Matern Child Health J (2014) 18:1023–1030
DOI 10.1007/s10995-013-1331-9
Satiety Responsiveness and the Relationship Between
Breastfeeding and Weight Status of Toddlers
of Overweight and Obese Women
Amber Hathcock • Katrina Krause •
Anthony J. Viera • Bernard F. Fuemmeler
Cheryl Lovelady • Truls Østbye
•
Published online: 8 August 2013
Ó Springer Science+Business Media New York 2013
Abstract Numerous studies indicate an association
between breastfeeding and decreased toddler adiposity. The
mechanism behind this association is still unknown. One
possibility is that children who are breastfed may have
increased responsiveness to internal satiety cues. This study
assessed the effect of satiety responsiveness on the association between breastfeeding and weight status among toddlers.
We conducted a secondary analysis of data from 428 toddlers
aged 2 years. Mothers’ body mass index (BMI) and children’s BMI z score were calculated from measured height and
weight. Mothers completed a detailed breastfeeding survey
and the satiety responsiveness subscale of the Child Eating
Behaviour Questionnaire. Multiple linear regression and
logistic regression were used to determine if satiety responsiveness mediated the effect of breastfeeding on BMI z score
or overweight/obesity (BMI C 85th percentile). Establishment of breastfeeding was associated with decreased BMI z
A. Hathcock (&)
Department of Pediatrics, Duke University Medical Center,
PO Box 3099, Durham, NC 27710, USA
e-mail: [email protected]; [email protected]
A. Hathcock A. J. Viera
Gillings School of Public and Global Health, University of North
Carolina at Chapel Hill, Chapel Hill, NC, USA
K. Krause B. F. Fuemmeler T. Østbye
Department of Community and Family Medicine,
Duke University Medical Center, Durham, NC, USA
A. J. Viera
Department of Family Medicine, University of North Carolina
at Chapel Hill, Chapel Hill, NC, USA
C. Lovelady
Department of Nutrition, University of North Carolina
at Greensboro, Greensboro, NC, USA
score (0.40 vs. 0.60; p = 0.04), and increased breastfeeding
intensity was associated with lower odds of overweight/
obesity (OR 0.97, p = 0.04). Satiety responsiveness was not
associated with either breastfeeding measures, suggesting it
does not play a meditational role in the relationship between
breastfeeding and toddler weight status. Furthermore, a
relationship between satiety responsiveness and obesity does
not exist after controlling for well-known confounders. This
study did not find a mediation effect of satiety responsiveness
on the association between breastfeeding and weight status in
toddlers. More research is needed to characterize satiety
responsiveness and its influence on the relationship between
breastfeeding and childhood obesity.
Keywords Breastfeeding Satiety response Body mass index z score Obesity Toddlers
Abbreviations
BMI
Body mass index
CEBQ Child Eating Behaviour Questionnaire
SES
Socioeconomic status
Introduction
Childhood obesity is an increasingly important public
health issue; in 2010, an estimated 32 % of children in
the United States were overweight or obese [1]. Several
studies have found that establishment and greater duration
of breastfeeding are associated with decreased adiposity
[2–9], and public health strategies for the prevention of
childhood obesity in the United States include the promotion of breastfeeding [10]. However, little is known about
the mechanisms by which breastfeeding may decrease
childhood obesity.
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1024
Breastfeeding and childhood obesity rates are affected
by similar maternal social factors, including education,
race, and weight status, though the relationships can vary
across populations. Higher parental education is associated
with lower rates of obesity and increased establishment and
duration of breastfeeding [6, 11]. Among African Americans and Mexican Americans, there is no association
between family socioeconomic status (SES) and overweight, while higher SES is related to higher prevalence of
overweight in white Americans, according to NHANES III
data [6]. Racial and ethnic differences in breastfeeding
establishment rates also exist. Non-white Hispanics are
more likely to establish breastfeeding, while non-Hispanic
blacks have the lowest rates of breastfeeding establishment
[11]. Despite these associations, maternal weight and body
mass index (BMI) are the greatest predictors of child BMI,
suggesting that child adiposity may be related to genetics
or environmental factors, such as learned eating behaviors
[12].
