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Supplement

Developmental Sequel from Early Nutritional Deficiencies: Conclusive and Probability Judgements¹

Department of Pediatrics, School of Medicine, Program of International Nutrition, University of California, Davis, CA 95616

	ABSTRACT

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
Results from quasi-experimental longitudinal studies of children and from experimental research with animal models have led several investigators to state that early iron deficiency anemia leaves a permanent cognitive deficit. However, neither source of information provides a basis for such a claim. Some key confounders were not controlled by the quasi-experimental studies, and the external validity of the animal data is questionable. Further, three decades of research on the functional consequences of protein-energy malnutrition have shown that the social environment moderates the effects of an early nutritional insult; it can keep such effect unchanged, or increase or decrease its severity. The prediction of later life on the basis of a particular nutritional event carries a large error factor, which suggests that the search would be more fruitful if we tracked probability statements.

KEY WORDS: • protein-energy malnutrition • iron • anemia • cognition • development.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
During the last 30 years, I have conducted research on the effects of protein-energy malnutrition (PEM) and iron deficiency on intellectual development in children. Over the course of this work, it has become increasingly evident that although these two conditions affect mental development and cognition, these are not the only developmental effects that are of concern. PEM and iron deficiency anemia negatively affect a broad range of developmental domains that are closely interrelated, including emotional regulation, motor development and motor activity.

Several researchers have attempted to determine whether the effects of PEM on child development are long lasting and permanent, particularly as they relate to cognition. A large body of data has been accumulated in an attempt to resolve this issue, using animal models and longitudinal studies of children. Conclusive answers are not yet available, but we are more knowledgable than we were two to three decades ago.

As investigators of iron deficiency anemia, we are now asking the same question. Is the cognitive delay incurred by iron deficiency anemia in infants irreversible? With new concepts of developmental psychobiology in mind and data from PEM research, I would like to address in this paper the putative permanent effects of early iron deficiency anemia on later developmental outcomes.

	Protein-energy malnutrition and development

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
PEM and children.

One distinct characteristic of the research on PEM and child development is the selective focus on learning and intelligence. Clinical and field studies used primarily mental development scales for infants and toddlers, and IQ tests or cognitive tasks for older children. Some studies that followed subjects up to the school years measured variables related to school readiness and performance (Chavez et al. 1995 , Pollitt et al. 1993 ). Researchers in the field today regret the adoption of such a restricted view because the oversight has been costly. Cognition maintains close functional ties with emotional regulation, motor development and motor activity; it is now recognized that these domains are the centerpieces of the psychobiology of human development (Thelen and Smith 1998 ) and that together they contribute to shape the course of child development (Gottlieb et al. 1998 ).

PEM and animal models.

Historically, work in animals on the functional consequences of energy and protein deprivation has moved in two directions. One approach has moved toward an understanding of the developmental changes in the anatomy and biochemistry of the brain in experimental animals (Dobbing J. 1990 , Winick and Noble 1966 ) The other approach has moved toward describing the compromise of behavioral competence (Barnes et al. 1970 , Cowley and Griesel 1963 , Platt and Stewart 1968 , Zimmermann 1969 ). This research on animal behavior goes far beyond learning. As early as the 1960s, researchers documented the long-lasting effects of malnutrition on alterations in eating behavior, increased emotionality and anxiety, increased reactivity to unfamiliar environment and disturbed social behavior (Levitsky and Strupp 1995 ).

The following section discusses the vulnerability of the human organism during the early stages of development and the validity of the critical period hypothesis for child development.

	PEM and the critical period hypothesis

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
An important and early outcome of PEM and neurobiology research on laboratory rodents was the observation that brain growth retardation induced by PEM during the suckling period was not entirely reversed with subsequent ad libitum feeding (Dobbing 1990 , Levistsky and Strupp 1995 ). These observations gave credibility to the hypothesis that a nutritional insult during suckling, which is a critical period of cerebral growth, has permanent functional effects. However, only part of this premise has been validated. Researchers who initially documented the effects on rodent cerebral growth did not allow enough time for catch-up growth to occur. After a period of malnutrition, cortical cell division lasts longer than that of controls. Although there is the opportunity for recovery, there is also evidence of permanent cortical injury. Limitations in the density and arborizations of dendrites and width of the cortical cells have been established. Neurotransmitter systems are also altered permanently. For example, the number of norepinephrine receptors is reduced compared with controls (Levitsky and Strupp 1995 ).

