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DOI: 10.1111/mcn.12010

Original Article
Nutrition in pregnancy and early childhood and
associations with obesity in developing countries
Zhenyu Yang* and Sandra L. Huffman
*National Institute of Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, Beijing, China, and Department of Nutrition and
Program in International and Community Nutrition, University of California, Davis, California, USA

Abstract

Concerns about the increasing rates of obesity in developing countries have led many policy makers to question
the impacts of maternal and early child nutrition on risk of later obesity. The purposes of the review are to
summarise the studies on the associations between nutrition during pregnancy and infant feeding practices with
later obesity from childhood through adulthood and to identify potential ways for preventing obesity in
developing countries.As few studies were identied in developing countries, key studies in developed countries
were included in the review.
Poor prenatal dietary intakes of energy, protein and micronutrients were shown to be associated with
increased risk of adult obesity in offspring. Female offspring seem to be more vulnerable than male offspring
when their mothers receive insufcient energy during pregnancy.
By inuencing birthweight,optimal prenatal nutrition might reduce the risk of obesity in adults.While normal
birthweights (25003999 g) were associated with higher body mass index (BMI) as adults, they generally were
associated with higher fat-free mass and lower fat mass compared with low birthweights (<2500 g). Low
birthweight was associated with higher risk of metabolic syndrome and central obesity in adults.
Breastfeeding and timely introduction of complementary foods were shown to protect against obesity later in
life in observational studies. High-protein intake during early childhood however was associated with higher
body fat mass and obesity in adulthood.
In developed countries,increased weight gain during the rst 2 years of life was associated with a higher BMI
in adulthood. However, recent studies in developing countries showed that higher BMI was more related to
greater lean body mass than fat mass.It appears that increased length at 2 years of age was positively associated
with height, weight and fat-free mass, and was only weakly associated with fat mass.
The protective associations between breastfeeding and obesity may differ in developing countries compared
to developed countries because many studies in developed countries used formula feeding as a control. Future
research on the relationship between breastfeeding, timely introduction of complementary feeding or rapid
weight gain and obesity are warranted in developing countries.
The focus of interventions to reduce risk of obesity in later life in developing countries could include:

1. improving maternal nutritional status during pregnancy to reduce low birthweight;

2. enhancing breastfeeding (including durations of exclusive and total breastfeeding);
3. timely introduction of high-quality complementary foods (containing micronutrients and essential fats) but
not excessive in protein;
4. further evidence is needed to understand the extent of weight gain and length gain during early childhood are
related to body composition in later life.

Keywords: nutritional status, pregnancy, infant, obesity, developing countries.

Correspondence: Zhenyu Yang, Institute of Nutrition and Food Safety, China Center for Disease Control and Prevention, No. 29
Nanwei Road, Xicheng District, Beijing 100050, China. E-mail: yang.zhenyuid@gmail.com

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
105
106 Z. Yang and S.L. Huffman

Fig. 1. Prevalence of overweight of male adults in 22 countries in 2005.

Data was based on WHO Global InfoBase. https://apps.who.int/infobase (Accessed 25 February 2011).

Introduction The increasing rates of obesity in developing coun-

tries have led many policy makers to question the
Based on the most recent estimation, about 297 impacts of maternal and early child nutrition on risk
million females and 205 million men (aged 20 years or of later obesity. Some have raised concerns that
older) were obese in 2008 worldwide (Finucane et al. improving complementary feeding with fortied
2011). Figures 1 and 2 gives recent estimates of adult products could exacerbate the problem of obesity by
obesity in developing countries (Alwan et al. 2010). enhancing weight gain from 624 months of age in
Now,overweight among women exceeds underweight countries such as SouthAfrica where rates of stunting
in most developing countries (UNSCN 2010). About at one to 3 years of age are similar to rates of over-
43 million children under 5 years old are overweight weight (Chopra et al. 2009).
or obese, with 80% of living in developing countries, The purpose of the review is to summarise the
even though the prevalence of obesity in industrial- existing major meta-analyses and systematic reviews
ised countries is about twice that of developing coun- updated with recent studies,which are about the asso-
tries (WHO 2009). Obesity is considered one of the ciations between nutrition during pregnancy and
leading risk factors for global mortality and disease infant feeding practices with later obesity from child-
burden.Although a high-energy dense diet,sedentary hood through adulthood. Although the focus of the
lifestyle and genetic factors are the main causes for review is on developing countries,the major studies in
adult obesity,nutrition in early life plays an important developed countries were included too,as few studies
role in the obesity epidemic. were identied in developing countries.

Key messages

Many of these studies were conducted in developed countries and studies on the topic in developing countries
should be strengthened.
Low-energy intake, very low-protein intake or inadequate micronutrient intakes in pregnancy was associated
with greater risk of obesity among offspring.
Low birthweight appeared to have a greater fat mass in adults.
Breastfeeding may have a protective effect on obesity occurrence. However, randomised controlled trials are
warranted to test the association. High-protein intake during early childhood is associated with higher body
fat mass and obesity in later life.
Greater weight gain during the rst 2 years of life was related to a higher BMI later in life, but in developing
countries, to lower fat mass.

