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PEDIATRICS Vol. 104 No. 3 September 1999, p. e33
,
, and
From the * Division of Epidemiology, Statistics and Prevention
Research, National Institute of Child Health and Human Development,
National Institutes of Health, Bethesda, Maryland;
PricewaterhouseCoopers, Washington, DC; § Division of Health
Examination Statistics, National Center for Health Statistics, Centers
for Disease Control and Prevention, Hyattsville, Maryland; and
Westat, Inc, Rockville, Maryland.
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ABSTRACT |
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Top
Abstract
MaterialsMethods
Results
Discussion
References
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Objective. To compare young children
3 to 6 years of age who were born small-for-gestational age (SGA;
<10th percentile for gestational age) or large-for-gestational age
(LGA; 
90th percentile) with those who were born
appropriate-for-gestational age (10th-89th percentile) to determine
whether there are differences in growth and fatness in early childhood
associated with birth weight status.
Design and Methods. National sample of 3192 US-born
non-Hispanic white, non-Hispanic black, and Mexican-American children
3 to 6 years of age (36-83 months) examined in the third National
Health and Nutrition Examination Survey and for whom birth
certificates were obtained. On the birth certificates, length of
gestation from the mother's last menstrual period was examined for
completeness, validity, and whether the pattern of missing
(n = 141) and invalid data (n = 147) on gestation was random. Gestation was considered invalid when
>44 weeks, or when at gestations of 
35 weeks, birth weight was
inconsistent with gestation. To reclaim cases with missing or invalid
data on gestation for analysis, a multiple imputation (MI) procedure
was used. MI procedures are recommended when, as in this case, a
critical covariate (length of gestation) is not missing at random, and
complete-subject analysis may be biased. Using the results of the MI
procedure, children were categorized, and growth outcome was assessed
by birth weight-for-gestational age status. The growth outcomes
considered in these analyses were body weight (kg), height (cm), head
circumference (cm), mid-upper arm circumference (MUAC; cm), and triceps
and subscapular skinfold thicknesses (mm). The anthropometric outcomes
first were transformed to approximate normal distributions and
converted into z scores (standard deviation units
[SDU]) to scale the data for comparison across ages. Outcomes at each
age then were estimated using regression procedures. SUDAAN software
that adjusts variance estimates to account for the sample design was
used in analysis for prevalence estimates and to calculate regression
coefficients (in SDU).
Results. Over these ages, children born SGA remained
significantly shorter and weighed less (
0.70 to 0.60 SDU). Children
born LGA remained taller and weighed more (0.40-0.60 SDU). For weight
and height among LGA children, there was a divergence from the mean with age compared with those born appropriate-for-gestational age
(10th-89th percentile). Head circumference and MUAC followed these
same patterns. The coefficients for MUAC show values for SGA children
fairly consistently at about 0.50 SDU and children born LGA show
increasing MUAC from +0.40 to +0.50 SDU from 36 to 83 months of age. As
with weight, there is a trend toward increased MUAC coefficients with
age. Measures of fatness (triceps and subscapular skinfolds), which are
more prone to environmental influences, showed less association with
birth weight-for-gestational age status. Only a single age group, the
oldest (6 years of age) group showed a significant deficit in fatness
for children born SGA. For children born LGA, there was an increase in
fatness at both the triceps and subscapular sites after 3 years of
age.
Conclusion. These findings on a national sample of US-born non-Hispanic white, non-Hispanic black, and Mexican-American children show that children born SGA remain significantly shorter and lighter throughout early childhood and do not seem to catch up from 36 to 83 months of age. LGA infants remain longer and heavier through 83 months of age, but unlike children born SGA, children born LGA may be prone to an increasing accumulation of fat in early childhood. Thus, early childhood may be a particularly sensitive period in which there is increase in variation in levels of fatness associated with size at birth. These findings have implications for the evaluation of the growth of young children. The results indicate that intrauterine growth is associated with size in early childhood. Particularly, children born LGA may be at risk for accumulating excess fat at these ages. Birth weight status and gestational age may be useful in assembling a prognostic risk profile for children. Key words: blacks, birth weight, growth, large-for-gestational-age, multiple imputation, Mexican-Americans, National Health and Nutrition Examination Survey, small-for-gestational age, whites.