Social factors only partially explain the link between
breastfeeding and childhood obesity. One physiologic factor
that may influence the relationship is satiety responsiveness,
in that breastfed children may have a stronger response to
internal satiety cues [12, 13]. Increased breastfeeding is
associated with less parental control over feeding. Less
parental control in feeding practices is associated with
greater satiety responsiveness and decreased adiposity
among children [12, 14–17]. Breastfeeding itself may also be
associated with increased satiety responsiveness: breastfed
infants may be able to maintain a natural response to internal
appetite cues due to greater control over intake while their
mothers adopt a less controlling feeding style [12].
We are unaware of literature exploring the influence of
satiety responsiveness on the association between breastfeeding and toddler adiposity. In this study, we hypothesize
that the interplay between the variables is as follows:
increased breastfeeding is associated with (1) weight status
(lower BMI z score and likelihood of being overweight/
obese), and (2) a more favorable satiety responsiveness score
at age 2 years; (3) a higher satiety score is associated with
more favorable weight status 2 years of age; and (4) satiety
score is a mediator of the relationship between breastfeeding
and being overweight (Fig. 1).
Matern Child Health J (2014) 18:1023–1030
Fig. 1 Model of interplay between satiety responsiveness and toddler
adiposity. Breastfeeding is associated with increased satiety responsiveness and decreased toddler obesity (black arrows 1 and 2). Satiety
response is itself associated with decreased toddler obesity (black
arrow 3) and may also mediate the relationship between breastfeeding
and toddler obesity
University of North Carolina at Greensboro. Study subjects
were children who completed adiposity assessments at age
24–35 months and whose mothers reported infant and toddler eating behaviors in conjunction with the above mentioned studies; all other children were excluded from the
study. Primary outcomes were BMI percentile, BMI z score,
and scores on the Child Eating Behaviour Questionnaire
satiety subscale [14]. Institutional Review Board approval
was obtained at both study sites.
Data Source and Participants
The source population comprised 850 children who participated in AMP and KAN-DO. Of the 450 participants in
AMP, 280 completed both the 12-month and 2-year surveys
and are included in this analysis. Of the 400 participants in
KAN-DO, 148 children were aged 24–35 months at baseline
and are included in the analysis. Participants were excluded
if they had not completed the 12-month and 2-year survey in
AMP or if they were not aged 24–35 months at the time of
their participation in the KAN-DO study. The final analysis
sample consisted of a total of 428 subjects. Data on study
sample characteristics was collected through surveys conducted in conjunction with the AMP and KAN-DO trials.
Methods
Active Mothers Postpartum (AMP)
Overall Design
We conducted a secondary analysis of data from Active
Mothers Postpartum (AMP) and Kids and Adults NowDefeat Obesity (KAN-DO), two randomized control trials
performed at Duke University Medical Center and
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AMP was a randomized control trial to evaluate the effect
of an intervention to promote physical activity and healthy
diet for weight loss among postpartum women with a
BMI [ 25. Participants were excluded if they were under
the age of 18 years, were unable to walk one mile
Matern Child Health J (2014) 18:1023–1030
unassisted, or did not speak English. Women were randomized to either minimal care or the AMP intervention,
which included telephone counseling and group classes
intended to educate and motivate mothers regarding healthy diet and increased physical activity. Women in the
study completed a survey at baseline and an annual followup survey. The study did not include interventions in infant
or toddler health. For this study, we used data collected
during the 12-month survey, in which mothers reported
infant feeding practices, and toddler adiposity and satiety
responsiveness measured at 24 month follow-up [18, 19].
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dichotomized as ‘‘high’’ (greater than 3) and ‘‘low’’ (less
than or equal to 3).
Breastfeeding Variables
KAN-DO was a randomized behavioral intervention trial
designed to promote healthy eating and increased physical
activity and to prevent or reduce overweight for dyads of
overweight and obese postpartum mothers and their toddlers, aged 2–5 years. KAN-DO incorporates assessments
and intervention components similar to those in AMP. We
used the data obtained from the baseline survey and adiposity assessment; only data from children who were
2 years old at the time of initial assessment are included in
this study.
Mothers completed a survey in which they reported infant
feeding for each month of the first year of life. Mothers were
asked ‘‘For each month, please tell me if you only breastfed,
combined breastfeeding and formula feeding or only formula
fed’’. We did not ask if the milk was fed from a bottle or the
breast. We included 2 different breastfeeding dimensions:
establishment of breastfeeding and intensity score. Breastfeeding establishment was defined as self-report of full
breastfeeding or mixed feeding (breastfeeding and formula
feeding) at age 1 month; no participants in the study started
breastfeeding after 1 month. Intensity score was determined
based on the duration and exclusivity of breastfeeding [22].
