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Community and International Nutrition

Growth and Diet Quality Are Associated with the Attainment of Walking in Rural Guatemalan Infants¹

Elena V. Kuklina^*, Usha Ramakrishnan^,2, Aryeh D. Stein, Huiman H. Barnhart^** and Reynaldo Martorell

^* Program in Nutrition and Health Sciences, Graduate Division of Biological and Biomedical Sciences, and Department of International Health, Rollins School of Public Health, Emory University, Atlanta, GA; and ^** Department of Biostatistics and Bioinformatics, Duke University, Durham, NC

²To whom correspondence should be addressed. E-mail: uramakr{at}sph.emory.edu.

	ABSTRACT

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The attainment of gross motor milestones is an important indicator of motor development in early life; however, little is known about factors affecting gross motor development in children from developing countries. The purpose of this study was to examine the relation of nutritional factors (physical growth and dietary intake) and morbidity during the first year of life to the age of walking without support. Multivariate regression models were used to analyze data collected prospectively between 1991 and 1999 in rural Guatemala. Attainment of children’s gross motor milestones was assessed monthly by trained field workers using the 17-milestone Gross Motor Development Scale, morbidity was assessed by biweekly recall, and dietary intakes were measured at 9 and 12 mo of age using repeated 24-h dietary recalls. Median age of walking was 15 mo (range 10–24 mo; n = 174) with no differences by gender. Models were adjusted for birth order, gender, gestational age, maternal age and education, socioeconomic status, and community. Growth in length (–0.57 ± 0.27 mo length for age Z-score; P = 0.04) and weight (–0.54 ± 0.19 mo weight for age Z-score, P = 0.005) during the first year of life, rather than size at birth, predicted age of walking. Animal protein intake from complementary foods, while low (mean < 1 g/d) overall, was positively associated with earlier age of walking (P = 0.02). Morbidity during infancy was not associated with age of walking. These findings indicate the importance of prevention of postnatal growth retardation and improvement of diet quality for children’s gross motor development.

KEY WORDS: • child growth • diet quality • morbidity • motor development

Since the 1930s it has been extensively documented that motor milestones are attained sequentially (1), but our understanding about the factors affecting this process is limited. Among the wide-ranging motor behaviors acquired during infancy, attainment of walking is an important milestone because it expands child independence, exploratory behavior, and physical activity, all of which are essential for the acquisition of motor, perceptual, and cognitive abilities (2). This milestone may be important for socioemotional development; children who begin to walk earlier have been shown to be more interactive, cooperative, and affectionate with their caregivers compared to those who begin to walk later (3,4).

Physical growth may constrain gross motor development. In developed countries, infants who are slimmer and more cylindrically proportioned begin walking sooner than do chubbier, top-heavier infants (5–7). Children in some developing countries begin to walk 1.5–3 mo later than their well-nourished American or European counterparts (6,8–10). However, little is known about the effects of physical growth on the motor development of children from settings with a high prevalence of growth retardation. In Pakistani infants, changes in both length-for-age (LAZ)³ and length-for-height Z-scores from 0 to 6 mo were inversely associated with age at commencement of independent walking (10).

In terms of diet, although several micronutrients such as iron, zinc, and essential fatty acids have been proposed to play a role in child development, few studies have examined the role of diet quality (11–14). Single nutrient deficiencies are uncommon in developing countries because the typical weaning diet often contains little or no animal foods, which are excellent sources of high-quality protein, fat, and bioavailable micronutrients (15). In the only intervention study published to date (4), children in Indonesia who received a high-energy food supplement (1171 kJ/d from condensed milk) along with iron (12 mg/d) supplements walked at an earlier age and were more active compared to those who received either the low-energy with iron (209 kJ/d + 12 mg/d of iron) or only low-energy (104 kJ/d) food supplement.

