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Community and International Nutrition

Iron Deficiency and Physical Growth Predict Attainment of Walking but Not Crawling in Poorly Nourished Zanzibari Infants¹

Patricia K. Kariger², Rebecca J. Stoltzfus, Deanna Olney^*, Sunil Sazawal, Robert Black, James M. Tielsch, Edward A. Frongillo, Sabra S. Khalfan^** and Ernesto Pollitt^*

Division of Nutritional Sciences, Cornell University, Ithaca, NY; ^* Program in International Nutrition, University of California, Davis, CA; Bloomberg School of Public Health, The Johns Hopkins University, Baltimore, MD; and ^** Pemba PHL-IdC, Zanzibar, United Republic of Tanzania

²To whom correspondence should be addressed. E-mail: pk75{at}cornell.edu.

	ABSTRACT

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Locomotion allows infants to explore their environment, promoting development in other domains. Motor progression involves biological systems and experiential factors. Nutritional deficiencies could interfere with systems involved in locomotion. This study examined the associations between height-for-age (HAZ), weight-for-height (WHZ) Z-scores and anemia-iron status on locomotion in 646 Zanzibari infants. Motor milestones were assessed by trained observers using a 14-item scale. Two mutually exclusive samples were created. The crawling sample (n = 167, 6–18 mo old) included infants that crawled only or did not crawl; the walking sample (n = 479, 9–18 mo old) included children that walked alone or did not walk alone. Of the crawling and walking samples, 82.6 and 83.9% respectively, were iron deficient and/or anemic (hemoglobin < 100 g/L; zinc protoporphyrin 90 µmol/mol heme). Stunting (HAZ less than –2) occurred in 30.5% of the crawling sample and 38.4% of the walking sample. Logistic regression models estimated the influence of factors on crawling vs. not crawling or walking vs. not walking. Two models were tested: 1) included sex, age, SES, HAZ and WHZ; 2) added anemia-iron status category to Model 1. HAZ improved the odds of crawling by 30%, but was not significant in either model. Model 2 fit the walking sample data best (P < 0.0001); an increase in HAZ doubled the odds of walking and nonanemic, noniron deficient children were 66% more likely to walk than those with anemia and/or iron deficiency. In this sample of poorly nourished infants, growth and anemia-iron status are significant predictors of walking, but not crawling.

KEY WORDS: • iron deficiency anemia • physical growth • motor development • infants • East Africa

Although there is some interindividual variability in the timing and sequence of motor milestone acquisition, it is now generally recognized that gross motor development follows a species-specific progression (1). In contrast to early assumptions (2) that cerebral and neuromuscular maturation were the sole determinants of motor milestone acquisition, it is now recognized that other developmental events such as physical growth and increasing independence from caregivers contribute to these transformations in motor skills. It is of particular interest that the acquisition of some motor milestones such as crawling and walking will in turn trigger changes in other developmental areas (e.g., cognition).

The onset of crawling and walking can occur only when biologically related systems, such as muscle strength and the ability to balance, reach critical values. The development of these systems may be asynchronous, and delay in the development of any one variable may impede the manifestation of the new motor skill (3–5). In addition, the capacity to practice appears to be important; 2 recent articles demonstrated that experience accounted for improvements in both crawling (6) and walking skills (7) after controlling for other factors such as body proportion and age.

Studies documenting motor progression have been conducted in well-nourished populations in which muscle strength, anthropometry and body dimensions are determined largely by age or normal biological variability. In poorly nourished populations, however, muscle strength, body size and body proportion are also affected by nutritional deficiencies. The influence of physiologic differences (due to nutritional deficiencies) on the acquisition of motor milestones may be more pronounced than is the case in well-nourished populations. Two nutrition-related problems common among infants and toddlers in developing countries are anemia and growth faltering.

