The Journal of Nutrition

Community and International Nutrition

Children Who Recover from Early Stunting and

Children Who Are Not Stunted Demonstrate
Similar Levels of Cognition1,2
Benjamin T. Crookston,3* Mary E. Penny,4 Stephen C. Alder,3 Ty T. Dickerson,5 Ray M. Merrill,6
Joseph B. Stanford,3 Christina A. Porucznik,3 and Kirk A. Dearden7
3
Department of Family and Preventive Medicine, University of Utah, Salt Lake City, UT 84108; 4Instituto de Investigación Nutricional,
La Molina, Lima-12, Peru; 5Department of Pediatrics, University of Utah, Primary Children’s Medical Center, Salt Lake City, UT 84113;

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6
Department of Health Sciences, Brigham Young University, Provo, UT 84602; and 7Department of International Health and Center for
Global Health and Development, Boston University, Boston, MA 02118

Abstract
Stunting is associated with adverse cognitive development in childhood and adolescence, fewer years of schooling,
decreased productivity, and reduced adult stature. Recovery from early stunting is possible; however, few studies explore
whether those who demonstrate linear catch-up growth experience long-term cognitive deficits. Using longitudinal data
on 1674 Peruvian children from the Young Lives study, we identified factors associated with catch-up growth and
assessed whether children who displayed catch-up growth have significantly lower cognition than children who were not
stunted during infancy and childhood. Based on anthropometric data for children 6–18 mo of age and again for the same
children when they were 4.5–6 y of age, we categorized participants as not stunted, stunted in infancy but not childhood
(catch-up), stunted in childhood, and stunted in infancy and childhood. Children who had grandparents in the home, had
less severe stunting in infancy, and had taller mothers were more likely to demonstrate catch-up growth by round 2.
Children who experienced catch-up growth had verbal vocabulary and quantitative test scores that did not differ from
children who were not stunted (P = 0.6 and P = 0.7, respectively). Those stunted in childhood as well as those stunted in
infancy and childhood scored significantly lower on both assessments than children who were not stunted. Based on
findings from this study, policy makers and program planners should consider redoubling efforts to prevent stunting and
promote catch-up growth over the first few years of life as a way of improving children’s physical and intellectual
development. J. Nutr. 140: 1996–2001, 2010.

Introduction
mean and is often categorized as mild (22 to 21 SD), moderate
Undernutrition contributes to more than one-half of the nearly (22 to 23 SD), and severe (, 23 SD) (4).
10 million childhood deaths that occur annually (1,2). Stunting For many countries in resource-poor settings, mean HAZ at
affects 150 million (24%) of all children worldwide (3). Stunting birth is close to the National Center for Health Statistics
is defined as a height-for-age Z-score (HAZ)8 , 22 SD from the reference score but begins faltering immediately after birth and
continues into the 3rd y of life (5). A majority of stunted children
become stunted adults (6).
1
Stunting is associated with adverse cognitive development in
Supported by the UK Department for International Development (DFID) for the
childhood and adolescence, delayed entrance into school, fewer
benefit of developing countries (core-funding for Young Lives). Substudies are
funded by the Bernard van Leer Foundation, the Inter-American Development years of schooling, decreased productivity, and reduced adult
Bank (in Peru), the International Development Research Centre (in Ethiopia), and stature (4,7–11). Stunting during childhood is associated with
the Oak Foundation. The views expressed here are those of the authors. They delays in motor development and lower IQ (12). Stunted
are not necessarily those of the Young Lives project, the University of Oxford, children are less likely than their nonstunted counterparts to
DFID, or other funders. Additional funding for this research came from the
University of Utah, the Instituto de Investigación Nutricional, Brigham Young
enroll in school; those who do enroll have lower grades and
University, and Boston University. poorer cognition (13,14).
2
Author disclosures: B. T. Crookston, M. E. Penny, S. C. Alder, T. T. Dickerson, Subsequent to growth faltering during the first 3 y, children
R. M. Merrill, J. B. Stanford, C. A. Porucznik, and K. A. Dearden, no conflicts of from resource-poor countries grow at rates similar to children
interest.
8
from more affluent nations, neither losing additional ground nor
Abbreviations used: CDA, Cognitive Development Assessment; HAZ, height-
for-age Z-scores; PPVT, Peabody Picture Vocabulary Test.
experiencing substantial recovery (5,12). There is no established
* To whom correspondence should be addressed. E-mail: benjamin.crookston@ definition for “catch-up growth.” (15). It can refer to acceler-
utah.edu. ation of growth or partial or complete recovery from stunting
ã 2010 American Society for Nutrition.
1996 Manuscript received November 16, 2009. Initial review completed December 28, 2009. Revision accepted August 11, 2010.
First published online September 15, 2010; doi:10.3945/jn.109.118927.
(15,16). We use HAZ for this study, and we define catch-up up. Data from both rounds were entered for analyses using Delphi
growth as HAZ , 22 during infancy (;1 y of age) and $ 22 software.
during childhood (;5 y of age) (9,15,17). Cognitive outcomes. This study used the Peabody Picture Vocabulary
Some consider the likelihood of catch-up growth to be Test (PPVT) to evaluate vocabulary skills and listening comprehension
limited, because children remain in environments that contribute and the Cognitive Development Assessment (CDA) to judge the
to growth restriction (17–20). A few studies show that partial quantitative reasoning of children 4.5–6 y of age. The PPVT is a
catch-up is possible among stunted children who remain in the commonly used measure for evaluating cognitive development in both
same environment (15,21–23). Identifying factors that allow industrialized and resource-poor countries (27–30). The PPVT is highly
children to catch up is important for developing programs to correlated with the Wechsler and McCarthy Scales, which are validated
improve nutrition and health. measures of intelligence (31–33). A validated, Spanish version of the
We tested the hypothesis that children who experience catch-up PPVT consisting of 125 questions was given to children participating in
the study (34,35).
growth have significantly lower scores on 2 cognitive assessments
The CDA was developed by the International Association for the
than children who were not stunted in infancy and childhood. Evaluation of Educational Achievement to study the effect of preschool
We also identified factors associated with catch-up growth. attendance on cognitive development in children 4 y of age (36). The
CDA has 3 main components: quantity, time, and spatial relations. Due
to the great amount of time it took to administer (spatial relations