Infants born small, defined as low birth
weight-for-gestational-age (BWGA), generally catch up over the first 6 months, whereas the growth of large infants slows.1,2
After this initial period of growth compensation, body weight and
height have been shown to track through childhood within birth weight categories in several large US studies.3-6 A number of
smaller, prospective studies also have demonstrated that BWGA status,
both small and large, is associated with growth status through infancy
and childhood up to 6 to 8 years of age.7-13 Whether
growth in early childhood (3-6 years of age) is associated with fetal
growth and growth status at birth when length of gestation is taken
into account has not been demonstrated for an ethnically diverse sample
of US-born children. The objective of this study was to compare
the growth of non-Hispanic white, non-Hispanic black, and
Mexican-American children born small-for-gestational age (SGA; birth
weight <10th percentile for gestational age) and large-for-gestational
age (LGA; Design and Sample
Nearly 40 000 people A total of 4262 children were sampled in the target age range. A
household interview, usually with a parent respondent, was completed
for 4121 of these children (96.7%). Informed consent was obtained from
parents or guardians at the time of interview to seek birth
certificates for these children. Health examinations including an
anthropometric measurement component were given to 3878 children
(91.0%), usually within 2 to 4 weeks of the interview. Among the
examined children, 3653 of 3878 (94.1%) were US-born.
Birth Certificates
Birth certificates were sought from the reported states of birth
and positively matched for 3428 (93.8%) of the US-born children. Excluded were 5 cases with missing birth weights, 5 cases in which sex
was discrepant between the birth certificates and NHANES III, and 83 children who were twins or triplets. The sample then was restricted to
non-Hispanic white, non-Hispanic black, and Mexican-American children.
Children of all other races/ethnicities (n = 143) were excluded, because the reference data used to categorize
BWGA15 are specific for the race (white vs black) given on
birth certificates. The final analytic sample was 3192 children.
Using procedures used earlier,16,17 length of gestation
determined from the mother's last menstrual period as reported on the
birth certificate was examined for validity. Gestation was considered
invalid when >44 weeks (n = 72) and when, at
gestations of However, an examination of the pattern of missing and invalid
gestations indicated that gestation was not missing or invalid at
random.18,19 Gestation was more likely to be missing or
invalid (>44 weeks) if the infant was Mexican-American, currently
residing in an urban area or in the West census region, and when
the interview was conducted in Spanish. Gestation was more likely to be
considered invalid because it was inconsistent with birth weight (early
for size) for non-Hispanic blacks and for those living in rural areas
or in the South census region. Because these factors (race/ethnicity
and urban/rural dwelling) are known also to be associated with the
dependent variables (childhood growth status and body composition),
there was concern that an analysis of the sample for whom data were
complete (complete-subject analysis) would yield results that were
biased.
Multiple Imputation (MI) Procedure
To reclaim the cases (n = 288) with missing or
invalid gestation for analysis, a MI procedure was
used.18,19 MI is a method of handling nonresponse that
retains the primary advantages of single imputation but avoids its
drawbacks by replacing each missing datum with two or more values drawn
randomly from a distribution of likely values. MI procedures are
recommended when, as in this case, a critical covariate (length of
gestation) is not missing at random, and complete-subject analysis may
be biased.19
Gestation was imputed (5 imputations) using a regression including
race/ethnicity, infant sex, mother's height and age, cigarette smoking, parity, family size, mother's race, and state of residence. A
total of 267 of the 288 (92.7%) missing or invalid gestations were
predicted using this model. Only 21 cases could not be reclaimed because of concurrent missing data (mother's height and cigarette smoking), leaving a final sample of 3171 for analysis of outcome.
BWGA Categories
To categorize BWGA status, a reference based on 1989 vital
statistics15 was used in which infants are categorized separately by race (white vs black) and within race by infant sex (male
vs female) and maternal parity (infants of primiparas vs multiparas).
Infants designated by NHANES III as non-Hispanic white were categorized
using the reference percentiles for whites, and infants designated as
non-Hispanic black were categorized using the reference percentiles for
blacks.15 Mexican-American infants were categorized using
the percentiles for whites consistent with the approach used to derive
the reference data.15
SGA indicating intrauterine growth retardation was defined as a BWGA
below the 10th percentile, AGA from the 10th to 89th percentile, and
LGA or macrosomia at or above the 90th percentile. For the
complete-subject sample (n = 2904) with complete or
valid information for gestation, the prevalence of SGA was 10.4% ± 1.1%, AGA was 77.7% ± 2.0%, and LGA was 11.9% ± 1.1%. For the
sample with complete or valid information for gestation, the prevalence of very preterm delivery (<33 weeks) was 1.4% ± 0.4%, preterm delivery (33 to 36 weeks) was 5.8% ± 0.7%, and term was 92.9 ± 0.8%.
