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© 2007 American Society for Nutrition J. Nutr. 137:2464-2469, November 2007

Community and International Nutrition

Early Childhood Stunting Is Associated with Poor Psychological Functioning in Late Adolescence and Effects Are Reduced by Psychosocial Stimulation1,2

Susan P. Walker3,*, Susan M. Chang3, Christine A. Powell3, Emily Simonoff4 and Sally M. Grantham-McGregor5

3 Epidemiology Research Unit, University of the West Indies, Kingston 7, Jamaica; 4 Institute of Psychiatry, London SE5 8AF, UK; and 5 Institute of Child Health, London WC1N 1EH, UK

* To whom correspondence should be addressed. E-mail: susan.walker{at}uwimona.edu.jm.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Participants and Methods
 Results
 Discussion
 LITERATURE CITED
 
Stunting is associated with deficits in cognition and school achievement from early childhood to late adolescence; however, there has been little investigation of emotional and behavioral outcomes. The objective of this study was to determine whether linear growth retardation (stunting) in early childhood is associated with poorer psychological functioning in late adolescence. The study was a prospective cohort study of stunted and nonstunted children. Participants were identified at age 9–24 mo by a survey of poor neighborhoods in Kingston, Jamaica, and a 2-y intervention trial of supplementation and stimulation was conducted in the stunted children. Psychological functioning was assessed at age 17 y in 103 of 129 stunted children enrolled and 64 of 84 nonstunted participants. Anxiety, depressive symptoms, self-esteem, and antisocial behavior were reported by participants using interviewer-administered questionnaires and attention deficit, hyperactivity, and oppositional behavior were reported by parent interviews. The stunted participants reported significantly more anxiety (regression coefficient = 3.03; 95% CI = 0.99, 5.08) and depressive symptoms (0.37; 95% CI = 0.01, 0.72) and lower self-esteem (–1.67; 95% CI = –0.38, –2.97) than nonstunted participants and were reported by their parents to be more hyperactive (1.29; 95% CI = 0.12, 2.46). Effect sizes were 0.4–0.5 SD. Participants who received stimulation in early childhood differed from the nonstunted group in hyperactivity only. Children stunted before age 2 y thus have poorer emotional and behavioral outcomes in late adolescence. The findings expand the range of disadvantages associated with early stunting, which affects 151 million children <5 y old in developing countries.


   Introduction
TOP
 ABSTRACT
 Introduction
Participants and Methods
 Results
 Discussion
 LITERATURE CITED
 
Growth retardation or stunting in children in developing countries occurs primarily as a result of chronic undernutrition and infectious diseases and affects 30% of children <5 y old (1). Stunting is associated with poor development in early childhood (2) and with deficits in cognition and school achievement compared with nonstunted children through late adolescence (3,4).

Children hospitalized for severe malnutrition in early childhood have been reported to have problems with aggressive behavior (5), attention deficits (6), and poor social relationships at school age (7). Although stunted children have been found to have behavior changes in early childhood, such as less happiness and more apathy and fussiness (8), there has been little investigation of whether their later emotional and behavioral functioning is affected.

We conducted a prospective cohort study of stunted and nonstunted Jamaican children beginning at age 9–24 mo. In the first 2 y, the stunted children participated in a randomized trial of supplementation and psychosocial stimulation. Each treatment benefited concurrent development (2). Stimulation had sustained benefits to cognitive functioning at ages 7, 11, and 17 y (9–11), whereas benefits from supplementation were not sustained. Neither intervention affected teacher- and parent-reported behavior problems at age 11 y (12). There were no benefits of supplementation to psychological functioning at age 17 y; however, stimulation had significant benefits, including fewer symptoms of anxiety and depression and better self-esteem (13).

Stunted children who did not receive stimulation continued to have poorer levels of cognitive functioning than nonstunted children (11). Here, we compare emotional and behavioral outcomes of stunted participants with nonstunted participants at age 17–18 y. As stimulation had significant benefits to psychological functioning, we compared the nonstunted participants with the stunted participants according to whether they received stimulation. There are considerable data showing that many of the functions measured (symptoms of depression, self-esteem, attention deficit, and oppositional and antisocial behavior) are related to poverty; however, general anxiety is sometimes associated with better socioeconomic conditions (14). We therefore measured extensive socioeconomic variables to allow for any differences between the groups when assessing the effect of stunting.