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Methods subtest) and low reliability among the Young Lives sample in Peru (time
subtest), only the quantity subtest was used in the study. The quantity
Study design and background. This study assessed a prospective subtest relies on 15 items to measure a child’s perception of amount. For
cohort of children who are part of a multicountry study called Young each item, interviewers show children images and ask a question such
Lives. The Young Lives study, which is funded by the United Kingdom’s as “Look at the cats and dogs and point to the picture where the dog
Department for International Development, explores childhood poverty, has less food than the cat.”
intergenerational poverty, and poverty reduction policies. Two cohorts It is possible that because the CDA was developed for children 4 y of
of children (1 and 8 y old) from Ethiopia, India, Peru, and Vietnam have age, it might not be an appropriate measure of cognition for children
been followed since 2002 with the intent to track the children for 15 y. older than 4 y. We compared the mean raw and Rasch scores for the CDA
Our study examines catch-up growth following early stunting among the from children without preschool, with preschool, and currently attend-
younger Peruvian cohort. Researchers from the Instituto de Investigación ing first grade. Rasch scores are used extensively in psychometrics and
Nutricional and Grupo de Analisis para el Desarrollo manage the increasingly in public health. Researchers use them to determine the
Peruvian cohort. quality of tests and to build true interval-scale measures based on raw
scores (37). With Rasch scores, one can judge the degree to which
Study participants. A detailed description of methods for this study has measurement has been successful. Rasch scores are based on a
been given elsewhere (24). Briefly, a total of 2052 children from 74 probability model that when a group of individuals is asked multiple
communities representing 20 districts in Peru were enrolled in 2002. As questions, e.g. as part of a cognitive assessment, individual j makes a
an initial step, we assembled a complete list of all districts in the country, mistake in answering question k.
excluding the 5% with the highest socioeconomic levels. To determine As expected, data from Young Lives suggest that children who had
socioeconomic levels, we ranked the 1818 districts in Peru according to a formal schooling performed better on the test than children who never
composite index of poverty (25). Using national census data, the size of attended preschool. Similarly, the longer children spent in preschool, the
the population for all districts was noted. The total population was higher the score. While test scores improved with increased levels of
divided by 2000 to establish the sampling interval and a random number education, we conclude that the CDA was an appropriate measure for
within the sampling interval was selected to determine the initial district. children 4.5–6 y of age, as noted below.
To identify the subsequent district, we added the total number of Items in the PPVT and the CDA are arranged in order of increasing
individuals in the sampling interval to the initial starting point and difficulty. A given child received only those items within his or her critical
continued in this fashion until all 20 districts were identified. Once the 20 range based on chronological age and ceiling. We reviewed all observa-
districts were chosen, we randomly selected a community and a specific tions to verify that basal and ceiling sets were correctly established for
house within the community. In many cases, there were ,100 children each child (36). Not all distributions of raw and Rasch scores were
aged 6–17.9 mo in a given community. In such cases, the closest normal. In rare cases, children achieved close to the highest possible
community was selected in systematic fashion until 100 families per score. Thus, test scores may have underestimated children’s abilities for
district were enrolled. Urban areas were subdivided into city blocks. The the construct measured. This appears to be a very infrequent occurrence.
sample represents ~95% of Peruvian children, includes participants from For example, only 1 child obtained a perfect score on the CDA.
urban and rural areas, and represents coastal, highland, and jungle regions. Validity and reliability for both tests were established by assessing the
Institutional review boards from London South Bank University, degree to which evidence and theory supported the interpretations of test
London School of Hygiene and Tropical Medicine, and the University of scores. Reliability was established according to Classical Test theory and
Reading approved of this research. Within Peru, the Ministry of Health Item Response theory. Details about the establishment of validity and
approved of the study. Ethical reviews were conducted by the Institutional reliability can be found elsewhere (36). For children who were native
Review Boards at the Instituto de Investigación Nutricional and the Spanish speakers, both tests were found to have appropriate psycho-
Peruvian Instituto Nacional de Salud. metric properties. However, each test proved unreliable for assessing
cognition among native Quechua speakers. Thus, only Spanish-speaking
Data collection. Interviews consisted of a core questionnaire for children (n = 1706) were included in the analysis. We used standardized
primary caregivers and included questions regarding household compo- scores for both the PPVT and the CDA.
sition, child health, caregiver characteristics, livelihoods, socioeconomic
status, social capital, childcare, and cognitive development. Field- Catch-up growth. Catch-up growth was examined both as an outcome
workers collected anthropometric data using digital scales (Soehnle) variable and as a determinant of cognitive scores. We defined “stunted in
and locally made wooden boards and measurement techniques were infancy but not childhood” (catch-up) as having a HAZ , 22 during
standardized per WHO guidelines (26). Fieldworkers were trained for 3 round 1 and a HAZ $ 22 at round 2 (i.e. during infancy but not
mo in data collection protocols and instruments. Based on a pilot study, childhood), “stunted in infancy and childhood” as having a HAZ , 22
instruments were revised. Three teams of 6 interviewers per team at rounds 1 and 2, “stunted in childhood” as having a HAZ $ 22 during
collected 2 rounds of data in 2002 when children were 6–17.9 mo of age round 1 and a HAZ , 22 at round 2, and “not stunted” as having
(round 1) and 2006–2007 when they were 4.5–6 y old (round 2). There HAZ $ 22 at both rounds (9,15,17). We used information from all
are 2052 children in the cohort. Only 4% of children were lost to follow- children when evaluating catch-up growth as a predictor of cognitive

