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,3
*
Carolina Population Center,
Department of Epidemiology, and
**
Department of Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, NC 27516
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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2 P = 0.000). Deficits in
children's scores were smaller at age 11 y than at age 8 y,
suggesting that adverse effects may decline over time. Results
emphasize the need to prevent early stunting and to provide adequate
schooling to disadvantaged children.
KEY WORDS: • developing countries • stunting • children • cognition • schooling
|
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Levitsky and Strupp 1995
, Wachs 1995
). Although many studies have
documented a relationship between early malnutrition and concurrent
performance on various tests of mental ability, it remains uncertain
whether the cognitive effects of early nutritional insults persist into
late childhood or adolescence (Grantham-McGregor 1995
,
Wachs 1995
). Lasting effects are likely to be manifested
as poor performance in school, and may have long-term implications
for well-being. This paper analyzes the relationship between
stunting and cognitive development in a cohort of Filipino children,
focusing on several dimensions of the relationship in which current
knowledge is limited.
The primary goal of this paper is to assess whether moderate or
severe stunting in the first 2 y is associated with poor
performance on cognitive tests in late childhood. Evidence of an
adverse relationship is fairly strong, albeit inconsistent, for severe
stunting (Grantham-McGregor 1995
); a link between more
moderate undernutrition and poor cognitive development is even less
certain (Wachs 1995
). A related objective is to evaluate
the importance of the persistence of early stunting for
cognitive development in late childhood. At present, it is not known
whether the cognitive deficits associated with undernutrition are
limited to children who remain persistently stunted from infancy into
late childhood, or whether deficits are also found among children who
later experience catch-up growth (i.e., those who are no longer
stunted) (Wachs 1995
).
The final dimension of stunting that will be assessed is the influence
of timing. Little is known about the importance of age of
onset of malnutrition for cognitive development
(Grantham-McGregor 1995
). Intervention research does not
suggest that there is a "critical period" in early infancy;
interventions initiated as late as 42 mo appear to be effective for
improving cognitive outcomes (Pollitt et al. 1995
,
Pollitt 1996
). In the absence of interventions, however,
children who first become stunted very early in infancy may be at
greater risk of adverse outcomes than those who become stunted later in
life.
Because stunting usually takes place in the context of multiple
psychosocial disadvantages, differences in the educational and
socioeconomic resources available to stunted and nonstunted children
must be taken into account to determine whether there is evidence of an
independent association between undernutrition and cognitive
development. Schooling is likely to be particularly important because
more time in school is strongly associated with higher scores on
cognitive tests (Ceci 1991
). Stunted children tend to
come from poor families and are likely to have lower quantities and
poorer quality of schooling than nonstunted children. Accordingly, an
additional objective is to estimate the confounding effect of schooling
and other aspects of the broader socioeconomic environment on the
relationship between stunting and intellectual development.
The issues to be addressed may be summarized in the following questions: 1) Is moderate or severe stunting in the first 2 y of life associated with performance on cognitive tests in late childhood? 2) Do the timing and persistence of stunting influence the severity of any effects? 3) Is there a meaningful association between early stunting and later cognitive ability after controlling for the confounding effects of schooling and other psychosocial factors?
Stunting, a measure of linear growth retardation, is a nonspecific
indicator of chronic undernutrition. Consequently, in interpreting this
analysis, it is important to keep in mind that stunting may be an
indicator of a broad range of insults (individually or in combination),
having such diverse origins as prenatal undernutrition, postnatal
deficiencies of energy or specific nutrients, infection or illness, and
inadequate attention or affection from care givers. Each of these has
also been hypothesized as a possible cause of poor cognitive
development in children (Brown and Pollitt 1996
,
Connally and Kvalsvig 1993
, Pollitt 1996
,
Zeitlin 1996
). The objective of this paper is to advance
understanding of the implications of the severity, timing and
persistence of early stunting from multiple causes for later cognitive
development, rather than to isolate effects of specific risk factors.
|
SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). A total of 2131 children had complete data on stunting at age 2 y and test scores at age 8 y; 2048 (96%) of these children also
had test scores at age 11 y.
|
, The Cebu Study Team 1991
). Cognitive ability.