There are no known studies relating differences in locomotion onset to iron status; however, the relation between iron status and the development of gross and fine motor skills has been studied. Young children with iron deficiency anemia (IDA)³ (6) perform worse on global tests of motor development compared with iron-replete children (8–14). Moreover, there is evidence from randomized control trials that deficient children treated with iron "catch up" with their nondeficient counterparts on post-treatment evaluations of motor development (8,15).

Growth faltering has also been related to delayed motor development in young children (16). In a cross-sectional study of infants, stunting was associated with slower acquisition of locomotive milestones (i.e., crawling, walking) compared with developmental norms from a healthy U.S. sample (17). Furthermore, a meta-analysis of studies on the effects of supplementary feeding on motor development indicated that supplementation improves motor development in nutritionally at-risk infants/toddlers (18). A recent year-long supplementation trial in a sample of malnourished infants in rural Indonesia found that children administered an energy-micronutrient supplementation walked earlier than children receiving a placebo (19).

The purposes of this study were as follows: 1) to describe the gross motor development in a cross-sectional sample of poorly nourished infants and toddlers from Zanzibar; and 2) to examine the development of crawling and walking in relation to (a) physical growth and (b) anemia-iron status. We hypothesized that anemia and/or iron deficiency (ID) would influence the development of crawling and walking independently of physical growth.

	SUBJECTS AND METHODS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Setting and sample. The study took place in Pemba, a small (68 km x 23 km), densely populated (350,000) island in the Zanzibar archipelago, United Republic of Tanzania. Pemba is predominately rural, and the main occupations are farming and fishing. The population for this study was a community-based, geographic subsample of a larger trial sample drawn from the entire island of Pemba. A house-to-house census was conducted, and all 5- to 18-mo-old children from 8 shehias or municipalities were invited to participate. A total of 932 gave their consent, of which 687 had complete baseline data. All participants were enrolled in a large, randomized, 2 x 2 factorial trial of daily zinc and/or iron-folic acid supplementation on growth, anemia, morbidity, mortality, and child development. Data for the present cross-sectional study were gathered at baseline, before the iron-folic acid and zinc supplementation intervention, between March 2002 and June 2002. The study was approved by human subjects review committees at the Johns Hopkins Bloomberg School of Public Health, the Zanzibar Health Research Council, the University of California at Davis, and Cornell University.

    Assessment of nutritional status. Medical personnel in local clinics drew 3 mL of blood by venipuncture; blood samples were stored in Vacutainer tubes (BD, Franklin Lakes). Hemoglobin (Hb) was measured with a HemoCue hemoglobinometer (HemoCue, Angelhom) using a small amount of whole blood (1–2 drops) from the venous blood sample. Zinc protoporphyrin (ZPP) was assessed by hematofluorometer (Aviv Biomedical) to indicate iron status.

All measures of growth were made in duplicate at the clinic by trained staff. Height was measured with a length board (Shorr Productions); weight was assessed with a digital scale (Seca). Height and weight Z-scores for age and sex were computed with a statistical package (Stata) using a program that implemented the 1983 WHO international growth references (20). In accordance with international guidelines, stunting was defined as height-for-age (HAZ) less than –2 Z-score; wasting as weight-for-height (WHZ) less than –2 Z score; and underweight as weight-for-age (WAZ) less than –2-Z score.

    Assessment of socioeconomic status (SES). Fieldworkers gathered information on socioeconomic variables from household members via questionnaire. These data served as indicators of gradients of SES. One refers to the personal and family resources to meet basic needs (annual cash income, the education of each parent, father’s employment); the other refers to physical properties of the environment and the quality of the immediate surroundings of the children (wall type, roof type, source of water). These individual variables were used in other nutrition-development studies (12,21). In our study, none of these individual variables were significantly related to the children’s Hb, ZPP, HAZ, or WHZ. A composite score was created as an index of SES that ranged from 3 to 25. This composite score maximized the reliability of the items following standard psychometric theory and practice (22). The reliability of the scale was good (Chronbach’s = 0.694), indicating the internal consistency of the variables. Furthermore, it is more efficient to use fewer, rather than more variables in regression models when the variables are consistent with one another. The SES index variable was used in all analyses.

