Higher fat mass and fat mass accretion during the first six months of life in exclusively breastfed infants
Higher fat mass and fat mass accretion during the first six months of life in exclusively breastfed infants
Ameyalli M Rodríguez-Cano 0
Jennifer Mier-Cabrera 0
Ana L Allegre-Dávalos 0
Cinthya Muñoz-Manrique 0
Otilia Perichart-Perera 0
0 Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes” , Ciudad de México , Mexico
BACKGROUND: Early nutrition influences infant growth and body composition, which may play a role in the infant's metabolic programming. Breastfed infants appear to have higher fat mass than formula-fed infants, but most comparisons have been crosssectional, and evidence is scarce. The aim of this study was to describe fat mass and fat mass accretion during the first six months of life and evaluate differences by type of feeding (OMS). METHODS: Prospective cohort of healthy pregnant women and their infants (Mexico City, 2009-2014). At 1 (T1), 3 (T2) and 6 (T3) months of age, fat mass (FM) (PEAPOD) and type of feeding (feeding questionnaire) were evaluated. RESULTS: We included 109 healthy infants (mean ± SD age: 39 ± 1.1 weeks; birthweight: 2959 ± 294 g). Exclusive/predominant breastfed (EBF) infants had higher FM at T2 and T3 compared with non-EBF (%FM T3: 29.7 ± 5.9% vs 24.7 ± 5.6%, respectively) (p < 0.05). All infants increased their FM throughout time (p < 0.001). EBF infants showed a significant higher FM accretion (β: 3.61; 95% CI: 1.57-5.66, p < 0.01); the difference was maintained after controlling for confounding variables. CONCLUSIONS: Exclusive/predominant breastfeeding promotes higher accretion of FM during the first six months of life which could have an important effect in the programming of health outcomes later in life.
Although global rates of childhood obesity have plateaued, its
prevalence remains high, occurring as one of the most important
public health problems worldwide.1 Intrauterine and early postnatal
nutrition have become relevant in the prevention of obesity and
other chronic diseases in childhood and adulthood.2 Adiposity at
birth and during the first months of life is influenced by maternal
weight status and the intrauterine environment.3,4 Body
composition, more than weight-based indices (body mass index,
weight-forlength), should be the basis for diagnosing obesity in different age
groups. Few studies have assessed body composition in this stage
of life.5–8 Postnatal nutrition is associated with infant growth and
body composition and may play a significant role in metabolic and
nutrition programming of the infant.9,10
Exclusive breastfeeding is the optimal nutrition
recommendation for all infants until 6 months of age. Breastmilk contains all the
essential nutrients the baby needs, and provides many bioactive
substances and microorganisms with specific properties, that
exert different functions in the infant.11
Some studies have measured fat mass (FM) and fat-free mass
(FFM) at birth and during the first months of life with an air
displacement plethysmography equipment,7,12,13 a validated
method to measure body composition in this age group.14
Evidence has shown that breastfed infants appear to have
higher FM at 3, 4 and/or 6 months of age. Most studies have
shown differences in each time frame, using cross-sectional
analysis.5–8 One recent study showed that duration of EBF was
independently associated with FM percentage at 6 months;
breastfeeding (BF) was only associated with subcutaneous
fat but not with visceral fat. Higher FM accretion during the
first 3 months of age has been associated also with higher FM at
6 months.8 In one longitudinal study, a higher increase in FM (as
a proportion of body weight) was observed from 3 to 4.5 months
of age in exclusive/predominant breastfed infants.7 In the
beginning of life, higher FM could be part of an optimal
phenotype influenced by BF, that may be related to protection
in later obesity.15,16
The aim of this study was to describe FM and FM accretion
during the first six months of life and to evaluate FM differences
by type of breastfeeding and other maternal and infant
This is a secondary analysis derived from a cohort study of healthy
pregnant women conducted at the National Institute of
Perinatology in Mexico City (INPer; 2009–2014).