Catch-up growth and improved cognition 1997

scores. When considering determinants of catch-up growth, we used data were tested for interaction and compliance with logistic and linear
only from children with a HAZ , 22 at round 1. Our assessment of regression model assumptions. No interaction terms were retained based
changes in nutritional status was based on data collection at 2 points in on P , 0.1. Significance was declared when P , 0.05.
time. We do not know whether children were stunted before round 1 or
between rounds 1 and 2.
Results
Covariates. Covariates were chosen based on results from an earlier Children’s mean age at round 1 was 12 (6 3.5) mo. Slightly less
study using Young Lives data, which used a well-known conceptual than one-half (49.5%) were female and only a few (1.0%) had
framework for the determinants and consequences of undernutrition begun formal schooling by round 2. A majority (74.1%) lived in
(24,38). Covariates included: urban/rural setting; geographic region urban areas. Highland and coastal regions had the greatest
(coast/highland/jungle); child’s age, sex, and preschool attendance; and
proportion of study participants, 43.0 and 40.2%, respectively.
maternal age, height, education, and ethnicity. Severity of stunting was
The remaining respondents lived in jungle regions (16.8%).
used when considering determinants of catch-up growth, where only
children with a HAZ , 22 at round 1 were examined. In this instance, Most mothers described themselves as mestizo (91.9%), with
severity of stunting was the HAZ for a given child. Thus, the lower the the principal religion being Catholicism (80.2%). Two-thirds
HAZ, the more severe the stunting experienced by the child. A composite (63.8%) of children were not stunted in either round 1 or round
indicator of wealth ranging from 0–1 reflected consumer durables, 2, whereas 8.4% were stunted at round 1 but not round 2 and