    Motor milestone assessments. Gross motor development was measured with a pictorial milestone chart, adapted from the work of Pollitt and colleagues (17). The scale was based on the work of McGraw (23), who proposed a sequential development of motor skills involved in movement, ranging from propulsion of the upper body to bipedal locomotion. The measure consists of 17 items, ordered from least advanced (i.e., sits with support) to most advanced (i.e., running) and was developed for use with undernourished infants 12–30 mo old. This measure is also the basis for the gross motor development reference currently under development by the WHO (24). For the present study, the scale was extended downward to include items appropriate for infants 6–12 mo old, and items were added at the upper end of the scale to avoid a ceiling effect. The added gross motor behaviors were drawn from the age-normative Bayley Psychomotor Index (25). Pilot testing of the milestone chart demonstrated that the ordering of the items generally captured the progression of infant motor development in Pemba. Behaviors that were not easily observed in the pilot study were dropped from the scale. The final scale was composed of 14 items (Table 1).

    Analyses. Binary logistic regression models were used to determine the influence of nutritional status on 2 locomotive behaviors, crawling and walking alone. Because the normative ages for the onsets of crawling and walking alone are typically different (26) and likely involve different psychobiological determinants (27), children were divided into 2 mutually exclusive samples before analyses. The crawling sample included noncrawlers, infants coded in milestones 1–6 (see Table 1), and crawlers, infants capable of hands and knees crawling (milestone 7), but not any of the upright milestones. Children in the crawling sample were 6–18 mo of age.

The walking alone sample consisted of nonwalkers, children whose highest achieved milestones were standing with help, walking with help or standing alone (milestone 8–10), and walkers, children able to walk independently, run, jump, or stand on 1 foot (milestones 11–14). The children in the walking sample were 9–18 mo old, the age span of children observed to be walking alone. To avoid biasing of the sample, 41 children < 9 mo old who were nonwalkers were excluded.

Two sets of analyses were conducted. The dichotomous dependent variables were either crawling vs. not yet crawling or walking alone vs. not yet walking alone. Each set of analyses included 2 models, which controlled for sex, age, and SES. Model 1 examined the effects of physical growth (HAZ and WHZ) on predicting locomotion. Model 2 added a categorical anemia-iron status variable to Model 1. Children were classified as iron sufficient (Hb 100 g/L, ZPP < 90 µmol/mol heme) or anemic and/or iron deficient (Hb < 100 g/L,ZPP 90 µmol/mol heme). The cutoff value used for Hb was determined to be 2 SD below the mean Hb concentration of iron-sufficient infants in a recent study (28). The ZPP cutoff corresponds to the value 2 SD above the mean ZPP concentration in the same sample. Iron-sufficient children were the referent group to whom the other groups were compared.

	RESULTS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Description of participants. There were 167 infants in the crawling sample, of which only 27 were crawling. The walking alone sample included 479 children; of these, 220 were capable of walking alone or had achieved a more advanced milestone. Approximately 48% of the children in each sample were female, and the ages of the children (mean ± SD) were 13.6 ± 2.7 mo for the walking sample and 8.0 ± 2.2 mo for the crawling sample (Table 2). Growth faltering was prevalent in both groups as were anemia and ID. When grouped according to Hb-iron status, nearly identical percentages of children in the walking and crawling samples were iron sufficient (16.1 and 17.4%, respectively).

View larger version (16K): [in this window] [in a new window]   FIGURE 1 Selected milestone attainment by age, in Pemba (present study) and comparable studies. Points are the median ages (mo) at which the milestones were observed.

View larger version (16K): [in this window] [in a new window]   FIGURE 2 Adjusted mean predicted probabilities of walking alone by age (mo) and anemia-iron status group. The probabilities were derived from Model 2, which controlled for sex, age, SES, HAZ, WHZ, and anemia-iron status. The groups were defined as nonanemic, iron sufficient (Hb 100 g/L and ZPP < 90 µmol/mol heme) and anemic and/or iron deficient (Hb < 100 g/L and/or ZPP 90 µmol/mol heme).