The Philippines Non-Verbal Intelligence Test, a cognitive test
designed to assess fluid ability (i.e., analytic or reasoning skills),
was administered at both follow-up rounds (Guthrie et al. 1977
). The test comprises a series of 100 cards, each of which
contains drawings of five objects. The objects depicted are culturally
appropriate for the Philippines and include simple geometric shapes,
local farm animals and familiar activities of daily life such as
washing clothing. On each card, one object differs from the others in a
meaningful way; children are asked to indicate which of the five is
different. Time limits were not given for responding to each item.
Difficulty increases as children advance through the test. Typical
cards from early in the series are shown in Figure 1
.
|
), including correlations in a cohort of 11- to 13-y
old Filipino girls in which the Otis Lennon Mental Abilities Test was
used to measure IQ (Watkins and Astilla 1980
).
The psychologists who developed the cognitive test did not develop
age-specific norms, recommending instead that the test should be
used for within-sample comparative purposes (Guthrie et al. 1977
). We generated standardized scores (Z-scores) for the
cognitive scores at each age, which allowed us to compare the extent to
which the scores of stunted children deviated at each point in time
from those of nonstunted children. There was greater variability in the
earlier scores, although mean scores were 17 points higher at age
11 y than at age 8 y. A single SD represented
12.5 points on the raw scale score (maximum = 100) at age 8 y, and 11.6 points at age 11 y.
Stunting status.
Four measures of stunting status were used to assess the presence or
absence of any early stunting, the severity of early stunting, the
timing of incidence and the persistence of stunting into late
childhood. Previously published work has shown that the prevalence of
stunting increases cumulatively with increasing age in the CLHNS,
peaking at age 2 y (Adair and Guilkey 1997
). The
presence of early stunting was defined as a height-for-age Z-score
(HAZ) at age 2 y of <-2 based on the World Health Organization
reference data. Severe early stunting was defined as HAZ <-3;
moderate stunting as HAZ <-2 and 
-3. For the analysis of timing of
stunting, children were grouped into 6-mo intervals according to the
time interval between birth and age 2 y when they first became
stunted. In constructing the first interval, stunting status at birth
was excluded, because of its low prevalence (5%), and because most
children stunted at birth experienced rapid growth spurts, recovering
from stunting in the 1st mo of postnatal life. Finally, to assess the
importance of persistent stunting, we classified children on the basis
of their stunting status in the first 2 y, as well as at age
8 y. Children stunted both at or before age 2 y and at age
8 y (48%) were classified as "persistent"; those stunted at
or before age 2 y but not age 8 y (25%) were labeled as the
"catch-up" or recovery group; and those stunted at neither age
2 y nor age 8 y (24%) were classified as "neither." A
small number of children (4%) stunted for the first time after age
2 y were classified as "late incident."
Schooling.
Level of schooling was represented by the highest grade achieved when the cognitive test was taken. Because 32% of children in the sample repeated at least one grade (often as a result of excessive absenteeism or after dropping out temporarily), alternative measures such as total months in school and age at first enrollment were less meaningful as indicators of children's cumulative exposure to formal education.
Data analysis.
Mean test scores were calculated for children classified by stunting
status; differences in scores were assessed using t
tests (to compare two groups) or chi-square tests (for three or
more groups). Linear regression was used to assess the relationship
between early stunting and test performance. The effect of adjusting
for schooling and other covariates was estimated by running a series of
models as follows: crude, schooling adjusted and multivariate adjusted.
The basic model was as follows:
 |
where Cj represents a vector of
confounding variables, described below. The coefficient for stunting
status in these models represented the mean difference in the scores of
stunted children relative to nonstunted children, adjusted for other
variables in the model. Results are presented as coefficients and 95%
confidence intervals (CI). Separate models were run for each cognitive
score at ages 8 and 11 y. Dummy variables represent any stunting
at age 2 y (model 1), severity of stunting at age 2 (model 2),
timing of stunting incidence (model 3) and persistence of stunting from
the first 2 y through age 8 y (model 4). In addition to main
effects, interactions between stunting status variables and schooling
were assessed to determine whether the effect of schooling appeared to
differ among stunted vs. nonstunted children. All analysis was
conducted with the use of software from Stata (1997)
.