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services, and housing quality (39). were considered to have experienced catch-up growth, 13.4%
were stunted at round 2 only (childhood), and 14.4% were
Data analysis. Anthropometric indicators were calculated using the stunted in both infancy and in childhood.
latest WHO International Growth Reference standard (26). SAS (version Children classified into these 4 categories differed signifi-
9.2) was used for statistical analyses. Pearson chi-square tests compared cantly with respect to sex, region, area of residence, preschool
distributions among stunting classifications; F tests compared means attendance, and sociodemographic conditions (Table 1). More
among groups.
males than females experienced catch-up growth. Children from
For analyses, we used mixed regression models to account for the
rural areas made up one-half of those stunted in infancy and
cluster sample design. The MIXED procedure from SAS was used for
linear models (cognitive outcomes) and the GLIMMIX procedure was childhood but only one-quarter of the overall sample. Mean
used for logistic models (catch-up growth outcomes). Covariates were wealth index was highest among those who were not stunted,
retained or dropped based on P-values (,0.1) and conceptual consid- followed by children experiencing catch-up growth.
erations. Regression coefficients (linear models), odds ratios (logistic Change in HAZ between rounds 1 and 2 differed by stunting
models), and 95% CI were calculated for retained variables. All models classification as follows: catch-up growth, 1.13 6 0.66; stunted

TABLE 1 Characteristics of study participants by stunting classification1

Independent Not Stunted in Stunted in infancy

variable2 stunted3 Catch-up4 childhood5 and childhood6 P-value7

n 1065 140 224 240

Sex, % 0.0001
Male 49.9 64.3 38.8 56.7
Female 50.1 35.7 61.2 43.3
Region, % 0.0001
Coast 50.9 30.7 25.5 12.9
Highland 34.6 53.6 52.7 64.2
Jungle 14.6 15.7 21.9 22.9
Area, % 0.0001
Urban 83.5 79.3 52.7 49.6
Rural 16.5 20.7 47.3 50.4
Attended preschool, % 0.0001
Yes 90.4 90.0 75.5 75.4
No 9.6 10.0 24.6 24.6
HAZ score (round 1) 20.6 6 0.9 22.6 6 0.5 21.1 6 0.8 22.8 6 0.7 0.0001
HAZ score (round 2) 20.9 6 0.8 21.4 6 0.5 22.5 6 0.5 22.8 6 0.6 0.0001
Child age, mo 11.8 6 3.5 13.8 6 3.2 10.9 6 3.4 13.1 6 3.5 0.0001
Maternal age, y 26.5 6 6.3 27.5 6 7.2 26.0 6 6.4 27.5 6 7.5 0.0366
Maternal height, cm 151.3 6 5.2 150.0 6 4.5 149.0 6 5.6 147.1 6 4.9 0.0001
Wealth index 0.47 6 0.20 0.44 6 0.20 0.33 6 0.19 0.29 6 0.18 0.0001
Maternal education, y 9.7 6 3.6 8.3 6 4.3 7.3 6 3.7 6.1 6 4.0 0.0001
Verbal vocabulary 95.9 6 19.9 90.2 6 20.3 82.1 6 19.0 76.9 6 18.3 0.0001
Quantitative score 10.9 6 2.2 10.9 6 2.1 9.4 6 2.7 9.4 6 2.6 0.0001
1
Values are mean 6 SD or %.
2
Data reported in table are from round 1 (when child was 6–18 mo of age) except for verbal vocabulary and quantitative score.
3
Not stunted: HAZ $ 22 at rounds 1 and 2.
4
Catch-up: HAZ , 22 at round 1 and HAZ $ 22 at round 2.
5
Stunted in childhood: HAZ $ 22 at round 1 and HAZ , 22 at round 2.
6
Stunted in infancy and childhood: HAZ , 22 at round 1 and at round 2.
7
Chi-square and F tests compare percents and means for each stunting classification for each independent variable.

1998 Crookston et al.

TABLE 2 Odds ratios from logistic regression model for catch- had significantly lower scores on the verbal vocabulary test.
up growth (1 = yes, 0 = no) among Peruvian children Children who had older mothers and mothers with more
who experienced stunting in infancy (n = 374) education, and children who lived in urban areas, attended
preschool, had fewer siblings, and came from better socioeco-
Independent variable1 Odds ratio P-value 95% CI
nomic conditions scored higher on the verbal vocabulary
Area population assessment.
Rural 1.00 0.08 – Differences between quantitative scores for the not stunted
Urban 1.70 0.94, 3.08 and catch-up groups did not differ (P = 0.7) (Table 5), but
Maternal education in y 1.06 0.07 1.00, 1.13 children who were stunted in childhood or stunted in infancy
Preschool attendance and childhood had significantly lower quantitative scores.
No 1.00 0.06 – Children who were older at round 1, had older mothers or
Yes 2.03 0.98, 4.17 mothers with more education, lived in urban areas, attended
Child age in mo 1.14 0.0006 1.05, 1.18 preschool, had fewer siblings, and came from better socioeco-
Grandparents live in home nomic conditions scored significantly better on the quantitative
No 1.00 0.04 – assessment.
Yes 1.89 1.05, 3.40

