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Published by Oxford University Press on behalf of the International Epidemiological Association International Journal of Epidemiology 2011;40:1215–1226

ß The Author 2011; all rights reserved. Advance Access publication 15 July 2011 doi:10.1093/ije/dyr094

Pre-natal and post-natal growth


trajectories and childhood cognitive
ability and mental health
Seungmi Yang,1* Kate Tilling,2 Richard Martin,2,3 Neil Davies,2,3 Yoav Ben-Shlomo2,3 and
Michael S Kramer1,4
1
Department of Paediatrics, McGill University, Montreal, Canada, 2Department of Social Medicine, University of Bristol, Bristol,
UK, 3Department of Social Medicine, MRC Centre for Causal Analyses in Translational Epidemiology, University of Bristol, Bristol,

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UK and 4Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, Canada
*Corresponding author. The Research Institute of McGill University Health Centre, 4060 Ste-Catherine West (Place Toulon),
Montreal, Quebec H3Z 2Z3, Canada. E-mail: seungmi.yang@mail.mcgill.ca

Accepted 17 May 2011


Background Most studies of the associations between pre-natal or post-natal
growth and cognitive ability have been based on children with
pathologically slow growth measured between two time points
only, rather than children with normal growth trajectories esti-
mated from multiple measures of growth.
Methods We investigated the associations of pre-natal and post-natal trajec-
tories in both weight and length/height through the first 5 years of
life with cognitive ability and mental health at 6.5 years of age
among healthy children. Our study is based on 11 899 children
who were born healthy at 537 completed weeks with birth
weight 52500 g and had up to 13 measures of weight and
length/height from birth to age 5 years and cognitive ability and be-
haviour measured at 6.5 years. Using a linear spline random-effects
model with 2 knots at 3 and 12 months, we estimated growth trajec-
tories for each child from birth to age 5 years in weight and length/
height in four periods: gestational age-specific birth weight and
length (pre-natal ‘growth’), early infancy (0–3 months), late infancy
(3–12 months) and early childhood (1–5 years). We used generalized
estimating equations to estimate mean differences in IQ and mental
health according to pre-natal and post-natal growth trajectory.
IQ was measured using the Wechsler Abbreviated Scales of
Intelligence, and mental health was assessed using the Strengths
and Difficulties Questionnaire.
Results A 1 standard deviation (SD) in birth weight was positively associated
with cognitive ability (0.82 IQ points, 95% CI: 0.54–1.10) after ad-
justing for confounders. For post-natal weight gain trajectories, a 1
SD faster weight gain was associated with an increase of 0.77 (95%
CI: 0.42–1.11) IQ points for early infancy, 0.30 (95% CI: 0.02–0.58)
points for late infancy, and 0.40 (95% CI: 0.04–0.76) for early child-
hood after adjusting for confounders and for earlier growth. For
length/height trajectories, the magnitudes of increase in cognitive
ability were similar to each other (0.6 points) across the four per-
iods. Pre-natal and infancy growth, but not early childhood growth,
were associated with reduced externalising behaviours.

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1216 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

Conclusions Although the effect sizes are small and residual confounding cannot
be excluded, our results suggest that among healthy children, faster
growth from the pre-natal period through age 5 years is positively
associated with cognitive ability, whereas faster growth in the
pre-natal period and infancy is positively associated with mental
health at early school age.
Keywords Term birth, pre-natal growth, post-natal growth, growth trajectory,
cognitive ability, child behaviour, child mental health

Introduction trial of a breastfeeding promotion intervention mod-

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elled on the WHO/UNICEF Baby-Friendly Hospital
The pre-natal period (particularly the third trimester Initiative. A total of 17 046 mothers and their healthy
of pregnancy) and the first few years of life are crucial infants in the Republic of Belarus born at 537 com-
for brain development.1,2 During this period, the brain pleted weeks of gestation and with birth weight
develops rapidly through the processes of neurogen- 52500 g were recruited from 31 maternity hospitals
esis, axonal and dendritic growth, synaptogenesis, cell and affiliated polyclinics during their postpartum stay
death, synaptic pruning, myelination and gliogenesis.3 between June 1996 and December 1997. They had
These processes occur sequentially and depend on scheduled follow-up study visits at 1, 2, 3, 6, 9 and
each other. Although cognitive ability has a heritable 12 months in the first year and at age 6.5 years.
component, environmental insults during the early Follow-up thorough the first year was achieved in
months and years of life are likely to have long- 16 491 infants (97%); 13 889 (81.5%) children were
lasting adverse effects on cognitive development.2 seen and examined at the 6.5-year follow-up. Our
Insults with demonstrated adverse effects include pre- study is based on 11 899 (86%) of the children who
term birth4–6 and failure to thrive in infancy.7 had cognitive ability and behaviour scores measured
Relatively few studies, however, have examined as- at the 6.5-year visit. The study received approval from
sociations of pre- and post-natal growth with cogni- the Institutional Review Board of the Montreal
tive ability in healthy children born at term without Children’s Hospital, and participating mothers signed
pathological growth restriction.8–13 Whereas most the consent in Russian.
have reported a positive association of weight gain
in infancy and early childhood with later cognitive
ability,8–10,12 some have found no association.11,13 Measures
Not only is the empirical evidence inconclusive, but Exposures (growth)
also most studies have estimated differences in Infant weight (grams) and length (centimetres) at
cognitive ability associated with a change in weight birth and gestational age in completed weeks were
between two time points only, rather than with tra- obtained from obstetric records during the postpar-
jectories estimated from multiple measures of growth. tum hospital stay. Weight and length during the
Finally, although cognitive ability is closely related to first year of life were measured by paediatricians at
mental health problems and poor pre-natal growth the scheduled PROBIT visits at 1, 2, 3, 6, 9 and
has been associated with later behavioural prob- 12 months. Weights and lengths/heights between
lems,14 behavioural sequelae of post-natal growth 12 months and 5 years were abstracted from the poly-
have rarely been studied. The aim of our study, there- clinic records of routine check-ups. A total of 2095
fore, was to examine the extent to which pre-natal (15%) children had no routine check-up visits, and
and post-natal trajectories in both weight and on average 4 (range 1–6) measures of weight and
length/height through the first 5 years of life are asso- height per child were abstracted from the clinic
ciated with cognitive ability and mental health at records.
6.5 years of age among children who had been born
at or after term. Outcomes
At the 6.5-year follow-up, cognitive ability was mea-
sured by the Wechsler Abbreviated Scales of
Methods Intelligence (WASI).16 The WASI consists of four
subtests of vocabulary and similarities to measure
Study participants verbal IQ and block designs and matrices to measure
Study children were participants in the Promotion of performance IQ. The WASI was translated from
Breastfeeding Intervention Trial (PROBIT). A full de- English to Russian and back-translated to ensure
scription of PROBIT has been published elsewhere.15 comparability of the Russian version. It was adminis-
In brief, PROBIT is a cluster-randomized controlled tered by the polyclinic paediatricians after extensive
PRE-NATAL OR POST-NATAL GROWTH AND CHILD DEVELOPMENT 1217