To account for differences in educational, health and social resources
that might confound the relationship between stunting and test
performance, we adjusted for several indices of socioeconomic status
(SES). These included household income quartile, highest grade
completed by mother and father, and type of settlement in which
household resides (urban squatter or rural remote, for example). These
variables represented SES during infancy and were therefore concurrent
with the stunting variables under study. Numerous studies suggest that
the early environment is particularly relevant for cognitive
development later in childhood (Brooks-Gunn and Duncan 1997
). Multivariate models also adjusted for change in
household income quartile over time (an indicator of SES mobility),
parity (used as an indicator of birth order), number of younger
siblings (to control for resource allocation among additional
dependents), maternal height (to account for inherited stature),
percentage of fat in the diet at age 8 y (an index of dietary
quality) and sex of the child. A dummy variable indicating whether the
child was in the care of the mother was also included. Interactions
between stunting and several covariates were tested to ensure that
there were no meaningful differences in the effect of stunting on the
performance of children with vs. without key characteristics that would
warrant the presentation of stratified rather than summary results.
Additional models were run to assess whether other variables might modify the association between stunting and cognitive development, including the following: 1) stratified by type of school (public vs. private, a proxy for school quality); 2) excluding children not enrolled in school; and 3) excluding children in the highest and lowest grade categories in which the number of children was sometimes small. Because mathematics draws on skills likely to be acquired in school, the inclusion of mathematics problems on the cognitive test may have overstated the importance of schooling relative to other factors. Models were therefore rerun using scores on the subset of questions that excluded the 18 mathematics problems. Models were also run after excluding children within ±0.2 SD of numbers used to define stunting status to ensure that results were not sensitive to the cutpoints selected. In all cases, results were very similar to those reported here.
The Heckman method (Heckman 1979
), a standard
econometric technique for evaluating selectivity bias, was used to
confirm that coefficients were not biased by loss to follow-up or
missing data. In addition, to ensure that attrition between the 1991
and 1994 rounds did not affect findings, models for cognitive test
performance at age 8 y were reestimated after restricting the
sample to the subset of children with data available for age 11 y.
Both strategies indicated that there was no bias.
|
RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The prevalence of early stunting was high, with 63% of children in the
sample stunted at age 2 y (Table 1)
. Of these, 43% were severely
stunted. Children stunted very early in infancy were more likely to be
severely stunted than those stunted later on. There was a
dose-response relationship between the timing (age at first onset)
and severity of stunting, i.e., the mean HAZ at age 2 y increased
from -3.44 among children stunted in the first 6 mo of infancy, to
-2.25 to those stunted between 18 and 24 mo.
About one third (34%) of children stunted at or before age 2 y
experienced catch-up growth (i.e., these children were no longer
stunted at age 8 y). The likelihood of persistent stunting vs.
catch-up by age 8 y was related to the severity of early
stunting. Children with persistent stunting had a mean HAZ of -3.10
SD at age 2 y, vs. -2.43 SD among those
with catch-up growth. Timing was also strongly associated with
persistence. For example, among 336 children stunted in the first 6 mo,
only 21 (6%) were no longer stunted at age 2 y. The correlation
between timing and persistence was high (Spearman's r
= 0.76). As is apparent from these data, children with very early
stunting tended to have severe and persistent stunting, making it
difficult to separate effects of timing from severity or persistence.
Additional analysis of catch-up growth in this cohort has been
reported elsewhere (Adair 1999
).
Unadjusted models.
