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Accepted Article Preview: Published ahead of advance online publication

Breastfeeding during the first six months of life, adiposity


rebound and overweight/obesity at eight years of age

M D Estévez-González, A Santana del Pino, P Henrı́quez-


Sánchez, L Peña-Quintana, P Saavedra-Santana

Cite this article as: M D Estévez-González, A Santana del Pino, P Henrı́quez-


Sánchez, L Peña-Quintana, P Saavedra-Santana, Breastfeeding during the first six
months of life, adiposity rebound and overweight/obesity at eight years of age,
International Journal of Obesity accepted article preview 26 October 2015; doi:
10.1038/ijo.2015.228.

This is a PDF file of an unedited peer-reviewed manuscript that has been accepted
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Received 12 June 2015; revised 22 September 2015; accepted 1 October 2015;


Accepted article preview online 26 October 2015

© 2015 Macmillan Publishers Limited. All rights reserved.


BREASTFEEDING DURING THE FIRST SIX MONTHS OF LIFE, ADIPOSITY REBOUND

AND OVERWEIGHT/OBESITY AT EIGHT YEARS OF AGE

Authors:

Estévez-González M.D. a ; Santana del Pino A. b ; Henríquez-Sánchez P. c ; Peña-

Quintana L. c, d, e ; Saavedra-Santana P. b

Departament of aNursery, bMathematics, cClinical Sciences. University of Las Palmas de

Gran Canaria, Las Palmas, Spain. dUnit of Pediatric Gastroenterology, Hepatology and

Nutrition. Complejo Hospitalario Universitario Insular Materno-Infantil. Las Palmas.

Spain. eCIBER OBN Spain.

Author to whom correspondence and offprint requests are to be sent:

Mª Dolores Estévez González

Facultad de Ciencias de la Salud. Departamento de Enfermería

C/ Paseo Blas Cabrera Felipe s/n 35016. Las Palmas de Gran Canaria. Spain

Telephone +34 928 451431

Fax +34 928 459478

The authors declare no conflict of interest

The running title: Breastfeeding, adiposity rebound and overweight

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Summary:

Background:

The question of whether breastfeeding protects the child from obesity is a still debated

issue; however, the relationship between early adiposity rebound and higher risk of

obesity is well known. This study was aimed at evaluating whether breastfeeding

(without formula supplement) during the first six months of life, delays the time of

adiposity rebound and consequently reduces the rates of obesity at the age of 8.

Methods

This retrospective cohort study included 1812 children born in Gran Canaria in 2004,

with follow-up until they were eight years of age. Anthropometrical data had been taken

during routine visits to the doctor and were extracted from medical record databases.

Only children with breastfeeding for the first six months of life (173 children) and

children without breastfeeding (192 children) were included. Children with mixed

feeding and children whose data were not available were excluded.

Results

No Body Mass Index differences were found between children with breastfeeding (17,7)

or without breastfeeding (17,3) during the first six months of life. The percentages of

children with normal weight, overweight and obesity were similar in both groups, as

well as the age of adiposity rebound breastfeeding 3,61 years; formula 3,64 years). Early

adiposity rebound was associated with increased BMI at the age of eight, both in male

and female children.

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Conclusion

Breastfeeding during the first six months of life was not demonstrated to delay the age

of the adiposity rebound, in our study.

Keywords: body mass index; adiposity rebound; infant; child; obesity; overweight;

breastfeeding; infant feeding

Introduction

Although breastfeeding has been suggested to protect children from infantile obesity (1)

and abundant research has been conducted on this issue (2-5) this proposal has not

been conclusively confirmed, due to the many potentially confusing factors involved

(mother Body Mass Index (BMI), weight gain during pregnancy, birthweight, mother’s

education, family income, parental occupation, etc.) (6).

The adiposity rebound is a physiological period related with infantile obesity (7).

Between the 3 and 7 years of age, the amount of fat in the body decreases to a minimum

(8), thus reducing the BMI down to a lowest point (nadir), which is followed by a

progressive BMI increase until adulthood (9). An early adiposity rebound is associated

with higher risk of obesity and the age at which the adiposity rebound begins has been

taken as a predictor of this infantile obesity (8, 10-16).

In this line, it would be useful to know whether breastfeeding during the first six months

of life could influence the time of occurrence of the adiposity rebound, potentially

reducing the risk of developing obesity later in life. This issue has been scarcely studied.

