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The Journal of Nutrition Community and International Nutrition

Children Who Recover from Early Stunting and Children Who Are Not Stunted Demonstrate Similar Levels of Cognition 1,2

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. Dearden 7

3 Department of Family and Preventive Medicin e, University of Utah, Salt Lake City, UT 84108; 4 Instituto de Investigacio´ n Nutricional, La Molina, Lima-12, Peru; 5 Department of Pediatrics, University of Utah, Primary Children’s Medical Center, Salt Lake City, UT 84113; 6 Department of Health Sciences, Brigham Young University, Provo, UT 84602; and 7 Department 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

Undernutrition contributes to more than one-half of the nearly 10 million childhood deaths that occur annually (1,2). Stunting affects 150 million (24%) of all children worldwide (3). Stunting is defined as a height-for-age Z-score (HAZ) 8 , 2 2 SD from the

mean and is often categorized as mild (2 2 to 2 1 SD), moderate ( 22 to 23 SD), and severe ( , 2 3 SD) (4). For many countries in resource-poor settings, mean HAZ at birth is close to the National Center for Health Statistics 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). Stunting is associated with adverse cognitive development in childhood and adolescence, delayed entrance into school, fewer years of schooling, decreased productivity, and reduced adult stature (4,7–11). Stunting during childhood is associated with delays in motor development and lower IQ (12). Stunted children are less likely than their nonstunted counterparts to enroll in school; those who do enroll have lower grades and poorer cognition (13,14). Subsequent to growth faltering during the first 3 y, children from resource-poor countries grow at rates similar to children from more affluent nations, neither losing additional ground nor experiencing substantial recovery (5,12). There is no established definition for “catch-up growth.” (15). It can refer to acceler- ation of growth or partial or complete recovery from stunting

ã 2010 American Society for Nutrition.

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.

1 Supported by the UK Department for International Development (DFID) for the benefit of developing countries (core-funding for Young Lives). Substudies are funded by the Bernard van Leer Foundation, the Inter-American Development Bank (in Peru), the International Development Research Centre (in Ethiopia), and the Oak Foundation. The views expressed here are those of the authors. They are not necessarily those of the Young Lives project, the University of Oxford, DFID, or other funders. Additional funding for this research came from the University of Utah, the Instituto de Investigacio´ n Nutricional, Brigham Young University, and Boston University.

2 Author disclosures: B. T. Crookston, M. E. Penny, S. C. Alder, T. T. Dickerson, R. M. Merrill, J. B. Stanford, C. A. Porucznik, and K. A. Dearden, no conflicts of interest.

8 Abbreviations used: CDA, Cognitive Development Assessment; HAZ, height- for-age Z-scores; PPVT, Peabody Picture Vocabulary Test. * To whom correspondence should be addressed. E-mail: benjamin.crookston@ utah.edu.

1996

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(15,16). We use HAZ for this study, and we define catch-up growth as HAZ , 2 2 during infancy ( ; 1 y of age) and $ 2 2 during childhood ( ;5 y of age) (9,15,17). Some consider the likelihood of catch-up growth to be limited, because children remain in environments that contribute to growth restriction (17–20). A few studies show that partial catch-up is possible among stunted children who remain in the same environment (15,21–23). Identifying factors that allow children to catch up is important for developing programs to improve nutrition and health. We tested the hypothesis that children who experience catch-up growth have significantly lower scores on 2 cognitive assessments than children who were not stunted in infancy and childhood. We also identified factors associated with catch-up growth.

Methods

Study design and background. This study assessed a prospective cohort of children who are part of a multicountry study called Young Lives. The Young Lives study, which is funded by the United Kingdom’s Department for International Development, explores childhood poverty, intergenerational poverty, and poverty reduction policies. Two cohorts of children (1 and 8 y old) from Ethiopia, India, Peru, and Vietnam have been followed since 2002 with the intent to track the children for 15 y. Our study examines catch-up growth following early stunting among the younger Peruvian cohort. Researchers from the Instituto de Investigacio´ n Nutricional and Grupo de Analisis para el Desarrollo manage the Peruvian cohort.