The external validity of observations in laboratory animals and their generalizability to the mental development of undernourished children were not obvious. It has taken >20 y to accumulate evidence from longitudinal studies of undernourished children to address some aspects of this issue. No definitive answers are yet warranted, but the available data show that improvements in the quality and quantity of the diet and in the satisfaction of basic needs prevent or remediate at least in part the early effects of malnutrition.

	Beneficial effects of nutritional interventions and environmental changes

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
This section reviews three studies on the cognitive effects of supplementary feeding at different periods of early life and two studies on malnourished children who were adopted before 36 mo of age. By pooling the data from these five studies, it is possible to see the complexity and probable error of making predictions regarding long-term developmental effects on the basis of a single event in early childhood, even in the case of PEM.

A study in Guatemala showed that adolescents who had received a supplement of 11.5 g of protein and 682 kJ pre- and postnatally during the first 24 mo of life scored significantly higher on tests of knowledge, numeracy, reading and vocabulary than subjects who had received a 246-kJ supplement during the same period (Pollitt et al. 1993 ). The subjects enrolled in the study after the first 24 mo of life also benefited from the high protein and energy supplement but to a lesser degree than those enrolled at an earlier age. Social and economic variables appear to moderate the effects because the beneficial effect was restricted to children at the lowest level of the socioeconomic scale.

Another study in Colombia (Pollitt and Perez-Escamilla, unpublished) showed that a comprehensive experimental intervention that included health care, supplementary feeding and educational opportunities, beginning at 42 mo of life, also benefited cognition. During the intervention period, beneficial cognitive effects were observed, but they faded away after the intervention ended. A third study demonstrated that a 90-d high energy supplement during infancy had long-lasting effects on cognition (Pollitt et al. 1997 ). Children (n = 334) aged 6–60 mo living on rural tea plantations in West Java participated in a 3-mo randomized trial to test the effects of a dietary supplement providing ~ 1672 kJ energy/d with about the same nutrient density as local foods. Two thirds of the original sample were enrolled in a follow-up study 8 y after the experiment. Several measures of intelligence and information processing were used to evaluate the study groups. The supplemented group showed no differences from those in the control group. However, when the analysis was limited to subjects who had received the supplement before the age of 18 mo, the supplemented children performed better than control children on a test of a very specific cognitive domain, working memory.

Grantham-McGregor and Buchanan (1982) published a case report study in Jamaica of an 8-mo-old severely malnourished child who was hospitalized. After rehabilitation, the child’s IQ was ~70 and he went back to the same environment that contributed to his original malnutrition. Two years later, the child was adopted by a school teacher. By age 5, the child’s IQ was higher than the average IQ of children of lower socioeconomic status in Jamaica.

Similar information exists for adopted girls from an orphanage in Korea (Winick et al. 1975 ). All of the children were taken to the adoption agency when they were <2 y old; they were adopted by American families when they were <3 y old. At the time of adoption, they were classified into groups indicating whether they were malnourished, moderately well nourished or healthy. When the children were in elementary school, the mean IQ of these three groups was 102, 106 and 112, respectively. The only significant difference was between the malnourished and the healthy group (P < 0.001). Although the IQ of the malnourished group was lower, it should be noted that it was within the normal range of the standardized U.S. population.

Tentative conclusions.

In communities in which malnutrition is endemic, supplementary feeding that meets nutritional requirements of children during the first 18–24 mo of life may help to prevent part of the cognitive delays caused by extreme poverty and malnutrition. At times, these effects will be restricted to fairly specific cognitive processes. Once past the 18- to 24-mo period, the developmental benefits of the supplement will vary as a function of the breadth (e.g., nutrition, health, education) and duration of the intervention, i.e., the broader and the longer the duration of the intervention, the higher the probabilities of recovery. In addition, moderating factors can either maintain such beneficial effects or modify them by either decreasing or increasing the severity of the functional insult.

	Gaps in knowledge

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
Experimental studies of laboratory animals, as well as clinical and field studies of children, are generally guided by the idea that within species, the breadth and depth of the effects on mental development are equivalent among malnourished organisms. Individual differences and moderating variables are usually ignored. A second notion commonly held is that cognition is the determinant of human adaptation, competence and productivity within societies. Other domains such as social competence and emotional regulation are often overlooked. Finally, with few exceptions, there is a de facto disregard of the potential relationships among different effects in different developmental domains.

	Areas that require further investigation

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
Emotions.

