Original Article Obesity

PEDIATRIC OBESITY

Longitudinal Body Composition of Children Born to Mothers

with Normal Weight, Overweight, and Obesity
Aline Andres1,2, Holly R. Hull3, Kartik Shankar1,2, Patrick H. Casey2, Mario A. Cleves1,2, and Thomas M. Badger1,2

Objective: The longitudinal trajectories of body composition of children born to mothers with normal
weight, overweight, and obesity have not been evaluated using precise body composition methods. This
study investigated the relationship between maternal prepregnancy BMI and offspring body composition
trajectories during the first 6 years of life.
Methods: Healthy infants (N 5 325) were assessed longitudinally (at ages 0.25, 0.5, 0.75, 1, 2, 3, 4, 5,
and 6 years) using dual-energy X-ray absorptiometry. Mixed-effects regression for repeated measures
was used to model each continuous outcome as a function of maternal BMI and covariates (race, gesta-
tional age, birth weight, and mode of infant feeding).
Results: Maternal obesity differentially impacted body fat, but not bone mineral content or density, of
girls and boys. Boys born to mothers with obesity have higher body fat from ages 2–6 years compared
to boys born to normal-weight and overweight mothers (P < 0.05), whereas body composition of girls
born to mothers with obesity was not different across groups during the first 6 years of life (P > 0.05).
Conclusions: This clinical observational study demonstrates a sexual dimorphism in offspring body com-
position until age 6 years based on maternal BMI, with a greater effect of maternal adiposity seen in
boys than in girls.
Obesity (2015) 23, 1252–1258. doi:10.1002/oby.21078

Introduction influences newborn body composition, longitudinal body composi-

tion data with repeated measures are largely absent from the litera-
With the current rates of childhood and adult obesity (1), ongoing ture. It is less clear whether the influence of maternal obesity is
research is attempting to understand the antecedents and critical long lasting or what factors may influence the trajectory for the
time periods that predict obesity development. Past focus has been development of offspring body composition in childhood. Kaar et al.
on the time periods surrounding pregnancy, early infancy, and child- (9) collected maternal data during pregnancy and performed mag-
hood as critical windows that relate to future obesity development. netic resonance imaging (MRI) scans when offspring were 10 years
Key indicators of the maternal in utero environment have been old. They found that offspring born to overweight/obese women had
found to influence offspring fat mass (FM). Maternal prepregnancy a greater BMI and greater volumes of subcutaneous and visceral adi-
BMI has been reported by several studies to be positively related to pose tissue when compared to offspring born to normal-weight
newborn FM (2-4), and offspring born to obese mothers have greater women. This relationship may continue beyond the first decade of
central FM (5). However, a 2012 study found maternal pre- life. As part of the Motherwell Birth Cohort Study, Reynolds et al.
pregnancy BMI was not related to infant FM (total or by region) at (10) estimated offspring FM using skinfolds. A positive relationship
1 year (6). Maternal gestational weight gain (GWG) was reported to was found between maternal BMI and adult offspring FM at 30
be positively related to offspring FM at 1 month and 6 years (7). years old. However, the study was conducted more than 40 years
Further, excessive GWG on newborn FM has been reported to vary ago when the average BMI at 17 weeks in pregnancy was 23.3 kg/
by maternal prepregnancy BMI (3). m2, and the average GWG was between 9.4 and 10 kg (10). Recent
data report the average maternal BMI before pregnancy is 25.0 kg/
Other reports suggest that the relationship between total FM and m2, and average GWG is 15.7 kg (11). Therefore, older cohort data
where that FM is located (central versus peripheral) is influenced by may under-represent the relationships when compared to more
prepregnancy maternal obesity (8). While it appears maternal obesity recent cohorts.

1
Arkansas Children’s Nutrition Center, Little Rock, Arkansas, USA. Correspondence: Aline Andres (E - mail: [email protected]) 2 Department of
Pediatrics, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA 3 School of Health Professions, University of Kansas Medical Center,
Kansas City, Kansas, USA.

