Department of Nutrition, School of Public Health, University of
Ann Hum Biol Downloaded from informahealthcare.com by Loughborough University on 04/18/12

São Paulo, Avenida Dr Arnaldo, 715, São Paulo, Brazil 01246-904

Background: The double burden of obesity and underweight is at risk of excess body fat generally relies on simpler and
increasing in developing countries and simple methods for the cheaper techniques, such as BMI or skinfolds. While BMI is
assessment of fat mass in children are needed. a useful index of adiposity for populations, skinfold
Aim: To develop and validate a new anthropometric prediction equations have generally been developed and
predication equation for assessment of fat mass in children. validated in cohorts that are not similar in terms of race or
Subjects and methods: Body composition was assessed in 145 past nutritional experience to cohorts in developing
children aged 9.8 ^ 1.3 (SD) years from São Paulo, Brazil using countries (Goran et al. 1996; Huang et al. 2003; Hoffman
For personal use only.

dual energy X-ray absorptiometry (DEXA) and skinfold et al. 2006). Thus, developing and validating new skinfold
measurements. The study sample was divided into prediction equations is needed for more accurate estimates
development and validation sub-sets to develop a new of body fatness in developing and transitional economies.
prediction equation for FM (PE). Anthropometric measures are among the cheapest and
Results: Using multiple linear regression analyses, the best most common methods available to assess human body
equation for predicting FM (R 2 ¼ 0.77) included body weight, composition, especially in developing countries (Ball et al.
triceps skinfold, height, gender and age as independent 2004). However, the use of skinfolds to estimate body fatness
variables. When cross-validated, the new PE was valid in this (BF) has not been without criticism (Slaughter et al. 1988;
sample (R 2 ¼ 0.80), while previously published equations Dezenberg et al. 1999; Ellis 2001; Kapoor and Anand 2002;
were not. Walker et al. 2002; Yao et al. 2002). Much of the criticism for
Conclusion: The PE was more valid for Brazilian children that skinfold prediction equations is focused on the outcome
existing equations, but further studies are needed to assess variable estimated, the population in which the equations
the validity of this PE in other populations. are derived and the validity of the equation in other cohorts
Keywords: Anthropometry, body composition, skinfolds, or populations (Bernal-Orozco et al. 2010). First, fat mass
stunting, developing countries (FM) is the univariate variable estimated with prediction
equations and has been reported to minimize some of the
complexity introduced into the prediction model process
INTRODUCTION and increase the predictive power of body-composition
The prevalence of overweight continues to increase in many models (Slaughter et al. 1988). Thus, equations that estimate
developing countries, even as the prevalence of under- %BF have limited predictive power and contribute to
nutrition remains relatively high (Doak et al. 2000; Kapoor potential bias of the prediction equation. Second, the
and Anand 2002; Caballero 2005). Access to body population in which the prediction equation is derived is
composition techniques available in wealthier countries, important as equations derived from adult cohorts may
such as dual energy x-ray absorptiometry (DEXA) or over-estimate body fatness by 3 –6% (Dezenberg et al. 1999)
bioelectrical impedance (BIA) (Eisenmann et al. 2004; and few of the many skinfold prediction equations
Ramirez-Zea et al. 2006), is limited and assessment of those published have been found to be valid across populations

Correspondence: Daniel J. Hoffman, Department of Nutritional Sciences, Rutgers, the State University of New Jersey, 26 Nichol Avenue, New
Brunswick, NJ 08901, USA. E-mail: dhoffman@aesop.rutgers.edu
(Received 12 August 2011; accepted 23 January 2012 )