Undernourished infants and toddlers are often irritable, clingy, fussy, easily frustrated and fearful of novel stimuli compared with better-nourished children (Graves 1976 ). Reports of these characteristics have a long history in the clinical descriptions of malnourished children. Similarly, as noted, alterations in emotion and motivation were among the first distinctive behaviors described in laboratory animals in experimental studies of malnutrition and behavior. Compared with controls, rodents with a history of undernutrition show erratic motivation, increased emotionality, greater anxiety and poor adaptation to distressing environmental stimuli (Levitsky and Strupp 1995 ).

Motor development and activity.

Although large amounts of data exist on the effects of PEM on physical growth and there is documentation that PEM also limits motor development, there has been little work done on the functional relationships among growth, motor development and motor activity (Meeks-Gardner and Grantham-McGregor 1998 ). Body size, body proportions and body mass along with muscle and bone strength also affect the onset of locomotion (Thelen and Smith 1998 ). The physics and engineering of the biological-mechanical system play key roles in motor actions. In humans, for example, the infant’s balance and extensor muscle strength must reach critical values to enable the infant to support its weight in a stable manner on one leg, while it lifts the other to take a step (Thelen and Smith 1998 ).

Comments.

Studies of PEM and child development have been compartmentalized in that only specific aspects have been assessed, without consideration of the different variables that also affect development. The developmental interrelationship of these variables has been ignored, yet early in life, physical growth, motor development, motor activity and emotional regulation are not independent of each other (Pollitt in press ). For instance, self-initiated locomotion (e.g., crawling, walking) represents motor changes that are critical for the development of visual perception, spatial orientation and emotional regulation (Adolph 1997 ). Further, as noted, the variability among children to deal with their social and physical environment does not depend on differences in cognition alone. Personal style such as the capacity to inhibit inappropriate behaviors and to cope effectively with internal and external stimuli will influence a child’s behavioral-emotional adjustment and the ability to function in different contexts.

	Iron deficiency anemia in children

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
The study of iron deficiency anemia in childhood, particularly during the 1970s and 1980s, also gave priority to the study of early mental development and to cognition among preschool and school-age children (Pollitt et al. 1985 , Seshadri et al. 1982 , Watkins and Pollitt 1998 ). However, there are noteworthy exceptions. Lozoff and her collaborators documented changes in the regulation of emotions among iron-deficient anemic infants through several publications (Lozoff and Brittenham 1986 , Lozoff et al. 1986 ). Such infants present wariness, hesitancy, tiredness, inattentiveness and general lack of involvement with testing stimuli (Lozoff et al. 1998 ). Furthermore, as in the case of PEM, several studies have shown that iron-deficient anemic children demonstrate delayed motor skills as documented by comparatively poor scores in the Bayley Scales of Motor Development. There is also evidence that iron deficiency in laboratory animals imposes limitations in physical activity levels (Hunt et al. 1994 ).

About 25 y ago, Cantwell (1974) first reported that iron deficiency anemia could produce long-lasting neuropsychologic effects. Thereafter, several studies have shown an association between iron deficiency and poor performance later in life (Palti et al. 1983 ). A recent epidemiologic study conducted in Florida addressed the relationship of early nutrition and mental function later in life (Hurtado et al. 1999 ); that study offers suggestive evidence of this association. The study linked the health records of 5411 children, 1–5 y old, who had been enrolled in the Special Supplemental Program for Women, Infants, and Children (WIC) with mental function assessed from school records. Researchers attempted to determine the association between anemia [hemoglobin (Hb) <2 SD of the median reference standard] and mental retardation. Mild-to-moderate mental retardation (i.e., educable mentally handicapped or trainable mentally handicapped) was evaluated according to the criteria used by the Florida Department of Education. Results indicated that after controlling for birth weight, maternal education, sex, race-ethnicity, age of mother and age of child, a decrement of one unit in Hb was associated with an increased risk of 1.28 (odds ratio) of mild-to-moderate mental retardation.