training and follow-up monitoring by child psycholo- SDQ in the polyclinic waiting room. Of the total of
gists and psychiatrists in Minsk, Belarus. 13 889 children, parents of 13 868 children completed
Interpaediatrician agreement was high, with Pearson the SDQ. The teachers of those who had begun school
correlation coefficients (95% confidence intervals) of also completed the teacher version of the SDQ distrib-
0.80 (0.67–0.89) for vocabulary, 0.72 (0.54–0.83) for uted by the polyclinic paediatricians. The SDQ items
similarities, 0.80 (0.67–0.89) for block designs and are identical in the parent and the teacher versions.
0.79 (0.66–0.88) for matrices in a convenience Of all children seen at the follow-up, the teacher SDQ
sample of 45 children during a 1-week training work- was obtained in 87% (n ¼ 12 016); most of the re-
shop.17 The present study used the full-scale IQ from mainder had not yet begun formal schooling at the
the WASI for the primary measure of general cogni- time of the follow-up. As previously reported,30 in-
tive ability of children. We also assessed the associ- ternal consistency and test–retest reliability of the
ations with verbal and performance IQ. Additionally, parent and teacher SDQ were high in our study;
at the 6.5-year follow-up visit, parents provided teach- Cronbach’s for total difficulties, for example, was
ers’ names if the child had started formal schooling 0.82 and 0.73 in the teacher and parent SDQ, respect-

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by the time of his/her follow-up visit, and the teachers ively. Correlations between the parent and the teacher
were asked to evaluate the child’s performance in SDQ scores were modest: 0.28 for total difficulties,
mathematics, reading, writing and other subjects ac- 0.39 for externalizing behaviours and 0.21 for inter-
cording to a 5-point Likert scale as far below (1), nalizing behaviours.
somewhat below, at, somewhat above, or far above
(5) his or her grade level, based on items in the Potential confounders
Teacher Report Form of the Child Behaviour Potentially confounding maternal and family charac-
Checklist.18 teristics included maternal and paternal age at the
Child mental health was measured using the time of the child’s birth, maternal smoking and alco-
Strengths and Difficulties Questionnaire (SDQ).19 hol consumption during pregnancy, breastfeeding,
The SDQ is a brief behavioural screening question- marital status, number of other children in the house-
naire for mental illness in children and adolescents hold, parental education and occupation (all based on
from ages 4 to 16 years and consists of five subscales maternal report at enrolment), and maternal and pa-
(hyperactivity, conduct problems, emotional symp- ternal height and body mass index (based on mater-
toms, peer problems and prosocial behaviour), each nal report at the 6.5-year follow-up).
with five items. Each item is rated as not true (0),
somewhat true (1) or certainly true (2). The score for Statistical analysis
each of the five scales is generated by summing the We examined the association of growth trajectories
scores for the five items, each ranging from 0 to 10. during the first 5 years to allow a time lag before
Scores for hyperactivity, conduct problems, emotional the outcome ascertainment (at 6.5 years). We esti-
symptoms and peer problems are summed to generate mated growth trajectories for each child from birth
a total difficulties score. A recent study20 has shown to age 5 years in weight and length/height using a
that although the four ‘difficulties’ subscales tap dis- linear spline random-effects model31 with MLwiN
tinct dimensions of behavioural problems, summariz- version 2.1 (www.cmm.bristol.ac.uk/MLwiN/index.
ing them into externalising behaviour (sum of shtml).32 Such models estimate mean growth trajec-
hyperactivity and conduct problem scores) and inter- tories based on the repeated measures of weight and
nalizing behaviour (sum of emotional symptoms and length/height over time and allow individual growth
peer problems) is more parsimonious and better able trajectories to randomly vary around the mean. This
to reduce measurement errors in a general population. approach allows for changes in scale and variance of
Thus, our behaviour measures of the SDQ are pre- growth measures over time and uses all available data
sented as total difficulties, externalizing behaviours, for each individual.
internalizing behaviours and prosocial behaviour. We used fractional polynomials to find the
The SDQ has been validated not only against other best-fitting growth trajectory for weight and length/
measures of child behaviour problems, including the height, and identified the best-fitting spline knots at 3
Child Behaviour Checklist (CBCL)21 but also clinical and 12 months for each sex. The model fits the data
diagnostic measures of mental disorder in children.22 well; 95% limits of agreement between observed and
The SDQ has been shown to compare favourably with expected growth measures were within 10% of the
other measures for identifying hyperactivity and at- mean values at each planned visit in the first year
tention problems.23–25 Several studies have demon- and at the 6.5-year follow-up. Thus, for both boys
strated the cross-cultural validity of the SDQ in and girls, linear random-effects models were fitted
European and developing countries.23,26–28 The for weight and length/height growth trajectory for
Russian version of the SDQ has previously been four periods: pre-natal ‘growth’ (birth weight and
used in clinical and research settings.29 length standardized by gestational age for each sex)
The parent accompanying the child (usually the and growth between 0–3 months (‘early infancy’),
mother) at the 6.5-year follow-up completed the 3–12 months (‘late infancy’) and 1–5 years (‘early
1218 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

childhood’). For instance, weight for child i at age j those excluded from the original sample of the
was modelled as: PROBIT due to loss to follow-up or missing informa-
tion on exposures or outcomes. Compared with those
yij ¼ 0 þ u0i þ ð 1 þu1i Þsi1 þð 2 þu2i Þsi2 þð 3 þu3i Þsi3 excluded, children included in our study were similar
þ eij j with respect to birth weight, gestational age, parental
age or parental size. Those excluded were slightly
where 0 is the population average birth weight more likely to have fathers with university education
(intercept) and 1, 2 and b3 are the population aver- (16% vs 12%) and non-manual occupation (30% vs
age velocities (slopes) of weight gain between 0–3 28%) and to be first-born children (61% vs 56%),
months, 3–12 months and 12–60 months, respectively but slightly less likely to have mothers with
(the fixed effects). u0i, u1i, u2i and u3i represent non-manual occupation (40% vs 43%).
individual-level random effects. u0i is the deviation Table 2 shows the association between the growth
from the average intercept for child i, and u1i, u2i trajectories and IQ at age 6.5 years. The patterns of
and u3i are the deviations for child i from the average association did not vary by sex (all P-values for