Funding agencies: USDA Agriculture Research Service CRIS 6251–51000-07D.

Disclosure: The authors declare no conflicts of interest.
Author contributions: TMB and PHC designed the study. TMB, PHC, and AA supervised data collection. MAC and AA analyzed the data. All authors were involved in
writing the paper and had final approval of the submitted and published versions.
Received: 30 October 2014; Accepted: 11 February 2015; Published online 9 May 2015. doi:10.1002/oby.21078

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Original Article Obesity
PEDIATRIC OBESITY

Data are emerging to suggest the impact of maternal prepregnancy fat percentage (trunk FM [kg]/total body mass [kg]) and peripheral
BMI on offspring FM appears early and is likely long lasting. How- fat percentage (peripheral FM [kg]/total body mass [kg]) were calcu-
ever, repeated longitudinal data assessing the trajectory of body com- lated in an attempt to dissect the contribution of central versus
position change from early infancy through childhood and beyond are peripheral adiposity to the whole body adiposity in boys and girls
lacking. Prior data have reported differences in offspring FM at spe- between ages 2 and 6 years. Adiposity in this manuscript refers to
cific time points (birth, etc.) based on maternal characteristics, but it the percentage of whole body fat.
is unknown whether children born to obese women have a different
trajectory for the development of body composition [FM, fat free
mass (FFM), bone mineral content (BMC), and bone mineral density Statistical analyses
(BMD)] across time and whether this effect varies by sex. The pur- Participant’s characteristics measured in the nominal scale are sum-
pose of this article was to investigate the association between mater- marized as counts and percentages and compared across the three
nal prepregnancy BMI and offspring body composition across infancy maternal prepregnancy BMI categories using Pearson’s Chi-Square
into childhood and to explore the influence of maternal obesity on the test or Fisher’s exact test. Participant’s characteristics measured in
trajectory of body composition development at ages 0.25, 0.5, 0.75, 1, the interval scale are summarized as means and standards deviations
2, 3, 4, 5, and 6 years. We also explored whether these effects differed (SD) and compared across the three prepregnancy BMI categories
by sex. We hypothesized that children born to obese mothers would using analysis of variance (ANOVA) followed by Tukey-Kramer post
have greater BMI-for-age Z-scores and body fat than children born to hoc tests. Mixed-effects regression for repeated measures was used to
normal-weight or overweight mothers during the first 6 years of life. model each continuous outcome as a function of maternal prepreg-
In addition, based upon experimental results, we postulated that boys nancy BMI category and covariates (race, gestational age, birth
would be more responsive to maternal obesity than girls (12). weight, and mode of infant feeding). Covariates were identified using
a stepwise regression analysis. Linear or restricted cubic splines for
child’s age were computed and interacted with maternal prepreg-
nancy BMI category to better model the association between age and
Methods each outcome. All models were fitted via maximum likelihood esti-
mation. From each fitted model, marginal effects, and delta-method
Participants standard errors were computed at each visit age and also for the over-
Participants were infants enrolled in a longitudinal cohort, the Begin-
all time trajectory (15). Computed marginal effects were compared
nings Study (www.clinicaltrials.gov, ID # NCT00616395). Pregnan-
across maternal prepregnancy BMI category using Wald tests. Mar-
cies were reported uncomplicated. All mothers were nonsmokers, who
ginal effects compared cross-sectional at each visit age were adjusted
denied alcohol use during pregnancy. Infants were term (>37 weeks).
for multiple testing using Simes’ multiple testing procedure, which is
Breast-fed infants were exclusively breast-fed until at least age 6
better suited than Bonferroni’s method when the hypotheses are cor-
months. Socioeconomic status [Hollingshead Four-Factor Index of
related (16). Data analysis was performed using Stata V13.1 statisti-
Social Status (13)], gestational age, race, birth weight, and birth
cal package (Stata Corporation, College Station, TX).
length were self-reported. At the child’s 3-month visit, maternal
height was measured using a stadiometer and prepregnancy weight
was self-reported. The study was approved by the Institutional
Review Board of the University of Arkansas for Medical Sciences. Results
Of the 325 infants who participated in this study, 125 children were
Anthropometrics born to normal-weight mothers (BMI 18.5–24.9), 94 were born to
Anthropometric measures (recumbent weight and length) were overweight mothers (BMI 25.0–29.9), and 106 were born to obese
obtained at each study visit using standardized methods. There were mothers (BMI  30, Table 1). There were no significant differences
no differences between groups in infant’s age at the time of mea- between groups in socioeconomic status or birth length. Infants born
surement for each study visit (P > 0.05). Briefly, infant weight was to normal-weight mothers had significantly higher gestational age
measured to the nearest 0.01 kg using a tarred scale (SECA 727, compared to infants born to overweight or obese women; whereas,
SECA, Ontario, CA) wearing a diaper only. Infant length or child infants born to obese mothers had higher birth weight as compared
height was measured to the nearest 0.1 cm by using a length board to infants born to normal-weight or overweight mothers (Table 1).
(Easy Glide Bearing Infantometer, Perspective Enterprises, Portage, Furthermore, children born to obese and overweight mothers were
MI) or a statiometer. BMI-for-age Z-scores were computed from the more likely to be fed infant formula than breast milk compared to
WHO growth standards according to the CDC recommendation (14) children born to normal-weight mothers (P < 0.001, Table 1). Thus,
using WHO Anthro software version 3.2.2. body composition results were adjusted for race, gestational age,
birth weight, and mode of infant feeding. Multiple comparison
adjustments were used when comparing feeding groups at each time
Body composition point independently.
Body composition was assessed using dual-energy X-ray absorpti-
ometry (DXA, Hologic QDR 4500 with discovery upgrade, Hologic, The adjusted BMI-for-age Z-scores overall time trajectories were
Bedford, MA). All scans without movement artifact were processed higher in girls born to overweight and obese mothers compared to
and analyzed using infant whole body mode or pediatric whole body girls born to normal-weight mothers over the course of the first 6
mode (QDR software for Windows XP, version 12.3, Hologic, Bed- years of life (P 5 0.0028). When analyzing each time point inde-
ford, MA). FM (kg), body fat (%), trunk FM (kg), BMC (g), and pendently, the adjusted BMI-for-age Z-scores were higher in girls
BMD (g/cm2) were computed by the QDR software. Peripheral FM born to overweight mothers at 0.75 years as compared to girls born
(kg) was obtained by adding FM (kg) values for all limbs. The trunk to normal-weight and obese mothers, whereas by ages 5 and 6 years,