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

On the basis of previous work in Pemba (31), it was expected that the majority of children in both the crawling and walking alone samples would be anemic and/or iron deficient, and that growth faltering would be prevalent, as was the case. Current nutritional guidelines generally identify nutritional risk in infants in developing countries as occurring at 4–6 mo of age, when perinatal micronutrient stores are no longer adequate for meeting infants’ needs (32), and exclusive breast-feeding is no longer sufficient to meet the dietary requirements and growth demands of infants (33). Thus, the prevalence of IDA, stunting, and thinness increases during the latter half of y 1 of life, due to a host of factors that may include inadequate diet (34), disease, and infection (35). In Pemba, Plasmodium falciparum is holoendemic, and geohelminth infections are highly prevalent (31); each of these is a causal factor for anemia. These parasitic infections, in combination with the depletion of iron stores during the latter half of y 1 of life, could increase infants’ vulnerability for developing anemia and/or ID.

    Milestone acquisition. The developmental curve for the pooled subjects’ attainment of motor milestones was similar to that of a sample of growth-faltering Indonesian infants (17) and was delayed compared with the developmental norms from a standardized assessment of infant gross motor skills (26). This delay is in contrast to cross-cultural research that suggests motor skill precocity in East African infants reared in traditional, nonindustrial settings (36,37). The earlier attainment of some motor skills among East African infants, compared with Western infants, is believed to result from caregivers’ training of young infants to develop by propping them up to sit or holding them in a standing position. The delayed motor progression among the Pemban infants indicates that the motor precocity attributed to East African infants is not evident in this sample, which may be due in part to the effects of severe nutritional deficiencies. It is also plausible that the caregiving practices in Pemba may not foster motor development as observed in other populations in Eastern Africa, or that the evidence for such precocity is overstated.

    Analyses of nutritional influences on walking independently and crawling. The results from the multivariate model with the walking sample indicate that both height-for-age and weight-for-height were positively associated with walking alone. In addition, the odds for nonanemic, iron-sufficient children to be observed walking were 66% greater than for anemic and/or iron-deficient children. Within the crawling sample, neither growth nor anemia-iron status were significant predictors of crawling, although a unit increase in HAZ improved the odds of crawling by 30%.

Given the prevalence of IDA in both samples, we did not expect to find that anemia and iron status were related to walking but not crawling. There are several possible explanations of why this might be. From a statistical perspective, the small number of crawlers relative to noncrawlers may have reduced the power to find a significant difference in crawling due to anemia and/or ID. It could also be that the infants in the crawling sample suffered from other health conditions that were more potent predictors of crawling, thus obscuring the capacity to detect the effect of ID and/or anemia on the development of crawling. From a developmental theory perspective, it is also possible that the components necessary for crawling differ from those necessary for walking and are not adversely affected by anemia or ID. During hands and knees crawling, a child must learn how to stay balanced on 2 limbs as the body pivots around the wrist; in walking, a child must learn to stay upright on 1 foot as the body pivots around the ankle (38). The underlying constituents that make walking possible could be limited by ID and/or anemia, whereas those necessary for crawling are not.

What are the mechanisms through which ID and anemia may function to affect factors important for walking? There is evidence that iron-deficient rats are delayed in acquiring motor skills requiring strength and balance; furthermore, these skills are associated with regional brain iron and neurotransmitter metabolism (39). Lack of iron was also related to other biological changes that may prevent a child from practicing newly acquired behaviors important or necessary for improving body strength, postural control, and balance to enable independent walking. Laboratory studies with adults performing physical exertion tasks demonstrated that ID reduces tissue oxidation capacity, whereas IDA reduces oxygen-carrying capacity (40). The effects of these impairments on physical performance in adults are decreased energy efficiency, and diminished endurance and aerobic capacity, respectively. Although it is unlikely that toddlers expend as much energy walking as adults do in physical exertion tasks, a recent study of healthy, middle-class, U.S. toddlers estimated they took, on average, 9000 steps and spent 6 h daily in upright, balancing positions (38). ID and/or anemia could delay the onset of independent walking by altering neurotransmitter functioning and by deterring infants from practicing motor skills that require effort, strength, and balance.