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
 Early nutrition and obesity 107

Fig. 2. Prevalence of overweight of female adults in 22 countries in 2005.

Data was based on WHO Global InfoBase. https://apps.who.int/infobase (Accessed 25 February 2011).

Obesity is dened by the World Health Organiza- Prenatal nutrition and obesity in
tion (WHO) as a body mass index (BMI) value 30, later life
which is a surrogate measure of excessive fat accumu-
lation.BMI is the most common measure of obesity at The association between prenatal nutrition (famine
the population level. Obesity for children under 5 during pregnancy, prenatal protein and energy sup-
years at the population level is commonly assessed by plementation, and micronutrient supplementation)
using BMI-for-age or weight-for-height based on the and obesity was reviewed in the section. Only a few
2006 WHO growth standard. Several types of meas- studies were identied. Famine studies were from
urements have been used to assess body mass and
area can be calculated by using triceps skinfold
body composition.These include body weight,height,
thickness and mid-upper arm circumference ((TSF * C)/2 - [p*
circumference (waist circumference and hip circum-
(TSF)2]/4). Fat mass and fat-free mass (sometimes called lean
ference), skinfold thickness (triceps, subscapular,
body mass) can be directly measured/estimated by using various
biceps, abdomen), underwater weighing, dual energy
techniques with different principles. For example, underwater
X-ray absorptiometry (DEXA), bioelectrical imped-
weighing can be used to estimate body density. Because of the
ance analysis (BIA) and air displacement plethys-
different density between fat mass and fat-free mass, the per-
mography.1
centage of fat mass can be estimated through body density.

1
Body weight and height can be used to calculate BMI (weight/ Underwater weighing is usually time consuming and cumber-

height2),a crude measurement for obesity used globally.Because some. DEXA was developed to assess bone mineral density. It
fat mass plus fat-free mass gives total body weight, BMI is a can also be used to measure body fat content. However, the
surrogate for excessive fat accumulation, but not a specic indi- accuracy, radiation and cost limit its use. BIA is to measure
cator.Several factors (including age,race,physical training et al.) impedance to small electrical current passed across body tissues.
affect BMI. Waist circumference alone or waist-to-hip ratio Fat mass has greater impedance to the electrical current than
could be used as a surrogate measurement of central obesity. non-fat tissue, which enables fat mass to be estimated. Air dis-
Besides the similar limitation as BMI, the measurement of cir- placement plethysmography is based on a similar principle as
cumference is not reliable in certain circumstances. Skinfold underwater weighing and the body volume is measured by using
thickness can measure fat usually in truncal (i.e. subscapular) displaced air.Then the fat percentage is estimated based on the
and in extremity (i.e. triceps) areas. However, the measurement density equation. Trunk-to-limb fat ratio is calculated based on
is prone to high variation and low reproducibility. Arm fat the measured trunk fat and limb fat from these techniques.

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
108 Z. Yang and S.L. Huffman