Age Groups and Anthropometry
The children were grouped into four age groups: 36 to 47 months
(3 years), 48 to 59 months (4 years), 60 to 71 months (5 years), and 72 to 83 months (6 years) based on age at examination. At 72 to 83 months,
the group included 39 children who were 84 months (n = 35) or 85 months (n = 4) at the time of examination but
who had been interviewed at 83 months of age.
The anthropometric measurements considered in these analyses were body
weight (kg), height (cm), head circumference (cm), mid-upper arm
circumference (cm), and triceps and subscapular skinfold thicknesses
(mm). The body measurements were recorded after standard anthropometric
protocols.20,21
Other Variables
Maternal parity was based on number of previous births reported
on the birth certificate. Categories of race/ethnicity were based on
parental self-reports from NHANES III using US Bureau of the Census
definitions.14 Other variables used only to determine the
pattern of missing or invalid gestation and in the imputation
regressions were taken from both birth certificates and NHANES III
data. These included mother's age, race, and state of residence from
the birth certificate; mother's height, smoking during pregnancy,
family size, language of interview, and region of residence were taken
from NHANES III. The distributions relative to birth weight status of
maternal variables used only to impute gestation are not reported.
Statistical Methods
Sample weights were used to account for the oversampling and
unit nonresponse. SUDAAN software, which uses a Taylor series expansion
to adjust variance estimates to account for the sample design, was used
to estimate standard error (SE) of the prevalence data and background
characteristics.22,23
Because the distributions can be skewed, the anthropometric variables
were transformed before analysis.24,25 Body weight,
mid-upper arm circumference (MUAC), and triceps skinfolds were
transformed to an approximate normal distribution using a power
transformation of To control for group differences (race/ethnicity and sex) and scale the
values for comparison across ages, the anthropometric variables were
converted into z scores28 (mean: 0; SD: 1) internally within the sample age, sex, and race/ethnicity groups. By
normalizing the distributions, percentiles corresponding to the
z scores (standard deviation units [SDU]) can be estimated using the area under the normal curve. Assuming normality, a
z score or SDU of zero represents both the mean and the
median; the 10th and 90th percentiles are Analyses of the growth and body composition variables were performed
using SUDAAN regression procedures.23 Eight separate
indicator variables were created representing SGA and LGA for each of
the four age groups and were entered into a single regression with the
anthropometry z scores as the dependent variables. Regression coefficients (±SE) in SDU from results of the MI for gestation were combined using the equations of Little and
Rubin18 and were tested for statistical significance
( Comparison of coefficients for the outcomes generated in
complete-subject analyses compared with the results using the MI procedures showed that there was little difference in magnitude by
reclaiming the 267 cases but that the inclusion of the additional cases
did reduce sufficiently the variance of the estimates so as to
strengthen statistical significance. Only results using the MI
procedure are reported here.
The background characteristics of the sample (N = 3192) are presented in Table 1 and are
estimated using the statistical weights for examined children to
account for the complex sample survey design.22 Births to
primiparous women represent >40% of the children. The proportion of
low birth weight (<2500 g, both preterm and term) is 10%; just over
10% are macrosomic ( TABLE 190th percentile) with the growth of normal birth weight
children (appropriate-for-gestational age [AGA]) at 3 to 6 years of
age.
MATERIALS AND METHODS
Top
Abstract
MaterialsMethods
Results
Discussion
References
2 months of age representative of the US
civilian, noninstitutionalized population, were selected to participate
in the third National Health and Nutrition Examination Survey (NHANES
III; 1988-1994) conducted by the National Center for Health
Statistics, Centers for Disease Control and
Prevention.14 The analyses reported here focus on
NHANES III children from 36 months of age, the age at which measures of
height generally are preferred over recumbent length, to 83 months of
age (3-6 years). The anthropometric measurements available for these
ages include weight, standing height, head circumference, and
anthropometric measurements of body composition (mid-upper arm
circumference and triceps and subscapular skinfolds).