Another possible determinant of motor development in developing countries may be infectious diseases, but there is a paucity of data on this topic. Diarrhea is of particular interest because it is the most common cause of child morbidity in the developing world (16) and has a significant impact on linear growth by exacerbating pre-existing nutrient deficiencies through loss of appetite and reduced food intake, impaired nutrient absorption, and increased nutrient losses (17). In addition, infections also cause general malaise and apathy, which result in decrease of motor activity and less psychosocial stimulation from adults (18).

The aim of the present study was to examine the relation of nutritional factors (physical growth and dietary intake) and morbidity during the first year of life to the age of walking without support using data from a longitudinal study of child growth and development in rural Guatemala.

	SUBJECTS AND METHODS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The data were collected in the course of 2 longitudinal studies on pregnancy outcomes and early childhood growth and development that were carried out between 1991 and 1999 by investigators at the Rollins School of Public Health at Emory University in collaboration with Instituto de Nutrición de Centro América y Panamá (INCAP) in 4 villages in eastern Guatemala. The villages were those previously included in a community-based, food supplementation trial conducted by INCAP during 1969–1977 (19). All pregnancies between 1991 and 1999 were identified by routine surveillance. Between 1991 and 1995, only birth information was obtained, and between 1996 and 1999 all children were studied through age 3 y or study closeout. For children born prior to 1996, birth size was obtained from the 1991–1995 study. Attainment of children’s gross motor milestones was assessed monthly, starting at 3 mo of age, by trained field workers using the 17-milestone Gross Motor Development Scale (4). In this scale, walking without support is milestone 15. The child was encouraged by the field worker, with assistance from the primary caregiver, to present behavioral evidence of the highest level of motor maturation that might be expected from him/her based on the child’s age. Supervisors held periodic standardization sessions and 5–10% of examinations were replicated to assess reliability. Interrater reliability for the scale among children with observed walking without support assessed in 6% of the sample (n = 263) was 85%. Field workers were rotated among the villages every 2 to 3 mo.

Anthropometric measurements of children were obtained by trained field workers in duplicate at birth, 15 d, and monthly from 1 to 15 mo of age. Standardized techniques were used to collect weight measurements to the nearest 10 g and length measurements to the nearest 1 mm (20). All birth size measurements were done within the first 48 h after birth. Routine standardization sessions were conducted during training and the course of data collection. LAZ and weight-for-age (WAZ) Z-scores were calculated using the SAS Program for the CDC Growth Charts developed at the Division of Nutrition and Physical Activity, Centers for Disease Control and Prevention (21). Gestational age (expressed in weeks) was estimated from recall of the date of the last menstrual period and was verified by ultrasound in a subsample. Morbidity was assessed using biweekly recalls (19). Trained field workers made home visits every 2 wk and interviewed mothers/caregivers about their child’s health. Precoded forms were used to record signs, symptoms, and duration. Diarrhea was defined as 3 or more liquid stools in 24 h. Data were later summarized as episodes, duration of episodes, and percentage of time ill. We summarized all morbidity into 2 groups: diarrhea and/or anorexia vs. other. The child’s breastfeeding status was also ascertained during these visits. Nutrient intakes were ascertained by 24-h recall using a protocol previously validated in this population (19). Food quantities were recorded in grams and then converted to energy and nutrient values using the INCAP food composition values and extensively tested computer programs. In the current analysis, we used the data from repeated 24-h dietary recalls (2 weekdays and 1 weekend day) administered at 9 and 12 mo of age. Animal protein intake was calculated by summing protein intake from 5 food groups: meat, dairy products, eggs, seafood, and a miscellaneous group, which included pizza, tacos, burritos, and other mixed dishes. Total energy (kJ/d) and fat (g/d) intakes were also calculated. The mean of intakes at 9 and 12 mo was used to represent infant diet. In the case of children missing data at 9 mo, data collected at 12 mo of age were used. Almost 71% of children had data at both 9 and 12 mo.