156
SKINFOLD PREDICTION EQUATIONS IN CHILDREN 157

(Brook 1971; Reilly et al. 1995) and contribute to random or bicep, tricep, subscapular, suprailiac, thigh and calf sites
systematic errors (Durnin and Rahaman 1967; Brook 1971; using a Harpenden skinfold caliper (Country Technologies)
Reilly et al. 1995; Dezenberg et al. 1999). Still, while some according to the protocol of Lohman and Martorell (1988).
equations derived from multi-racial cohorts exist (Dezen- Measurements were made in triplicate using a standardized
berg et al. 1999), they have not been found to be valid for protocol and the mean value were used in all analyses.
Latino children, in whom new equations have been The development of a new prediction equation was
developed (Huang et al. 2003). Third, the specific predictive compared to previously published child-specific prediction
variables to be included in skinfold prediction equation is equations to calculate FM (in kg) using skinfold thickness
open to debate and some authors have suggested that (in millimetres), as follows:
measures of body size (e.g. height) should be included along
. Goran et al. (1996), both genders:
with measures of body mass (e.g. weight) to account for
difference in the predictive capacity of skinfold measures FM ¼ 0:18* weight þ 0:23* subscapular þ 0:13* tricep 2 3:0;
between the shortest and tallest individuals of a population
(Burton and Cameron 2009). . Slaughter et al. (1988):
It is important and necessary to continue to develop novel
skinfold prediction equations for use in transitional Boys : FM ¼ weight* ½ð1:21* SUMTRSB
Ann Hum Biol Downloaded from informahealthcare.com by Loughborough University on 04/18/12

countries, especially as the prevalence of obesity continues


to increase in these less-developed and non-Western 2 0:008* ðSUMTRSBÞ2 2 1:7Þ=100;
countries. By convention, such equations are best charac-
terized by the use of acceptable reference methods to obtain
Girls : FM ¼ weight* ½ð1:33* SUMTRSB
criterion measures of body composition (e.g. DEXA or
stable isotopes), the use of large, randomly selected samples 2 0:013* ðSUMTRSBÞ2 2 2:5Þ=100;
(n . 100), a high correlation between the reference measure
and predicted scores (R . 0.80) and cross-validation of the where SUMTRSB is the sum of the tricep and
Equation (Fields and Goran 2000). However, given that no subscapular skinfolds.
skinfold prediction equations exist for populations in . Huang et al. (2003):
For personal use only.

developing countries, the focus of this project was to


develop and evaluate a new prediction equation for FM ¼ ð0:632*weightÞ2ð1:606*ageÞ2ð1:882*genderÞþ3:330;
estimating FM in children from developing countries.
FMa ¼ ð0:764* weightÞ 2 ð0:471* heightÞ þ 45:955:
METHODS
Study cohorts Body fat and FFM were measured with a Hologic
Three independent cohorts were included in this study. The QDR – 4500A DXA (Hologic Inc., Bedford, MA) for the
first two were composed of children, studied at the Federal two cohorts in São Paulo and a Lunar Prodigy (General
University of São Paulo, who had been volunteers in studies Electic, Inc., Chalfont St. Giles, UK) for the cohort in
of metabolism and growth retardation. The third cohort was Jundiai using adult quick-scan software programs and the
composed of children from Jundiai, São Paulo as part of a children positioned according to standard protocols.
study on maternal diet and growth conducted by the Phantoms were used to calibrate the DXA before each
University of São Paulo. All children were examined by a measurement.
paediatrician prior to enrolling in theses studies and were
free from acute or chronic diseases. Informed consent was Statistical analyses and development of prediction
obtained from the parents of the children and the protocols equations
were approved by the ethical committees at each participat- To develop the prediction equation studied, the data from
ing university. the three cohorts were combined into one dataset. From this
dataset, using the random sample command in Systat, a
Body composition random sample of 30 subjects was selected. The randomly
Body composition was assessed using skinfold measure- selected subjects formed the Validation sample while those
ments as well as dual energy x-ray absorptiometry (DEXA). not selected formed the Development sample. According to
Anthropometric measurements were made in the mornings, Student’s t-test, there were no significant differences
with the children wearing shorts and t-shirts. Each cohort between the two samples with respect to the proportion of
had a single research assistant conduct the measurements on boys and girls, age, body weight, percentage fat mass or lean
all of the children in that particular cohort. Height was body mass. Using the Development sample, forward stepwise
measured to the nearest 0.5 cm using a mounted measuring linear regression analyses were conducted to determine
stick (Stadi-o-meter, Country Technologies, Green Bay, WI). which variables, including weight, tripceps skinfolds, height,
Weight was measured using a digital electronic scale gender and age, best predicted FM. The final equation
(Country Technologies) accurate to within 0.1 kg. Skinfold developed (model R 2 ¼ 0.77) and used in the subsequent
measurements were made on both sides of the body at the analyses and comparisons included the independent
q Informa UK, Ltd.
158 D. J. HOFFMAN ET AL .