   Participants and Methods
TOP
 ABSTRACT
 Introduction
 Participants and Methods
Results
 Discussion
 LITERATURE CITED
 
    Initial study. In 1986–1987, we identified children aged 9–24 mo by a house-to-house survey of poor neighborhoods of Kingston, Jamaica (2). All 129 stunted children [length-for-age < –2 SD of the National Center for Health Statistics references (15)] identified were assigned to 1 of 4 groups: control, supplementation, stimulation, or both interventions. The order of group assignment was determined randomly. Supplementation comprised 1 kg milk-based formula provided weekly (16). Stimulation comprised weekly 1-h home visits by trained community health workers who conducted play sessions with the mother and child. Both interventions were provided for 2 y. Thirty-two nonstunted children (length-for-age > –1 SD) were enrolled matched to the control group for age, sex, and neighborhood.

The children were reexamined at ages 7 and 11 y. To increase the power of comparisons between stunted and nonstunted groups, an additional 52 nonstunted children were studied from age 7 y. They had been identified in the original survey when they were aged 9–24 mo and fulfilled all inclusion criteria. They lived in the same neighborhoods as the study children and were comparable to the original group of nonstunted children in social background (9).

    Follow-up at 17–18 y. Psychological functioning was assessed when participants were aged 17–18 y. The aim was to assess emotional and behavioral symptoms and no attempt was made to diagnose specific disorders. Written informed consent was obtained from the participants and their parents. Ethical approval for the study was given by the Ethics Committees of the University of the West Indies and the Institute of Child Health, University College London.

    Psychological functioning. Self-esteem was assessed with the How I Think about Myself questionnaire (17), anxiety symptoms were assessed with the Manifest Anxiety (What I Think and Feel) Questionnaire (18), and depressive symptoms were assessed with the Short Mood and Feelings Questionnaire (19). Antisocial behavior was assessed with the Behavior and Activities Checklist (20). Questionnaires were administered in a private interview at our research unit. All were obtained by self report.

Although young people are considered valid informants for most behaviors by age 17 y, attention deficit and hyperactivity symptoms are exceptions. Therefore, the Conners' Parent Rating Scale (short form) (21) was administered to the mothers (or primary caregiver if not the mother) to obtain information on attention deficit. The Conners' Scale also provides scores for cognitive problems/inattention, hyperactivity, and oppositional behavior.

All questionnaires were piloted and reworded as necessary to ensure comprehension. This involved replacing words or short phrases not easily understood with others more familiar to the participants. For example, the item "often I feel sick in my stomach" was changed to "you often feel sick/upset in your belly." No items were omitted from any of the questionnaires. All questionnaires were interviewer administered; therefore, for 3 of the scales (How I Think about Myself, What I Think and Feel, and Short Mood and Feelings), which were written to allow self-administration, we changed portions of the questions from first- to second-person (i.e. "I felt ..." to "You felt...").

Test-retest reliabilities (intraclass correlation coefficient) after a 2-wk interval, in 18 nonstudy subjects recruited from schools attended by the study subjects, were ≥0.7 and internal consistency (Cronbach's {alpha}) ranged from 0.55 to 0.85 (Table 1). Participant interviews were administered by one interviewer and parent questionnaires by another interviewer. Interviewers were unaware of the participants' group. Inter-observer agreement with another trained interviewer in 23 interviews was ≥97% for all items.


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  		TABLE 1 Reliability and internal consistency of emotional and behavioral measures

 
    Socioeconomic background. Participants were asked about the frequency of hunger because of lack of food in the home during the previous year. They were also asked to report if they had ever been a victim of violent crime (e.g. robbery, stabbing, or shooting) and if they had witnessed violent acts (involving knives, guns, or other weapons) during the past year. If yes, they were asked to say how many times they had witnessed such acts. The homes were visited and information obtained on water and toilet facilities (each rated on a scale of 1–6), the number of persons per room, and the number of household possessions from a list of 11 items. A housing score was derived by factor analysis of these variables. The mothers' or primary caregivers' occupation was recorded. Mothers' verbal intelligence had been assessed previously with the Peabody Picture Vocabulary Test (PPVT) when the children were aged 11 y.