Since children may have skipped 1 or more milestones between monthly observations, age at walking was interpolated for those who skipped this milestone. Specifically, we used data from children with records on milestones 14, 15, and 16 to estimate the relative intervals 14–15 and 15–16. For children missing milestone 15 but for whom milestones 14 and 16 were available, we used the mean relative intervals to assign an interpolated date for milestone 15. We extended this approach to cases with up to 3 missing milestones (e.g., a child who was observed to go from milestone 12 to milestone 16 between visits). Our data are interval censored and the motor milestone observed at a given visit had, in reality, been achieved at some time since the previous visit. We adjusted our estimates of age of walking by subtracting a randomly assigned unit of time within the range of the preceding interval.

    Sample selection. Children with data on age of walking, anthropometry at birth and 12 mo of age, and dietary intakes at 12 mo of age were included. Children for whom 4 milestones were not observed (n = 10) or only motor milestone 15 or higher were observed (n = 5) were excluded. All ages are expressed in months. For analyses that included morbidity, only children with at least 50% follow-up during the first year of life were included. The majority of the children (83%) had morbidity data for at least 75% of time.

    Statistical methods. Descriptive statistics (means and standard deviations for normally distributed variables and medians for non-normally distributed variables) were calculated. Multiple linear regression models were used to assess the relation of nutritional factors and morbidity to age of walking without support. To address the collinearity problem between energy intake and animal protein/fat intake we adjusted nutrient intakes for energy using the residuals approach (22). Energy, fat, and animal protein intakes were first log-transformed before the energy adjusted residuals were calculated. We used a similar approach to account for collinearity between measures of size at birth and 12 mo of age as we have done in previous work (23,24).

We examined crude associations between birth size (weight and length considered separately), infant growth, dietary factors, and morbidity with age of walking without support. We then adjusted the coefficients for maternal (community, socioeconomic status (SES), age, and education) and infant (gender, gestational age, birth order, breastfeeding status at 12 mo) factors. A third set of models also included birth size, postnatal growth, dietary intakes, and morbidity.

Age of walking without support, LAZ and WAZ scores, and energy, fat, and animal protein intakes were entered as continuous variables. Mother’s education was categorized as completed primary school if the highest grade of schooling completed was 6, noncompleted primary school, or missing. Breastfeeding status at 12 mo was categorized as yes, no, or missing. Maternal age was categorized as <25 y, 25–30 y, >30 y, or missing. Gestational age was categorized as <37 wk (preterm), 37–41 wk (term), >41 wk (postterm), or missing. Birth order was categorized as first born, non-first born, or missing. SES was expressed as the score derived from principal components analysis from data on household characteristics and possessions (25) and was categorized into tertiles and a missing group. Morbidity was categorized using tertiles. We also adjusted for the number of dietary assessments (12 mo only or 9 and 12 mo) and duration of follow-up for morbidity in days in models that included dietary and morbidity factors, respectively.

Regression coefficients were used to estimate the change in age of walking without support (mo) per unit increase in continuous variables (per Z-score or per g residual of log-transformed nutrient) and between low (2.2 and 9.8% for diarrhea/anorexia and other morbidity, respectively) and high (>7.0 and >19.6% for diarrhea/anorexia and other morbidity, respectively) morbidity groups.

All statistical calculations were performed using SAS (Version 8.2, SAS Institute) software packages for personal computers. The SAS GLM procedure was used for multiple linear regression analysis. Wilcoxon’s rank-sum test was used to compare the median age of walking between boys and girls. Two-sample t test and ² test were used to compare samples with complete and missing data. The level of significance for statistical tests was P < 0.05.