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velocities of weight gain between 0–3 months, 3–12 sex-interaction 40.10), and thus we present
months and 12–60 months, respectively. si1, si2 and si3 sex-adjusted results. For weight gain trajectory, the
are the amount of time spent in each period for child i unadjusted associations show that a 1 SD greater
at age j. Finally, eij is the deviation from the predicted birth weight for gestational age (e.g. 447 g in boys
weight for child i at age j (the occasion-level random and 434 g in girls at 40 weeks) was associated with
effects) and is related to age to allow for the increase a 0.94-point (95% CI: 0.62–1.25) increase in full-scale
in weight (and therefore the increase in the size of
IQ. A 1 SD faster weight gain during early infancy
the measurement error of weight) with age. The
was associated with a 1.25-point (95% CI: 0.88–
individual-level random effects correlation matrix
1.62) increase; the corresponding increases were 0.68
was unstructured, i.e. each random effect was allowed
(95% CI: 0.44–0.93) points for late infancy and 0.99
to be correlated with all other random effects. The
(95% CI: 0.70–1.29) points for early childhood growth.
occasion-level random effects were independent;
After adjusting for potential confounders (adjusted 1),
thus we assumed that measurement error at one
age was unrelated to measurement error for that in- the associations were attenuated by 15–50%, with
dividual at another age. Occasion- and individual- greater attenuation for associations with weight gain
level random effects were independent. during late infancy and early childhood. Of the con-
From these models, individual-specific estimates of founding factors included, parental socioeconomic
growth trajectory (i.e. each child’s deviation from the position and size, education and height in particular,
mean) in weight and length/height for the four peri- most attenuated the associations and were responsible
ods were obtained for each child.33 These weight and for 30% of the attenuation. Further adjustment for
length/height trajectory parameters were then stan- earlier growth (adjusted 2) did not substantially
dardized (z-scored) for sex, and additionally for ges- change the patterns of association. Stronger associ-
tational age for pre-natal growth. ations with birth weight and early infancy weight
Mean differences in IQ and SDQ scores by pre-natal gain were also observed when verbal and performance
and post-natal growth trajectory in weight and IQ scores were analysed separately.
length/height were estimated by generalized estimat- For length/height gain trajectories, faster growth
ing equations (GEE) regression analysis using STATA was positively associated with full-scale IQ scores in
10. We used the GEE approach to account for cluster- all four periods, with the largest association observed
ing in the data by hospitals and associated polyclinics for height gain during early childhood in unadjusted
and thereby correctly estimate standard errors of the associations. After adjustment for potential confoun-
regression coefficients. Associations with each growth ders and earlier growth (adjusted 2), the positive as-
parameter were examined in three models: (i) un- sociations in the unadjusted model were attenuated
adjusted; (ii) adjusted for potential confounding fac- by 30–50%, especially for early childhood height gain.
tors (‘adjusted 1’); and (iii) adjusted for potential As seen with weight gain trajectories, parental educa-
confounders and for earlier growth (‘adjusted 2’) tion and height were mainly responsible for the at-
models. tenuation. The attenuated associations between
infancy length gain and IQ in adjusted 1 were
strengthened with adjustment for earlier growth (ad-
justed 2), because infancy length gain was negatively
Results correlated with birth length (r ¼ 0.31 for early in-
Table 1 shows the baseline characteristics of the fancy and r ¼ 0.49 for late infancy). The patterns
PROBIT children in our study, their growth measures of association between length/height trajectories and
from birth to age 5 years, and the mean IQ, teachers’ verbal and performance IQ were essentially the same
ratings of the children’s academic performance, and as observed for full-scale IQ.
parent and teacher SDQ scores. Only minimal differ- Whereas growth measures in all four periods were
ences were observed between our analytic sample and positively associated with school performance,
PRE-NATAL OR POST-NATAL GROWTH AND CHILD DEVELOPMENT 1219

Table 1 Means (standard deviation) of growth measures, outcomes and covariates in the study sample

Growth measures
Weight (kg)
Birth weight 3.44 (0.42)
3 months 6.11 (0.67)
12 months 10.58 (1.01)
6.5 years 22.81 (3.61)
Length/height (cm)
Birth length 51.9 (2.13)
3 months 60.9 (2.4)
12 months 75.9 (2.7)

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6.5 years 120.7 (5.2)
Estimated growth velocity
Weight (kg/year)
0–3 months 10.82 (1.58)
3–12 months 6.38 (0.87)
1–5 years 1.89 (0.36)
Length/height (cm/year)
0–3 months 36.0 (6.21)
3–12 months 21.54 (1.95)
1–5 years 8.88 (0.80)
IQ
Full-scale IQ 105.2 (15.8)
Verbal IQ 103.2 (16.9)
Performance IQ 106.2 (15.1)
School performance [1 (far below) – 5 (far above) the grade level]
Mathematics 3.2 (0.8)
Reading 3.2 (0.8)
Writing 3.2 (0.8)
Other 3.3 (0.6)
Average 3.2 (0.7)
Parental SDQ
Total difficulties 11.5 (5.0)
Externalizing behaviours 6.3 (3.2)
Internalizing behaviours 5.2 (3.0)
Prosocial behaviour 8.3 (1.6)
Teacher SDQ
Total difficulties 9.6 (5.8)
Externalizing behaviours 5.3 (4.0)
Internalizing behaviours 4.3 (3.0)
Prosocial behaviour 7.5 (2.2)
Gestational age (weeks) 39.4 (1.0)
Mother’s pregnancy behaviour [n (%)]
Smoking (yes) 249 (2.1)
Drinking (yes) 281 (2.4)
Mother’s age (years) 24.5 (4.9)
Father’s age (years) 27.4 (5.1)
(continued)
1220 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

Table 1 Continued
Parental body size
Mother’s weight (kg) 66.2 (12.5)
Mother’s height (cm) 164.4 (5.7)
Father’s weight (kg) 80.2 (11.7)
Father’s height (cm) 176.1 (6.6)
Mother’s marital status [n (%)]
Married 10,618 (89.2)
Cohabitating 814 (6.8)
Unmarried 467 (3.9)
No. of children