    Statistical analysis. Outcome variables were screened for normality and the depressive symptoms and antisocial behavior scales were normalized using square root transformations. Associations between participant characteristics and psychological outcomes were determined by Pearson's product-moment correlation coefficient (age, housing, mothers' PPVT) or Spearman rank correlation (hunger, occupation, and witnessing and victim of crime). Gender differences were determined by t test. An {alpha} of P < 0.05 was used to assess significance. Because stimulation but not supplementation had significant benefits on psychological functioning, to determine the effect of stunting, the nonstunted group was compared with the stunted children who had not participated in the stimulation program (nonstimulated stunted: control and supplement only groups) and with those who had received stimulation (stimulated stunted: stimulation only and stimulated and supplemented groups). Group was coded as 2 dummy variables to compare each of the stunted groups with the nonstunted group. The dummy variables were: nonstimulated stunted = 1, other groups = 0; and stimulated stunted = 1, other groups = 0. Our interest in this report is on the impact of early childhood stunting. We report the unadjusted effects of stunting followed by the effects after adjusting for possible confounders. In multiple regression analyses, participants' age, sex, and social background variables that either differed between stunted and nonstunted groups at follow-up or were correlated with the outcomes were offered stepwise before entering the 2 dummy variables for group. Social background variables offered in the analyses were hunger, housing score, mothers' PPVT and occupation, father present in the home, and whether the participants had witnessed or been a victim of violent crime in the past year.


   Results
TOP
 ABSTRACT
 Introduction
 Participants and Methods
 Results
Discussion
 LITERATURE CITED
 
    Loss from study. Ten of 65 children (15.4%) from the nonstimulated stunted group did not participate in the follow-up study, 16 of 64 (25.0%) children from the stimulated stunted group did not participate, and 20 of 84 (23.8%) from the nonstunted group did not participate. The proportion of subjects lost was not significantly different by group. Most of the loss was due to migration, which accounted for 70% of children lost. Participants and those who did not take part in the study did not differ in any enrollment measure (initial age, developmental level, height-for-age, home stimulation, mothers' verbal intelligence and education, and housing quality), except within the nonstimulated stunted group, children who did not participate had younger mothers (P < 0.001) than those assessed.

    Participant characteristics. The nonstunted children had higher birth weight (P < 0.001), height-for-age (P < 0.001), and better housing (P = 0.002) on enrollment than the stunted groups (Table 2). The nonstunted participants remained taller than the stunted groups (P < 0.001) at follow-up. The mothers/caregivers of the nonstunted group had better verbal scores than the combined stunted groups (P = 0.03). There were no other differences between the nonstunted and stunted groups in any measured social background variables. The nonstimulated stunted participants reported more hunger than the stimulated stunted group (P = 0.03).


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  		TABLE 2 Participant characteristics at enrollment (9–24 mo) and follow-up (17–18 y)1

 
    Psychological functioning. The emotional and behavioral outcomes are shown in Table 3. Several of the participants' characteristics were associated with their psychological functioning. Older adolescents reported better self-esteem (P < 0.001). Participants who reported experiencing hunger and those who had been victims of crime reported more anxiety (P < 0.005). Participants whose fathers lived with them had better self-esteem (P < 0.05). Participants reported more antisocial behavior if they had witnessed violence (P < 0.001) or had been a victim of crime (P < 0.05), although it is possible that being a victim or witnessing violence could be due to the children themselves being antisocial. Girls reported less antisocial behavior than boys (P < 0.05) and were reported by their mothers/caregivers to have fewer problems with attention (P < 0.05). Mothers/caregivers with better verbal scores reported fewer problems with attention in their children (P < 0.01) and higher occupation level was associated with better self-esteem (P < 0.02) and less oppositional behavior (P < 0.02). Poorer housing was associated with more hyperactivity (P < 0.001), poorer attention (P < 0.01), and more oppositional behavior (P < 0.004).


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  		TABLE 3 Emotional and behavioral outcomes at age 17–18 y in nonstunted participants and in stunted participants who did or did not receive psychosocial stimulation1

 
    Effect of stunting. Multiple regression analyses were used to determine the effects of stunting on psychological functioning (Table 4). Nonstunted participants reported significantly fewer symptoms of anxiety and depression and better self-esteem than nonstimulated stunted participants. The nonstunted participants did not differ from the stimulated stunted group for these outcomes. Parents of the nonstunted group also tended to report less oppositional behavior than in the nonstimulated stunted group (P = 0.06) but similar to the stimulated stunted group. Both stimulated and nonstimulated stunted participants were reported by their parents to be more hyperactive than the nonstunted children. Because the children's behavior might influence the likelihood of their being exposed to violence, the analyses were repeated omitting the covariates "victim of crime" and "witnessing violent crime." The results did not change.