	RESULTS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Age of walking without support was ascertained for 383 children, among whom it was interpolated for 119 children. A total of 218 children were included in our analysis based on the availability of data on age of walking, birth length, and length at 12 mo of age. The reduction in the sample size is due to the fact that postnatal growth was not measured between 1991 and 1995. Data analysis was performed among children from the above sample with dietary data (n = 174; walking data, observed n = 121 + interpolated, n = 53) and both dietary and morbidity data (n = 154; walking data, observed n = 112 + interpolated, n = 42). Few children (<5%) had missing data on maternal age, maternal education, SES, birth order, or gestational age. Breastfeeding data, however, were missing for more children (20% in sample with n = 174 and 10% in sample with n = 154). There were no significant differences in age of walking without support, child growth, and several maternal and infant characteristics, but children who were missing breastfeeding data also had shorter gestational age (38.7 vs. 40.2 wk; P < 0.0001) and younger mothers (24.4 vs. 26.3 y; P = 0.03) when compared to those in the final sample. Similar differences were seen among children without morbidity data when compared to those with complete data.

The median and range for age of walking without support were 15 and 10–24 mo, respectively (Table 1). There were no differences by gender. Mean birth weight was 3.06 kg, about 6% of children were born premature (all had birth weight > 1.5 kg), and 14% of children were from postterm pregnancies. Mean LAZ and WAZ scores at birth were –0.5 and –0.7, respectively, and both LAZ and WAZ decreased by 1 Z-score over the first year. Maternal educational status was low; only 28% had completed primary school. There were 17% of first-born children in the sample. Breastfeeding was widespread, with 89% of children still breastfed at 12 mo. The average energy intake from complementary foods was 1563 kJ/d and the contribution of fat was 24%. Protein intakes were <10 g/d and animal foods, primarily dairy and eggs, contributed only 9% of total protein intake. Meat and poultry products contributed only 17% of total animal protein intake. Fifty percent of children had diarrhea/anorexia < 5% of the time.

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The ages at which children start to walk vary considerably. The median or mean age at walking is 12–13 mo for American and European infants (26,27). Children in Nigeria, Kenya, and Gambia attained most milestones earlier than described in developed countries (11 mo for walking without support) (27). Compared to these populations, the children in our study population began walking at least 2–3 mo later and 1 mo later than children in Indonesia (9) and Pakistan (10) but are similar to Gumane infants from Papua New Guinea (6). Several factors, namely differences in the definition of motor milestones, the methods and frequency of data collection, childrearing practices, and genetics could explain the variation around the world in age of walking without support (27). In our data, correction for interval censoring reduced the age at walking without support by 0.5 mo on average.

We demonstrated that growth during the first year of life, rather than size at birth, was the relevant predictor of age of walking and that both growth in length and growth in weight remained significant predictors even after adjustment for a wide range of covariates. The relation of motor development with body size, biological maturation, balance, and strength of bone and muscle tissue is not well understood (28). Sufficiently high muscle-to-fat ratio and muscle strength in lower limbs play a role in balance maintenance (29). Finally, leg length is related to step length, which is essential for learning to walk (28).

We used residuals to adjust for energy intake and size at birth. This method is better than the use of simple models where both birth and subsequent size or energy and nutrient intakes are simultaneously entered because it addresses issues related to multicollinearity, common measurement error, and allows for better interpretation of regression coefficients (22,25,30,31). The residuals for nutrient intakes and postnatal growth that we used in our models by definition provide measures that are uncorrelated with total energy intake and size at birth, respectively (22,31).

Growth retardation and poor diet may directly affect the developing central nervous system, resulting in disturbances of brain maturation, particularly affecting the division of cortical cells, coordinated development of the dendritic synaptic apparatus of neurons, myelinization, and the activity of neurotransmitter systems (32). The processing and integration of perceptual information and motor signals are dependent on the maturation of the nervous system; this in turn can affect muscle strength and balance, factors key to the acquisition of walking skills (28). Gross and fine motor development is delayed in visually impaired infants (33).

Indirect pathways are also possible. Inadequate intakes of energy and some micronutrients may be related to decreased motor activity (4,34–36), which is necessary for practicing of motor skills. Practice helps improve muscle strength and balance (28). Motor milestones and motor activity were highly correlated in Indonesian infants (4) and activity levels explained a large portion of variability in achievement of motor milestones in Jamaican children (37). Second, the perception of maturation status often plays a vital role in regulating adult-infant interaction (38). Thus, infant size might play an important role in initiating age-appropriate style and frequency of caretaker contact, which might determine the infant’s speed of mastering new motor skills.