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Obesity Maternal Obesity and Offspring Body Composition Andres et al.

TABLE 1 Cohort characteristics

Maternal BMI category

All Normal weight Overweight Obese P-value

N 325 125 94 106

Race
Caucasian, N (%) 285.0 (87.7) 117.0 (93.6) 81.0 (86.2) 87.0 (82.1) 0.0123
African-American, N (%) 29.0 (8.9) 3.0 (2.4) 12.0 (12.8) 14.0 (13.2)
Other/unknown, N (%) 11.0 (3.4) 5.0 (4.0) 1.0 (1.1) 5.0 (4.7)
Infant’s sex
Female, N (%) 167.0 (51.4) 69.0 (55.2) 44.0 (46.8) 54.0 (50.9) 0.4666
Male, N (%) 158.0 (48.6) 56.0 (44.8) 50.0 (53.2) 52.0 (49.1)
Mode of infant feeding
Breast-fed, N (%) 105.0 (32.3) 60.0 (48.0) 25.0 (26.6) 20.0 (18.9) <0.0001
Milk-formula fed, N (%) 114.0 (35.1) 36.0 (28.8) 31.0 (33.0) 47.0 (44.3)
Soy-formula fed, N (%) 106.0 (32.6) 29.0 (23.2) 38.0 (40.4) 39.0 (36.8)
Gestational age, weeks, mean (SD) 39.3 (0.9) 39.5 (0.9) 39.1 (0.9) 39.2 (0.8) 0.0004
Birth weight (kg), mean (SD) 3.5 (0.4) 3.4 (0.3) 3.4 (0.3) 3.6 (0.4) 0.0038
Birth length (cm), mean (SD) 51.0 (2.2) 51.0 (2.1) 51.1 (2.4) 51.0 (2.1) 0.9466
Socioeconomic status, mean (SD) 39.6 (17.3) 37.8 (17.3) 41.6 (17.5) 39.9 (17.0) 0.2891