Subjects’ recruitment and selection
Singleton pregnant women (<14 weeks) who did not have
comorbidities (diabetes mellitus, autoimmune diseases, or other
pathologies) and did not use medication (metformin, prednisone,
etc.) during pregnancy that could affect metabolism or body
composition were selected consecutively by convenience. Until
resolution of pregnancy, women were followed-up monthly. All
newborns were followed-up approximately at 1, 3, and 6 months
For this analysis, we included healthy newborns. We did not
include newborns from adverse maternal outcomes (gestational
diabetes or preeclampsia), with postnatal and/or congenital
diseases, preterm birth (<37 weeks), low birthweight (<2500 g),
macrosomia (>4000 g), lost to follow-up or that had incomplete
feeding information at 6 months.
Ethical approval and consent to participate
This study was approved by the National Institute of
Perinatology’s Institutional Review Board and Ethics Committee (reference
number: 212250-49511). All procedures were conducted
according to the Declaration of Helsinki. We obtained signed informed
consent from all participants; in adolescents (<19 years old) both
parents and participants gave consent.
Maternal data collection
Pregestational maternal weight was self-reported. Height was
measured using a wall-mounted wireless digital stadiometer SECA
242 (SECA, Hamburg, Germany). Pregestational BMI (preBMI) was
computed and women were classified as low weight, normal
weight, overweight, or obesity according to the World Health
Organization (WHO) criteria.17 Taking into consideration women’s
preBMI, gestational weight gain (GWG) in the third trimester (last
visit recorded) was classified as low, adequate, or high according
to the Institute of Medicine (IOM) recommendations.18 Parity was
classified as either nulliparous or primiparous/multiparous.
Women were classified in the following categories regarding level
of education: basic (elementary and middle school), middle (high
school and/or technical level) or high (bachelor and postgraduate).
Infant data collection, anthropometry, and body composition
Gestational age (weeks) was estimated by ultrasound during the
first trimester. In cases where no ultrasound was available,
gestational age was calculated according to woman’s last
Infants were measured at birth (first 72 h) and the follow-up
consisted in three visits around 1 (T1), 3 (T2) and 6 (T3) months of
age. While infants were without clothes, weight, and length were
measured by an experienced and trained nutritionist using a
standardize technique proposed by Lohman et al.19 Weight at
birth was recorded using a pediatric scale 1582 Baby/Mommy
Scale (Tanita, Tokyo, Japan) whereas for subsequent visits, the
PEAPOD Infant Body Composition System digital scale (COSMED
USA Inc, Concord, California) was used. Recumbent length was
measured (by duplicate and the average computed) using an
infantometer SECA 207 (SECA, Hamburg, Germany).
Nutritional status was assessed using the WHO reference data20
for BMI-for-age (BMI/A). Sex-specific z-scores were calculated using
the Anthro software v. 3.2.2 (WHO, Geneva, Switzerland). Risk of
overweight, overweight, and obesity was defined by means of
BMI/A (>1, >2 and >3 z-score, respectively), while a z-score < −2
was considered as wasted/severely wasted.
FM (percentage—%FM and kilograms—kgFM) was measured at
T1, T2, and T3 using the PEAPOD, an air displacement
plethysmography system. Before starting the measurements, the
PEAPOD was calibrated following the manufacturer’s protocol.
First, the infant was naked and was weighed using the PEAPOD
scale. Then, to minimize air trapped in the hair, a cap was put on
his/her head. Thereafter, the infant was placed in the PEAPOD’s
test chamber tray to begin the measurement of body
composition.14,21 The whole process took about 5 min. Finally, based on
Fomon’s density values, the PEAPOD’s software calculated the
infant’s body composition. FM index (FMI) was calculated dividing
kgFM/length2 to account for body size natural variations.22
Feeding practices questionnaire
In every visit, except at birth, mothers were asked about their
infant feeding practices. The main purpose was to evaluate
whether infants were breastfed, formula-fed or both, as well as if
they had ever been fed any other food/liquid (e.g. water, juices,
infusions, other types of milk, semi-solid or solid food) during the
first six months of life. Duration of BF was recorded in months.