Chivers et al. (17) published a study including 171 children, where they related the

adiposity rebound with the type of feeding during the first months of life. They found

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that children with breastfeeding (including mixed breast and formula feeding) during

four months or more experienced adiposity rebound at a similar age than children with

breast or mixed feeding for less than four months; although they found differences when

other factors were considered, such as gestational age at birth, gender and weight. This

study was designed in line with their research.

The objective of this study was to evaluate whether children breastfed (without formula

supplement) during the first six months of life experience a delay in adiposity rebound,

and consequently exhibit lower obesity rates at the age of eight, than children without

breastfeeding.

Material and methods

Study population

This retrospective cohort study included children born during year 2004. Data were

recorded during routine visits to the doctor and were extracted from the medical

records of the Infantile Health Program of the Canarian Health Service of Gran Canaria.

The study included 1812 children, whose anthropometric measurements had been

recorded at least once before age 4 and once after age 8. Date, weight and height were

extracted from every record, and the children’s age and BMI were calculated. The

maximum follow-up age was 8.96 years. Anthropometric measurements were made

with conventional scales and height rods. Our criteria for normal weight, overweight

and obesity were established in accordance with the WHO recommendations (18). Thus,

children were considered to be overweight for BMI values between the mean plus

standard deviation (SD) and the mean plus twice the SD of their corresponding gender

and age population, while they were considered to be obese for BMIs higher than the

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mean plus twice the SD. All other BMI values were considered to reflect normal weight.

Adiposity rebound or nadir was considered to occur at the time (age in years) of the

lowest recorded BMI, just before the beginning of the physiological BMI increase (7).

Only children with breastfeeding for at least six months (173 children) and without

breastfeeding (192 children) were included. Children with mixed feeding and children

whose data were not available were excluded.

Data were provided by the Direction of Primary Healthcare of the Gran Canaria Health

Area (Canarian Health Service) from their Infantile Health Program databases and we

were authorized to the use and publication of these data.

Statistical analysis

The children included in the study were split into two groups according to their type of

feeding: breastfeeding or formula during the first six months of life. Two consecutive

analyzes were conducted. First, the time of adiposity rebound was estimated for every

child. Second, the time of adiposity rebound and the percentages of normal weight,

overweight and obese children, were compared between groups.

In order to estimate the time of adiposity rebound, it was assumed that the evolution of

the BMI logarithm (log (BMI)) follows a cubic spline in children under nine. In this

analysis, we used the below described mixed effects model, where 𝑎𝑔𝑒𝑖,𝑗 and 𝐵𝑀𝐼𝑖,𝑗

were the age and BMI of child ith at the time of the jth visit to the doctor (19)

2 3 3
log 𝐵𝑀𝐼𝑖,𝑗 = 𝛼0 + 𝛼1 ∙ 𝑎𝑔𝑒𝑖,𝑗 + 𝛼2 ∙ 𝑎𝑔𝑒𝑖,𝑗 + 𝛼3 ∙ 𝑎𝑔𝑒𝑖,𝑗 + 𝛼4 ∙ 𝑎𝑔𝑒𝑖,𝑗 − 1 +

2
𝑏0,𝑖 + 𝑏1,𝑖 ∙ 𝑎𝑔𝑒𝑖,𝑗 + 𝑏2,𝑖 ∙ 𝑎𝑔𝑒𝑖,𝑗 + 𝑒𝑖,𝑗

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Parameters 𝛼0 , 𝛼1 , 𝛼2 , 𝛼3 and 𝛼4 denote the fixed effects of the model (common to all

children) while 𝑏0,𝑖 , 𝑏1,𝑖 and 𝑏2,𝑖 correspond to random effects (specific for every child),

𝑒𝑖,𝑗 corresponds to the variability within child ith and 𝑧+ corresponds to the positive

values of number z. Whitaker et al (10) proposed a cubic fit for log (BMI) in children

between 2 and 16 years. A graphical analysis of our data suggested that log (BMI)

follows cubic splines of different shapes before and after the first year of. For that
3
reason, the term 𝛼4 𝑎𝑔𝑒 − 1 + was introduced into the model.

The frequencies and percentages of normal weight, overweight and obese children in

each group were calculated. The time of adiposity rebound was expressed as median

and interquartile ranges (IQR) for each group; their distributions were compared with

the Kruskal-Wallis test and the percentages were compared with the χ2 test; statistical

significance was considered for p values < .05. Data were analyzed using the Package R

statistical software (20).