Children stunted at age 2 y had significantly lower mean cognitive
test scores than nonstunted children, with greater differences at age
8 y than at age 11 y (Table 2
; model 1). There was a dose-response relationship between severity
of stunting and cognitive scores (Table 2
; model 2). At age 8 y,
children with severe early stunting had mean cognitive scores 0.61
SD below the mean for nonstunted children (P
< 0.000). This was more than twice the shortfall in children with
moderate stunting, whose mean scores were 0.25 SD lower
than those of nonstunted children (P < 0.001). Again,
deficits among children with either moderate or severe stunting were
smaller at age 11 than at age 8 y. The discrepancy in scores was
reduced over time because children stunted at age 2 y had
relatively large improvements in scores compared with nonstunted
children. Between age 8 y and age 11 y, the cognitive scores
of children stunted at age 2 y improved by an average of 18.3
points, compared with 16.9 points among nonstunted children
(t test P < 0.003).
|
; model 3). As with severity, there was a dose-response effect of
the timing of stunting. Compared with children never stunted in the
first 2 y, the cognitive scores of children stunted in the first 6
mo of infancy were 0.60 SD lower at age 8 y, and 0.47
SD lower at age 11 y (adjusted for stunting in other
6-mo intervals, P < 0.001). In contrast, the shortfall
in scores among children stunted later on, i.e., between 18 and 24 mo
of age, was 0.19 SD at age 8 y, and 0.08
SD at age 11 y.
Children with persistent stunting through age 8 y had
significantly lower cognitive test scores than children who were never
stunted, as well as children with catch-up growth (Table 2
; model
4). Children with catch-up growth also had significantly lower
scores than those who were never stunted, although deficits were more
moderate.
Relationship between stunting at age 2 y and schooling.
Children stunted in the first 2 y of life tended to start school
later than nonstunted children. Children who started school at age 5 or
6 y were substantially taller at age 2 y than children who
started school only at age 7 or 8 y (Fig. 2
). In addition, at age 11 y, children stunted at age 2 y were
3.0 (95% CI 1.5–5.8) times more likely to have dropped out of school
in the past, 1.8 (1.4–2.2) times more likely to have repeated a grade
and 1.2 (1.0–1.5) times more likely to have been absent in the month
before the interview date. As a result, on average, stunted children
had been in school for fewer months than nonstunted children at both
age 8 y (11.7 vs. 13.6 mo, t test P < 0.001) and age 11 y (42.4 vs. 44.5 mo, t test
P < 0.001).
|
). This association remained strong after controlling for SES and other
covariates. Thus part of the apparent effect of stunting on cognitive
scores was attributable to the lower level of schooling received by
children stunted in early life.
|
Adjusting for schooling substantially attenuated the deficits in
cognitive scores associated with stunting in the first 2 y (Table 2
, column 2). Despite this attenuation, the association between
stunting at age 2 y and later cognitive scores remained
significant. The dose-response relationship between the severity of
early stunting and later cognitive ability also persisted after
adjusting for schooling. As before, the deficit in cognitive test
scores associated with stunting at age 2 was consistently smaller at
age 11 y than at age 8 y, regardless of the severity of early
stunting (Table 2
, model 2). Similarly, the dose-response effect of
the timing of stunting was attenuated in the schooling-adjusted
models for cognition at both ages (Table 2
, model 3). Deficits in
cognitive scores associated with persistent stunting and early stunting
with catch-up by age 8 y were also significant, albeit
attenuated, after this adjustment (Table 2
, model 4).
No interaction between schooling and stunting.
Interactions between schooling and each stunting status variable were
included in the multivariate models; none were significant. The lack of
a significant interaction indicates, as shown in Figure 3
, that the
effect of increased schooling on cognitive test scores was similar
among stunted and nonstunted children.
Multivariate-adjusted models.
Further adjustment for SES and other covariates considerably
reduced the association between early stunting and later cognitive
scores. Even after multivariate adjustment, stunting at age 2 y
was associated with significant deficits in cognitive test Z-scores
at age 8 y (-0.14 SD) (Table 2)
. By age 11 y,
however, the shortfall in cognitive scores among children stunted at
age 2 y was small and nonsignificant (-0.05 SD).
Although moderate stunting at age 2 y was no longer associated
with meaningful deficits in cognitive ability at either age 8 or
11 y, severe stunting at age 2 y was associated with
significant deficits in cognitive test performance at both ages even
after multivariate adjustment. In contrast, neither very early onset of
stunting nor persistent stunting was associated with significant
shortfalls in cognitive test performance by age 11 y in the
multivariate models (Table 2)
.
Severity vs. timing or persistence of early stunting.