Full breastfeeding was awarded 2 points for each month
reported; combination of breast and formula feeding was
assigned 1 point, and formula feeding only was assigned 0
points. Total intensity score was the sum of these points and
ranged from 0 (formula feeding only for 12 months) to 24
(full breastfeeding for 12 months). Breastfeeding recall has
been shown to be valid up to 3 years postpartum [23].
Variables
Analysis
Body Mass Index (BMI) Outcomes
The main aim of the study was to assess mediation effects of
satiety responsiveness on breastfeeding and BMI outcomes.
To accomplish this, we used the methodology outlined by
Barron and Kenny [24]. First, we assessed relationships
between the dimensions of breastfeeding and the main outcomes of scores on the CEBQ satiety subscale and the BMI
measures. We then assessed the relationship between satiety
responsiveness scores and the BMI measures. In these
bivariate analyses, we tested for significance using Chi
square, t test, or ANOVA as appropriate. Multivariate linear
and logistic regressions were then used to assess whether the
relationship between breastfeeding and BMI outcomes
changed after adjusting for satiety responsiveness. Results
from the multivariate analysis are reported as mean BMI z
score and odds ratios of being overweight or obese. We
considered a p value B0.05 to be statistically significant. We
used SAS (SAS, Cary, NC) and Stata 11.0 (StataCorp, College Station, TX) for all analyses.
Kids and Adults Now—Defeat Obesity (KAN-DO)
Children were measured in light clothing and without
shoes. We used BMI z score to assess toddler adiposity. To
determine the BMI z score, BMI was calculated based on
measured weight and height and adjusted for age and
gender [20]. Overweight/obesity is defined as BMI C 85th
percentile [21].
Satiety Responsiveness
To assess satiety responsiveness, we used parent responses
to questions derived from the original 5-question Satiety
Response scale of the Child Eating Behaviour Questionnaire (CEBQ) [14]. Parents rated how often their children
displayed the following eating behaviors: ‘‘leaves food on
his/her plate,’’ ‘‘gets full before his/her meal is finished,’’
‘‘gets full up easily,’’ ‘‘cannot eat a meal if she/he has had a
snack just before,’’ and ‘‘has a big appetite.’’ Individual
item scores range from 1 (never) to 5 (always), with the
exception of ‘‘my child has a big appetite,’’ which was
assigned a score of 1 (always) to 5 (never). The total satiety
responsiveness score was calculated as the mean of the
individual ratings [14]. Higher scores denote increased
satiety responsiveness; because they were not normally
distributed and for ease of reporting, responses were
Results
Characteristics of Sample
The mean BMI z score for children included in the pooled
dataset was 0.45 (SD 0.97); roughly, a quarter of the
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Matern Child Health J (2014) 18:1023–1030
children were classified as overweight/obese (BMI C 85th
percentile) (Table 1). The characteristics for children from
each of the two studies differed, though not significantly.
Compared to the children from KANDO, the mean BMI z
score was higher for children from AMP (0.50 vs. 0.35)
and a greater proportion of the AMP children were overweight/obese (27.3 vs. 19.6 %).
Average maternal age was 31 years, and mean maternal
BMI was 33 kg/m2 (Table 1). Most of the women were
Table 1 Key characteristics of the children and mothers in the study
population
Variable
N (%)
AMP
KANDO
280 (65.4 %)
148 (34.6 %)
BMI z score (mean [SD])
0.45 (0.97)
BMI C 85th percentile (%)
24.8 %
Breastfeeding establishment (frequency, %)
Yes
329 (76.9 %)
No
99 (23.1 %)
Breastfeeding Intensity Score (mean [SD])
9.5 (8.77)
Satiety Score (mean [SD])
3.06 (0.62)
Maternal age (years; mean [SD])
31.1 (5.4)
Maternal BMI (kg/m2; mean [SD])
32.8 (6.2)
Parity
2.0 (0.9)
Marital status
Single
69 (15.3 %)
Living with partner or married
372 (82.3 %)
S/D/W
11 (2.4 %)
Race
Non-African American
African American
277 (61.2 %)
175 (38.7 %)
Ethnicity
married, Caucasian, and non-Hispanic; a little more than
half had at least a college education, worked full-time, and
had an income of at least $60,000. Compared to women
from the KAN-DO, more of the AMP women were single
and black. AMP women were also less educated and had
lower levels of income (Table 1).