Dutch population during World War II. Supplemen- 2003; Corvalan et al. 2007). The relationship between
tation trials (protein/energy and micronutrients) were birthweight and obesity in later life is discussed in
from developing countries. detail below.
Early studies showed that the risk of obesity at 19 A recent cohort study in the UK assessed the asso-
years of age was signicantly higher for offspring ciation between maternal dietary intake (using a food
whose mothers were exposed to the Dutch Hunger frequency questionnaire at 32 weeks of gestation) and
Winter famine (19441995) during the rst half of child dietary intake (using three 1-day unweighted
their pregnancy compared to offspring whose dietary diary records) and adiposity (assessed using
mothers were not exposed. By contrast, the opposite DEXA) at 10 years of age (Brion et al. 2010). The
was observed in those who were exposed to the results showed that maternal protein and fat intake
famine during the last trimester of pregnancy and in were signicantly associated with the offsprings
early post-natal life, in that they had a lower risk of protein and fat intake,which was positively associated
obesity (Ravelli et al. 1976; Stocker & Cawthorne with their fat mass. There was no signicant associa-
2008). Recent studies from the Dutch famine popula- tion between maternal dietary intake and their off-
tion further showed that low-energy intake (<900 kcal springs fat mass or fat-free mass.
day-1) during pregnancy was associated with higher
weight and greater fat deposition at several sites in
Micronutrient intake during pregnancy and
female offspring at ~58 years of age, but not in males
obesity in later life
(Stein et al. 2007). The associations were stronger
when exposed famine during the middle 20 weeks of Christian and Stewart recently reviewed the topic of
gestation than when exposed during the rst and last maternal prenatal micronutrient deciency and the
10 weeks of gestation. Another investigation found developmental consequences extensively and con-
that exposure to famine during pregnancy increased cluded that micronutrients also play an important
offsprings BMI and waist circumference in women at role in obesity development (Christian & Stewart
~50 years of age, but not in men (Ravelli et al. 1999). 2010). A randomised controlled trial in Nepal found
There may also be some small and weak positive asso- that children 68 years old whose mothers received
ciations between exposure to famine during preg- vitamin A, iron, zinc and folic acid supplements
nancy and energy balance, physical activity and during pregnancy from ~11 weeks of gestation had
percent energy from fat for their offspring in later life signicantly greater height, smaller triceps skinfold
in the Dutch famine population (Stein et al. 2009). thickness, subscapular skinfold thickness and arm fat
area than those in the control group whose mothers
were receiving vitamin A only. However, groups
Protein and energy supplements during
receiving folate alone, folate plus iron or a multiple
pregnancy and obesity in later life
micronutrient supplement (with the same amount of
In a cluster-randomised study in Guatemala, subjects iron, zinc and folate) did not show similar results
were randomly given a higher protein supplement or (Stewart et al. 2009). A longitudinal cohort in India
a non-protein supplement during pregnancy,lactation investigated the association between vitamin B12 and
and early childhood. Subjects in the high-protein folate status in pregnant women at 18 weeks and 28
group were born heavier,gained more height and had weeks of gestation and adiposity and insulin resist-
lower plasma glucose than subjects in the non-protein ance of their children at 6 years of age (Yajnik et al.
group (Habicht et al. 1973; Oken 2009). The study 2008). Lower maternal vitamin B12 status and higher
found that a higher birthweight was generally associ- maternal folate status were associated with greater fat
ated with less adiposity in later life. There was no mass (assessed by using DEXA) and insulin resist-
signicant difference in adiposity of the adults ance. However, a longitudinal observational study in
between these two treatments, which may be due to the UK found that neither folate supplements admin-
low power of the long-term follow-up study (Li et al. istered between 1832 weeks of gestation nor folate

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
 Early nutrition and obesity 109

intake at 32 weeks were associated with total body insulin resistance in later life (Morrison et al.2010).A
mass, fat mass or lean mass of children at 9 years of recent study in the UK further supported the nding
age, measured using DEXA (Lewis et al. 2009). that lower birthweight was associated with higher
Overall,adequate and balanced protein and energy trunk fat (trunk-to-limb fat ratio), measured using
intakes during pregnancy could be a protective factor DEXA in the elderly (Kensara et al. 2005). Another
for adult obesity, and female offspring seem to be study in the UK also found that birthweight was
more vulnerable than male offspring.Very low energy inversely associated with total body fat after adjusting
and protein intakes (e.g.famine) seem to increase the for age, gender, height and weight (Gale et al. 2001).
risk of overweight in later life. Iron, zinc and folic Studies from developing countries also support the
acid supplements starting from early pregnancy may nding that low birthweight is associated with lower
prevent childhood fatness, but not folic acid alone, BMI,but subjects with lower birthweight tend to have
iron plus folic acid or multiple micronutrient supple- higher body fat mass and lower lean body mass (Li
ments.Vitamin B12 status during pregnancy could also et al. 2003; Sachdev et al. 2005; Corvalan et al. 2007;
be negatively associated with adiposity later in life. Victora et al. 2007). In a longitudinal study in India,
Most of these studies were observational studies, birthweight (mean 2851 g) was positively associated
for example, famine and protein intake during with lean body mass residual (the residual of BMI
pregnancy. Randomised controlled trials are war- regressed on sum of skinfold thickness and height)
ranted to further assess the impacts of protein/energy and height, but not waist-to-hip ratio at ~30 years of
supplementation/intake or micronutrient supplemen- age (Sachdev et al. 2005). For female subjects, there
tation on obesity in developing countries to conrm was a positive relationship between birthweight and
the current ndings. sum of triceps skinfold thickness and subscapular
skinfold thickness and BMI. Subjects with birth-
weight <2500 g had signicantly higher subscapular-
Low birthweight and obesity in triceps ratio (1.48 vs.1.38 and 1.00 vs.0.95 for females
later life and males, respectively) than those with birthweight
As we cannot easily observe intrauterine develop- >3250 g. In the Guatemala trial mentioned earlier,
ment, birthweight is used as a proxy.The relationship higher birthweight was associated with greater height,
between birthweight and obesity from childhood higher body weight and fat-free mass (estimated by a
through adulthood was summarised in this section. population-specic equation) at 2127 years of age.
A great amount of observational studies were con- There was a positive association between birthweight
ducted in both developing countries and developed and fat mass for females only, but the magnitude of
countries. the relationship was smaller than the one for fat-free
Most studies have shown that higher birthweight is mass (Li et al. 2003). In a later follow-up of the Gua-
associated with higher BMI in later life. Eight of 10 temala cohort, BMI at birth was positively associated
studies reviewed by Oken and Gillman showed a with adult BMI and adult fat-free mass at ~33 years
positive relationship, even though there may have old (Corvalan et al.2007).A longitudinal cohort study
been some residual confounders (e.g. gestational age, in Brazil showed that birthweight was negatively
maternal factors including smoking and socio- associated with fat mass/lean mass ratio (assessed by
economic status; Oken & Gillman 2003). using adjusted bioimpedance) at 18 years of age, and
By contrast,lower birthweight has often been asso- positively related to height, BMI, body lean mass and
ciated with higher risk of metabolic syndrome (i.e. weakly related to fat mass (Victora et al. 2007). More
insulin resistance) and central obesity, measured by recent analyses from these cohorts showed that birth-
subscapular/triceps skinfold thickness ratio or waist- weight was more strongly associated with fat-free
to-hip ratio,even after adjusting for adult BMI (Oken mass than fat mass (Kuzawa et al. 2012). A J- or
& Gillman 2003). Lower birthweight was associated U-shaped relationship between birthweight and adult
with post-natal catch-up growth (Ong et al. 2000) and fat mass has been shown in a few studies, that is, both