To better evaluate the role of severity vs. the timing of incidence or
persistence of early stunting, children were cross-classified based
on both severity and timing and severity and persistence (see
Table 3
). Analysis using this cross-classification (see Table 4
) suggested that the severity of early stunting was more important than
either timing of incidence or persistence. Children with severe
stunting had substantial deficits in cognitive scores regardless of the
timing of incidence, whereas deficits among children with moderate
stunting incident in any time interval were negligible. Similarly,
children with severe early stunting had significant deficits in
cognitive scores relative to children never stunted through age 8 y, regardless of whether they were persistently stunted or experienced
catch-up growth.
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|
Models were also run to assess the association between stunting and performance on Mathematics and English achievement tests. Results were consistent with the findings for cognitive test performance, i.e., severity and very early onset of stunting were associated with substantial deficits in test scores. To further evaluate the importance of the timing of stunting, children were also classified on the basis of the prevalence of any stunting during each 6-mo interval. The results obtained using prevalent rather than incident stunting were similar. Supplementary analysis was also conducted to assess whether prenatal growth was associated with the cognitive scores. Neither stunting status at birth nor small size for gestational age was significantly associated with deficits in test scores. This could be attributable in part to the small proportion of children with these exposures in this sample.
|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Martorell et al. 1992
).
Stunting in the first 2 y was more strongly associated with
cognitive test performance at age 8 y than at age 11 y,
suggesting that the effects of early undernutrition on cognitive
abilities may decline over time, even among severely stunted children.
Gradual declines in the effects of early malnutrition on cognition have
been reported previously, and suggest that the effects of early
undernutrition may be largely a result of delay rather than permanently
impaired mental development (Cravioto and Cravioto 1996
,
Pollitt 1996
). Over time, schooling and other learning
experiences may attenuate the effects of early undernutrition on
cognition (Pollitt 1996
).
Although each dimension of stunting in early life assessed in this
paper was associated with children's test scores at age 8 y, only
severe stunting appeared to have lasting effects at age 11 y;
these effects were independent of differences in educational,
socioeconomic and psychosocial resources. Several other studies have
reported associations between severe malnutrition in early childhood
and poor performance on tests of intellectual functioning in later
childhood (Galler et al. 1983
, Sigman et al. 1991
), adolescence (Stoch and Smythe 1976
) and adulthood (Grantham-McGregor 1995
, Martorell et al. 1992
). At present, few
studies have investigated the long-term consequences of moderate
stunting in infancy and early childhood (Wachs 1995
).
This study suggests that by age 11 y, direct effects of moderate
undernutrition in early life on children's intellectual development
may not be independent of schooling and other socioeconomic and
psychosocial factors.
Although the association between timing of stunting and cognitive test
scores was not significant after multivariate adjustment, this study
suggests that it is particularly important to prevent very early
stunting to protect children's cognitive development. Early stunting
is critical largely because it increases risk of severe, persistent
stunting. i.e., 67% of children stunted in the first 6 mo were
severely stunted at age 2 y, and another 26% were moderately
stunted; 80% of children stunted by mo 6 remained stunted at age
8 y. As shown in Table 4
, persistence appears to be less important
for basic cognitive ability than the severity of early stunting and
differences in educational, socioeconomic and psychosocial resources
made available to stunted children. Children with severe early stunting
had meaningful deficits in cognitive scores regardless of whether
stunting persisted through age 8 y or children experienced
catch-up growth.
As expected, reduced schooling was an important factor contributing to
the poor intellectual development of children stunted in the first
2 y of life. After adjusting for schooling, associations between
stunting in the first 2 y and later cognitive development were
strongly attenuated. In this cohort, children stunted at age 2 y
had a marked delay in initial school enrollment and were much more
likely to experience absences and to drop out of school than nonstunted
children. Deficiencies in educational flow may reflect poorer health.
They may also be attributable to greater ability and motivation among
higher SES parents to initiate and maintain children's schooling.
Perhaps, as suggested by Brown and Pollitt (1996)
,
parents may tend to enroll well-nourished children who appear more
alert and ready for schooling earlier than children who seem small and
poorly developed. Essentially, stunted children may be treated
differently from nonstunted children because they are smaller and often
appear younger than their age (Brown and Pollitt 1996
).