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0 6741 (56.6)
1 4128 (34.7)
2þ 1030 (8.7)
Mother’s education [n (%)]
University degree 1579 (13.3)
Partial university 6075 (51.1)
Secondary education 3800 (31.9)
<Secondary education 445 (3.7)
Mother’s occupation [n (%)]
Non-manual 5134 (43.1)
Manual 4041 (34.0)
Unemployed 2724 (22.9)
Father’s education (n (%))
University degree 1467 (12.3)
Partial university 5460 (45.9)
Secondary education 4297 (36.1)
<Secondary education 277 (2.3)
Missing 398 (3.3)
Father’s occupation [n (%)]
Non-manual 3294 (27.7)
Manual 6506 (54.7)
Unemployed 1617 (13.6)
Unknown 482 (4.0)

associations between pre-natal and infant growth (95% CI: 0.00–0.03), 0.04 (95% CI: 0.02–0.06), 0.04
were larger than those for early childhood growth (95% CI: 0.02–0.06) and 0.02 (95% CI: 0.00–0.04)
(data not shown). For example, a 1 SD greater birth points, respectively, in fully adjusted models.
weight for gestational age was associated with a Table 3 summarizes the associations between
0.03-point (95% CI: 0.02–0.05) higher teacher rating growth trajectories and teacher SDQ scores. In un-
in mathematics after adjusting for potential confoun- adjusted analyses, a 1 SD increase in birth weight
ders. A 1 SD faster weight gain in early infancy, late for gestational age was negatively associated with
infancy and early childhood was associated with total difficulties, externalizing behaviours and inter-
increased mathematics ratings by 0.02 (95% CI: nalizing behaviours and positively associated with
0.01–0.04), 0.03 (95% CI: 0.02–0.05) and 0.01 (95% prosocial behaviour. After adjustment for potential
CI: 0.01 to 0.03) points, respectively, after adjusting confounders, inverse associations between birth
for confounders and earlier growth. The corres- weight and total difficulties (0.28, 95% CI: 0.40
ponding figures for length/height gain were 0.01 to 0.15), externalizing behaviours (0.16,
PRE-NATAL OR POST-NATAL GROWTH AND CHILD DEVELOPMENT 1221

Table 2 Associations between pre-natal and post-natal growth trajectories (z-scores) through 5 years of age and IQ at age
6.5 years

Unadjusted Adjusted 1 Adjusted 2


Weight trajectory
Full-scale IQ
Birth weight 0.94 (0.62, 1.25) 0.82 (0.54, 1.10) –
Weight gain from 0 to 3 months 1.25 (0.88, 1.62) 0.87 (0.52, 1.21) 0.77 (0.42, 1.11)
Weight gain from 3 to 12 months 0.68 (0.44, 0.93) 0.32 (0.06, 0.56) 0.29 (0.01, 0.58)
Weight gain from 1 to 5 years 0.99 (0.70, 1.29) 0.54 (0.27, 0.81) 0.40 (0.04, 0.76)
Verbal IQ
Birth weight 0.89 (0.54, 1.24) 0.81 (0.50, 1.12) –

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Weight gain from 0 to 3 months 1.26 (0.86, 1.66) 0.80 (0.44, 1.65) 0.70 (0.34, 1.05)
Weight gain from 3 to 12 months 0.68 (0.41, 0.95) 0.28 (0.001, 0.56) 0.27 (-0.03, 0.58)
Weight gain from 1 to 5 years 1.07 (0.76, 1.38) 0.63 (0.31, 0.95) 0.52 (0.08, 0.95)
Performance IQ
Birth weight 0.77 (0.50, 1.04) 0.65 (0.37, 0.93) –
Weight gain from 0 to 3 months 0.96 (0.65, 1.27) 0.75 (-0.04, 1.30) 0.67 (0.34, 1.00)
Weight gain from 3 to 12 months 0.53 (0.29, 0.76) 0.26 (0.01, 0.51) 0.23 (-0.06, 0.53)
Weight gain from 1 to 5 years 0.69 (0.41, 0.98) 0.34 (0.06, 0.63) 0.22 (-0.13, 0.56)
Length/Height trajectory
Full-scale IQ
Birth length 0.89 (0.61, 1.18) 0.62 (0.32, 0.92) –
Length gain from 0 to 3 months 0.86 (0.48, 1.23) 0.42 (0.04, 0.81) 0.65 (0.24, 1.05)
Length gain from 3 to 12 months 0.68 (0.27, 1.09) 0.23 (-0.15, 0.61) 0.68 (0.28, 1.08)
Height gain from 1 to 5 years 1.38 (0.94, 1.82) 0.77 (0.39, 1.16) 0.64 (0.16, 1.13)
Verbal IQ
Birth length 0.80 (0.53, 1.06) 0.53 (0.25, 0.81) –
Length gain from 0 to 3 months 0.89 (0.51, 1.27) 0.38 (0.02, 0.74) 0.57 (0.17, 0.97)
Length gain from 3 to 12 months 0.83 (0.36, 1.30) 0.39 (-0.06, 0.84) 0.84 (0.33, 1.33)
Height gain from 1 to 5 years 1.44 (0.97, 1.91) 0.82 (0.40, 1.24) 0.62 (0.10, 1.14)
Performance IQ
Birth length 0.81 (0.51, 1.11) 0.59 (0.27, 0.91) –
Length gain from 0 to 3 months 0.62 (0.25, 0.99) 0.35 (-0.01, 0.72) 0.56 (0.18, 0.94)
Length gain from 3 to 12 months 0.38 (0.07, 0.69) 0.01 (-0.30, 0.31) 0.37 (0.05, 0.70)
Height gain from 1 to 5 years 1.03 (0.67, 1.39) 0.57 (0.23, 0.91) 0.55 (0.14, 0.97)
Adjusted 1: adjusted for sex, term status (early term/term/post-term), maternal smoking and drinking during pregnancy, duration
of breastfeeding, number of older children, parental marital status, parental education and occupation, and parental height and
BMI.
Adjusted 2: adjusted for all variables in Adjusted 1 plus earlier growth trajectory.