Study participants. A detailed description of methods for this study has been given elsewhere (24). Briefly, a total of 2052 children from 74 communities representing 20 districts in Peru were enrolled in 2002. As an initial step, we assembled a complete list of all districts in the country, excluding the 5% with the highest socioeconomic levels. To determine socioeconomic levels, we ranked the 1818 districts in Peru according to a composite index of poverty (25). Using national census data, the size of the population for all districts was noted. The total population was divided by 2000 to establish the sampling interval and a random number within the sampling interval was selected to determine the initial district. To identify the subsequent district, we added the total number of individuals in the sampling interval to the initial starting point and continued in this fashion until all 20 districts were identified. Once the 20 districts were chosen, we randomly selected a community and a specific house within the community. In many cases, there were ,100 children aged 6–17.9 mo in a given community. In such cases, the closest community was selected in systematic fashion until 100 families per district were enrolled. Urban areas were subdivided into city blocks. The sample represents ~95% of Peruvian children, includes participants from urban and rural areas, and represents coastal, highland, and jungle regions. Institutional review boards from London South Bank University, London School of Hygiene and Tropical Medicine, and the University of Reading approved of this research. Within Peru, the Ministry of Health approved of the study. Ethical reviews were conducted by the Institutional Review Boards at the Instituto de Investigacio´ n Nutricional and the Peruvian Instituto Nacional de Salud.

Data collection. Interviews consisted of a core questionnaire for primary caregivers and included questions regarding household compo- sition, child health, caregiver characteristics, livelihoods, socioeconomic status, social capital, childcare, and cognitive development. Field- workers collected anthropometric data using digital scales (Soehnle) and locally made wooden boards and measurement techniques were standardized per WHO guidelines (26). Fieldworkers were trained for 3 mo in data collection protocols and instruments. Based on a pilot study, instruments were revised. Three teams of 6 interviewers per team collected 2 rounds of data in 2002 when children were 6–17.9 mo of age (round 1) and 2006–2007 when they were 4.5–6 y old (round 2). There are 2052 children in the cohort. Only 4% of children were lost to follow-

up. Data from both rounds were entered for analyses using Delphi software.

Cognitive outcomes. This study used the Peabody Picture Vocabulary Test (PPVT) to evaluate vocabulary skills and listening comprehension and the Cognitive Development Assessment (CDA) to judge the quantitative reasoning of children 4.5–6 y of age. The PPVT is a commonly used measure for evaluating cognitive development in both industrialized and resource-poor countries (27–30). The PPVT is highly correlated with the Wechsler and McCarthy Scales, which are validated measures of intelligence (31–33). A validated, Spanish version of the PPVT consisting of 125 questions was given to children participating in the study (34,35). The CDA was developed by the International Association for the Evaluation of Educational Achievement to study the effect of preschool 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 subtest) and low reliability among the Young Lives sample in Peru (time subtest), only the quantity subtest was used in the study. The quantity subtest relies on 15 items to measure a child’s perception of amount. For each item, interviewers show children images and ask a question such as “Look at the cats and dogs and point to the picture where the dog has less food than the cat.” It is possible that because the CDA was developed for children 4 y of age, it might not be an appropriate measure of cognition for children older than 4 y. We compared the mean raw and Rasch scores for the CDA from children without preschool, with preschool, and currently attend- ing first grade. Rasch scores are used extensively in psychometrics and increasingly in public health. Researchers use them to determine the 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 measurement has been successful. Rasch scores are based on a probability model that when a group of individuals is asked multiple questions, e.g. as part of a cognitive assessment, individual j makes a mistake in answering question k. As expected, data from Young Lives suggest that children who had formal schooling performed better on the test than children who never attended preschool. Similarly, the longer children spent in preschool, the higher the score. While test scores improved with increased levels of education, we conclude that the CDA was an appropriate measure for children 4.5–6 y of age, as noted below. Items in the PPVT and the CDA are arranged in order of increasing difficulty. A given child received only those items within his or her critical range based on chronological age and ceiling. We reviewed all observa- tions to verify that basal and ceiling sets were correctly established for each child (36). Not all distributions of raw and Rasch scores were normal. In rare cases, children achieved close to the highest possible score. Thus, test scores may have underestimated children’s abilities for the construct measured. This appears to be a very infrequent occurrence. For example, only 1 child obtained a perfect score on the CDA. Validity and reliability for both tests were established by assessing the degree to which evidence and theory supported the interpretations of test scores. Reliability was established according to Classical Test theory and Item Response theory. Details about the establishment of validity and reliability can be found elsewhere (36). For children who were native Spanish speakers, both tests were found to have appropriate psycho- metric properties. However, each test proved unreliable for assessing cognition among native Quechua speakers. Thus, only Spanish-speaking children ( n = 1706) were included in the analysis. We used standardized scores for both the PPVT and the CDA.