girls born to overweight and obese mothers had higher adjusted and 5 years and an increase in peripheral body fat between ages 4
BMI-for-age Z-scores as compared to girls born to normal-weight and 6 years in girls born to obese and overweight mothers compared
mothers (P < 0.05; Figure 1, Panel A). Similarly, adjusted BMI-for- to girls born to normal-weight mothers (Figure 2, Panel A and C).
age Z-scores overall time trajectories were higher in boys born to
obese mothers compared to boys born to normal-weight mothers In boys, body fat was very similar between groups during the first
over the course of the first 6 years of life (P 5 0.0004). Interestingly, year of life (Figure 1, Panel D). At age 2 years, there was a greater
the overall adjusted BMI-for-age Z-scores trajectories of boys born increase in body fat (4.8%) in boys born to obese mothers compared
to overweight mothers followed the trajectories of boys born to nor- to boys born to normal-weight and overweight mothers (0.9%), lead-
mal-weight mothers. Whereas the opposite was seen in girls; girls ing to a 4.3% difference in body fat between the groups. From ages
born to overweight mothers were more similar to the trajectories of 2 to 6 years, body fat decreased in all groups but to a lower extent
girls born to obese mothers. When analyzing each time point inde- in the boys born to obese mothers (23.3%) as compared to boys
pendently, the adjusted BMI-for-age Z-scores were higher in boys born to normal-weight mothers (24.5%) yielding a difference in
born to obese mothers at ages 3–6 years compared to boys born to body fat at ages 4–6 years (P < 0.05). Thus, the difference observed
overweight or normal-weight mothers (P < 0.05; Figure 1, Panel B). at age 6 years seemed to be a consequence of the increase in body
fat between ages 1 and 2 years and a slower decrease in body fat
While BMI-for-age Z-scores results offer a good overall trend for during the following 4 years of life. This difference in body fat
the effect of maternal obesity in both girls and boys, it does not pro- appears to be driven by an increase in peripheral fat between ages 2
vide a true measure of adiposity. Our data found the trajectories of and 6 years and an absence of decrease of trunk fat percentage after
adjusted body fat (%) were different from the BMI-for-age Z-scores age 3 years in boys born to obese mothers compared to boys born to
trajectories. In addition, the adjusted body fat (%) trajectories were normal-weight and overweight mothers (Figure 2, Panel B and D).
different between girls and boys. In girls, adjusted body fat (%) FFM trajectories and results for boys and girls closely reflect the
overall time trajectories over the course of the first 6 years of life ones observed for body fat (Figure 1, Panel E and F).
were not different across groups in girls (P 5 0.1068); whereas, they
were different in boys born to obese mothers compared to boys born There were no differences in BMC and BMD for overall time trajec-
to normal-weight mothers (P 5 0.0047). tories between the groups (P 50.3456 and P 5 0.4722, respectively,
for girls and P 5 0.1894 and P 5 0.3105, respectively for boys).
Girls born to obese mothers had higher body fat (%) at ages 0.75 and There were also no differences noted at each time point suggesting
1 year as compared to girls born to overweight and normal-weight that maternal obesity does not modulate offspring bone mineral
mothers (P < 0.05; Figure 1, Panel C). From ages 2 to 4 years, there accretion during the first 6 years of life (Figure 3, panel A–D).
were no differences in body fat percentages between the groups.
However, between ages 4 and 6 years, girls born to normal-weight
mothers decreased their body fat by 1.2% whereas girls born to obese
mothers increased their body fat by 1.52% creating a significant dif- Discussion
ference between the two groups by age 6 years. This difference This study investigated the relationship between maternal pre-
appears to be driven by an increase in trunk body fat between ages 4 pregnancy BMI and offspring body composition trajectories during