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  		TABLE 4 Effect of stunting in early childhood on emotional and behavioral outcomes at age 17–18 y in participants who did or did not receive psychosocial stimulation1

 
Early childhood stunting is associated with poor home environments. Although the HOME scores for the stunted groups were not significantly lower than that of the nonstunted group, the scores tended to be lower. We therefore repeated the analyses offering the HOME score. (These analyses included the stunted groups and the nonstunted participants enrolled at age 9–24 mo only, as HOME scores were not available for nonstunted participants enrolled at age 7 y). The HOME was not a significant predictor of any of the psychological outcomes.

The analyses were repeated entering birth weight. Higher birth weight was associated with less anxiety (coefficient = –1.77, 95% CI = –3.52, –0.02; P = 0.05). The difference in anxiety between nonstunted and nonstimulated stunted participants remained significant (coefficient = 2.57, 95% CI = 0.47, 4.67; P = 0.02). Birth weight was not a significant predictor of any of the other outcomes.

    The role of IQ. Most psychosocial problems are more common in children with low IQ (14) and we previously reported that the stunted children had lower IQ than the nonstunted children (11). IQ scores were significantly correlated with all the psychological scores. We therefore examined whether cognitive ability mediated the effect of stunting by repeating the multiple regressions entering IQ before the dummy variables for group. The change in the regression coefficients comparing the nonstimulated stunted group and the nonstunted group was tested using the method of Freedman and Schatzkin (22). The coefficients decreased (P < 0.05) for anxiety (24.8%), depressive symptoms (43%), and self-esteem (33.1%). The change in the regression coefficient for hyperactivity was not significant. The difference between stunted and nonstunted children in anxiety remained significant (P < 0.05), but the groups no longer differed in depressive symptoms or self-esteem.


   Discussion
TOP
 ABSTRACT
 Introduction
 Participants and Methods
 Results
 Discussion
LITERATURE CITED
 
Children stunted in the first 2 y of life had poorer psychological functioning in late adolescence than nonstunted participants. This included more symptoms of anxiety and depression, poorer self-esteem, and more hyperactive behavior. There was also a tendency for higher levels of oppositional behavior.

A critical question is whether the association between early childhood stunting and poor psychological functioning in late adolescence is causal or whether stunting is a proxy for poor environments that independently affect psychological outcomes. The stunted and nonstunted children came from the same neighborhoods and we had measures of their socioeconomic status, maternal characteristics, and exposure to violence. Several of these measures were related to the outcomes, but after adjusting for their effects, significant differences remained between stunted and nonstunted participants, with effect sizes ranging from 0.37 SD for depressive symptoms to 0.51 SD for anxiety. The HOME score did not predict psychological functioning; however, we did not have this measure for the nonstunted participants enrolled at age 7 y. Therefore, the power of the analyses for the HOME score was less than for the other measures included. It thus remains possible that differences in the quality of the home environment, or residual confounding from unmeasured aspects of socioeconomic status, may contribute to differences between the nonstimulated stunted group and the nonstunted group. Nonetheless, it is likely that at least part of the differences in psychological functioning is due to undernutrition in the first 2 y of life. Increased internalizing problems were also found in children aged 11–14 y treated for iron deficiency anemia in infancy compared with nonanemic children (23), suggesting that psychological functioning may also be affected by specific nutrient deficiencies.

The stunted children had a more negative affect in early childhood (8) and were more inhibited at 9–10 y (24). Thus, differences in affect may have persisted since early childhood. The stunted participants also had higher conduct disorder at age 11 y (12) and the tendency to higher levels of oppositional behavior at age 17 y is consistent with this.

We cannot be certain of the mechanism whereby stunting is associated with poor psychological functioning. Animal research shows that early undernutrition can affect brain structure and function, leading to lasting cognitive and emotional effects (25). Thus, alterations to the brain as a result of childhood undernutrition could be 1 mechanism for the observed differences in psychological functioning. Lower IQ is a well-recognized risk factor for a range of child psychopathology (26). IQ was lower in the stunted participants, and when IQ was controlled for in the analyses, stunting was no longer significantly associated with depressive symptoms or self-esteem. It is possible that low IQ led to the children having lower self-esteem and more depressive symptoms. However, the stunted children had a more negative affect in early childhood (8). It is therefore also possible that stunting could have affected cognitive and psychological functioning concurrently.

Unlike the other behaviors that were more prevalent in the stunted children, hyperactivity was not affected by intervention, suggesting the effects may be difficult to reverse. In adequately nourished children, hyperactivity is associated with altered functional anatomy of several areas of the brain, including the frontal lobe and basal ganglia (27). It is possible that stunting in the first 2 y also affects these areas. Whereas hyperactivity is genetic in general populations, there is also substantial evidence for longer term effects of inadequacies in the early rearing environment on attention and hyperactivity (28).