Catch-up growth. Catch-up growth was examined both as an outcome variable and as a determinant of cognitive scores. We defined “stunted in infancy but not childhood” (catch-up) as having a HAZ , 22 during round 1 and a HAZ $ 22 at round 2 (i.e. during infancy but not childhood), “stunted in infancy and childhood” as having a HAZ , 22 at rounds 1 and 2, “stunted in childhood” as having a HAZ $ 22 during round 1 and a HAZ , 22 at round 2, and “not stunted” as having HAZ $ 22 at both rounds (9,15,17). We used information from all children when evaluating catch-up growth as a predictor of cognitive

Catch-up growth and improved cognition 1997

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scores. When considering determinants of catch-up growth, we used data only from children with a HAZ , 22 at round 1. Our assessment of changes in nutritional status was based on data collection at 2 points in time. We do not know whether children were stunted before round 1 or between rounds 1 and 2.

Covariates. Covariates were chosen based on results from an earlier study using Young Lives data, which used a well-known conceptual framework for the determinants and consequences of undernutrition (24,38). Covariates included: urban/rural setting; geographic region (coast/highland/jungle); child’s age, sex, and preschool attendance; and maternal age, height, education, and ethnicity. Severity of stunting was used when considering determinants of catch-up growth, where only children with a HAZ , 22 at round 1 were examined. In this instance, severity of stunting was the HAZ for a given child. Thus, the lower the HAZ, the more severe the stunting experienced by the child. A composite indicator of wealth ranging from 0–1 reflected consumer durables, services, and housing quality (39).

Data analysis. Anthropometric indicators were calculated using the latest WHO International Growth Reference standard (26). SAS (version 9.2) was used for statistical analyses. Pearson chi-square tests compared distributions among stunting classifications; F tests compared means among groups. For analyses, we used mixed regression models to account for the cluster sample design. The MIXED procedure from SAS was used for linear models (cognitive outcomes) and the GLIMMIX procedure was used for logistic models (catch-up growth outcomes). Covariates were retained or dropped based on P-values ( ,0.1) and conceptual consid- erations. Regression coefficients (linear models), odds ratios (logistic models), and 95% CI were calculated for retained variables. All models

were tested for interaction and compliance with logistic and linear regression model assumptions. No interaction terms were retained based on P , 0.1. Significance was declared when P , 0.05.

Results

Children’s mean age at round 1 was 12 (6 3.5) mo. Slightly less than one-half (49.5%) were female and only a few (1.0%) had begun formal schooling by round 2. A majority (74.1%) lived in urban areas. Highland and coastal regions had the greatest proportion of study participants, 43.0 and 40.2%, respectively. The remaining respondents lived in jungle regions (16.8%). Most mothers described themselves as mestizo (91.9%), with the principal religion being Catholicism (80.2%). Two-thirds (63.8%) of children were not stunted in either round 1 or round 2, whereas 8.4% were stunted at round 1 but not round 2 and were considered to have experienced catch-up growth, 13.4% were stunted at round 2 only (childhood), and 14.4% were stunted in both infancy and in childhood. Children classified into these 4 categories differed signifi- cantly with respect to sex, region, area of residence, preschool attendance, and sociodemographic conditions ( Table 1). More males than females experienced catch-up growth. Children from rural areas made up one-half of those stunted in infancy and childhood but only one-quarter of the overall sample. Mean wealth index was highest among those who were not stunted, followed by children experiencing catch-up growth. Change in HAZ between rounds 1 and 2 differed by stunting classification as follows: catch-up growth, 1.13 6 0.66; stunted