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Severity of stunting (HAZ at round 1)2 2.10 0.0009 1.36, 3.25 Discussion
Maternal height Z-score 1.66 0.0002 1.28, 2.17
Results suggest that one-third of children who were stunted in
1
Data reported in table come from round 1 (when child was 6–18 mo of age) except
infancy (at 1 y of age) recovered by the time they were 5 y old.
preschool attendance and child age.
2
HAZ at round 1 is a continuous variable.
Those who demonstrated catch-up growth had cognitive test
scores similar to children who were not stunted at either age.
These results are important because they demonstrate that
in childhood, 21.38 6 0.96; not stunted, 20.28 6 0.85; and children can recover from early nutritional insult, identify
stunted in infancy and childhood, 0.02 6 0.76. Changes in HAZ predictors of catch-up growth, and suggest that catch-up growth
for children demonstrating catch-up growth, those stunted in contributes to cognition. These findings can guide future
childhood only, and those not stunted were significantly differ- research about the impact of stunting on cognition as well as
ent from children who were stunted in infancy and childhood. policy and program efforts to improve children’s physical and
We conducted logistic regression to identify determinants of intellectual well-being.
catch-up growth, limiting our analyses to children with HAZ ,
22 at round 1 (Table 2). Predictors of catch-up growth included Potential for catch-up growth. The proportion of stunted
maternal height, child age at round 2, grandparents living at children who experienced catch-up growth (36.8%) is consistent
home, and severity of stunting in round 1. Severity of stunting with findings from previous research (9,15,17,40,41). In a study
was the most important predictor of catch-up growth; children of 2131 Filipino children, researchers reported that 34% of
who were less stunted at round 1 (i.e. higher HAZ) were more stunted children experienced catch-up growth by 8 y of age (18).
likely to experience catch-up growth. It is worth pointing out More than one-half of 239 Peruvian children in Lima who were
that although not significant, area of residence, maternal stunted in the first 2 y exhibited catch-up growth by 9 y (9). These
education, and preschool attendance were retained in the model studies used similar methods for collecting anthropometry and
for conceptual reasons (P , 0.10). defining catch-up growth. But the timing of assessment, cognitive
Estimates for unadjusted regression models predicting verbal tests administered, and setting differed from our study. The
vocabulary and quantitative scores are reported in Table 3. For severity of stunting varied across studies discussed here. Finally,
verbal vocabulary scores, the reference group (not stunted) the magnitude of recovery (1.13 SD) in our catch-up group was
scored significantly higher than the 3 comparison groups. nearly identical to that described by Adair (15) (1.14 SD).
However, for quantitative cognition, children who were not
stunted and those who demonstrated catch-up growth did not Predictors of catch-up growth. According to our results,
differ (P = 0.5). children with higher HAZ at initial assessment (i.e. children who
When adjusted for maternal age and education, area of experienced less severe stunting) were more likely to experience
residence, preschool attendance, wealth index, and number of catch-up growth. Others (15,17,22) also report that higher HAZ
siblings, verbal vocabulary scores did not differ between the not at initial assessment improves the chances of experiencing catch-
stunted and catch-up groups (Table 4). However, children who up growth, although variables included in their models differ
were stunted in childhood or stunted in infancy and childhood somewhat from ours. Additional factors associated with catch-

TABLE 3 Unadjusted differences in cognitive scores by stunting status in infancy and early childhood
among Peruvian children (n = 1674)

Verbal vocabulary score Quantitative score

Characteristics Estimate P-value 95% CI Estimate P-value 95% CI

Intercept 92.33 ,0.0001 87.17, 97.49 10.64 ,0.0001 10.20, 11.08

Not stunted – – – – – –
Catch-up 23.15 0.04 26.18, 20.12 0.14 0.50 20.26, 0.53
Stunted in childhood 26.21 ,0.0001 28.77, 23.67 20.91 ,0.0001 21.24, 20.59
Stunted in infancy and childhood 210.03 ,0.0001 212.57, 27.49 20.86 ,0.0001 21.19, 20.54