Breastfeeding and BMI
For the pooled data set, children who had ever been breastfed
had lower mean BMI z scores than children who had not
(mean BMI z score 0.40 vs. 0.60, p = 0.04); no significant
difference between the proportions of children above the
85th percentile existed based on establishment of breastfeeding (Table 2). BMI z score was negatively associated
with intensity of breastfeeding; a higher intensity score was
associated with a lower BMI z score (correlation = -0.10,
p = 0.03; Table 2). Odds of overweight/obesity were lower
with a higher intensity score (OR = 0.97; p = 0.04;
Table 2). Compared to those with a BMI below 85th percentile, children with a BMI above 85th percentile had lower
intensity scores (10 vs. 8, p = 0.016). When intensity of
breastfeeding was analyzed as a categorical variable, a significantly greater proportion of children with an intensity
score of 0 were above 85th percentile compared to those with
an intensity score of 24 (30.3 vs. 16.7 %, p = 0.03; Table 2);
BMI z score did not differ significantly based on categorical
intensity of breastfeeding (Table 2). No significant relationship between the breastfeeding variables and BMI z
score or overweight existed in the AMP data set alone. In the
KAN-DO data set, BMI z score and percentile were affected
only by establishment of breastfeeding; toddlers who
established breastfeeding had significantly lower BMI z
scores (0.29 vs. 0.69, p = 0.04) and fewer of them were
above the 85th percentile (16.5 vs. 38.1 %, p = 0.02).
Hispanic
18 (4.0 %)
Non-Hispanic
434 (96.0 %)
Breastfeeding and Satiety
Up to $15,000
34 (7.7 %)
$15,001–30,000
82 (18.6 %)
$30,001–45,000
59 (13.4 %)
$45,001–60,000
53 (11.9 %)
Over $60,001
214 (48.4 %)
In the pooled data set, neither establishment nor intensity of
breastfeeding was associated with satiety score (Table 3).
No significant relationship between the two breastfeeding
variables and satiety responsiveness existed in either the
AMP or KAN-DO data sets when analyzed separately.
83 (18.4 %)
Satiety and BMI
Income
Education
High school (grades 9–12) or less
Some college
113 (25.0 %)
College graduate
Graduate school
149 (33.0 %)
107 (23.6 %)
Maternal work status
Does not work outside of home
40 (27.0 %)
Works part-time
25 (16.9 %)
Works full-time
83 (56.1 %)
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Compared to children with a satiety score of 3 or less, children who scored [3 on the satiety responsiveness subscale
had significantly lower BMI z scores (0.59 vs. 0.27,
p \ 0.01) in the pooled dataset. Similarly, significantly more
children with satiety scores B3 were above 85th percentile
(28.9 vs. 20.4 %, p = 0.04) (Table 2). In the AMP data set,
lower satiety score was significantly associated with a higher
Matern Child Health J (2014) 18:1023–1030
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Table 2 Associations of breastfeeding and satiety responsiveness with mean BMI z score and BMI C 85th percentile, from pooled dataset;
bivariate analyses (aims 1&2)
BMI z score
(mean [SD])
p value
BMI C 85 percentile
(% or OR and 95 % CI)
p value
Breastfeeding establishment
Yes (329)
No (99)
Breastfeeding intensity
Continuous
0.40 (1.1)
23.4 %
0.60 (0.9)
-0.10 0.04*
30.3 %
0.17**
0.03 0.97 (0.95, 1.00)
0.04¥
Categorical
0 (99)
0.60 (1.1)
1–6 (101)
0.45 (1.0)
30.3 %
7–12 (82)
0.48 (1.0)
13–18 (56)
0.27 (1.0)
21.4 %
19–24 (90)
0.35 (0.8)
16.7 %
23.8 %
0.29***
31.7 %
0.03**
Satiety responsiveness
B3 (232)
0.59 (0.9)
[3 (196)
0.27 (1.0)
28.9 %
\0.01*
20.4 %
0.04**
* p value obtained from a t test; ** p value obtained from Chi squared test; *** p value obtained from one-way ANOVA;
correlation and p value; ¥ p value obtained from logistic regression
Spearman’s
Table 3 Association between breastfeeding and satiety responsiveness, from pooled data; bivariate analyses (aim 3)
Satiety score
(mean [SD])
p value
0 \ SR B 3
(% or mean score)
3 \ SR B 5
(% or mean score)
55.0 %
45.0 %
p value
Breastfeeding establishment
Yes (329)
3.1 (0.6)
No (99)
3.1 (0.7)
0.45*
51.5 %
48.5 %
0.54**
0.04 0.43 7.5 points
7 points
0.94**
Breastfeeding intensity (continuous)
Breastfeeding intensity (categorical)
0 (99)
3.1 (0.7)
51.5 %
48.5 %