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Original Article Obesity
PEDIATRIC OBESITY

Figure 1 Body composition (mean 6 SE) of children born to normal-weight, overweight, and obese mothers from ages 3 months to 6
years adjusted for race, gestational age, birth weight, and mode of infant feeding. (A,B) BMI-for-age Z-scores for age for girls and boys,
respectively. (C,D) Body fat (%) for girls and boys, respectively. (E,F) Fat-free mass (%) for girls and boys, respectively. *Simes’ adjusted
P-value <0.05; #Simes’ adjusted P-value < 0.1.

infancy and childhood using DXA. Further, sex differences in these mothers have not been evaluated using precise body composition
trajectories were explored. Numerous previous studies have success- methods during the first 6 years of life. In addition, sex differences
fully validated and used the DXA technology to measure body fat, in response to maternal BMI during this period of life have not been
FFM, BMC, and BMD in infants and children (17-26). Previous reported.
studies have demonstrated higher BMI-for-age Z-scores and body
fat in infants and children born to obese mothers compared to As predicted, children born to obese mothers had greater body fat
infants and children born to normal-weight mothers (2,3,10,27-31). than children born to normal-weight mothers. These results are in
However, the longitudinal trajectories of body composition of line with previous studies demonstrating higher FM in children born
infants and children born to normal-weight, overweight, and obese to obese mothers compared to normal-weight mothers at age 5 years

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Obesity Maternal Obesity and Offspring Body Composition Andres et al.

Figure 2 Regional fat distribution (mean 6 SE) of children born to normal-weight, overweight, and obese mothers from ages 3 months to
6 years adjusted for race, gestational age, birth weight, and mode of infant feeding. (A,B) Trunk fat mass (kg) for girls and boys, respec-
tively. (C,D) Peripheral fat mass (kg) for girls and boys, respectively. *Simes’ adjusted P-value <0.05; #Simes’ adjusted P-value < 0.1.

(1.41 vs. 0.94 kg, respectively, at age 5 years) (32). They are also in cohort because body composition was tracked only until age 6 years.
line with numerous studies demonstrating higher neonatal FM in It is also possible that maternal obesity does not affect body compo-
infants born to obese mothers compared to infants born to normal- sition of girls during early childhood. These results would be in line
weight mothers (4,5,8,33). with various experimental models which have demonstrated a strong
maternal programming of offspring adiposity in male offspring but
A novel finding from our data demonstrated for the first time a sex- not in female offspring (34,35). Indeed, most experimental models,
ual dimorphism in offspring body composition up to age 6 years including ones used at our center, have focused on male offspring to
based on maternal BMI. Boys born to obese mothers displayed investigate the mechanisms underlying maternal programming of
higher BMI-for-age Z-scores and body fat and lower FFM starting at offspring adiposity (12).
age 2 years which was sustained until age 6 years when compared
to boys born to normal-weight or overweight mothers. These pat- There is a paucity of clinical studies investigating both maternal
terns appear to be driven by greater peripheral fat accretion between BMI and offspring sex with offspring outcomes. A recent study
ages 2 and 6 years and the absence of a decrease in trunk fat after demonstrated an interaction between fetal sex and maternal BMI on
age 3 years. These data are in line with previous findings demon- placental fatty acid uptake of oleic acid, suggesting that the placenta
strating a similar sexual dimorphism when infants were evaluated at from boys born to overweight and obese mothers have inadequate
birth, where positive adjusted associations were also found between acquisition of the unsaturated fatty acid oleic acid compared to boys
prepregnancy overweight and adiposity in boys (29). born to normal-weight mothers (36). While the study is unique in
identifying a similar offspring sex and maternal BMI interaction as
Conversely, body fat patterns in girls are not as clearly separated the one presented here, at present, data are lacking to investigate the
between maternal BMI groups. Girls born to obese mothers role of placental oleic acid uptake on offspring body composition
increased their body fat at ages 5 and 6 years, whereas girls born to later in life.
normal-weight mothers saw a decline in their body fat after age 3
years. However, these differences were not significant after adjusting Another interesting finding was the body fat trajectories of girls and
for multiple comparisons. It is possible that the maternal obesity boys born to overweight mothers. While girls born to overweight
effect in girls is delayed and the effect was not captured in this mothers followed the trajectories of girls born to obese mothers,