Taking into account WHO definition of breastfeeding,23 infants
were classified as exclusive/predominant breastfed (EBF), when
lactation lasted 6 months, or non-exclusive/predominant
breastfed (nEBF), which included mixed feeding and formula
feeding. Complementary feeding (CF) was recorded as the age (in
months) when an infant received solid/semi-solid food different
from breastmilk, infant formula, water or infusions for the first
time. CF was classified as “early” if it started <4 months of age.
Descriptive statistics and frequencies were performed for all
variables. Mean differences were analyzed using t test/U
Mann–Whitney or ANOVA/Kruskal–Wallis tests. Chi-square test
was used to analyze differences between infant and maternal
categories. Pearson’s and Spearman’s correlations were used to
evaluate bivariate associations.
Generalized linear mixed models (GLMM) were used to evaluate
the association between EBF and FM (%, kg, FMI) during the first
six months of life. According to the literature and based on our
exploratory analysis, three GLMM were performed. The first GLMM
did not include confounding variables; the second, included
variables that were associated with FM in the exploratory analysis
(parity, level of education, and category of GWG). The third model
included the same variables of the second model (parity, level of
education, and category of GWG) and independent variables that
have been reported to influence FM (gender, gestational age at
birth, BMI/A at birth, start of CF).
A p-value < 0.05 was considered statistically significant. Statistical
analyses were performed with SPSS Statistics Software v.24 (IBM
Corp, Armonk, New York). GLMM were performed with Stata
statistical software package v.12 (StataCorp, College Station, Texas).
A total of 263 babies from the cohort were born at INPer facilities.
One hundred and fifty-four newborns were not included in this
analysis because their mothers developed preeclampsia (n = 5) or
gestational diabetes (n = 6), they were born prematurely (n = 30),
had low birthweight (n = 13), were lost to follow-up (n = 67) or
n = 263 infants were born at
n = 109 infants were
included in the analysis
n = 154 infants were not included
because their mothers developed
preeclampsia/diabetes, they were
born prematurely, had low
birthweight, were lost to follow-up,
had incomplete feeding practices
information at 6 months
n = 75 infants with all (T1, T2,
T3) body composition
n = 85 infants with body
n = 101 infants with body
n = 92 infants with body
Data is showed either as Mean ± SD; Median (25° percentile–75° percentile); n (percentage)
U Mann–Whitney *p = 0.023, All (EBF vs nEBF); §p = 0.033, Boys (EBF vs nEBF)
EBF exclusive/predominant breastfeeding, nEBF non-exclusive/predominant breastfeeding, PreBMI pregestational BMI, GWG gestational weight gain, BMI/A
Body-mass-index/age, CF complementary feeding
had incomplete feeding practices information available at
6 months (n = 33). Finally, data from 109 infants were analyzed
in this study (Fig. 1).
Mothers’ mean age was 27.1 ± 8.9 years; 23% (n = 25) of them
were adolescents and 58.7% (n = 64) were nulliparous. Their mean
preBMI was 25.3 ± 5.4 kg/m2 and the prevalence of pregestational
overweight and obesity was 27.5% (n = 30) and 15.6% (n = 17),
respectively (Table 1). GWG was low in 30.9% (n = 30) and
excessive in 47.4% (n = 46) of women. Most of them were
classified in the low or middle category regarding level of
Mean duration of BF was 5.0 ± 1.9 months. Throughout their first
six months of life, only 25.7% (n = 28) of the infants were EBF.
Infants from women with obesity did not show a lower EBF
exposure or duration of BF; there was no linear association
between preBMI and duration of BF. Duration of BF and EBF
exposure were not different by GWG categories.
Boys and girls had similar EBF exposure and duration of BF.
Infants from women classified as nulliparous or in the high level of
education category did not show a higher EBF exposure or BF
duration. Infants started CF at a mean age of 4.1 ± 1.3 months and
early CF was observed in 25.7% (n = 28) of them. nEBF infants
started CF earlier (p = 0.023) (Table 1).