Results

All the parameters corresponding to fixed effects in the mixed model were statistically

significant with p-values lower than 0.001.

Figure 1 shows the recorded BMI values, the estimated fixed effects from the model, and

the individual BMI increase curves for 100 randomly selected children. We found that

the time of adiposity rebound tends to be delayed in children with lower BMI values.

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Figure 2 shows the final BMI (at age of 8) in relation to the age of adiposity rebound. Our

data clearly showed that early adiposity rebound is associated with higher BMI at age 8

(Pearson’s correlation -0.856).

Table 1 summarizes the estimated age of adiposity rebound for the different BMI and

gender groups expressed as median and interquartile range. Approximately 50% of 8

years old children were overweight or obese. Furthermore, children with overweight or

obesity at the age of 8 had earlier adiposity rebound than others, both males and

females.

Table 2 shows the age of adiposity rebound for each feeding type group. No differences

were found in 8-years BMI between both groups. The percentages of normal weight,

overweight and obese children were similar. No differences were found in the age of the

adiposity rebound.

Discussion

The question of whether breastfeeding protects children from childhood and teenage

obesity is a still open debate, despite a large amount of related publications, probably

because definitive conclusions have not been reached. In some published systematic

reviews (2-3, 21) it was concluded that breastfeeding protects against infantile obesity.

Furthermore, a dose-effect relationship was observed, with longer breastfeeding

periods associated to lower risks of obesity. It has been postulated that such a protective

effect could be due to the lower protein contents of breast milk, as compared with other

types of feeding, which could result in lower plasmatic insulin and consequent reduced

fat storage, thus preventing early development of adipocytes (22). In other reviews (4,

5) only mild protective effects of breastfeeding against obesity were found, a result that

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could be influenced by other different factors. In a cohort study with two decades

follow-up (23), results showed that introducing milk other than maternal before six

months of age, was a risk factor for overweight or obesity at the age of 20 (OR 1.47; 95%

CI 1.12-1.93; p = 0.005).

However, not much research has been done on the relationship between breastfeeding

and adiposity rebound. Among the scarce studies on this issue, we would like to mention

that of Chivers et al. (17) with 171 children, where the age of adiposity rebound was

compared between children (118) with breast or mixed feeding during four months or

more and children (53) with breast or mixed feeding for less than four months, without

significant differences. However, using predicted BMI based on the linear mixed model,

adjusted for age, gestational age, gender and wight status, significant differences in age

at nadir were found. The timing of adiposity rebound (age at nadir) was earlier for the

group that stopped breastfeeding at ≤ 4 months (63 ± 23.8 months in those

breastfeeding for less than four months or without breastfeeding; 73.6 ± 18.5 months in

children breastfeeding during four months or more; p<0.005).

For the sake of clarity, only children with either breastfeeding or formula feeding were

included in our study, while all children with mixed feeding were excluded. Our results

(age of adiposity rebound 3.61 years with breastfeeding and 3.64 years with formula) do

not support the statement that breastfeeding during the first six months of life delays

the time of the adiposity rebound.

With the aim of exploring the possible relationship between the time of adiposity

rebound and obesity, some authors studied the protein intake of children during the

first years of life in connection with the time of the adiposity rebound. Dorosty et al. (24)

studied the diet of infants of 8 months of age or more and Günther et al. (25) studied the

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diet of children of 12 months or more. Both studies failed to show a consistent

relationship with the adiposity rebound.

Moreover, consensus on the age of the adiposity rebound is not complete. Different

authors consider the adiposity rebound to occur between ages 5 and 7 (9), 4 and 8 (26)

or 3 and 7 (8). In our study, the adiposity rebound occurred earlier than reported by

other authors and it is worth noting that our population also presented higher rates of

obesity. Similarly to other studies (8,10-15,26), we found that earlier adiposity rebound

was associated with higher overweight or obesity rates at later ages, in particular at age

8. Chivers et al. (17) found the age of adiposity rebound to be 2.6 years (SD 1.4) for

obese children and 3.8 years (SD 2.2) for overweight ones. In our population, the age of

adiposity rebound was different between genders (males: 4.37 years for normal weight,

3.56 for overweight and 2.83 for obesity; females: 4.19 for normal weight; 3.34 for

overweight and 2.60 for obesity), in agreement with Williams et al. (15). These authors

found the adiposity rebound to occur at age 6.6 in males and 6 in females (their study

included 458 children and a follow-up period from age 3 to 26).