Catch-up growth and improved cognition 1999

TABLE 4 Estimates from mixed linear regression model for deficit between children who were not stunted and children who
predictors of verbal vocabulary score among Peruvian experienced catch-up growth (9,17). Although Berkman (9)
children (n = 1649) documented differences in cognition between children who were
stunted in infancy and childhood and children who were not
Independent variable1 Estimate P-value 95% CI
stunted during either period, he found no differences in
Intercept 59.0 ,0.0001 53.2, 64.9 cognition between children who were not stunted and children
Stunting who demonstrated catch-up growth, even after adjusting for
Not stunted – – – covariates. Mendez and Adair (17) found moderate differences
Catch-up 20.7 0.62 23.5, 2.1 in cognition between children who had catch-up growth and
Stunted in childhood 22.5 0.04 24.8, 20.1 those who were not stunted but found no difference when
Stunted in infancy and childhood 24.6 0.0002 27.0, 22.2 adjusting for many of the same confounding factors used in this
Maternal age in y 0.3 0.0001 0.1, 0.4 study, such as number of siblings, area population (urban vs.
Maternal education in y 1.4 ,0.0001 1.2, 1.7 rural), maternal education, and wealth. Given the apparent lack
Area population of difference in cognitive scores between those who experienced
Rural – – – catch-up growth and those who were never stunted, children
Urban 4.5 0.002 1.7, 7.3 who were at greatest risk of cognitive deficits were those who did

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Preschool attendance not experience catch-up growth after stunting in infancy (41).
No – – – This study has limitations. First, there is no standard
Yes 3.9 0.002 1.5, 6.3 definition for catch-up growth; thus, our interpretations may
Wealth index 21.1 ,0.0001 14.0, 28.2 be different from those in other studies. However, we used a
Number of siblings 21.2 0.0002 21.9, 20.6 definition that was employed by 3 other authors (15,17,22) and
our results are consistent with findings where the same definition
1
Data reported in table come from round 1 (when child was 6–18 mo of age) except
was used. Second, our sample is not nationally representative;
preschool attendance, wealth index, and number of siblings.
we were unable to include non-Spanish speakers, because each
test proved unreliable for assessing cognition among non-
Spanish speakers. Third, we have measures at only 2 points in
up growth included child’s age at second assessment, maternal
time and therefore do not have measures of the frequency or
height, and grandparents living in the home. Although child’s
duration of stunting. Thus, it is not possible to determine
age and presence of grandparents in the home cannot be changed
whether lack of cognitive impact in childhood (round 2) is due to
by program planners and implementers, maternal height is
catch-up growth alone or whether differences in the severity,
amenable to improvement and should be considered as one
frequency, and duration of stunting as well as access to
option among several that can improve the potential for catch-
interventions designed to improve nutritional status account
up growth.
for this effect. For example, some infants at round 1 may have
been moderately stunted only once (i.e. only at the time of data
Catch-up growth and cognition. Our results are different
collection).
from previous research that suggests that stunting has long-term
Our results suggest that children can recover from early
consequences from which children do not recover (20). Similar
nutritional insult, the severity of stunting influences potential for
to our findings, 2 previous studies found no significant cognitive
recovery, and children who demonstrate catch-up growth
display levels of cognition (as measured by the PPVT and the
CDA) that are similar to those of children who are not stunted in
TABLE 5 Estimates from mixed linear regression model for
predictors of quantitative score among Peruvian infancy nor childhood. They also suggest that preschool is
children (n = 1649) important in improving the cognition of children who were
stunted. Reducing the severity of early stunting is critical to
Independent variable1 Estimate P-value 95% CI improving children’s chances of recovery. Additionally, im-
provements in maternal education can increase the possibility of
Intercept 6.63 ,0.0001 5.83, 7.42 catch-up growth. Programs and policies designed to improve
Stunting physical growth and cognition should focus first and foremost
Not stunted – – – on children , 2 y of age. However, interventions that include
Catch-up 0.08 0.69 20.30, 0.46 older children may also improve their growth and intellectual
Stunted in childhood 20.49 0.003 20.81, 20.17 development.
Stunted in infancy and childhood 20.60 0.0003 20.93, 20.28
Child age in mo 0.11 ,0.0001 0.08, 0.14 Acknowledgments
Maternal age in y 0.02 0.01 0.00, 0.04 B.T.C., M.E.P., S.C.A., T.T.D., R.M.M., J.B.S., C.A.P., and
Maternal education in y 0.09 ,0.0001 0.06, 0.12 K.A.D. designed the research; B.T.C. and K.A.D. conducted the
Area population research and analyzed data; B.T.C., M.E.P., S.C.A., T.T.D.,
Rural – – – R.M.M., J.B.S., C.A.P., and K.A.D. wrote the paper; and B.T.C.
Urban 0.52 0.005 0.16, 0.89 and K.A.D. had primary responsibility for its final content. All
Preschool attendance authors read and approved the final manuscript.
No – – –
Yes 0.52 0.002 0.19, 0.85
Wealth index 1.6 0.001 0.66, 2.59 Literature Cited
Number of siblings 20.10 0.02 20.19, 20.02
1. Caulfield LE, Richard SA, Black RE. Undernutrition as an underlying
1
Data reported in table come from round 1 (when child was 6–18 mo of age) except cause of malaria morbidity and mortality in children less than five years
preschool attendance, wealth index, and number of siblings. old. Am J Trop Med Hyg. 2004;71 Suppl 2:55–63.