Anthropometry and body composition
Mean gestational age at birth was 39.0 ± 1.1 weeks. Newborns
weighed 2959 ± 294 g and were 47.2 ± 1.8 cm long. Median age
(min–max) at T1, T2, and T3 was 4.9 (3.6–8.7), 13.4 (11–17.4) and
26.4 (21.3–38.1) weeks, respectively. Boys had a higher weight
throughout the study (except at birth) and higher length in all
visits (except at T1) (p < 0.05). Most of them (93.8%, n = 91) had a
normal BMI/A at birth. Although no infants were classified with
Data is showed either as Mean ± SD. Median (25° percentile–75° percentile)
t test: EBF vs nEBF, *p < 0.05, **p < 0.01; EBF (girls vs boys), ‡p = 0.0034; nEBF (girls vs boys), †p < 0.05; girls (EBF vs nEBF), §p < 0.05, §§p < 0.01, §§§p < 0.001
EBF exclusive/predominant breastfeeding, nEBF non-exclusive/predominant breastfeeding, T1/T2/T3 Median (Min–Max) weeks time frame at each assessment,
kgFM kilograms of fat mass, %FM fat mass percentage, FMI fat mass index, BMI body-mass-index
obesity during the first six months of life, overweight reached its
highest prevalence at T3 (5.0%, n = 5).
Table 2 shows the increase of FM throughout time (T1, T2, and
T3) according to feeding practices. Respectively, boys’ and girls’
mean %FM were as follows: T1: 16.3 ± 4.9%, 17.3 ± 5.4%; T2: 24.9 ±
5.1%, 24.4 ± 5.3% and T3: 25.5 ± 5.5%, 25.9 ± 6.3%.
FM was not different according to preBMI, gender, BMI/A at
birth, or gestational age in any visit. At T3, FMI was higher in
babies from mothers in the basic level of education category in
comparison to those in the middle category (p = 0.029). At T2 and
T3, those infants from mothers with low GWG showed lower FM
when compared with those with adequate (T2: %FM p = 0.001;
kgFM p = 0.002; FMI p = 0.001; T3: %FM p = 0.008; kgFM p =
0.012; FMI p = 0.003) or excessive GWG (T2: %FM p = 0.003, kgFM
p = 0.001; FMI p = 0.003; T3: kgFM p = 0.042). A higher FM (%FM
p = 0.049; kgFM p = 0.027; FMI p = 0.036) at T2 was observed in
infants born from primiparous/multiparous mothers.
EBF infants had higher FM at T2 (%FM, p = 0.008; kgFM p =
0.027; FMI, p = 0.021) and T3 (%FM, p < 0.001; kgFM, p = 0.004;
FMI, p = 0.001) compared with nEBF ones (Table 2). Positive
correlations were found between duration of BF and FM (kgFM:
r = 0.234, p = 0.018; FMI: r = 0.200, p = 0.045) at T2. Infants with
early CF did not show differences in FM (%FM, kgFM, FMI). FM did
not correlate with starting of CF.
General linear mixed models: type of breastfeeding and FM
All infants increased their FM (%, kg, and FMI) significantly
throughout time (p < 0.001; a*) (Fig. 2). The greatest increase in
FM was observed from T1 to T2 (kg [β = 0.72 (95% CI 0.63, 0.82)]; %
[β = 7.42 (95% CI 6.35, 8.48)]. EBF infants showed a significant higher
accretion in FM (%, kg, and FMI) when compared with those nEBF (p
< 0.01; b*) (Fig. 2). This difference was maintained after controlling
for maternal and infant variables in the three models (p < 0.01).
None of the confounding variables or co-variables showed a
significant effect on FM, except for GWG in the second model;
infants from women with excessive GWG, compared with those with
low GWG, had a higher increase of FM (kg [β = 0.25 (95% CI 0.06,
0.45) p = 0.008]; % [β = 2.79 (95% CI 0.53, 5.05) p = 0.015]) and FMI
[β = 0.62 (95% CI 0.11, 1.12) p = 0.016] (Table 3).