Table I. Physical characteristics of the development and validation slope statistically different from the line of identity or an
samples (mean ^ SD). intercept different from 0 (Table III).
Variable Development Validation Neither the Goran, Slaughter nor Huang equations was
n 115 30 successfully cross-validated in our sample and the mean
Age (years) 9.8 ^ 1.3 10.1 ^ 1.5 differences in estimated BF compared with DEXA are
Weight (kg) 25.48 ^ 6.00 25.52 ^ 7.03 depicted in Figure 1.
Height (cm) 1.25 ^ 0.10 1.25 ^ 0.11
Fat Mass (kg) 4.84 ^ 2.34 4.82 ^ 2.90
Fat-Free Mass 20.64 ^ 4.37 20.70 ^ 5.00
Fat Mass (% weight) 18.4 ^ 5.9 18.06 ^ 6.21 DISCUSSION
Gender 42% M and 58% F 40% M and 60% F
As the global prevalence of overweight among children
continues to increase, the need for a simple method to
variables weight, sex, age, tricep skinfolds and height. estimate FM is great, especially for less developed countries
This equation was applied to the Validation sample for that lack the infrastructure or technology to use more
accuracy using paired Student’s t-test and deviation from advanced techniques. Anthropometric prediction equations
the line of identity in which a multiple linear regression have often been used for both individual and population
model was created with predicted FM entered as the
Ann Hum Biol Downloaded from informahealthcare.com by Loughborough University on 04/18/12

assessments of body composition in developing countries.


dependent variable and measured FM was entered as the However, such equations have generally been developed
independent variable. The equation was found to not and/or validated in well-nourished Caucasian children in
deviate from the line of identity if the model had a developed countries and may not be appropriate for
statistically significant X-intercept at 0 and the slope of the different racial groups or populations with broad variations
regression was equal to one. Student’s t-tests were conducted in height associated with nutritional stunting. The focus of
to determine statistically significant differences between this study was to use body composition data from DEXA to
measured FM and predicted FM. Each equation, published develop and validate a paediatric skinfold prediction
and developed, was considered valid if it was not equation in racially-mixed children from a developing
significantly different from the measured FM and did not country and compare it to existing equations. Briefly, in our
deviate from the line of identity. Statistical significance was group of Brazilian pre-pubertal children, the novel skinfold
For personal use only.

determined using a p-value of 0.05 and all statistical analyses prediction equation performed better than standard
were conducted using Systat 12 (SPSS Inc, Evanston, IL). published equations, even those developed for ‘Latino’
populations (Slaughter et al. 1988; Goran et al. 1996; Huang
et al. 2003). These results emphasize the need for continued
development of skinfold prediction equations for different
RESULTS
populations to minimize bias when assessing adiposity in
Selected physical characteristics of the children from this less developed regions of the world.
study subjects used in this study appear as means ^ SD in The validity of our proposed prediction equation differed
Table I. The mean values for the validation group were not in agreement with established equations and two potential
significantly different from the development group. areas are likely to have contributed to these differences. First,
Table II shows the model developed with the variables technical issues remain a threat to the internal validity of
entered for each step of the forward stepwise regression. anthropometric measurements. For example, investigator
Weight accounted for only 62% of the variance of fat mass. error (i.e. improperly chosen physical landmarks, not
The introduction of tricep skinfolds accounted for another following standard protocols, etc.) is a common issue that is
7%, while height accounted for an additional 5%. The usually minimized through the use of a small number of
introduction of gender and age accounted for an additional well-trained investigators and frequent quality control
1% and 2% of the variance of fat mass, respectively. measures. However, if the development of one equation is
The new equations were more accurate than the biased as a result of investigator error, that bias will persist
equations of Slaughter et al. (1988), Goran et al. (1996), when the equation is used in different cohorts. Also, the use
and Huang et al. (2003) in predicting FM (Table III) when of different gold standards used to develop the prediction
regressed against measured FM. When the novel and Equation (e.g. using hydrostatic weighing vs the four-
published prediction equations were regressed against compartment model) may influence the equation, as each
measured body fat, only the novel equation did not have a method may produce an inherent bias in the estimation of

Table II. Stepwise regression analysis for the determination of total fat mass (FM) as measured by dual energy X-ray absorptiometry.
Step and variable Regression equation for FM (kg) Model R 2 Model SEE (kg)
1. Weight 2 3.019 þ 0.308 * weight 0.62 1.453
2. Triceps 2 3.790 þ 0.266 * weight þ0.196 * triceps 0.69 1.325
3. Height 6.583 þ 0.460 * weight þ 0.183 * triceps – 12.110 * height 0.74 1.202
4. Gender 6.921 þ 0.464 * weight þ 0.157 * triceps (12.548 * height þ 0.580 * gender 0.75 1.180
5. Age 6.371 þ 0.488 * weight þ 0.128 * triceps (11.138 * height þ 0.645 * gender – 0.188 * age 0.77 1.204
Units for variables are as follows: Weight (kg), Triceps (mm), Height (m), Gender as Male ¼ 0 and Female ¼ 1, Age (years).