Raised cortisol levels are associated with depression and anxiety in adequately nourished subjects (29,30). Alterations in the stress response were found in a sub-sample of the stunted children at 9–10 y of age (24) and could be another mechanism by which childhood undernutrition might affect later psychological functioning. We plan to investigate this possibility in the future.

We previously reported that an early childhood stimulation program had significant benefits to the stunted children's psychological functioning (13). We have shown here that the stunted children who received stimulation reported levels of anxiety, depressive symptoms, and self-esteem similar to those of the nonstunted participants. This is very encouraging and emphasizes the importance of early interventions. The only detectable remaining deficit in the stimulated stunted group was in hyperactive behavior.

There is some evidence of associations between growth in utero and adult psychological functioning. Exposure to famine in utero increased the risk of schizophrenia (31) and antisocial behavior (32), and birth weight was associated with psychological distress, depression, and suicidal behavior (33–35). In the present study, birth weight was related to anxiety but not to any other psychological outcomes; however, few participants had birth weights <2500 g. There is less information relating postnatal growth to later psychological functioning. In the UK, weight at 1 y was related to incidence of suicide (36) and weight gain from birth to 7 y was related to psychological distress (33).

A limitation to this study is that the instruments used have not been validated in Jamaica. However, the associations between the scores of the scales and socioeconomic background, gender, and IQ were theoretically sensible, the test retest reliability was good, and the internal reliability of the scales acceptable. We made minor modifications to the wording to facilitate better understanding by the participants and gave the questionnaires by interview because the participants' reading ability was not always adequate. We did not remove any items and it is likely that the external validity of the revised instruments would be similar to that of the original scales; however, it would be desirable to have this confirmed with clinical assessments in the future.

We used a conservative approach to examine differences between the nonstunted and stunted groups, including as covariates any variables that were correlated with the outcomes even if they did not differ among the groups. To achieve the most parsimonious model, we included covariates using stepwise analyses. Thus, although the associations found between covariates and the outcomes are plausible and consistent with the literature, it is possible that some of these may be due to chance.

Maternal depression has been shown to be associated with poor growth and undernutrition in children (37,38). Maternal psychological status, including depression and anxiety, is also an important contributor to poor adolescent mental health (39,40). We did not measure maternal affect or depression; however, it is unlikely to have been the main cause of stunting in this study. In a subsequent study of undernourished and adequately nourished Jamaican children (41), mothers of undernourished children were more likely to report depressive symptoms. However, depression did not predict the likelihood of the child being undernourished once socioeconomic factors were considered.

In conclusion, we have previously shown that stunting in early childhood is associated with deficits in cognition and educational achievement in late adolescence (11). This study provides probably the first evidence, to our knowledge, linking stunting and poor psychological functioning, extending the range of disadvantages attributed to early childhood stunting. Deficits were seen in emotional outcomes and in some aspects of behavior. Poor psychological functioning is likely to affect the participants' quality of life and may influence their social competence and parenting. The etiology of stunting may vary between settings with low or high prevalence. Further studies of the association between stunting and later psychological functioning are needed, particularly from countries where early childhood stunting is more prevalent than in Jamaica. Considering that 151 mil-lion children <5 y old in developing countries are estimated to be stunted (42), the findings further emphasize that stunting in early childhood is a serious public health concern.


   ACKNOWLEDGMENTS
 
We thank Amika Wright and Sydonnie Shakespeare-Pellington for conducting the interviews.


   FOOTNOTES
 
1 Supported by a grant from the Wellcome Trust (no. 066088). Back

2 Author disclosures: S. P. Walker, S. M. Chang, C. A. Powell, E. Simonoff, and S. M. Grantham-McGregor, no conflicts of interest. Back

Manuscript received 14 March 2007. Initial review completed 10 May 2007. Revision accepted 29 August 2007.


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 ABSTRACT
 Introduction
 Participants and Methods
 Results
 Discussion
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H. Baker-Henningham, J. D. Hamadani, S. N. Huda, and S. M. Grantham-McGregor
Undernourished Children Have Different Temperaments Than Better-Nourished Children in Rural Bangladesh
J. Nutr., September 1, 2009; 139(9): 1765 - 1771.
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F. H. G. Ferreira and N. Schady
Aggregate Economic Shocks, Child Schooling, and Child Health
World Bank Res. Obs., August 1, 2009; 24(2): 147 - 181.
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