TABLE 1 Characteristics of study participants by stunting classification 1

Independent

Not

Stunted in

Stunted in infancy and childhood 6

 

variable 2

stunted 3

Catch-up 4

childhood 5

P -value 7

n Sex, % Male Female Region, % Coast Highland Jungle Area, % Urban Rural Attended preschool, % Yes No HAZ score (round 1) HAZ score (round 2) Child age, mo Maternal age, y Maternal height, cm Wealth index Maternal education, y Verbal vocabulary Quantitative score

1065

140

224

240

 

0.0001

49.9

64.3

38.8

56.7

50.1

35.7

61.2

43.3

 

0.0001

50.9

30.7

25.5

12.9

34.6

53.6

52.7

64.2

14.6

15.7

21.9

22.9

 

0.0001

83.5

79.3

52.7

49.6

16.5

20.7

47.3

50.4

 

0.0001

90.4

90.0

75.5

75.4

9.6

10.0

24.6

24.6

2 0.6 6 0.9 2 0.9 6 0.8 11.8 6 3.5 26.5 6 6.3 151.3 6 5.2 0.47 6 0.20 9.7 6 3.6 95.9 6 19.9 10.9 6 2.2

2 2.6 6 0.5 2 1.4 6 0.5 13.8 6 3.2 27.5 6 7.2 150.0 6 4.5 0.44 6 0.20 8.3 6 4.3 90.2 6 20.3 10.9 6 2.1

2 1.1 6 0.8 2 2.5 6 0.5 10.9 6 3.4 26.0 6 6.4 149.0 6 5.6 0.33 6 0.19 7.3 6 3.7 82.1 6 19.0 9.4 6 2.7

2 2.8 6 0.7 2 2.8 6 0.6 13.1 6 3.5 27.5 6 7.5 147.1 6 4.9 0.29 6 0.18 6.1 6 4.0 76.9 6 18.3 9.4 6 2.6

0.0001

0.0001

0.0001

0.0366

0.0001

0.0001

0.0001

0.0001

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.

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TABLE 2 Odds ratios from logistic regression model for catch- up growth (1 = yes, 0 = no) among Peruvian children who experienced stunting in infancy ( n = 374)

Independent variable 1

Odds ratio

P-value

95% CI

Area population Rural Urban Maternal education in y Preschool attendance No Yes Child age in mo Grandparents live in home No Yes Severity of stunting (HAZ at round 1) 2 Maternal height Z-score

1.00

0.08

1.70

0.94, 3.08

1.06

0.07

1.00, 1.13

1.00

0.06

2.03

0.98, 4.17

1.14

0.0006

1.05, 1.18

1.00

0.04

1.89

1.05, 3.40

2.10

0.0009

1.36, 3.25

1.66

0.0002

1.28, 2.17

1 Data reported in table come from round 1 (when child was 6–18 mo of age) except preschool attendance and child age. 2 HAZ at round 1 is a continuous variable.