95% CI: 0.24 to 0.07), internalizing behaviours observed for length/height gain trajectories. Birth
(0.12, 95% CI: 0.18 to 0.05) remained (although length was negatively associated with total difficulties
were considerably attenuated), but the positive asso- (0.21, 95% CI: 0.33 to 0.08) and externalizing
ciation with prosocial behaviour attenuated towards behaviours (0.15, 95% CI: 0.23 to 0.06) after ad-
the null. When potential confounders and (for the justing for potential confounders. Length/height gain
post-natal period) earlier growth were adjusted for, in later periods (particularly in infancy) was also
weight gain in late infancy was negatively associated negatively associated with problem behaviours, show-
with externalising behaviours and positively with pro- ing very similar effect sizes observed in weight gain
social behaviour. Similar patterns of association were but with wider confidence intervals after adjusting
1222 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

Table 3 Associations between pre-natal and post-natal growth trajectories (z-scores) through 5 years of age and teacher
SDQ scores at age 6.5 years

Weight trajectory Length/Height trajectory


a
Unadjusted Adjusted Unadjusted Adjusteda
Total difficulties
At birth 0.38 (0.48, 0.27) 0.28 (0.40, 0.15) 0.29 (0.40, 0.17) 0.21 (0.33, 0.08)
Gain from 0 to 3 months 0.15 (0.26, 0.04) 0.07 (0.19, 0.05) 0.05 (0.17, 0.07) 0.07 (0.21, 0.06)
Gain from 3 to 12 months 0.09 (0.20, 0.02) 0.13 (0.26, 0.01) 0.01 (0.10, 0.12) 0.11 (0.25, 0.03)
Gain from 1 to 5 years 0.07 (0.17, 0.03) 0.05 (0.07, 0.18) 0.10 (0.20, 0.002) 0.01 (0.12, 0.15)
Externalizing behaviours
At birth 0.23 (0.31, 0.16) 0.16 (0.24, 0.07) 0.20 (0.28, 0.12) 0.15 (0.23, 0.06)

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Gain from 0 to 3 months 0.09 (0.17, 0.01) 0.03 (0.12, 0.06) 0.04 (0.12, 0.04) 0.06 (0.16, 0.03)
Gain from 3 to 12 months 0.05 (0.13, 0.02) 0.09 (0.18, 0.01) 0.01 (0.07, 0.08) 0.08 (0.18, 0.01)
Gain from 1 to 5 years 0.003 (0.07, 0.07) 0.07 (0.01, 0.16) 0.06 (0.13, 0.02) 0.02 (0.07, 0.11)
Internalizing behaviours
At birth 0.14 (0.20, 0.08) 0.12 (0.18, 0.05) 0.08 (0.14, 0.02) 0.05 (0.13, 0.01)
Gain from 0 to 3 months 0.06 (0.12, 0.004) 0.04 (0.10, 0.03) 0.01 (0.07, 0.05) 0.02 (0.09, 0.05)
Gain from 3 to 12 months 0.04 (0.09, 0.02) 0.04 (0.11, 0.02) 0.003 (0.05, 0.06) 0.03 (0.11, 0.05)
Gain from 1 to 5 years 0.07 (0.12, 0.02) 0.02 (0.08, 0.05) 0.04 (0.09, 0.01) 0.00 (0.07, 0.07)
Prosocial behavior
At birth 0.07 (0.03, 0.11) 0.03 (0.01, 0.08) 0.04 (0.002, 0.09) 0.01 (0.04, 0.06)
Gain from 0 to 3 months 0.02 (0.02, 0.07) 0.02 (0.07, 0.02) 0.01 (0.04, 0.05) 0.02 (0.07, 0.04)
Gain from 3 to 12 months 0.04 (0.01, 0.08) 0.06 (0.01, 0.11) 0.01 (0.03, 0.05) 0.02 (0.04, 0.07)
Gain from 1 to 5 years 0.02 (0.02, 0.05) 0.02 (0.06, 0.03) 0.03 (0.01, 0.07) 0.01 (0.04, 0.07)
a
Adjusted models include all potential confounding factors and earlier growth trajectory estimates for post-natal growth.

additionally for earlier growth. Most of the attenu- gain trajectories, in particular for cognitive ability. For
ation from the unadjusted to the fully adjusted asso- weight gain trajectory, mean IQ differences associated
ciations was due to adjustment for confounding with growth during the pre-natal period and early
factors rather than for earlier growth. infancy (0–3 months) were larger than with later
Similar results were observed for parental SDQ growth, whereas the contributions of length/height
scores. Birth weight and early infancy weight gain gain trajectories to mean IQ differences across the
were negatively associated with total difficulties and four periods were similar to one another. These pat-
externalizing behaviours in unadjusted analyses (data terns were observed not only with full-scale IQ scores,
not shown). The associations were small in magni- but also for verbal and performance IQ. Nevertheless,
tude, however, and were not observed after adjusting we found that irrespective of earlier growth, faster
for potential confounding factors, except for the asso- growth at later ages was associated with increased
ciation between birth weight and externalizing behav- full-scale IQ scores. For child behaviour, pre-natal
iours (0.07, 95% CI: 0.13 to 0.01). Similar growth showed larger associations than did post-natal
patterns were observed with length/height gain trajec- growth.
tories (data not shown). The large sample size, prospective cohort design and
large number of growth measures from birth to age
5 years (up to 13) are strengths of study. Our frac-
tional linear spline random-effects model is an im-
Discussion provement on the approaches used in previous
In this cohort of healthy children born at or after studies. It allowed us to identify important time
term, we found small, positive associations of points at which the rate of growth differs in the
growth trajectories from the pre-natal period through first 5 years of life, rather than using arbitrary time
the first 5 years of life with both cognitive ability and points limited by availability of data, as was often the
mental health at age 6.5 years. However, the pattern case in previous studies. The time points identified by
of associations across the four periods defined in our our linear spline approach were based solely on
study differed somewhat for weight and length/height growth measures to represent distinct biological
PRE-NATAL OR POST-NATAL GROWTH AND CHILD DEVELOPMENT 1223

growth patterns over the 5 years and were not influ- were also measured by the paediatricians) was not as
enced by the choice of our outcome measures. Our strong, however, as reflected by intra-class coefficients
analytical approach also enabled us to estimate indi- of 0.01 to 0.19. The clustering of IQ thus does not
vidual trajectories by allowing random variation confound the association but widens CIs of the esti-
across individuals and their associations with differ- mates of the association when statistically accounted
ences in cognitive ability and behaviour scores. for in our analysis.37 In regard to behaviour measures,
The associations observed in our study are probably having multiple informants—both the parent and the
generalizable to other developed country settings. teacher—is likely to have reduced potential reporting
First, our findings are not based on children with bias of child behaviour. The parent and teacher SDQ
growth problems but rather on normal, healthy chil- scores have been observed to provide complementary
dren. Second, Belarus resembles Western developed information; teachers appear better able to assess
countries with respect to readily accessible basic externalising behavioural problems, whereas parents
health care services, high levels of sanitation, high appear better at assessing internalizing behaviours.25
immunization rates, low incidence of infection and Despite larger effect sizes for the teacher SDQ scores,