Annals of Human Biology


SKINFOLD PREDICTION EQUATIONS IN CHILDREN 159

Table III. Cross-validation of previously published fat mass prediction equations and the new equations DEXA FM vs predicted FM.
Equation n R2 Slope (kg) Intercept Measured-Predicted (kg)
Novel equation 30 0.80 1.152 ^ 0.109 2 0.630 ^ 0.571 0.088
Goran et al.a 30 0.67 1.365 ^ 0.180* 2 0.621 ^ 0.781** 0.834**
Slaughter et al.b 30 0.51 1.317 ^ 0.846 0.760 ^ 0.846** 1.736**
Huang et al.c 30 0.33 0.471 ^ 0.127* 2.692 ^ 0.722 0.304
Huang et al.c ‘simple’ 30 0.23 0.694 ^ 0.239 0.279 ^ 1.635** 1.722**
* Slope significantly different from 1.0; ** intercept significantly different.
a
Goran et al. (1996); b Slaughter et al. (1988); c Huang et al. (2003).

FFM or FM. It was reported that FM from skinfold new prediction equations for FM, mostly due to differences
prediction equations compared to estimates from five in the distribution of subcutaneous fat in different
precise body composition methods (DXA, total body populations. Furthermore, differences between specific
potassium, total body water, whole body electrical equations may also arise from the fact that not all prediction
conductivity and BIA), the mean difference in FM varied equations include the Tanner Stage of the children studied
from 2.72 to (0.14 kg (Ellis 2001). Thus, inconsistent use of (Dezenberg et al. 1999). Not only does FM and fat
gold standards as newer and more valid techniques have distribution change through pubertal development, but the
Ann Hum Biol Downloaded from informahealthcare.com by Loughborough University on 04/18/12

been developed, such as DEXA or stable isotopes, will most density and hydration of FFM are also influenced by age and
likely generate bias in the development and subsequent use maturation (Ortiz et al. 1992). Therefore, the inclusion of
of prediction equations. Tanner Stage in regression equations used to determine
Second, established equations have been developed in predictive factors of FM in cohorts of children can increase
racially homogeneous groups of children from developed not only the specificity of the equation, but also control for
countries (Slaughter et al. 1988; Goran et al. 1996). A confounding factors that may lead to bias between cohorts.
number of studies have reported that racial/ethnic Moreover, beyond the fact that the skinfold prediction
differences in either body composition or body fat equation developed in our cohort of low-income, racially
distribution exists, both of which can bias the accuracy of diverse children in Brazil, it is worth noting that height was a
skinfold prediction equations from one racial/ethnic major predictor in the validated equation. A review of the
For personal use only.

group to another. For example, in a study with Guatemalan most widely used skinfold prediction equations shows that
adults, equations developed specifically for this cohort height has been used as a predictive variable in only one
performed better than equations developed from other Equation (Huang et al. 2003). This is of concern given the
ethnic groups (Ramirez-Zea et al. 2006). Dezenberg et al. relatively recent paper in which the use of height to better
(1999) reported that neither the Goran nor the Slaughter predict body fat mass relative to body size, rather than body
equation were valid in a heterogeneous population of Black mass, is described (Burton and Cameron 2009). Briefly, the
and White children in the US. Several studies have reported authors reported that including a term for height2 improved
differences in body composition and body fat distribution the estimates of fat mass for the tallest and shortest persons.
between ethnic groups, such that Hispanic boys have more This observation is of particular relevance for developing
body fat mass than White and Black boys (Ellis 1997). regions where the prevalence of growth faltering (i.e.
Another group reported that, despite having similar total stunting) remains high. Thus, developing a skinfold
body fat mass, Black girls had more adipose tissue in the prediction equation that incorporates height may markedly
arms and trunk compared to White girls (Yanovski et al. improve the ability for investigators in transitional countries
1996). This highlights the importance of developing to better monitor changes in adiposity, rather than just BMI.
There has been a marked paucity of prediction equations
10 from cohorts in transitional countries and the validation of
an equation that may also accommodate large variations
8 in height contributes greatly to the existing literature
on methods to assess adiposity in developing regions of the
Fat mass (kg)