This study presents evidence about the influence of BF on body
composition in healthy term infants during the first six months of
No significant association was observed with other variables besides EBF and Time in the 3 models and GWG only in Model 2
kgFM kilograms of fat mass; %FM fat mass percentage; FMI Fat mass index; EBF exclusive/predominant breastfeeding; T2/T3 Time frame
aCrude GLMM (type of feedinge -when compared with nEBF- and T2/T3f -when compared with T1-)
bModel 1 + adjustment by parity, maternal level of education and category of gestational weight gain (GWG) (when compared to low GWG)
cModel 2 + adjustment by gestational age at birth, gender, BMI/A at birth (z-score), start of complementary feeding (month)
life, where FM accretion was higher in EBF infants. We also
observed higher FM from week 11 to week 38.1 of age in EBF
Our results are in line with previously reported findings where
differences in FM have been observed, either at a specific time or
in regard to its increase throughout time. In our analysis, we found
differences in both scenarios. Butte et al.5 found a higher FM (kg
and %) at 3 and 6 months in EBF infants vs formula-fed (FF) ones,
although FM was evaluated with different methodologies (TOBEC,
multicomponent body composition model). Carberry et al.7 is the
only previous longitudinal study that found a higher increase in
FM as a proportion of weight gain in EBF infants, but the time
frame studied was very short (from 3 to 4.5 months). Our analysis
showed FM accretion (kg, %, FMI) over an 8-month time frame.
Some other authors have found discrepancies. In a descriptive
study by Gianni et al.,6 no differences in FM according to type of
feeding were observed, but a higher FFM was reported in FF
infants. Probably, these different outcomes were as a result of
their hypothesis focused on finding differences in FFM (the power
proposed was not enough to find differences in FM) and also
women with a preBMI > 25 were excluded. Inconsistent findings in
the literature could be as a result of methodologic differences,
such as sample size, inclusion/exclusion criteria, time frame, and
methods for anthropometric/body composition assessment,
statistical analysis, etc.
Breij et al.12 assessed %FM and visceral fat at 1, 3 and 6 months.
Duration of EBF was positively associated with %FM (PEAPOD) at
6 months, but not with visceral fat (ultrasound). This finding is of
particular interest because location of body fat storages
determines metabolic risk.24
Our results showed that EBF appears to increase FM accretion
during the first six months of life. This may be a desirable outcome
that could be supporting other aspects of healthy growth (e.g.
ensure infant’s normal brain development).25 Leptin and
adiponectin, present in human milk, have important roles on energy
homeostasis, satiety regulation, immune system, glycemic control,
among other functions that are related to growth and changes in
body composition.26,27 Brunner et al.26 found that milk leptin is
inversely associated with FFM, and adiponectin could be directly
associated to infant FM (based on skinfolds) at 4 months of age. In
addition, Breij et al.12 found a positive correlation between infant
serum leptin and %FM at 3 months of age. There is a strong need
to understand how these substances modulate growth, body
composition, and long-term health.
As previously reported, FM has its higher increase during the
first 4 months of life,9,28 and thereafter accretion velocity appears
to decrease. Our model showed this rapid increase from week 3.6
to week 17.4 of age, and an attenuation from week 17.4 to week
21.3 of age. We hypothesize that in EBF infants, FM could continue
with this slow accretion and result in a lower FM (and lower
obesity risk), noticeable by 12 months of age, when compared
with those infants with previous formula exposure. Interestingly,
Gale et al. found that higher FM at 3 and 6 months tends to invert
at 12 months of age, showing higher FM in FF infants when
compared with those EBF.29 Studies in older children have shown
that greater duration of BF was associated with a lower FM at 430
and at 9–10 years of age.31 Furthermore, as opposite to EBF
infants, those exposed to formula have higher protein intake5 and
may be introduced to solid foods earlier;31 both practices have
been related to higher adiposity and associated disorders.32,33 This
could reflect the long-term protective effect of breastmilk,
showing the lower risk of obesity in childhood.16 This panorama
emphasizes the importance of studying changes and distribution
of FM since birth, as well as the need of FM reference values
in order to better assess nutrition status and metabolic risks in
Besides feeding type, there are other factors known to
influence FM in infants. Our results showed FM differences
according to category of GWG. GWG is correlated with preBMI,
and both have been related to adiposity in the newborn3,34 and
with a higher long-term obesity risk.35,36 However, the
association between excessive GWG and FM disappeared when other
infant variables were considered, suggesting an intermediary
role between fetal programming and the extra uterine
environment. Extremes of BMI/A at birth may have an influence on
susceptibility to later obesity. Our results did not show any
influence of BMI/A at birth on FM during the first six months of
life. This could be related to the fact that most infants had
normal weight, and there were no low weight or obese infants.