35 weeks, birth weight was inconsistent with gestation
(n = 75).15 Gestation from the last
menstrual period was missing for 141 cases. Because we have shown
previously that differences in growth relating to preterm delivery do
not contribute to the overall group differences among BWGA groups after
the first year,16 very preterm and preterm deliveries were
not excluded from the analyses.
1/
x. Subscapular skinfolds were
transformed using a negative reciprocal (1/x) to minimize
the effects of very large values of the subscapular skinfold. Height
and head circumference were not transformed, because both are nearly
normally distributed at these ages.26,27
1.28 SDU and +1.28 SDU,
respectively.
= .05) from zero (AGA reference). As expected, the intercepts
from the regression equations representing the mean for the AGA
reference did not differ significantly from zero in any analysis.
RESULTS
Top
Abstract
MaterialsMethods
Results
Discussion
References
4000 g).
Distribution* of US-born non-Hispanic White, non-Hispanic Black, and
Mexican-American Singletons by Selected Characteristics 36 to 83 months
of Age, NHANES III, 1988-1994
The growth outcomes include measures of overall body mass and size
(weight and MUAC), linear measurements (height and head circumference),
and measures of fatness (triceps and subscapular skinfolds). Weight in
early childhood shows the clearest pattern of association with BWGA
status. This is not unexpected, because deviations in weight form the
bases of the classification (Fig 1). Children born SGA stay at ~0.70 SDU for weight from 36 to 83 months
of age (Table 2). Children born LGA increase
in size over these ages from +0.40 to ~+0.70 SDU (Fig 1).
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The coefficients for MUAC show values for SGA children fairly
consistently at ~0.50 SDU and children born LGA show increasing MUAC from +0.40 to +0.50 SDU from 36 to 83 months of age (Table 2). As
with weight, there is a trend toward increased MUAC coefficients with
age.
The results for height (Fig 2) and head circumference show coefficient patterns that are similar to measures of body size. All coefficients are significantly different from zero with the exception of that for height for the children born LGA at 48 to 59 months of age (Table 2). For both height and head circumference children born LGA seem to show a tendency to deviate from the mean with age, but particularly for head circumference the trend is not as sharply linear.
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Measures of fatness, which are more prone to environmental influences and measurement error, show less association with BWGA status (Table 2). The coefficients are significant for triceps and subscapular skinfolds indicating a relative deficit in fatness only at 72 to 83 months (6 years) of age for children born SGA. For children born LGA, skinfolds are progressively higher from 4 years of age onward especially at the triceps site (Fig 3).
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DISCUSSION |
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Top
Abstract
MaterialsMethods
Results
Discussion
References
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The objective of these analyses was to compare the growth status
of children 3 to 6 years of age born SGA (<10th percentile BWGA) and
LGA (90th percentile) with those born AGA. We show that there are
effects of BWGA status on measurements of body mass and size (weight
and MUAC) and linear measurements (height and head circumference) in
early childhood from 36 to 83 months of age. The coefficients
(z scores) for children born SGA remain at fairly consistent
levels below the mean. However, for children born LGA, there is
increasing deviation from the mean (AGA reference: 0) with age.
Measures of MUAC follow this pattern. The levels of deficit in height
are fairly consistent across the ages for children born SGA, and there
is again an increase in the SDU with age for children born LGA.
Measures of head circumference followed this same pattern based on BWGA
status.
These findings are in agreement with the few large US studies that have considered the entire range of birth weight and demonstrated that weight and length or height status based on size at birth (independent of gestation) tend to track during early childhood.3-6 Smaller clinical studies that have followed SGA infant growth prospectively have also consistently found significant differences attributable to SGA status in childhood and beyond.7-9
In the largest clinical study, Ounsted et al10-12 in Oxford conducted a 7-year longitudinal study comparing 238 SGA (18 with gestational ages of <37 weeks), 246 AGA (8 preterm), and 241 LGA (1 preterm) white, singleton infants. Follow-up at 4 years10,11 and 7 years12 showed significant differences among the groups in height and weight. The Oxford children born SGA were 3 cm shorter at 4 years of age than were the AGA children and weighed 2 kg less. The children born LGA were taller by 3 cm and heavier by 2 kg.10,11 The SGA group was still about 3 cm shorter at 7 years of age, whereas the LGA group was 3 to 4 cm taller. The SGA group was 2 kg lighter and the LGA group 2 to 3 kg heavier than was the AGA group.12 Our findings on a much larger, national sample of non-Hispanic white, non-Hispanic black, and Mexican-American children clearly confirm these earlier studies on white children on the effects of birth weight status on height and weight in early childhood. However, it should be noted that the weighted NHANES III sample reflects a US population that is primarily non-Hispanic white, and findings may still be most applicable to that group.