2000 Crookston et al.

2. UNICEF [Internet]. The state of the world’s children 2008. 2007 [cited 22. Tanner JM. Catch-up growth in man. Br Med Bull. 1981;37:233–8.
2009 18 Mar]. Available from: http://www.unicef.org/sowc08/. 23. Kulin HE, Bwibo N, Mutie D, Santner SJ. The effect of chronic
3. de Onis M. Child growth and development. In: Semba RD, Bloem MW, childhood malnutrition on pubertal growth and development. Am J
editors. Nutrition and health in developing countries. 2nd ed. Totowa Clin Nutr. 1982;36:527–36.
(NJ): Humana Press; 2008. p. 113–37. 24. Crookston BT, Dearden KA, Alder SC, Porucznik CA, Stanford JB,
4. Caulfield L, Richard S, Rivera J, Musgrove P, Black R. Stunting, wasting, Merrill RM, Dickerson TT, Penny ME. Impact of early and concurrent
and micronutrient deficiency disorders. In: Jamison D, Breman J, stunting on cognition. J Matern Child Nutr. In press 2010.
Measham A, Alleyne G, Claeson M, Evans D, Jha P, Mills A, Musgrove 25. Wilson I, Huttly SRA, Fenn B. A case study of sample design for
P, et al, editors. Disease control priorities in developing countries. 2nd ed. longitudinal research. Young Lives. Int. J. Social Research Methodol-
Washington, DC: Oxford University Press; 2006. p. 551–67. ogy. 2006;9:351–6.
5. Shrimpton R, Victora C, de Onis M, Costa Lima R, Blössner M, 26. WHO Multicentre Growth Reference Study Group. WHO child growth
Clugston G. Worldwide timing of growth faltering: implications for standards based on length/height, weight and age. Acta Paediatr Suppl.
nutritional interventions. Pediatrics. 2001;107:E75. 2006;450:76–85.
6. Frongillo EA. Symposium: causes and etiology of stunting. Introduc- 27. Grantham-McGregor SM, Walker SP, Chang SM, Powell CA. Effects of
tion. J Nutr. 1999;129 Suppl 2S:S529–30. early childhood supplementation with and without stimulation on later
7. Grantham-McGregor S, Cheung YB, Cueto S, Glewwe P, Richter L, development in stunted Jamaican children. Am J Clin Nutr. 1997;66:
Strupp B. Developmental potential in the first 5 years for children in 247–53.
developing countries. Lancet. 2007;369:60–70. 28. Kordas K, Lopez P, Rosado JL, Vargas GG, Rico JA, Cebrián ME,

Downloaded from https://academic.oup.com/jn/article/140/11/1996/4630522 by guest on 12 January 2023