Diet quality, specifically intake of animal-source foods, during infancy was independently related to age at walking. It is possible that specific developmental domains are particularly sensitive to diet quality, but the significance of animal protein intake per se remains to be explained, because this may be a marker not only for intakes of several micronutrients in a highly bioavailable form, but also proxy for quality of caregiver interaction and stimulation. In a Dutch study, vegetarian infants (4–18 mo) had slower gross motor and language development compared to those who were nonvegetarian (39). In Kenya, animal protein intake was positively associated with play behaviors and language development among stunted toddlers, even after controlling for parental and SES factors (40). However, in that study dietary factors were not related to overall child development, measured by the Bayley Scales of Infant Development.

One concern is that the between-tester correlation for the Gross Motor Development Scale in our study was <90%. This may have been due to the fact that we measured the agreement between scores assigned by 2 raters at separate, independent administrations. In addition, scores of children who were tested for reliability in our study had smaller SD and, thus, lower variability. We also lack quantitative information on the contribution of human milk to nutrient intakes in this population. Although human milk is a poor source of iron and zinc (41), it can be an important source of protein, vitamin A, several water soluble vitamins including B-12, and minerals such as iodine and selenium, nutrients which may be related to development and also influenced by maternal nutritional status (42). Another limitation is that our measures of socioeconomic and environmental quality may have been inadequate. Although we adjusted for maternal factors such as age, education, and SES as well as infant birth order, these variables may not serve as adequate proxies of factors such as parent-child interaction and quality of home environment. Additional data on measures such as social support, family size, and directly measured parent-child interaction and child-rearing practices should be included in future investigations. For example, children who are carried a lot or not encouraged to move around may start to walk later. Finally, our sample size was not adequate to test small effects or effect modification (43).

In conclusion, postnatal growth retardation and low animal source food intake are risk factors for delay in attainment of walking. Our results indicate the importance of prevention of postnatal growth retardation and improvement of diet quality for child gross motor development.

	ACKNOWLEDGMENTS

 
The authors are grateful to the Guatemalan participants in this study for their cooperation and to Morgen Hickey for her contribution to the data management.

	FOOTNOTES

 
¹ Supported by Grant HD-29927 from the National Institutes of Health.

³ Abbreviations used: LAZ, length-for-age Z-score; INCAP, Instituto de Nutrición de Centro América y Panamá; SES, socioeconomic status; WAZ, weight-for-age Z-score.

Manuscript received 13 February 2004. Initial review completed 11 April 2004. Revision accepted 28 September 2004.

	LITERATURE CITED

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

1. Shirley, M. M. (1931) The first two years, a study of twenty-five babies. Postural and Locomotor Development 1931 University of Minnesota Press Minneapolis, MN.

2. Pollitt, E. (2000) A developmental view of the undernourished child: background and purpose of the study in Pangalengan, Indonesia. Eur. J. Clin. Nutr. 54:S2-S10.

3. Birengen, Z., Emde, R., Campos, J. & Appelbaum, M. (1995) Affective reorganization in the infants, the mother, and the dad—the role of upright locomotion and timing. Child Dev. 66:499-514.[Medline]

4. Jahari, A. B., Saco-Pollitt, C., Husaini, M. A. & Pollitt, E. (2000) Effects of an energy and micronutrient supplement on motor development and motor activity in undernourished children in Indonesia. Eur. J. Clin. Nutr. 54(suppl. 2):S60-S68.