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Original Article Obesity
PEDIATRIC OBESITY

Figure 3 Bone mineral content and density (mean 6 SE) of children born to normal-weight, overweight, and obese mothers from ages 3
months to 6 years adjusted for race, gestational age, birth weight, and mode of infant feeding. (A,B) Bone mineral content (g) for girls
and boys, respectively. (C,D) Bone mineral density (g/cm2) for girls and boys, respectively.

boys born to overweight mothers followed the trajectories of boys offspring metabolism. In a cohort of 308 African-American mother-
born to normal-weight mothers. Such results are difficult to interpret infant pairs, methylation of 20 CpG sites were associated with
because of the paucity of literature reporting results from overweight maternal BMI, suggesting that maternal obesity may influence off-
mothers. Most clinical studies focus on obese mothers and all exper- spring metabolism via DNA methylation mechanisms (39).
imental models are clearly obese models resulting either from excess
calories or major macronutrient imbalances that are not reflective of There were no differences in BMC or BMD based on maternal BMI
what is observed in overweight mothers. If future studies replicate in this cohort, which is a unique finding as no other study has inves-
these findings and find the trend to continue into adulthood, inter- tigated the effect of maternal obesity on child’s skeletal health thus
ventions to prevent childhood obesity would need to differentially far. While experimental evidence suggests a negative effect of
target girls (born to mothers with BMI  25) and boys (only born to maternal obesity on offspring bone mass, the use of a high fat diet
mothers with BMI > 30). Indeed, the findings presented could guide to induce obesity in these models may have yielded different out-
obesity prevention and treatment strategies which would most likely comes as ones observed in clinical studies (40).
be effective. These strategies may need to target boys born to obese
mothers prior to age 2 years, whereas such strategies would less While this study has numerous strengths, including measured child-
likely be successful in girls. More importantly, these findings, if hood adiposity using validated and reliable methodology, longitudi-
replicated and sustained during later childhood and adulthood, may nal evaluation of adiposity from ages 3 months to age 6 years,
help identify individuals who may be at higher risk for other meta- adjustment for important covariates, and use of multiple compari-
bolic programming such as cardiometabolic diseases, diabetes, and sons correction to ensure the robustness of significant results, it also
metabolic syndromes. has limitations. First, maternal prepregnancy weight was self-
reported, which could lead to underreporting of maternal BMI in
The mechanisms underlying maternal programming of offspring adi- this cohort. However, the incidence of overweight (BMI  25, 62%)
posity are still under debate. Several studies have demonstrated that and obesity (BMI  35, 33%) in this cohort was similar to the rate
lipotoxicity can alter fetal development pathways via high oxidative of obesity reported in the state of Arkansas (34.6%, BRFSS, CDC,
stress and inflammation in the mother-placenta-fetus unit (37,38). 2013) and higher than overweight (48.5%) and obesity (23.9%) inci-
Yet, it is unclear how lipotoxicity and inflammation influence the dence reported in women of reproductive age in Arkansas (PRAMS,

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Obesity Maternal Obesity and Offspring Body Composition Andres et al.

CDC, 2011), suggesting that the self-reported weights are close esti- 14. Grummer-Strawn LM, Reinold C, Krebs NF. Use of World Health Organization and
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1258 Obesity | VOLUME 23 | NUMBER 6 | JUNE 2015 www.obesityjournal.org