1–6 (101)
7–12 (82)
3.0 (0.6)
3.1 (0.4)
57.4 %
56.1 %
42.6 %
43.9 %
13–18 (56)
3.0 (0.6)
53.6 %
46.4 %
19–24 (90)
3.2 (0.5)
52.2 %
47.8 %
0.70***
* p value obtained from a t test; ** p value obtained from Chi squared test; *** p value obtained from one-way ANOVA;
correlation and p value
BMI z score (0.60 vs. 0.36, p = 0.05) and a greater likelihood of being above 85th percentile (32.5 vs. 22.0 %,
p = 0.05). Higher satiety score was associated with lower
BMI z score in the KAN-DO data set (0.122 vs. 0.568,
p = 0.01); proportions of children above 85th percentile did
not differ based on satiety score.
Breastfeeding and BMI, Adjusted for Satiety
Responsiveness
After adjusting for confounders, such as maternal BMI
and education, the main effects of breastfeeding establishment on BMI z score and odds of being overweight
0.91**
Spearman’s
no longer existed in the pooled dataset (Table 4). Similarly, a statistically significant relationship between
breastfeeding establishment and BMI z score, or odds of
being overweight, did not exist after adjusting for satiety
score (Table 4). No statistically significant relationship
was established between breastfeeding intensity and BMI
z score or between breastfeeding intensity and odds of
being overweight. Similarly, no statistically significant
relationship was established between the above variables
after adjusting for confounders or after adjusting for
satiety score (Table 4). Similar results were obtained
when analyzing data from AMP and KAN-DO
separately.
123
123
¥
* Adjusted for satiety score; ** adjusted for maternal BMI and education; other variables did not significantly affect the relationship; *** p value obtained from multiple linear regression;
p value obtained from logistic regression
0.05
0.97 (0.95, 1.00)
0.04
0.97 (0.95, 1.00)
0.79
-0.009
0.730
-0.012
0.03
0.10
Coefficient
p value
0.04
0.60 (0.40, 0.79)
No (99)
Pearson’s
correlation
p value
0.46 (0.23, 0.69)
0.51 (0.37, 0.65)
0.40 (0.29, 0.51)
Yes (326)
Breastfeeding
establishment
Breastfeeding intensity
p value¥
OR adjusted for SR
p value
Unadjusted OR
p value***
0.81
0.72
0.47 (0.24, 0.70)
0.51 (0.37, 0.64)
Adjusted BMI z score
with Sat. Score
(mean [95 % CI])*
p value***
Adjusted BMI z score
with confounders (mean
[95 % CI])**
p value***
Unadjusted BMI
z score (mean
[95 % CI])
BMI z score
Adjusted coefficient
with Sat. Score*
0.70 (0.43, 1.16)
0.17
p value¥
Unadjusted OR
p value***
BMI C 85th percentile
OR adjusted
for SR
0.70 (0.43, 1.16)
0.17
p value¥
Matern Child Health J (2014) 18:1023–1030
Table 4 Mean BMI z score and odds and 95 % CI of being overweight/obese (BMI C 85th percentile) by breastfeeding, unadjusted and adjusted for satiety score; multivariate analyses (aim 4)
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Discussion
In our study, increased breastfeeding and greater satiety
responsiveness were each associated with decreased toddler
adiposity in unadjusted analysis. The mean BMI z score was
significantly lower for children who established breastfeeding, and breastfeeding intensity was associated with both
significantly lower BMI z scores and lower odds of overweight/obesity. Satiety responsiveness was also significantly
associated with adiposity; toddlers with a higher satiety score
were less likely to be overweight. However, satiety responsiveness was not significantly associated with breastfeeding,
suggesting the effect of breastfeeding on toddler obesity is
independent of responsiveness to internal satiety cues. The
association between breastfeeding and child weight status and
the association between child weight status and satiety
responsiveness disappeared after controlling for other cofounders in the mediational analysis, suggesting that the
confounding variables contribute greatly to the relationships
between both breastfeeding and satiety responsiveness and
toddler overweight. In short, mothers who breastfeed are
different from mothers who do not, and mothers of overweight
toddlers differ from mothers of non-overweight toddlers. The
manner in which these mothers differ, and not differences in
satiety responsiveness, explains the relationship between
breastfeeding and toddler overweight [24].