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low rates of infant and child mortality. the direction of associations observed with the parent
Some limitations in our study also require discus- and the teacher SDQs in our study were consistent
sion, however. First, although we adjusted for a wide with each other. Finally, the Russian version of the
range of maternal and paternal characteristics, WASI has never been formally validated. Nonetheless,
residual confounding by family characteristics (both WASI scores in PROBIT children were associated
genetic and environmental factors) cannot be strongly with parental education and other family
excluded. All coefficients were attenuated (by up to characteristics in the expected directions and were
50%) with adjustment for the confounders included also positively correlated with children’s academic
here, and it seems likely that other confounders exist performances (correlation coefficients 0.3).38
(not measured here) which would attenuate these re- Research on long-term effects of post-natal growth
lationships further. Parental cognitive ability, a strong has focused mostly on children with very slow growth
predictor of cognitive ability of offspring,34 for ex- characterized as ‘growth faltering’ or ‘failure to
ample, may also affect growth trajectory via parenting thrive’. Only recently have researchers directed atten-
behaviours such as feeding practices and physical ac- tion to child growth and its association with cognitive
tivity. The lack of maternal psychological distress data development in general, healthy populations. Wide
in our data may also explain the observed association variations in the growth period examined, growth
for behaviour. However, Alati et al.35 showed that the measures used and ages at which cognitive ability
association between birth weight and behavioural was assessed characterize these studies; most have
problems is not affected by the adjustment for mater- reported small but positive associations,8,10,12,39–41
nal anxiety and depression in a relatively large birth consistent with our results. One exception is the
cohort. Second, although we deliberately chose a min- study by Belfort et al.,11 which reported no association
imum of 1.5 years between the growth and outcome between weight gain in the first 6 months and cog-
measures, reverse causation could theoretically nitive ability measured at age 3 years. The authors
explain our findings; children with higher cognitive argue that among healthy, term-born children,
ability and/or better mental health might grow post-natal growth is not related to cognitive develop-
faster via better eating practices.36 Third, weight and ment, but the relatively small sample size (n ¼ 872) is
length/height measures in our study were not stan- likely to have been underpowered to detect a modest
dardized across hospitals and polyclinics, which is effect.
likely to increase measurement errors. These measure- Studies have reported that early infancy is a ‘sensi-
ment errors are unlikely to vary systematically by tive’ period for cognitive development, but most such
child cognitive ability and behaviour across study studies were largely based on children with failure to
sites, however, and would therefore tend to attenuate thrive.9,42,43 The term ‘sensitive period’ denotes an age
associations toward the null. range during which exposure effects are increased,
Measurement errors for IQ and behaviour are also a although such effects can be modified or even re-
potential source of bias. Despite our efforts to stand- versed over time.44 Among studies from generally
ardize measurements across paediatricians at 31 poly- healthy populations, the existence of a sensitive
clinics, mean IQ scores across polyclinics were highly period in post-natal growth for later cognitive devel-
clustered, as indicated by the intra-class coefficient of opment remains unclear, mainly owing to limitations
0.31. Since a single paediatrician measured IQ at 24 of in their analytical approach, usually based on avail-
the 31 polyclinics (two paediatricians shared the work able growth data collected at arbitrary limited time
at the seven busiest polyclinics), this clustering prob- points. Our approach to examining growth trajectories
ably reflects differences in strictness or leniency in suggests that effects may vary somewhat by growth
scoring or timing of responses among paediatricians, measure and by outcome. Birth weight and early in-
rather than true geographic differences in IQ across fancy weight gain seem more important for cognitive
polyclinics. The clustering of growth measures (which ability, whereas growth in length/height seem equally
1224 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

important across all periods. It is not clear why the A possible biological mechanism underlying the
patterns of association with cognitive ability differ positive association observed in our study is the
across weight and length/height trajectories. The growth hormone (GH)/insulin-like growth factor
different patterns observed in our study suggest that (IGF)-I system. GH/IGF-I system plays a key role in
growth throughout the first 5 years contributes to somatic growth regulation, particularly for longitudin-
later cognitive ability but does not provide strong al growth at pre-pubertal ages.50 A recent trial has
evidence for a true sensitive period of cognitive devel- shown that children born small for gestational age
opment. The different patterns may merely reflect who underwent GH treatment showed not only
greater errors in measuring length than weight, catch-up growth in height, but also improvements
especially for infants. in IQ and problem behaviour scores.51 In addition,
We conceptualized family socioeconomic character- serum IGF-I level has been positively associated
istics as potentially confounding the association be- with cognitive ability in healthy children with
tween growth trajectory and IQ. This view is normal growth.52
supported by the substantial attenuation of the Concerns and debate have arisen about the adverse

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observed associations with adjustment for parental effects of rapid weight gain in infancy, including
socioeconomic position and height, which is also increased long-term risk of obesity,53,54 high blood
closely related to socioeconomic position.45 However, pressure55–57 and insulin resistance.58 Although the
it could be hypothesised that the effects of family magnitudes of association are small, we have also
background on child cognitive ability are mediated observed positive associations of pre-natal and
by child growth. In an attempt to test this hypoth- post-natal growth and blood pressure at 6.5 years of
esized pathway, we examined associations of parental age in our study sample.33 In the present study, how-
education and occupation with IQ and the degree of
ever, our results suggest that rapid growth in infancy
attenuation after adjustment for child growth.
and early childhood is positively associated with the
Although the socioeconomic factors were positively
development of cognition and mental health.
associated with IQ independently of growth trajectory,
Increased susceptibility to infection,59 smaller adult
the associations were only trivially attenuated by ad-
stature60 and mental illness61 are among other ad-
justment for child growth (data not shown).
To our knowledge, no previous study has examined verse health consequences associated with slower
the association between post-natal growth and child infant growth. The overall evidence suggests that
behaviour in healthy children. Children with experi- the long-term consequences of rapid infant weight
ences of extreme malnutrition and stunting have been gain may vary according to outcome,62 and clinical
reported to show problem behaviours, including and public health practice therefore needs to consider
aggressiveness, attention deficits, peer problems, de- both the risks and benefits of potential interventions.
pressive symptoms and hyperactivity.46–49 Our results
are consistent in direction, although smaller in mag-
nitude, with those observed in children with severe
growth restriction in infancy or early childhood. Funding
Given the linear relationship between total difficulties
scores of the SDQ and the likelihood of having mental This research was supported by a grant from the
disorder observed in a recent study,22 our results sug- Canadian Institutes of Health Research (MOP-53155).
gest that faster post-natal growth may also have Conflict of interest: None declared.
beneficial effects in mental health among healthy
children.