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
110 Z. Yang and S.L. Huffman

the high and low ends of birthweight could be associ- 2005;Owen et al.2005a,b;Horta et al.2007) were con-
ated with higher adult obesity (McMillen et al. 2009). ducted to assess the relationship between breastfeed-
The nurses health study in the United States found ing and childhood obesity and consistently showed
that women with birthweight at the category of 5.0 the protective effects of breastfeeding except one
7.0 lb (i.e. ~2.53.0 kg) had lower prevalence of over- study (Owen et al. 2005a). Arenz et al. found that
weight, when birthweight was categorised into six seven of nine studies showed protective effects of
groups (<5.0 lb, 5.05.5 lb, 5.67.0 lb, 7.18.5 lb, 8.6 breastfeeding on childhood obesity (dened by using
10 lb and >10 lb) and the sample size of the two BMI cut-offs). The adjusted pooled odds ratio was
extreme categories (<5.0 lb and >10 lb) was 3390 and 0.78, which means breastfeeding reduced the odds of
1676, respectively. British birth cohort showed that obesity by 22% (Arenz et al. 2004; Koletzko et al.
the relationship between birthweight and BMI 2009a).
(obesity) was non-linear, where the lowest quintile Harder et al. conducted a meta-analysis between
birthweight was <2950 g for male and <2860 g for duration of breastfeeding and overweight. The
female with around 1000 subjects in each quintile. A adjusted pooled odds ratio was 0.75 and a signicant
J-shape relationship was observed between birth- dose-response association was observed (1 month of
weight and adult BMI.Both undernutrition and over- breastfeeding reduced the odds of being overweight
nutrition could be risk factors for adult obesity (Fall in later life by 4%),but no confounders were adjusted
2011). in the analyses (Harder et al. 2005). Horta et al. con-
Overall, although all these studies were observa- ducted a systematic review of 39 observational and
tional studies, the results were quite consistent. Sub- randomised studies of the effect of breastfeeding
jects with lower birthweights had less lean body mass on prevalence of overweight/obesity and found a sta-
and lower BMI, but greater fat mass, which is a direct tistically signicant protective effect among those
risk factor for cardiovascular and other chronic dis- studies that controlled for socio-economic status and
eases. The relationship might not hold for females in parental anthropometry (pooled odds ratio of 0.78
some studies. The gender difference needs further (95% CI: 0.720.84) ; Horta et al. 2007).
investigation. More research on the relationship Another systematic review included 29 studies, 28
between high birthweight (>4000 g) and body compo- of which showed that breastfeeding was a protective
sition are also warranted. factor against becoming overweight or obese (Owen
et al. 2005b). The pooled odds ratio was 0.87 and the
studies with smaller sample sizes tended to have
Infant feeding and obesity in later life
greater impacts. After supplementing these analyses
Breastfeeding and obesity in later life with unpublished data,the same author conducted an
additional meta-analysis and found that mean BMI
Although exclusive breastfeeding is recommended (0.030.19) was lower in breastfed children,compared
for the rst 6 months of life by WHO, the prevalence
to formula fed children later in life (2 years old or
of exclusive breastfeeding is still low globally. Mean-
beyond). However, after adjusting for maternal
while, the prevalence of obesity increased rapidly. It
smoking, maternal BMI and socio-economic status,
is unclear whether low rates of breastfeeding and
the difference disappeared (Owen et al. 2005a).
increased subsequent obesity coexist or whether
Besides residual confounders and publication bias,
there is a causal relationship.The section will summa-
another possible explanation could be that breast-
rise the relationship between breastfeeding and
feeding during early life could reduce risk of very high
obesity. Most studies were conducted in developed
BMI during later life and would shift the high end of
countries with formula feeding as a comparison
the BMI distribution to the left, but may but not
group.The ndings might not be simply generalised to
change mean BMI (Beyerlein et al. 2008). Seventeen
developing countries.
of 21 studies in a more recent review showed that
Multiple systematic reviews or meta-analyses
breastfeeding was associated with lower risk of
(Dewey 2003, 2008; Arenz et al. 2004; Harder et al.