The concerning high rates (up to 48%) of overweight and obesity in our population

confirm the results of earlier studies published in our country (27). Thus, the Canarian

rates of childhood overweight and obesity are higher than the Spanish national mean

(44.5%) (28), especially due to obesity rates (23.8% in our population; 18.3% at the

national level). It should be taken into account however, that our study only included

children between 8 and 9 years of age, while national studies included children between

6 and 9.9 years.

Given that our data were extracted from the databases of the Canarian Health Service,

which include all children attending medical appointments with the public health

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service (at least 95% coverage according to the Canarian Health Service), biases of social

status, parents’ education, maternal BMI, etc. are improbable; although such information

would have enabled an interesting evaluation of possible sociocultural influences on

children overweight and obesity (29,30). Additionally, using the information in medical

records on the type of feeding during the first months of life prevents memory bias from

relatives’ reports.

Retrospective studies have certain limitations e.g. they are not specifically designed for

collecting certain data. We however, accepted this limitation in order to work with a

large sample and few biases.

In conclusion, our results do not support the claim that breastfeeding during the first six

months of life delays the adiposity rebound or reduces the prevalence of overweight or

obesity at the 8 years of age.

The time of occurrence of the adiposity rebound is a predictor of obesity; thus, detection

of early adiposity rebound in routine monitoring of a child’s growth should trigger alert

on the probabilities of developing obesity and lead to instauration of measures aimed at

reducing the risk. In this way, already established obesity, so difficult to revert in later

ages, could be prevented.

The influence of breastfeeding on the time of adiposity rebound requires more

investigation. Given the growing tendency to a prolonged breastfeeding, the possibility

that it could delay the adipose rebound and consequently reduce the rates of obesity is

worth the effort. Moreover, understanding the relationship between the duration of the

breastfeeding period and the time of adiposity rebound could provide interesting and

useful information.

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Conflict of interest

The authors declare no conflict of interest

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Figure Legend 1

 Data points
Fixed effects
Individuals curves

Figure Title 1. Body mass index versus age in 100 children.

Figure Title 2. BMI at 8 years of age according the age of adiposity rebound.

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Acknowledgements

We are grateful to all study participants, their families and health professionals who

participated anonymously at work. Also, we are grateful to the Direction of Primary

Healthcare of the Gran Canaria Health Area (Canarian Health Service).

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Table 1. Age (years) of adiposity rebound according to the BMI at 8 years of age

Normal weight Overweight Obesity P


N=943 (52.04%) N=436 (24.06%) N = 433 (23.8%)
Global 4.28 (3.92 ; 4.68) 3.43 (3.17 ; 3.67) 2.70 (2.27 ; 3.06) < .001
(N=1812)
Males 4.37 (4.02 ; 4.73) 3.56 (3.34 ; 3.83) 2.83 (2.39 ; 3.14) < .001
(N=928)
Females 4.19 (3.84 ; 4.61) 3.34 (3.06 ; 3.54) 2.60 (2.11 ; 2.95) < .001
(N=884)
Data are expressed as global and gender-specific frequencies, median (interquartile
range) and p values (Kruskal-Wallis test)

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Table 2. Age of adipose rebound and body status at 8 years of age according to the

type of feeding during the first few months of life.

Breastfeeding during the first six months

Breastfeeding Formula P

n = 173 n = 192

Males / females % 43.4 / 56.6 53.1 / 46.9 .062

Final body mass index 17.7 (15.5 ; 20.7) 17.3 (15.2 ; 20.9) .947

Body status at 8 years, n (%) .062

Normal weight 88 (50.9) 103 (53.6)

Overweight 41 (23.7) 35 (18.2)

Obesity 44 (25.4) 54 (28.1)

Age of adiposity rebound 3.61 (2.97 ; 4.27) 3.64 (2.81 ; 4.28) .650

Data are expressed as percentages and medians (IQR)

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Body Mass Index (kg m2)

25
20
15
10

0 1 2 3 4 5 6 7 8 9

Age (years)

Figure 1. Body mass index versus age in 100 children.

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Body mass index at age 8 years

25
20
15

0 1 2 3 4 5 6 7

Age of adiposity rebound

Figure 2. BMI at 8 years of age according the age of adiposity rebound.

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