KEY MESSAGES
 Most studies of the associations between pre-natal or post-natal growth and cognitive and behav-
ioural development have been based on children with pathologically slow growth or with growth
measured between two time points only.
 In this large cohort of healthy children who were born at term or later with birth weight of at least
2500 g, children with faster growth from the pre-natal period through the first 5 years of life showed
higher scores in IQ at age 6.5 years.
 For behavioural development, it seems that faster growth in the pre-natal period and infancy but not
in early childhood is associated with lower scores in problem behaviours, suggestive of better mental
health.
PRE-NATAL OR POST-NATAL GROWTH AND CHILD DEVELOPMENT 1225

17
References Kramer MS, Aboud F, Mironova E et al. Breastfeeding and
child cognitive development: new evidence from a large
1
Smart JL. Malnutrition, learning and behavior – 25 years randomized trial. Arch Gen Psychiatry 2008;65:578–84.
on from the Mit symposium. Proc Nutr Soc 1993;52: 18
Achenback TM, Rescola LA. Manual for the ASEBA
189–99. School-Age Forms and Profiles. Burlington, VT: University
2
Grantham-McGregor S, Cheung YB, Cueto S, Glewwe P, of Vermont, Research Center for Children, Youth, and
Richter L, Strupp B. Developmental potential in the first 5 Families, 2001.
years for children in developing countries. Lancet 2007; 19
Goodman R. The strengths and difficulties questionnaire:
369:60–70. a research note. J Child Psychol Psychiatry 1997;38:581–86.
3
Webb SJ, Monk CS, Nelson CA. Mechanisms of postnatal 20
Goodman A, Lamping D, Ploubidis G. When to use
neurobiological development: implications for human de- broader internalising and externalising subscales instead
velopment. Dev Neuropsychol 2001;19:147–71. of the hypothesised five subscales on the Strengths and
4
Casey PH, Whiteside-Mansell L, Barrett K, Bradley RH, Difficulties Questionnaire (SDQ): data from British par-
Gargus R. Impact of prenatal and/or postnatal growth ents, teachers and children. J Abnorm Child Psychol 2010;
problems in low birth weight preterm infants on 38:1179–91.

Downloaded from https://academic.oup.com/ije/article/40/5/1215/657775 by guest on 15 June 2023


school-age outcomes: an 8-year longitudinal evaluation. 21
Goodman R, Scott S. Comparing the strengths and diffi-
Pediatrics 2006;118:1078–86.
5
culties questionnaire and the child behavior checklist: Is
Hack M, Merkatz IR, Gordon D, Jones PK, Fanaroff AA. small beautiful? J Abnorm Child Psychol 1999;27:17–24.
The prognostic significance of postnatal growth in very 22
Goodman A, Goodman R. Strengths and Difficulties
low–birth weight infants. Am J Obstet Gynecol 1982;143:
Questionnaire as a dimensional measure of child mental
693–99.
6 health. J Am Acad Child Adolesc Psychiatry 2009;48:400–03.
Ehrenkranz RA, Dusick AM, Vohr BR, Wright LL, 23
Goodman R, Renfrew D, Mullick M. Predicting type of
Wrage LA, Poole WK. Growth in the neonatal intensive
care unit influences neurodevelopmental and growth out- psychiatric disorder from Strengths and Difficulties
comes of extremely low birth weight infants. Pediatrics Questionnaire (SDQ) scores in child mental health clinics
2006;117:1253–61. in London and Dhaka. Eur Child Adolesc Psychiatry 2000;9:
7 129–34.
Corbett SS, Drewett RF. To what extent is failure to 24
thrive in infancy associated with poorer cognitive devel- Goodman R, Ford T, Richards H, Gatward R, Meltzer H.
opment? A review and meta-analysis. J Child Psychol The development and well-being assessment: description
Psychiatry 2004;45:641–54. and initial validation of an integrated assessment of child
8 and adolescent psychopathology. J Child Psychol Psychiatry
Cheung Y, Ashorn P. Continuation of linear growth fail-
2000;41:645–55.
ure and its association with cognitive ability are not de- 25
pendent on initial length-for-age: a longitudinal study Goodman R, Ford T, Simmons H, Gatward R, Meltzer H.
from 6 months to 11 years of age. Acta Paediatr 2010;99: Using the Strengths and Difficulties Questionnaire (SDQ)
1719–23. to screen for child psychiatric disorders in a community
9 sample. Br J Psychiatry 2000;177:534–39.
Emond AM, Blair PS, Emmett PM, Drewett RF. Weight 26
faltering in infancy and IQ levels at 8 years in the Avon Smedje H, Broman J, Hetta J, Von Knorring A.
Longitudinal Study of Parents and Children. Pediatrics Psychometric properties of a Swedish version of the
2007;120:e1051–58. ‘Strengths and Difficulties Questionnaire’. Eur Child
10
Heinonen K, Raikkonen K, Pesonen AK et al. Prenatal Adolesc Psychiatry 1999;8:63–63.
27
and postnatal growth and cognitive abilities at 56 Klasen H, Woerner W, Wolke D et al. Comparing the
months of age: a longitudinal study of infants born at German versions of the Strengths and Difficulties
term. Pediatrics 2008;121:e1325–33. Questionnaire (SDQ-Deu) and the Child Behavior
11
Belfort MB, Rifas-Shiman SL, Rich-Edwards JW, Checklist. Eur Child Adolesc Psychiatry 2000;9:271–71.
28
Kleinman KP, Oken E, Gillman MW. Infant growth and Koskelainen M, Sourander A, Kaljonen A. The Strengths
child cognition at 3 years of age. Pediatrics 2008;122: and Difficulties Questionnaire among Finnish school-
e689–95. aged children and adolescents. Eur Child Adolesc
12
Corbett SS, Drewett RF, Durham M, Tymms P, Psychiatry 2000;9:277–77.
29
Wright CM. The relationship between birthweight, Goodman R, Slobodskaya H, Knyazev G. Russian child
weight gain in infancy, and educational attainment in mental health. A cross-sectional study of prevalence and
childhood. Paediatr Perinat Epidemiol 2007;21:57–64. risk factors. Eur Child Adolesc Psychiatry 2005;14:28–33.
13 30
Boddy J, Skuse D, Andrews B. The developmental seque- Kramer MS, Fombonne E, Igumnov S et al. Effects of
lae of nonorganic failure to thrive. J Child Psychol prolonged and exclusive breastfeeding on child behavior
Psychiatry 2000;41:1003–14. and maternal adjustment: evidence from a large, rando-
14
Bhutta AT, Cleves MA, Casey PH, Cradock MM, mized trial. Pediatrics 2008;121:e435–40.
31
Anand KJ. Cognitive and behavioral outcomes of Goldstein H. Efficient statistical modeling of longitudinal
school-aged children who were born preterm: a data. Ann Hum Biol 1986;13:129–41.
meta-analysis. JAMA 2002;288:728–37. 32
Rabash J, Charlton C, Browne WJ, Healy M, Cameron B.
15
Kramer MS, Chalmers B, Hodnett ED et al. Promotion of MLwiN Version 2.1. Centre for Multilevel Modeling,
Breastfeeding Intervention Trial (PROBIT): a randomized University of Bristol, 2009.
trial in the Republic of Belarus. JAMA 2001;285:413–20. 33
Tilling K, Davies N, Windmeijer F et al. Does accelerated
16
Wechsler D. Wechsler Abbreviated Scales of Intelligence. San weight gain in infancy increase blood pressure in child-
Antonio, TX: Psychological Corp, 1999. hood? An observational analysis of the Promotion of
1226 INTERNATIONAL JOURNAL OF EPIDEMIOLOGY