in childhood, 2 1.38 6 0.96; not stunted, 2 0.28 6 0.85; and stunted in infancy and childhood, 0.02 6 0.76. Changes in HAZ for children demonstrating catch-up growth, those stunted in childhood only, and those not stunted were significantly differ- ent from children who were stunted in infancy and childhood. We conducted logistic regression to identify determinants of catch-up growth, limiting our analyses to children with HAZ , 2 2 at round 1 (Table 2). Predictors of catch-up growth included maternal height, child age at round 2, grandparents living at home, and severity of stunting in round 1. Severity of stunting was the most important predictor of catch-up growth; children who were less stunted at round 1 (i.e. higher HAZ) were more likely to experience catch-up growth. It is worth pointing out that although not significant, area of residence, maternal education, and preschool attendance were retained in the model for conceptual reasons (P , 0.10). Estimates for unadjusted regression models predicting verbal vocabulary and quantitative scores are reported in Table 3. For verbal vocabulary scores, the reference group (not stunted) scored significantly higher than the 3 comparison groups. However, for quantitative cognition, children who were not stunted and those who demonstrated catch-up growth did not differ ( P = 0.5). When adjusted for maternal age and education, area of residence, preschool attendance, wealth index, and number of siblings, verbal vocabulary scores did not differ between the not stunted and catch-up groups (Table 4). However, children who were stunted in childhood or stunted in infancy and childhood

had significantly lower scores on the verbal vocabulary test. Children who had older mothers and mothers with more education, and children who lived in urban areas, attended preschool, had fewer siblings, and came from better socioeco- nomic conditions scored higher on the verbal vocabulary assessment. Differences between quantitative scores for the not stunted and catch-up groups did not differ (P = 0.7) ( Table 5), but children who were stunted in childhood or stunted in infancy and childhood had significantly lower quantitative scores. Children who were older at round 1, had older mothers or mothers with more education, lived in urban areas, attended preschool, had fewer siblings, and came from better socioeco- nomic conditions scored significantly better on the quantitative assessment.

Discussion

Results suggest that one-third of children who were stunted in infancy (at 1 y of age) recovered by the time they were 5 y old. 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 children can recover from early nutritional insult, identify predictors of catch-up growth, and suggest that catch-up growth contributes to cognition. These findings can guide future research about the impact of stunting on cognition as well as policy and program efforts to improve children’s physical and intellectual well-being.

Potential for catch-up growth. The proportion of stunted children who experienced catch-up growth (36.8%) is consistent with findings from previous research (9,15,17,40,41). In a study of 2131 Filipino children, researchers reported that 34% of stunted children experienced catch-up growth by 8 y of age (18). More than one-half of 239 Peruvian children in Lima who were stunted in the first 2 y exhibited catch-up growth by 9 y (9). These studies used similar methods for collecting anthropometry and defining catch-up growth. But the timing of assessment, cognitive tests administered, and setting differed from our study. The severity of stunting varied across studies discussed here. Finally, the magnitude of recovery (1.13 SD) in our catch-up group was nearly identical to that described by Adair (15) (1.14 SD).

Predictors of catch-up growth. According to our results, children with higher HAZ at initial assessment (i.e. children who experienced less severe stunting) were more likely to experience catch-up growth. Others (15,17,22) also report that higher HAZ at initial assessment improves the chances of experiencing catch- up growth, although variables included in their models differ 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 Not stunted Catch-up Stunted in childhood Stunted in infancy and childhood

92.33

, 0.0001

87.17, 97.49 – 2 6.18, 2 0.12 2 8.77, 2 3.67 2 12.57, 2 7.49

10.64

, 0.0001

10.20, 11.08 – 2 0.26, 0.53 2 1.24, 2 0.59 2 1.19, 2 0.54

 

23.15

0.04

0.14

0.50

26.21

,

0.0001

2

0.91

,

0.0001

2 10.03

, 0.0001

2 0.86

, 0.0001

Catch-up growth and improved cognition 1999

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TABLE 4 Estimates from mixed linear regression model for predictors of verbal vocabulary score among Peruvian children ( n = 1649)

Independent variable 1

Estimate

P -value

95% CI

Intercept Stunting Not stunted Catch-up Stunted in childhood Stunted in infancy and childhood Maternal age in y Maternal education in y Area population Rural Urban Preschool attendance No Yes Wealth index Number of siblings

59.0

,0.0001

53.2, 64.9

 

2 3.5, 2.1 2 4.8, 2 0.1 2 7.0, 2 2.2 0.1, 0.4 1.2, 1.7

2

0.7

0.62

2

2.5

0.04

2 4.6

0.0002

 

0.3

0.0001

1.4

,0.0001

4.5

0.002

1.7, 7.3

3.9

0.002

1.5, 6.3 14.0, 28.2 2 1.9, 2 0.6

21.1

,0.0001

2 1.2

0.0002

1 Data reported in table come from round 1 (when child was 6–18 mo of age) except preschool attendance, wealth index, and number of siblings.

up growth included child’s age at second assessment, maternal height, and grandparents living in the home. Although child’s age and presence of grandparents in the home cannot be changed by program planners and implementers, maternal height is amenable to improvement and should be considered as one option among several that can improve the potential for catch- up growth.