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 Early nutrition and obesity 111

overweight or obesity in the offspring in later life, breastfeeding was signicantly higher in the interven-
after controlling for potential confounders. The tion group than in the control group.The differences
strength of these associations ranged from 0.55 to 0.80 between intervention and control groups for preva-
for the adjusted odds ratio. The relationship had a lence of any breastfeeding in the rst year ranged
dose-response effect for some studies (i.e. longer from ~8% to 14%. There were no signicant differ-
duration of breastfeeding or exclusivity of breastfeed- ences in weight, height or skinfold thickness between
ing with lower risks of overweight; Dewey 2003, the breastfeeding promotion and control groups at 6.5
2008). years of age.The small difference in the prevalence of
A longitudinal study observed a negative associa- any breastfeeding between the two groups may have
tion between full breastfeeding for more than 4 contributed to the non-signicant ndings. However,
months and rapid weight gain during the rst 2 years even when comparing children exclusively breastfed
of life,a risk factor for obesity in later life and fat mass for greater than or equal to 6 months and those who
development (Karaolis-Danckert et al. 2007). Most were breastfed for at least 12 months with children
recent observational studies also support that breast- who stopped breastfeeding at less than 1 month,
feeding was a protective factor for obesity/overweight breastfeeding did not show protective effects against
(OTierney et al. 2009; Kramer 2010; Krause et al. childhood adiposity. Other investigators have specu-
2010; Monasta et al. 2010; Papandreou et al. 2010; lated that the low power of the study contributed to
Seach et al. 2010; Dedoussis et al. 2011; van Rossem the lack of signicant ndings (Ruckinger & von
et al. 2011; Davis et al. 2012).A study in India showed Kries 2009).
that longer duration of breastfeeding was associated Bartok et al. tried to delineate the mechanisms
with lower BMI, but not skinfold thickness (Caleya- of the association between breastfeeding and
chetty et al. 2011). overweight/obesity (Bartok & Ventura 2009). One of
However, an observational study using DEXA to possible explanations is that the relationship is spuri-
measure fat mass and found either breastfeeding or ous because confounders could not be well controlled
time of introducing complementary food was not in the observational studies, which was supported by
associated with fat mass at 5 year of age (Burdette most non-association studies. Secondly, breastfeeding
et al. 2006). Sibling studies found mixed results could help infants self-regulate its intake.Thirdly,bio-
between breastfeeding and obesity (Stettler 2011).A active factors (e.g. protein content, leptin resistant,
comparison of children from Pelotas, Brazil, where adipokines) could regulate energy intake, expendi-
breastfeeding is not related to socio-economic status ture and cellular chemistry (Gillman & Mantzoros
as it is in developed countries,found a non-signicant 2007).
relationship of duration of breastfeeding with BMI
(Brion et al. 2011).The authors suggest that the asso-
ciations of breastfeeding for developed countries with Timing of introducing complementary food and
child BMI is likely to reect residual confounding. obesity in later life
In addition, a large-scale cluster-randomised
Only a few studies focused on timing of introducing
breastfeeding promotion trial in Belarus (PROBIT) complementary food in developed countries. Results
did not nd the protective effects of breastfeeding are mixed (Dewey 2008).A cross-sectional study from
on obesity (Kramer et al. 2007). Intervention group NHANES-III in the United States showed that there
received breastfeeding promotion information based was0.1%reductioninoddsofoverweightat35years
on the 10 steps of baby friendly hospital initiative. of age for each 1 month delay in introducing comple-
Control group received regular health care service. mentary foods, after controlling for duration of
During the 1-year follow-up, 19.7% of mothers in the breastfeeding, maternal obesity, race, birthweight and
intervention group and 11.4% of mothers in the child age (Hediger et al. 2001).Although the associa-
control group were still breastfeeding at 12 months. tion was signicant, the magnitude of the association
The prevalence of any breastfeeding and of exclusive is too small to be meaningful.Another observational