An indirect effect of ID and/or anemia on walking could occur through behavioral manifestations associated with IDA in infants, including clinginess, withdrawal, and fussiness (41) that may inhibit a child’s motivation to walk independently. These behaviors may also influence how others interact with the child, i.e., a caregiver may hold a fussy child more than a child who does not fuss much, which could also contribute to a child’s moving around less (42). Moreover, the combination of ID and poor growth may serve to further hinder a child’s movement through the involvement of more of the integrated biological systems necessary for bipedal locomotion.

There is evidence that protein-energy malnutrition results in loss of muscle and a decrease in muscle fiber size, causing delayed locomotion in studies with animal models (43). To date, there is no research confirming comparable findings in humans, but it is possible that motor development in infants could be delayed through a similar mechanism. In addition, protein-energy malnutrition alters the body proportions of infants, which could also impede the onset or advancement of locomotive skills.

In our cross-sectional study, we cannot rule out the possibility that walking and, to some extent crawling, are simply markers of a more resilient child. That is, the relatively better growth and/or anemia-iron status of the crawlers and walkers suggests they had different responses to the conditions that typically cause anemia and stunting in Pemban infants. Their responses may have been modified by biological or environmental processes that buffered the effect these conditions would normally have on physical growth and anemia-iron status by enhancing their resiliency or resistance to such factors (44).

The reason for this is unclear. Neither the SES composite variable nor the individual components of that variable were predictive of growth, the anemia/iron indices, or locomotion. However, it is possible that the caregivers of walkers and crawlers engaged in behaviors that promoted better nutritional and health outcomes in their children. These caregivers may have had easier access to health services, or knowledge of practices that would reduce illness and disease as well as those that would encourage better nutritional status and motor development. The children themselves may reinforce these types of practices through their appearance or behaviors. Children who are growing well (relative to others), are more active, or have more mature motor skills may elicit different types of responses from caregivers, which in turn help to maintain their better health and development (45,46).

This study suggests the importance of examining how different types of malnutrition may alter various systems necessary for locomotion. Both growth and anemia/ID were independently involved in walking, but this was not the case for crawling. Such differences may be moderated by the biomechanics of the locomotive behaviors themselves as well as the biological mechanisms through which iron affects motor development. Care-giving practices are also likely to be involved in both the within- and between-sample differences in nutritional factors and motor skill observed.

Understanding the influences of nutritional factors on motor development in nutritionally at-risk infants is essential because delays in motor skills could reduce young children’s chances to partake in activities that typically lead to progression in other areas of development. For example, among the Yoruba in southwestern Nigeria, early walkers are more likely to be asked by caregivers to complete errands that take them outside of the house, giving them opportunities to use and develop language, memory, and problem-solving skills. In a study of 2-y-old Yoruba children, those who were sent to buy things for their parents had better cognitive test scores than children who were not given such responsibilities (47). Thus, the ability to move independently greatly changes a child’s engagement with the social and physical environment in ways that could advance development in other domains. Conducting studies aimed at further clarifying the relations between nutritional deficits and the course of development is indicated.

	FOOTNOTES

 
¹ Funded by the Gates Foundation and the U.S. Agency for International Development, Office of Health and Nutrition.

³ Abbreviations used: HAZ, height-for-age Z-score; Hb, hemoglobin; ID, iron deficiency; IDA, iron deficiency anemia; SES, socioeconomic status; WAZ, weight-for-age Z-score; WHZ, weight-for-height Z-score; ZPP, zinc protoporphyrin.

Manuscript received 16 August 2004. Initial review completed 30 August 2004. Revision accepted 12 January 2005.

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