Catch-up growth and cognition. Our results are different from previous research that suggests that stunting has long-term consequences from which children do not recover (20). Similar to our findings, 2 previous studies found no significant cognitive

TABLE 5 Estimates from mixed linear regression model for predictors of quantitative score among Peruvian children ( n = 1649)

Independent variable 1

Estimate

P -value

95% CI

Intercept Stunting Not stunted Catch-up Stunted in childhood Stunted in infancy and childhood Child age in mo Maternal age in y Maternal education in y Area population Rural Urban Preschool attendance No Yes Wealth index Number of siblings

 

6.63

, 0.0001

5.83, 7.42

0.08

0.69

2 0.30, 0.46 2 0.81, 2 0.17 2 0.93, 2 0.28 0.08, 0.14 0.00, 0.04 0.06, 0.12

2

0.49

0.003

2

0.60

0.0003

0.11

,

0.0001

0.02

0.01

0.09

, 0.0001

0.52

0.005

0.16, 0.89

0.52

0.002

0.19, 0.85 0.66, 2.59 2 0.19, 2 0.02

1.6

0.001

2 0.10

 

0.02

1 Data reported in table come from round 1 (when child was 6–18 mo of age) except preschool attendance, wealth index, and number of siblings.

2000 Crookston et al.

deficit between children who were not stunted and children who experienced catch-up growth (9,17). Although Berkman (9) documented differences in cognition between children who were stunted in infancy and childhood and children who were not stunted during either period, he found no differences in cognition between children who were not stunted and children who demonstrated catch-up growth, even after adjusting for covariates. Mendez and Adair (17) found moderate differences in cognition between children who had catch-up growth and those who were not stunted but found no difference when adjusting for many of the same confounding factors used in this study, such as number of siblings, area population (urban vs. rural), maternal education, and wealth. Given the apparent lack of difference in cognitive scores between those who experienced catch-up growth and those who were never stunted, children who were at greatest risk of cognitive deficits were those who did not experience catch-up growth after stunting in infancy (41). This study has limitations. First, there is no standard definition for catch-up growth; thus, our interpretations may be different from those in other studies. However, we used a definition that was employed by 3 other authors (15,17,22) and our results are consistent with findings where the same definition was used. Second, our sample is not nationally representative; 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 time and therefore do not have measures of the frequency or duration of stunting. Thus, it is not possible to determine whether lack of cognitive impact in childhood (round 2) is due to catch-up growth alone or whether differences in the severity, frequency, and duration of stunting as well as access to interventions designed to improve nutritional status account 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 collection). Our results suggest that children can recover from early nutritional insult, the severity of stunting influences potential for 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 infancy nor childhood. They also suggest that preschool is important in improving the cognition of children who were stunted. Reducing the severity of early stunting is critical to improving children’s chances of recovery. Additionally, im- provements in maternal education can increase the possibility of catch-up growth. Programs and policies designed to improve physical growth and cognition should focus first and foremost on children , 2 y of age. However, interventions that include older children may also improve their growth and intellectual development.

Acknowledgments B.T.C., M.E.P., S.C.A., T.T.D., R.M.M., J.B.S., C.A.P., and K.A.D. designed the research; B.T.C. and K.A.D. conducted the research and analyzed data; B.T.C., M.E.P., S.C.A., T.T.D., R.M.M., J.B.S., C.A.P., and K.A.D. wrote the paper; and B.T.C. and K.A.D. had primary responsibility for its final content. All authors read and approved the final manuscript.

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