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
112 Z. Yang and S.L. Huffman

study followed infants from birth to 1 year of age in length between the high-protein and low-protein
Denmark.Weight gain during the rst year of life was groups. The growth pattern of the low-protein
signicantly greater for children introduced to com- formula group was similar to that of the breastfeeding
plementary foods before 16 weeks of age compared group.Another randomised controlled trial in the UK
to those introduced to complementary foods at or showed that 28% more protein in the infants diet
after16 weeks (but only for those who were breastfed increased childrens body fat by 30% at 8 years of age
<20 weeks),after adjusting for maternal pre-pregnant (Singhal 2010). An observational study in Denmark
BMI, smoking during pregnancy, birthweight, length assessed the association between protein intake at 9
at 1 year and gender (Baker et al. 2004). Another months and weight, height and skinfold thickness at
longitudinal study in the UK compared weight and 10 years (Hoppe et al. 2004). There was a positive
body composition at 7 years of age for children association between protein intake and weight and
receiving early introduction of complementary foods height, but no association was observed for BMI and
(<15 weeks) and those receiving delayed introduction skinfold thickness. Another longitudinal study in
of complementary foods ( 15 weeks) (Wilson et al. Germany evaluated the relationship between protein
1998). After controlling for breastfeeding, birth- intake at 6,12 and 1824 months and growth (weight,
weight,weight at rst introduction of complementary height, BMI and skinfold thickness) at 7 years of age
foods, and gender, early introduction of complemen- (Gunther et al. 2007).There were no signicant asso-
tary foods increased body fat by 2%.Another cohort ciations between high-protein intake for both 6 and
in Denmark observed that later introducing comple- 12 months and BMI or percentage of body fat at 7
mentary food (vegetables, meat or rm food) was years of age.However,high-protein intake (dened as
associated with less risk of obesity (Schack-Nielsen protein intake greater than the median of protein
et al. 2010). However, the Avon cohort study in intake in the study population, ~2.63 g kg-1 day-1,
England found that the timing of introduction of com- which is more than twice the Food and Agriculture
plementary foods was not associated with obesity at 7 Organization of the United Nations/WHO recom-
years of age, after adjusting for birthweight, gender, mended protein intake) for both 12 months and 1824
maternal prenatal smoking, breastfeeding, parental months increased BMI and percentage of body fat by
BMI,TV watching, weight gain in rst year, catch-up 0.29 standard deviation (SD) and 1.36%,respectively.
growth, weight at 8 and 18 months of age and short A longitudinal study in Sweden also found that
sleeping duration (Reilly et al. 2005). An early case protein intake at 1718 months was positively associ-
control study also showed that delayed introduction ated with BMI at 4 years of age after controlling for
of complementary foods did not have additional paternal and maternal BMI,energy intake and carbo-
benet on obesity prevention (Kramer 1981). hydrate intake at 1718 months and 4 years (Ohlund
et al. 2010).

Protein intake during the rst 2 years and

obesity in later life Sugar and fat intake during the rst 2 years and
obesity later in life
A multi-centre double-blinded, randomised control-
led trial in Belgium,Germany,Italy,Poland and Spain A recent review done by Mace et al. found no asso-
compared the effects of a low-protein infant formula ciations between fat intake (percentage of energy)
with a high-protein formula starting from 2 months during infancy and early childhood and weight, BMI
of age on length, BMI and weight-for-length at 24 or fat mass in later childhood for 10 of 11 studies
months (Koletzko et al. 2009b). After adjusting for (Mace et al. 2006). A longitudinal study in the UK
baseline status, BMI z-score and weight-for-length showed that fat intake at 18 months was not associ-
z-score were 0.23 and 0.20 greater in the high-protein ated with weight, height or BMI at 43 months. In the
formula group than in the low-protein formula group, study, the mean fat intake in the lowest quartile was
respectively. There were no signicant differences in about 37 g per day, which was equivalent to 31%

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
 Early nutrition and obesity 113