8. Behrman JR, Hoddinott J, Maluccio JA, Soler-Hampejsek E, Behrman Stoltzfus RJ. Blood lead, anemia, and short stature are independently
EL, Martorell R, Quisumbing A, Ramirez M, Stein AD. What determines associated with cognitive performance in Mexican school children.
adult skills? Impacts of preschool school-years and post-school experi- J Nutr. 2004;134:363–71.
ences in Guatemala. Philadelphia: University of Pennsylvania; 2006. 29. Walker SP, Grantham-McGregor SM, Powell CA, Chang SM. Effects of
9. Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM. Effects of growth restriction in early childhood on growth, IQ and cognition at
stunting, diarrhoeal disease, and parasitic infection during infancy on age 11–12 years and the benefits of nutritional supplementation and
cognition in late childhood: a follow-up study. Lancet. 2002;359:564–71. psychosocial stimulation. J Pediatr. 2000;137:36–41.
10. Martorell R, Rivera J, Kaplowitz J, Pollitt E. Long term consequences of 30. Walker SP, Chang SM, Powell CA, Grantham-McGregor SM. Effects of
growth retardation during early childhood. In: Hernandez M, Argenta early childhood psychosocial stimulation and nutritional supplementa-
J, editors. Human growth: basic and clinical aspects. Amsterdam: tion on cognition and education in growth-stunted Jamaican children:
Elsevier; 1992. p. 143–9. prospective cohort study. Lancet. 2005;366:1804–7.
11. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Ritcher L, Sachdev 31. Campbell JM. Review of the Peabody Picture Vocabulary Test Third
HS. Maternal and child undernutrition: consequences for adult health Edition. J Psychoed Assess. 1998;16:334–8.
and human capital. Lancet. 2008;371:340–57. 32. Campbell JM, Bell SK, Keith LK. Concurrent validity of the Peabody
12. Martorell R. Undernutrition during pregnancy and early childhood: Picture Vocabulary Test Third Edition as an intelligence and achieve-
consequences for cognitive and behavioral development. In: Young ME, ment screener for low SES African American children. Assessment.
editor. Early child development: investing in our children’s future. 2001;8:85–94.
Amsterdam and New York: Elsevier Science BV; 1997. p. 39–83. 33. Gray S, Plante E, Vance R, Henrichsen M. The diagnostic accuracy of
13. Beasley NMR, Hall A, Tomkins AM, Donnelly C, Ntimbwa P, Kivuga J, four vocabulary tests administered to preschool-age children. Lang
Kihamia CM, Lorri W, Bundy DAP. The health of enrolled and non- Speech Hear Serv Sch. 1999;30:196–206.
enrolled children of school age in Tanga, Tanzania. Acta Trop. 2000; 34. Dunn L, Padilla E, Lugo D, Dunn L. Manual del Examinador para el
76:223–9. Test de Vocabulario en Imágenes Peabody (Peabody Picture Vocabulary
14. Ivanovic DM, Perez HT, Olivares MD, Diaz NS, Leyton BD, Ivanovic Test): Adaptación Hispanoamericana (Hispanic-American adaptation).
RM. Scholastic achievement: a multivariate analysis of nutritional, Circle Pines (MN): AGS; 1986.
intellectual, socioeconomic, sociocultural, familial, and demographic 35. Dunn L, Dunn L. Examiner’s manual for the PPVT-III. Form IIIA and
variables in Chilean school-aged children. J Nutr. 2004;20:878–89. IIIB. (MN): AGS; 1997.
15. Adair LS. Filipino children exhibit catch-up growth from age 2 to 12 36. Cueto S, Leon J, Guerrero G, Muñoz I. Psychometric characteristics of
years. J Nutr. 1999;129:1140–8. cognitive development and achievement instruments in round 2 of
16. Ashworth A, Milward DJ. Catch-up growth in children. Nutr Rev. Young Lives. Technical Note 15. Oxford: Young Lives. 2009.
1986;44:157–63. 37. Rasch G. Probabilistic models for some intelligence and attainment
17. Mendez MA, Adair LS. Severity and timing of stunting in the first two tests. Copenhagen: Denmarks Paedagogiske Institut; 1960.
years of life affect performance on cognitive tests in late childhood. 38. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M,
J Nutr. 1999;129:1555–62. Mathers C, Rivera J. Maternal and child undernutrition: global and
18. Checkley W, Epstein LD, Gilman RH, Cabrera L, Black RE. Effects of regional exposures and health consequences. Lancet. 2008;371:243–60.
acute diarrhoea on linear growth in Peruvian children. Am J Epidemiol. 39. Filmer D, Pritchett L. Estimating wealth effects without expenditure
2003;157:166–75. data or tears: an application to educational enrolments in states of
19. de Onis M. Commentary: socioeconomic inequalities and child growth. India. Demography. 2001;38:115–32.
Int J Epidemiol. 2003;32:503–5. 40. Vella V, Tomkins A, Borghesi A, Miglori GB, Oryem VY. Determinants
20. Martorell R, Khan LK, Schroeder DG. Reversibility of stunting: of stunting and recovery from stunting in northwest Uganda. Int J
epidemiologic findings from children in developing countries. Eur J Epidemiol. 1994;23:782–6.
Clin Nutr. 1994;48 Suppl:S45–57. 41. Cheung YB, Khoo KS, Karlberg J, Machin D. Association between
21. Golden MH. Is complete catch-up growth possible for stunted psychological symptoms in adults and growth in early life: longitudinal
malnourished children? Eur J Clin Nutr. 1994;48 Suppl 1:58–70. follow up study. BMJ. 2002;325:749–52.

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