5. McGraw, M. B. (1990) The Neuromuscular Maturation of the Human Infant 1990 Cambridge University Press Cambridge, UK.

6. Groos, A. D. (1991) Delayed motor development in relation to nutritional status among children under two years of age in two districts of Simbu Province. P. N. G. Med. J. 34:238-245.[Medline]

7. Adolph, K. E. (1997) Learning in the development of infant locomotion. Monogr. Soc. Res. Child Dev. 62:I-VI 1–158.

8. Pollitt, E. & Oh, S.-Y. (1994) Early supplementary feeding, child development, and health policy. Food Nutr. Bull. 15:76-99.

9. Pollitt, E., Husaini, M. A., Harahap, H., Halati, S., Nugraheni, A. & Sherlock, A. O (1994) Stunting and delayed motor development in rural West Java. Am. J. Hum. Biol. 6:627-635.

10. Cheung, Y. B., Yip, P. S. & Karlberg, J. P. (2001) Fetal growth, early postnatal growth and motor development in Pakistani infants. Int. J. Epidemiol. 30:66-72.[Abstract/Free Full Text]

11. Uauy, R. & Castillo, C. (2003) Lipid requirements of infants: implications for nutrient composition of fortified complementary foods. J. Nutr. 133:2962S-S2972.[Abstract/Free Full Text]

12. Wainwright, P. E. (2002) Dietary essential fatty acids and brain function: a developmental perspective on mechanisms. Proc. Nutr. Soc. 61:61-69.[Medline]

13. Ramakrishnan, U. & Huffman, S. L. (2001) Multiple micronutrien malnutrition. What can be done?. Semba, R. D. Bloem, M. W. eds. Nutrition and Health in Developing Countries 2001 Humana Press Totowa, NJ. .

14. Bhan, M. K., Sommerfelt, H. & Strand, T. (2001) Micronutrient deficiency in children. Br. J. Nutr. 85(suppl. 2):S199-S203.

15. Neumann, C., Harris, D. M. & Rogers, L. M. (2002) Contribution of animal source foods in improving diet quality and function in children in the developing world. Nutr. Res. 22:193-220.

16. Kosek, M., Bern, C. & Guerrant, R. L. (2003) The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Org. 81:197-204.[Medline]

17. Stephensen, C. B. (1999) Burden of infection on growth failure. J. Nutr. 129:534S-538S.

18. Grantham-McGregor, S. M., Fernald, L. C. & Sethuraman, K. (1999) Effects of health and nutrition on cognitive and behavioural development in children in the first three years of life. Part 1: Low birthweight, breastfeeding, and protein-energy malnutrition. Food Nutr. Bull. 20:53-75.

19. Martorell, R., Habicht, J. P. & Rivera, J. A. (1995) History and design of the INCAP longitudinal study (1969–77) and its follow-up (1988–89). J. Nutr. 125:1027S-1041S.

20. Lohman, T. G., Roche, A. F. & Martorell, R. (1988) Anthropometric Standardization Reference Manual 1988 Human Kinetics Books Champaign, IL.

21. Mei, Z. (2001) A SAS Program for the CDC Growth Charts 2001 http://www.cdc.gov/nccdphp/dnpa/growthcharts/sas.htm.

22. Willett, W. (1998) Implications of total energy intakes for epidemiological analysis. Nutritional Epidemiology 1998:273-301 Oxford University Press New York, NY.

23. Li, H., Stein, A. D., Barnhart, H. X., Ramakrishnan, U. & Martorell, R. (2003) Associations between prenatal and postnatal growth and adult body size and composition. Am. J. Clin. Nutr. 77:1498-1505.[Abstract/Free Full Text]

24. Li, H., DiGirolamo, A. M., Barnhart, H. X., Stein, A. D. & Martorell, R. (2004) Relative importance of birth size and postnatal growth for women’s educational achievement. Early Hum. Dev. 76:1-16.[Medline]

25. Tabachnick, B. G. & Fidell, L. S. (2000) Using multivariate statistics 2000 Allyn & Bacon Boston, MA.

26. Malina, R. M. & Bouchard, C. (1991) Growth, maturation and physical activity 1991 Human Kinetics Books Champaign, IL.