of total energy intake (Rogers & Emmett 2001). short-term growth (Ramakrishnan et al. 2009), zinc
Another recent study showed that a high-fat intake supplementation has had positive impacts on weight-
(>35% E) at 12 months or 18 months of age was for-height z-scores (Ramakrishnan et al. 2009). It is
positively associated with a higher percent body fat usually difcult to follow the micronutrient interven-
percentage at 25 years of age for those having rapid tions during rst 2 years to later life and the sample
weight gain. By contrast, a high-fat intake during this size for these type studies is usually powered for
period was not associated with a higher body fat per- biomarkers,which could not be sufcient to detect the
centage for children with normal weight gain at 25 impacts on overweight/obesity. Multiple micronutri-
years of age (Karaolis-Danckert et al. 2007). ents are commonly used preparations,which limit the
A longitudinal study in Finland examining children capability of isolating single micronutrient effects.
aged 13 months to 9 years showed that a higher Most of these studies were conducted in Africa or
sucrose intake (dened as the upper 10th percentile South Asia, where prevalence of overweight/obesity
for mean sucrose intake) was not associated with is still low, which limits generalisation.
higher BMI (Ruottinen et al. 2008). Overall, the relationship between breastfeeding
and overweight/obesity was not conclusive and ran-
domised controlled trials remain warranted. As it is
Micronutrient intake during rst 2 years not ethical to randomise subjects into either breast-
and obesity feeding or formula feeding group, breastfeeding
promotion could be an intervention to test the
There are few studies that directly assess the effects
of micronutrient status during early childhood on hypotheses. Interventions could focus on breastfeed-
obesity in later life. One study assessed the effects of ing promotion in high formula using population (for
dietary modication to improve micronutrient status example, more than 50% of infants before 6 months
on body composition after a 1-year intervention in of age used formula in China), which is expected to
Malawi (Yeudall et al.2002).Intervention with higher have greater effects. High-protein intake during early
zinc and iron bioavailability had no effects on arm fat childhood is associated with higher body fat mass and
area z-scores or triceps skinfold thickness z-scores. obesity in later life. Research on the association
A cross-sectional study in Zambia compared the between micronutrient status during early childhood
growth and body composition of infants at 9 months and obesity in later life is urgently needed, as the
receiving fortied complementary foods (either with prevalence of obesity increases rapidly during recent
amylase or without amylase for 3 months) with con- years even in developing countries,where micronutri-
trols (Owino et al. 2007). Infants who received forti- ent deciency is also common.
ed complementary foods had signicantly greater
subscapular skinfold thickness and suprailiac skinfold
Weight and length gain during the
thickness than the infants in the control group, but
rst 2 years and obesity later in life
there were no differences in weight and the means
weight-for-age z-scores of the three groups were all Growth (weight and length) during the rst 2 years of
greater than zero. Other investigators observed an the life reects the nutritional status of infants and
association between micronutrient status (e.g. iron young children and is the consequence of breastfeed-
and zinc) and obesity in cross-sectional analyses ing and complementary feeding.An early study found
(Marreiro et al. 2002; Pinhas-Hamiel et al. 2003). that rapid weight gain during rst half year of age
However, no long-term relationship has been identi- (>90 percentile) was associated with higher risk of
ed between early micronutrient status and obesity obesity in 68 years of age (Eid 1970).A multicenter
later in life. cohort study in the United States showed that rapid
Even though the majority of studies have shown weight gain during the rst 4 months (>100 g month-1)
that iron or vitamin A supplementation for children was associated with overweight at 7 years (Stettler
under 5 years of age has no signicant impact on et al. 2002) and at 20 years (Stettler et al. 2003). A

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
114 Z. Yang and S.L. Huffman

more recent study consistently observed this associa- risk of obesity, higher total body fat mass, visceral
tion (Ong et al. 2009).Thus, the beginning of life was adipose tissue mass and abdominal subcutaneous
considered as critical for later obesity (Stettler et al. adipose tissue mass (Ong & Loos 2006; Demerath
2005). More than 27 studies have shown that rapid et al. 2009). Because of the inconsistency of dening
weight gain in infancy is positively associated with rapid growth, the recently published WHO work on
obesity in later of life (Singhal 2010). Thirteen of 15 growth velocity standards could further clarify the
studies (with only three in developing countries) in relationship between rapid growth and obesity.
one systemic review found that rapid growth (pon- A few recent studies conducted in low- and middle-
deral growth and linear growth) increased the risk of income countries provide additional information
overweight, obesity or adiposity measurements; one about the relationship between weight or length gain
of the other two studies did not nd a relationship during early childhood and lean body mass in later
between length-for-age z-score changes from 15 days life.A study of an Indian cohort found that BMI gain
to 3 years of age and body fat (from Guatemala),and in the rst 2 years of life was positively related to BMI
the other study (Sweden) showed an inverse relation- and lean body mass residual at 2127 years of age,
ship between rapid linear growth and risk of over- after controlling for potential confounders (e.g.
weight (Monteiro & Victora 2005). This review did maternal weight and socio-economic status) (Sachdev
not separate out gain in the rst 6 months to later et al. 2005). Higher BMI change during the rst 2
gain.Wells et al.(2005) found in Brazil that rapid gain years of life was associated with greater lean body
in the rst 6 months was associated with BMI,but not mass residual, but only weakly related to the sum of
with fatness. However, gain from 14 years was asso- skinfold thickness. In the Guatemala trial mentioned
ciated with increased fatness. It is likely that the previously, length at 2 years of age was positively
timing of rapid weight gain may inuence later associated with weight and fat-free mass, and was
obesity.This needs to be claried because weight and weakly associated with fat mass at 2127 years of age
length gain in the rst 2 years of life is especially poor (Li et al. 2003). No association was found between
in developing countries. length at 2 years of age and waist-to-hip ratio.Recent
Seven of 10 studies in another systematic review follow-up of the Guatemala study found that length
showed that rapid weight growth during the rst year gain during infancy and the rst 3 years of life was
of life was related to obesity,higher BMI or weight in positively associated with fat-free mass more than fat
later of life (Baird et al.2005).In another more recent mass at 33 years of age (Corvalan et al. 2007). A
review, 21 studies found a positive relationship cohort study in Brazil found that weight gain during
between rapid weight gain during rst 2 years of life the rst 2 years was positively related to greater BMI,
and obesity in later life (Ong & Loos 2006).Different lean body mass and weakly associated with fat mass,
exposures (various denition and timing of rapid but not associated with fat mass/lean mass ratio later
weight gain, linear growth) and various outcomes in life (Victora et al. 2007).The pooled analyses from
(continuous BMI, obesity/overweight, weight) were these cohorts consistently demonstrated that weight
used in these four systematic reviews. These data gain during the rst 24 months was more strongly
support a hypothesis called the growth acceleration associated with fat-free mass than fat mass (Kuzawa
hypothesis, which proposes that early nutrition and et al. 2012).
growth will make a major contribution to long-term Overall, higher weight gain during the rst 2 years
cardiovascular risk (Singhal & Lucas 2004). of life was associated with greater BMI later in life.
The denition of rapid weight gain was inconsistent Recent studies in developing countries have shown
acrossthesestudies.Itisespeciallydifculttomeasure that higher BMI was more related to lean body mass
weight gain at population level, as repeated measure- than fat mass, and length gain also predicted lean
ments are not commonly done.A few studies dened body mass. Further evidence is required to under-
rapid weight gain between birth and 2 years of age as stand the extent that weight gain during early child-
>0.67 SD scores, which was associated with elevated hood is related to fat mass and lean mass in