49
Breastfeeding Intervention Trial (PROBIT) cohort, in Walker SP, Chang SM, Powell CA, Simonoff E,
press. Grantham-McGregor SM. Early childhood stunting is
34 associated with poor psychological functioning in late
Deary IJ, Strand S, Smith P, Fernandes C. Intelligence
and educational achievement. Intelligence 2007;35:13–21. adolescence and effects are reduced by psychosocial
35
Alati R, Najman JM, O’Callaghan M, Bor W, stimulation. J Nutr 2007;137:2464–69.
50
Williams GM, Clavarino A. Fetal growth and behaviour Le Roith D. Insulin-like growth factors. N Engl J Med
problems in early adolescence: findings from the Mater 1997;336:633–40.
51
University Study of Pregnancy. Int J Epidemiol 2009;38: van Pareren YK, Duivenvoorden HJ, Slijper FS, Koot HM,
1390–400. Hokken-Koelega AC. Intelligence and psychosocial func-
36 tioning during long-term growth hormone therapy in
Birch LL, Fisher JO. Development of eating behaviors
among children and adolescents. Pediatrics 1998; children born small for gestational age. J Clin Endocrinol
101(3 Pt 2):539–49. Metab 2004;89:5295–302.
37 52
Kramer MS, Martin RM, Sterne JAC, Shapiro S, Gunnell D, Miller LL, Rogers I, Holly JM. Association of
Dahhou M, Platt RW. The ‘double jeopardy’ of clustered insulin-like growth factor I and insulin-like growth
measurement and cluster randomization. BMJ 2009;339: factor-binding protein-3 with intelligence quotient

Downloaded from https://academic.oup.com/ije/article/40/5/1215/657775 by guest on 15 June 2023


501–03. among 8- to 9-year-old children in the Avon
38
Yang S, Platt RW, Kramer MS. Variation in child cogni- Longitudinal Study of Parents and Children. Pediatrics
tive ability by week of gestation among healthy term 2005;116:e681–86.
53
births. Am J Epidemiol 2010;171:399–406. Baird J, Fisher D, Lucas P, Kleijnen J, Roberts H, Law C.
39
Silva A, Metha Z, O’Callaghan FJ. The relative effect of Being big or growing fast: systematic review of size and
size at birth, postnatal growth and social factors on cog- growth in infancy and later obesity. BMJ 2005;331:
nitive function in late childhood. Ann Epidemiol 2006;16: 929–34.
54
469–76. Monteiro POA, Victora CG. Rapid growth in infancy and
40
Gale CR, O’Callaghan FJ, Bredow M, Martyn CN. The childhood and obesity in later life - a systematic review.
influence of head growth in fetal life, infancy, and child- Obes Rev 2005;6:143–54.
55
hood on intelligence at the ages of 4 and 8 years. Huxley RR, Shiell AW, Law CM. The role of size at birth
Pediatrics 2006;118:1486–92. and postnatal catch-up growth in determining systolic
41
Martorell R, Horta BL, Adair LS et al. Weight gain in the blood pressure: a systematic review of the literature.
first two years of life is an important predictor of school- J Hypertens 2000;18:815–31.
56
ing outcomes in pooled analyses from five birth cohorts Belfort MB, Rifas-Shiman SL, Rich-Edwards J,
from low- and middle-income countries. J Nutr 2010;140: Kleinman KP, Gillman MW. Size at birth, infant
348–54. growth, and blood pressure at three years of age.
42 J Pediatr 2007;151:670–74.
Skuse D, Pickles A, Wolke D, Reilly S. Postnatal-growth
57
and mental-development - evidence for a sensitive-period. Ben-Shlomo Y, McCarthy A, Hughes R, Tilling K,
J Child Psychol Psychiatry 1994;35:521–45. Davies D, Davey Smith G. Immediate postnatal growth
43 is associated with blood pressure in young adulthood:
Drotar D, Nowak M, Malone CA, Eckerle D, Negray J.
Early psychological outcomes in failure to thrive: predic- the Barry Caerphilly Growth Study. Hypertension 2008;
tions from an interactional model. J Clin Child Psychol 52:638–44.
58
1985;14:105–11. Soto N, Bazaes RA, Pena V et al. Insulin sensitivity and
44 secretion are related to catch-up growth in small-
Kuh D, Ben-Shlomo Y, Lynch J, Hallqvist J, Power C. Life
course epidemiology. J Epidemiol Commun Health 2003; for-gestational-age infants at age 1 year: results from a
2003:778–83. prospective cohort. J Clin Endocrinol Metab 2003;88:
45
Batty GD, Shipley MJ, Gunnell D et al. Height, wealth, 3645–3650.
59
and health: an overview with new data from three lon- Victora CG, Barros FC, Horta BL, Martorell R. Short-term
gitudinal studies. Econ Hum Biol 2009;7:137–52. benefits of catch-up growth for small-for-gestational-age
46
Richardson SA, Birch HG, Grabie E, Yoder K. Behavior of infants. Int J Epidemiol 2001;30:1325–30.
60
children in school who were severely malnourished in Ong KK, Loos RJF. Rapid infancy weight gain and sub-
first 2 years of life. J Health Soc Behav 1972;13:276–84. sequent obesity: systematic reviews and hopeful sugges-
47
Richardson SA, Birch HG, Ragbeer C. Behavior of chil- tions. Acta Paediatr 2006;95:904–08.
61
dren at home who were severely malnourished in 1st 2 Barker DJP, Osmond C, Rodin I, Fall CHD, Winter PD.
years of life. J Biosoc Sci 1975;7:255–67. Low-weight gain in infancy and suicide in adult life. BMJ
48
Galler JR, Ramsey F. A follow-up-study of the influence 1995;311:1203–03.
62
of early malnutrition on development - behavior at home Victora CG, Adair L, Fall C et al. Maternal and child
and at school. J Am Acad Child Adolesc Psychiatry 1989;28: undernutrition: consequences for adult health and
254–61. human capital. Lancet 2008;371:340–57.

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