27. Goetghebuer, T., Ota, M.O.C., Kebbeh, B., John, M., Jackson-Sillah, D., Vekemans, J., Marchant, A., Newport, M. & Weiss, H. A. (2003) Delay in motor development of twins in Africa: a prospective cohort study. Twin Res. 6:279-284.[Medline]

28. Adolph, K. E., Vereijken, B. & Shrout, P. E. (2003) What changes in infant walking and why. Child Dev. 74:475-497.[Medline]

29. Okamoto, T. & Okamoto, K. (2001) Electromyographic characteristics at the onset of independent walking in infancy. Electromyogr. Clin. Neurophysiol. 41:33-41.[Medline]

30. Esrey, S., Casella, G & Habicht, J. P. (1990) The use of residuals for longitudinal data analysis: the example of child growth. Am. J. Epidemiol. 131:365-372.[Abstract/Free Full Text]

31. Lucas, A., Fewtrell, M. S. & Cole, T. J. (1999) Fetal origins of adult disease-the hypothesis revisited. Br. Med. J. 319:245-249.[Free Full Text]

32. Pollitt, E. (2000) Developmental sequel from early nutritional deficiencies: conclusive and probability judgements. J. Nutr. 130:350S-353S.

33. Elisa, F., Josee, L., Oreste, F.-G., Claudia, A., Antonella, L., Sabrina, S. & Giovanni, L. (2002) Gross motor development and reach on sound as critical tools for the development of the blind child. Brain Dev. 24:269-275.[Medline]

34. Sazawal, S., Bentley, M., Black, R. E., Dhingra, P., George, S. & Bhan, M. K. (1996) Effect of zinc supplementation on observed activity in low socioeconomic Indian preschool children. Pediatrics 98:1132-1137.[Abstract/Free Full Text]

35. Bentley, M. E., Caulfield, L. E., Ram, M., Santizo, M. C., Hurtado, E., Rivera, J. A., Ruel, M. T. & Brown, K. H. (1997) Zinc supplementation affects the activity patterns of rural Guatemalan infants. J. Nutr. 127:1333-1338.[Abstract/Free Full Text]

36. Black, M. M. (2003) The evidence linking zinc deficiency with children’s cognitive and motor functioning. J. Nutr. 133:1473S-1476S.[Abstract/Free Full Text]

37. Meeks, G. J., Grantham-McGregor, S. M., Chang, S. M., Himes, J. H. & Powell, C. A. (1995) Activity and behavioral development in stunted and nonstunted children and response to nutritional supplementation. Child Dev. 66:1785-1797.[Medline]

38. Alley, T. R. (1983) Growth-produced changes in body shape and size as determinants of perceived age and adult caregiving. Child Dev. 54:241-248.

39. Dagnelie, P. C., van Staveren, W. A., Vergote, F. J., Burema, J., van’t Hof, M. A., van Klaveren, J. D. & Hautvast, J. G. (1989) Nutritional status of infants aged 4 to 18 months on macrobiotic diets and matched omnivorous control infants: a population-based mixed-longitudinal study. II. Growth and psychomotor development. Eur. J. Clin. Nutr. 43:325-338.[Medline]

40. Sigman, M., Neumann, C., Baksh, M., Bwibo, N. & McDonald, M. A. (1989) Relationship between nutrition and development in Kenyan toddlers. J. Pediatr. 115:357-364.[Medline]

41. Lutter, C. K. & Dewey, K. G. (2003) Proposed nutrient composition for fortified complementary foods. J. Nutr. 133:3011S-3020S.[Abstract/Free Full Text]

42. Allen, L. H. (1994) Maternal micronutrient malnutrition: effects on breast milk and infant nutrition, and priorities for intervention. SCN News 11:21-24.

43. Cohen, J. (1988) Statistical power analysis for the behavioral sciences 2nd ed. 1988 Earlbaum Hillsdale, NJ.

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