world.
6
There were two limitations to our study that merit
discussion, neither of which compromise the interpretation
4 or public health relevance of the results. First, the
anthropometric data were collected at different locations
2 by different technicians. However, the protocol used by each
technician was the same and the same procedures and
equipment were used for establishing landmarks and taking
0
DEXA Slaughter Goran Latino Novel skinfold measurements. Second, the time between the data
Technique to estimate fat mass
collection of one cohort was , 6 years before that of the
second cohort. Still, it is unlikely that this time difference
Figure 1. Comparison of published prediction equations with an would influence any aspect of body composition in two
equation developed in pre-pubertal children from Brazil. cohorts of the same age. Finally, the population in which our
q Informa UK, Ltd.
160 D. J. HOFFMAN ET AL .

equation was derived is a heterogeneous group living in the Doak CM, Adair LS, Monteiro C, Popkin BM. 2000. Overweight and
shantytowns of São Paulo and Jundiai. As with most underweight coexist within households in Brazil, China and Russia.
J Nutr 130:2965– 2971.
shantytowns in urban areas of São Paulo state, most families
Durnin JV, Rahaman MM. 1967. The assessment of the amount of fat
originate from the northeastern region of Brazil and are of in the human body from measurements of skinfold thickness. Br J
mixed ethnicity (e.g. Portuguese, African and Indigenous). Nutr 21:681 –689.
Thus, there may be limited generalizability to children from Eisenmann JC, Heelan KA, Welk GJ. 2004. Assessing body composition
Asian or European families, perhaps more so for children of among 3- to 8-year-old children: anthropometry, BIA, and DXA.
Obes Res 12:1633 – 1640.
mixed ancestry, but the novel prediction equation can be
Ellis KJ. 1997. Body composition of a young, multiethnic, male
validated in other cohorts in Latin America and elsewhere. population. Am J Clin Nutr 66:1323 – 1331.
Ellis KJ. 2001. Selected body composition methods can be used in field
studies. J Nutr 131:1589S– 1595S.
CONCLUSION Fields DA, Goran MI. 2000. Body composition techniques and the
four-compartment model in children. J Appl Physiol 89:613 – 620.
Based on the data from the cohorts studied, the use of the
Goran MI, Driscoll P, Johnson R, Nagy TR, Hunter G. 1996. Cross-
new prediction equation is more valid compared to calibration of body-composition techniques against dual-energy X-
equations developed in the US or other developed nations. ray absorptiometry in young children. Am J Clin Nutr 63:299 –305.
Thus, this equation may better serve investigators in Hoffman DJ, Sawaya AL, Martins PA, McCrory MA, Roberts SB. 2006.
Ann Hum Biol Downloaded from informahealthcare.com by Loughborough University on 04/18/12

developing nations as our novel equation was developed Comparison of techniques to evaluate adiposity in stunted and
nonstunted children. Pediatrics 117:e725– e732.
using advanced body composition techniques and from
Huang TT, Watkins MP, Goran MI. 2003. Predicting total body fat
cohorts of racially mixed children. Future studies should from anthropometry in Latino children. Obes Res 11:1192 – 1199.
focus on testing the novel prediction equation on children in Kapoor SK, Anand K. 2002. Nutritional transition: a public health
other developing countries and/or combining data from challenge in developing countries. J Epidemiol Community Health
different ethnic groups to develop additional equations that 56:804– 805.
Lohman TG, Martorell R, editors. 1988. Anthropometric standardiz-
could be used across cultures and ethnic groups.
ation reference manual. Champaign, IL: Human Kinetics.
Ortiz O, Russell M, Daley TL, Baumgartner RN, Waki M, Lichtman S,
Declaration of interest: The authors report no conflict of Wang J, Pierson RN, Jr, Heymsfield SB, et al. 1992. Differences in
interest. The authors alone are responsible for the content skeletal muscle and bone mineral mass between black and white
For personal use only.

and writing of the paper. females and their relevance to estimates of body composition. Am J
Clin Nutr 55:8– 13.
Ramirez-Zea M, Torun B, Martorell R, Stein AD. 2006. Anthropo-
metric predictors of body fat as measured by hydrostatic weighing in
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