Differences in schooling experiences played an important role in
explaining cognitive score deficits among moderately stunted children.
Like children with severe early stunting, children with moderate
stunting at age 2 y received significantly less schooling than
nonstunted children (2 P = 0.000). However, differences in schooling did not explain why moderate
stunting was not associated with significant deficits in cognitive
scores after multivariate adjustment. Coefficients for moderate
stunting were not significant even after dropping schooling from
multivariate models.
The absence of significant interactions between level of schooling and
stunting in the first 2 y in models predicting cognitive scores
indicates that the gains in basic cognitive ability associated with
schooling exposure are similar for stunted and nonstunted children
(Fig. 3)
. Earlier studies have also suggested that schooling may act as
a buffer against the effects of poverty and malnutrition on
intellectual development (Gorman and Pollitt 1996
).
Ensuring that children with early stunting receive schooling comparable
in quantity and quality to that received by nonstunted children may
help to improve their cognitive development.
Although schooling was associated with improved cognitive scores,
adjusting for schooling did not eliminate the adverse effects of severe
early stunting on cognitive or achievement test scores. This suggests
that other mechanisms may be important. In addition to lower levels of
schooling, chronic undernutrition (manifested in stunting) early in
life may affect later intellectual development via deficiencies of
nutrients such as vitamin B-6 or iron, which are vital for brain
function (Guilarte et al. 1993
, Pollitt 1997
). In extreme cases, malnourished children may suffer from
brain damage (Brown and Pollitt 1996
,
Grantham-McGregor 1995
). As a result of their poor
physical development, stunted children may also have delayed
development of motor skills. This could affect their ability and
interest in exploring their environment, delaying their intellectual
development (Brown and Pollitt 1996
,
Grantham-McGregor 1995
). Children who are persistently
malnourished may have little energy to learn in the classroom
(Brown and Pollitt 1996
). Finally, a number of
nondietary influences on child development exist, including parental
attention and affection, as well as risk of infection or illness
(Connally and Kvalsvig 1993
, Monckeberg 1992
).
This study suggests that optimizing healthy growth in early life is important for the intellectual development of children in developing countries. The study also makes it clear, however, that other aspects of children's early environment—most notably adequate schooling—are also critical. Although the association between stunting status and children's test scores was significant, stunting variables explained only 3–6% of the variance in these models (the R2 varied depending on the outcome and stunting variables used). Incorporating schooling and other covariates increased the R2 to nearly 40%. However, a substantial proportion of the variance remained unexplained by these models; we were unable to account for important factors such as inherited ability and differences in the quality of care and stimulation.
In summary, this analysis suggests that there may be a direct effect of severe chronic undernutrition in early life on cognitive development later in childhood, independent of psychosocial factors such as schooling and SES. It is unclear whether these deficits represent developmental delays that may persist into adolescence or adulthood, rather than permanent impairment. Children with severe stunting at age 2 y appeared to sustain these cognitive deficits through age 11 y, regardless of when they first became stunted. These deficits persisted even when children had recovered from early stunting. The fact that both moderately and severely stunted children received significantly less schooling than nonstunted children suggests that there are important indirect effects of chronic undernutrition; that is, the effect of early stunting is mediated in part through reduced schooling. Thus, although direct effects of moderate stunting on children's performance may not be significant, there may well be significant indirect effects mediated through changes in educational flow. Future research should focus on the indirect as well as the direct effects of children's nutritional status on cognitive development.
|
FOOTNOTES |
|---|
2 The Cebu Longitudinal Health and Nutrition
Survey is a collaborative project with the Office of Population Studies
of the University of San Carlos. Data collection for the follow-up
surveys was supported by grants from The World Bank and The Asian
Development Bank.
4 Abbreviations used: CI, confidence interval;
CLHNS, Cebu Longitudinal Health and Nutrition Survey; HAZ,
height-for-age Z-score; SES, socioeconomic status.
Manuscript received June 29, 1998. Initial review completed November 25, 1998. Revision accepted April 27, 1999.
|
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