Lozoff et al. (in press) recently reported on the mental and motor function of 12-y-old subjects who had been treated for iron deficiency anemia in infancy. Biochemical tests had been used to establish the iron status of the children when they were infants, ~12–23 mo old. All of the 191 iron-deficient anemic infants had been placed on a successful iron therapy program for 3 mo. Those infants classified as moderately anemic obtained lower mental and motor scores before and after treatment than those classified as normal. The mildly anemic subjects were also at a disadvantage in motor, but not in mental development. Ten years later, 87% of the original sample were enrolled in the follow-up study and were classified into one of four groups: 1) moderate iron deficiency anemia; 2) iron deficiency before and after treatment (children with higher Hb levels who still had biochemical evidence of iron deficiency after 3 mo of therapy); 3) iron deficiency fully corrected; and 4) good iron status before and after treatment. For statistical purposes, the first two groups were combined (i.e., iron-deficient group) and compared with the last-mentioned group. After adjustment for covariates, the iron-deficient anemic group had poorer scores than the comparison group in the arithmetic and reading component of the wide-range achievement test. These findings are consistent with the 5-y follow-up data (Lozoff et al. 1991 ).

The results of the Lozoff studies are noteworthy but there are concerns regarding study design. Even though the investigators controlled carefully for some of the potential confounders, the quasi-experimental design did not allow them to ensure the control of other confounders of perhaps greater importance. In particular, there was no way to determine whether the internal family environment and caretaking processes among the severely anemic children were different from those of the well-nourished children.

	Support from neurobiological data

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
Since the early 1970s, several investigators have shown that the presence of iron deficiency anemia affects the availability of brain iron within specific anatomical regions and biochemical systems (Chen et al. 1995 , Dallman and Spirito 1977 ). For example, Dallman et al. (1975) showed substantive reduction of cerebral iron after the full repletion of body iron in rats that became iron deficient for short periods at the time of weaning [see also Felt and Lozoff (1996) ]. In normal rats during this period, brain iron is accumulating at its highest pace (Beard et al. 1993 ). The depletion of iron in the brain (Erikson et al. 1997 ) affects neuronal processes and neurotransmitter metabolic changes critically involved in the development of particular behavioral domains. For example, it is plausible that either delays in the timing of myelination (Connor and Menzies 1996 ) or changes in D2 dopamine receptors (Ashkenazi et al. 1982 ), or both, may explain the delays in motor development that have been reported in iron-deficient anemic infants and children.

Comments.

Data from animal models provide some support for the claims that early iron deficiency anemia is a cause of impaired cognitive function in later life. Changes in D2 receptors, delays in the formation of the myelin sheath or alterations in neural networks would be the intervening variable between deficiency and function. Despite this evidence, I would still advocate caution and scientific objectivity based on the following arguments.

1) Studies of PEM show that environmental factors can moderate the relationship between early nutritional insult and later developmental disadvantage.

2) Profound salutary developmental changes can occur after the age of fastest brain growth when the environment changes and the child’s basic needs are met without interruption.

3) There are no data that show that the observed delays of cognition reported for children in middle or late childhood, who were iron deficient as infants, were not a result of intrafamily process variables. Control of potential confounders in studies is usually restricted to structural variables rather than to variables depicting caretaking and interactive processes within the family.

4) There is no documentation that shows that the cerebral alterations produced by experimentally induced iron deficiency anemia in rodents are the underpinning for cognitive delays of children.

	SUMMARY

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 
The limitations in the prediction of future development based on early assessments are not a problem of research design or methods. In fact, the data on early nutritional insult and later performance show that it is sometimes possible to predict the developmental trajectory on the basis of a single biological or psychological event during the first 24 mo of life. However, the probabilities that such a prediction will be internally valid are quite low. In other words, there is a large margin of error. What the data do show is that the strength of the prediction depends in part on the documentation of the nature and characteristics of the child’s development before and after the predictive event.

	FOOTNOTES

 
¹ Presented at the symposium entitled "Dietary Zinc and Iron—Recent Perspectives Regarding Growth and Cognitive Development" as part of the Experimental Biology 99 meeting held April 17–21 in Washington, DC. This symposium was sponsored by the American Society for Nutritional Sciences and was supported in part by an educational grant from the National Cattlemen’s Beef Association. Symposium proceedings are published as a supplement to The Journal of Nutrition. Guest editors for this supplement publication were Harold H. Sandstead, University of Texas Medical Branch, Galveston, TX and Phil A. Lofgren, National Cattlemen’s Beef Association, Chicago, IL.

	REFERENCES

TOP ABSTRACT INTRODUCTION Protein-energy malnutrition and... PEM and the critical... Beneficial effects of... Gaps in knowledge Areas that require further... Iron deficiency anemia in... Support from neurobiological... SUMMARY REFERENCES

 

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Pollitt, E. Search for Related Content PubMed PubMed Citation Articles by Pollitt, E.