In addition, early CF (<4 months) could increase the risk of
childhood overweight (classified by BMI), but data is
inconclusive.32 We did not find that FM was influenced by an early
start of CF.
There is also conflicting evidence about differences in FM by
gender. Although there is some data that females have higher FM
compared with males, some authors had not found differences at
birth or very early in life.7,37 Our reported %FM is very similar to
what has been previously reported.38,39
Association between BF and obesity may be affected by
residual confounding, especially as a result of mothers’
socioeconomic status and level of education. Higher education and
income has been associated with higher frequency and duration
of BF.5,16 We found that a lower level of education was associated
with higher FMI at T3; however, this effect was not significant in
the GLMM. Durmusx et al.40 found that when associating BF and
FM, maternal level of education was the strongest confounder,
leading to a non-significant association. Others have found that
the duration of BF has a significant effect in FM, even after
adjusting for maternal characteristics.30,31
This study has some strengths. This is one of the few studies
that have assessed BF and FM prospectively during the first six
months of life. FM was measured using a validated method in
infants. Changes in FM are rapid and nonlinear in the first months
of life;37 therefore, longitudinal studies are needed during
this time frame. One of the most common critiques of BF studies
is their lack of control for confounders (maternal and infant
variables, ethnicity, socioeconomic status, etc.).27 We included
variables that are known to influence adiposity (parity, level of
education, BMI/A at birth, gender, gestational age, and CF),
although neither showed statistical significance. Finally, our
sample comes from a low-/middle-income population from a
developing country where evidence is scarce, as most of the
studies have been reported from high-income countries.16
This analysis presents some limitations. Weeks of FM
measurements were not the same for all infants. Although the variability in
the time frame within the three FM measurement periods was
high, when we adjusted the model including “time” as a
continuous variable (weeks), the effect of EBF on FM was
maintained (data not shown). Feeding type classification is
complex as it relies on the mother’s report and is subject to
recall bias. Women in our study are not representative of all women
because they may have high-risk factors as they were selected
from a tertiary referral hospital.
Exclusive/predominant breastfeeding promotes higher
accretion of fat mass during the first six months of life which could have
an important effect in the programming of health outcomes later
in life. Accretion of fat mass is higher in the first 3 months of life,
representing a critical period of growth. More longitudinal studies
are needed to explain the effect of EBF on fat mass at early age
and the implication of this on nutrition status and later
The authors would like to thank all the undergraduate students, as well as PhD. Felipe
Vadillo Ortega, PhD. Salvador Espino y Sosa and MsSc. Margie Balas Nakash for their
This research study did not receive a specific grant from any funding agency,
commercial or not-for-profit sectors.
O.P-P. designed the study and formulated the research question. A.M.R-C. and A.A-D.
conducted the data collection examination. A.M.R-C. and J.M-C. analyzed the data. A.
M.R-C. wrote the first draft of the manuscript. O.P-P. and C.M-M supervised the quality
standards of the statistical analyses. A.M.R-C., J.M-C., A.A-D., C.M-M. and O.P-P.
contributed to the interpretation and discussion of the results and commented on
the draft. All authors have read and approved the final manuscript.
Competing interests: A.M.R-C. and O.P-P. are speakers of the Nestlé Nutrition
Institute in Mexico. There is no conflict of interest of any kind in this manuscript
regarding this institution. The rest of the authors declare that they have no
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