Results relating breastfeeding to decreased obesity are
consistent with previous studies, though specifics of the
link differed slightly [2–9]. Other studies showed that
duration and exclusivity of breastfeeding were related to
odds of obesity but not BMI [5, 7, 8, 25]. In our study,
establishment and intensity were linked to toddler adiposity, as measured by BMI z score rather than BMI.
We found little published data directly relating satiety
responsiveness to breastfeeding. A greater proportion of the
published research addressed the relationship between parental
control of feeding for children and that relationship between
obesity or breastfeeding. These studies measured satiety
responsiveness using parental report of the volume and characteristics of food the children ingested, and did not address
satiety responsiveness as estimated by CEBQ satiety subscale
scores, specifically. Furthermore, these studies focused on
older children, rather than focusing on toddlers [12, 15, 17, 26].
Some limitations exist in our study. The sample size was
relatively small. Numerous statistical comparisons were
completed; statistically significant findings close to p \ 0.05
should therefore be interpreted with caution. More participants established breastfeeding than did not in each study,
which may overestimate differences in outcomes between
breastfeeding establishment groups. Our data did not distinguish between mothers who bottle-fed breast milk from those
who did not; it is possible that infants who were bottle-fed
breast milk may be categorized as breast-fed infants. We
Matern Child Health J (2014) 18:1023–1030
attempted to address this by using maternal work status as a
proxy for mode of feeding, with the assumption that working
mothers who report breast-feeding their infants may actually
be pumping and bottle-feeding their infants breast milk.
Satiety responsiveness scores for these infants may more
closely resemble those of bottle-fed infants, as opposed to
breast-fed infants, masking any true differences in satiety
responsiveness between the groups. The initial surveys used in
this study were not intended to ascertain information on
pumping, and analysis of the data, using maternal work status
as a proxy for mode of feeding, did not yield significant results.
Our analysis sample comprised data from two separate
studies and results may be affected by differences between
these two studies. This was addressed by analyzing data from
each study separately in addition to the pooled data set; the
results obtained from the separate study groups did not differ
substantially from those obtained from the pooled analysis
sample. Observed differences in results obtained using data
from the separate studies compared to results obtained from
the pooled dataset may be due to sample size effects. Furthermore, the measure of satiety responsiveness may not be
sensitive enough to find a relationship with breastfeeding
given the sample size. All the mothers in the study were
overweight or obese; inclusion of normal weight women may
have increased variability and the ability to find statistically
significant differences in child BMI z scores and obesity rates
that may be more applicable to the general population.
Strengths of this study include the anthropometric measure of toddler adiposity. Previous studies used BMI as a
measure of toddler adiposity; this measure is less than ideal
due to normal BMI variations among toddlers. This study
used BMI z score, which is age- and gender-adjusted, as an
adiposity measure [20]. This study further benefitted from
the assessment of toddlers within a narrow age window,
making the sample less susceptible to confounding variables
due to developmental differences. Furthermore, the data are
based on actual weights, rather than self-reported weights.
Maternal BMI is the greatest predictor of child BMI,
suggesting genetics influence child adiposity. However,
social factors, such as learned eating behaviors, may also
play a role [12]. This study did not find an effect of satiety
responsiveness on the association between breastfeeding
and toddler obesity. Research that further characterizes the
role of satiety responsiveness in breastfeeding and early
childhood obesity would be beneficial.
Conflict of interest
None to report.
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