Measures of fatness do not show the same association with BWGA status,
especially for children born SGA. Overall, for children born SGA, the
coefficients for skinfolds are negative, although small and not
generally significant through these ages in childhood. Our findings for
SGA children 83 months of age follow on and overlap our previous
analyses of the growth outcomes of NHANES III infants and young
children 2 to 47 months of age.16,17 In previous analyses,
we showed that the discrepancies in weight at 2 to 47 months of age
among SGA children are attributable primarily to deficits in
muscularity.16,17 At the earlier ages, there were
consistent differences among the BWGA status groups for measures of
body size and linear measures, but no comparable differences in levels
of fatness for either SGA or LGA children through 3 years of
age.17
However, for children born LGA, there seems to be an increase in fatness after 3 years of age. Because skinfolds are measured less precisely than weight or linear measurements, it might be expected that the relationship of the skinfold levels to birth weight status is attenuated because of measurement error. Reliability estimates for the anthropometric measurements from the two HANES surveys before NHANES III have indicated that skinfold measurements have greater interobserver measurement error than other linear measurements or weight.29,30 In fact, in our analyses the magnitude of the coefficients for skinfolds is diminished. Nevertheless, the increasing levels of fatness among LGA children parallel the increase over these ages in weight and MUAC and are thus unlikely to be attributable to measurement error.
Skinfold levels for children born LGA are virtually identical to those of children born AGA at 3 years of age (SDU close to zero), but by 6 years of age, the levels of skinfolds have diverged considerably to >+0.60 SDU. This is consistent with findings from the British National Study of Health and Growth of children 5 to 11 years of age in which it was shown that by 5 years of age, birth weight contributed significantly and positively to the variation in triceps and subscapular skinfolds.31
Early childhood may be a particularly sensitive period in which there is increase in the variation in levels of fatness.32,33 The development of overweight and increase in fatness among some 4- to 5-year-old children may be associated with the timing of the adiposity rebound, the point at which body mass index (and skinfolds) begins to rise from the childhood trough.34-36 Rolland-Cachera et al34 have noted that as many as 30% of all children have their adiposity rebound at as early as 4 years of age, and an earlier adiposity rebound has been associated with both larger size in early childhood and a high-protein diet in very early childhood (2 years of age).35 Children born LGA, because they are both heavier and taller at 4 to 5 years, may be more likely to have an earlier adiposity rebound and show increased fatness at 4 to 6 years of age relative to their more slowly maturing counterparts.34,36 This increase in fatness may be of concern if it leads to overweight in childhood, thereby increasing the risk for overweight in adulthood.37,38
The findings reported here on a national sample of US-born non-Hispanic white, non-Hispanic black, and Mexican-American children confirm that children born SGA continue to remain significantly shorter and lighter throughout early childhood, and they do not seem to catch up from 36 to 83 months of age. LGA infants remain longer and heavier through 83 months of age, but unlike children born SGA, children born LGA may be prone to the increasing accumulation of fat in early childhood. Thus, these findings have implications for the evaluation of the growth of young children. Intrauterine growth is associated with size in early childhood, and birth weight status and gestational age may be useful in assembling a prognostic risk profile for children.
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FOOTNOTES |
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This work was completed in part when Dr Maurer was with the Division of Health Examination Statistics, National Center for Health Statistics, and Ms McGlynn and Dr Davis were with the Klemm Analysis Group in Hyattsville, MD.
Received for publication Oct 29, 1998; accepted Feb 10, 1999.
Reprint requests to (M.D.O.) Division of Epidemiology, Statistics and Prevention Research, NICHD/NIH, Bldg 6100, Rm 7B03, 9000 Rockville Pike, Bethesda, MD 20892-7510. E-mail: mary-overpeck{at}nih.gov
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ABBREVIATIONS |
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BWGA, birth weight-for-gestational-age; SGA, small-for-gestational age; LGA, large-for-gestational age; AGA, appropriate-for-gestational age; NHANES III, third National Health and Nutrition Examination Survey; MI, multiple imputation; MUAC, mid-upper arm circumference; SDU, standard deviation units.
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REFERENCES |
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Abstract
MaterialsMethods
Results
Discussion
References
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