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
 Early nutrition and obesity 115

adulthood. More evidence is needed to better under- of foods and supplements that promote linear growth
stand the effects of length gain on body composition is thus a priority to prevent obesity.
in later life. Studies including randomised controlled trials con-
sistently showed that higher protein intake during
infancy was associated with higher risk of obesity.
Lack of breastfeeding, low birthweight or rapid
Conclusion weight gain was associated with obesity in many
Obesity is an increasing problem in developing coun- observational studies. However, a randomised con-
tries, and nding means to reduce it is essential. trolled trial did not nd protective effects of breast-
Improving maternal, infant and young child nutrition feeding on obesity.More randomised controlled trials
is an approach that will have multiple health benets are needed to test the hypotheses of effects of breast-
in addition to reducing obesity in adulthood. feeding on obesity,especially in developing countries.
Adequate and balanced protein,energy and micronu- It is unethical and non-practical to conduct a ran-
trient intakes during pregnancy might be a protective domised trial for low birthweight or rapid weight
factor for adult obesity. Improving womens nutri- gain. Generalisation of these observational studies
tional status prior to and during pregnancy can sub- might be an option for the topic. As long-term
stantially reduce the risk of low birthweight. Low follow-up for this type of study is required to assess
birthweight appeared to have less lean body mass, causal relationship, the cost is still a big barrier for it.
lower BMI and greater fat mass in adults. If the the effects of breastfeeding,low birth weight or
Exclusive breastfeeding is associated with a slower rapid weight gain on obesity do exist, they tend to
rate of weight gain and possibly a decreased risk of attenuate with longer follow-up time, which also
overweight in childhood and adolescence compared requires a larger sample size to assess. Most of these
to formula feeding (e.g. breastfeeding is associated studies were observational and were conducted in
with ~20% reduction in odds of being overweight). developed countries, which differed from developing
Use of breast milk substitutes is associated with countries in many factors (socio-economic factors,
increased growth, perhaps due to higher protein feeding behaviour, lifestyle, aetiology of low birth-
content of breast milk substitutes or lack of self- weight et al.). Thus, generalisation of these results
regulation in intake, and thus, higher energy intakes could be affected.
when infants are bottle-fed. As with low birthweight
reduction, there are numerous other health and
Acknowledgements
development benets of enhanced breastfeeding.
Rapid weight gain during early infancy in develop- The authors would like to thank the Global Alliance
ing countries is associated with improved height and for Improved Nutrition (GAIN) for its support to
BMI, and fat-free mass, but not fat mass. However, produce the paper and make it available for the
rapid weight gain in infants in developed countries benet of all those working to improve maternal and
and in childhood (rather than early infancy) increases infant and young child nutrition.
fat mass instead of fat-free mass (bone and muscle)
and also increases risk of later obesity. Ensuring
breast milk intake (with lower protein content than Conicts of interest
infant formula or cows milk) is benecial, in part The authors declare no conicts of interest.
because excessive protein intake is associated with
increased risk of obesity. Monitoring of weight gain
can identify children growing too fast or too slow. Contributions
Identication of rapid weight gain early on may lead
Both ZY and SLH were involved in the conceptuali-
to interventions that would improve diet and prevent
zation of the study, drafting and reviewing the manu-
accumulation of fat mass later in life.Ensuring intake
script.

2012 Blackwell Publishing Ltd Maternal and Child Nutrition (2013), 9 (Suppl. 1), pp. 105119
116 Z. Yang and S.L. Huffman

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