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*
Division of Human Nutrition and Epidemiology, Wageningen University, The Netherlands;
SEAMEO TROPMED Regional Center for Community Nutrition, University of Indonesia, Jakarta, Indonesia;
**
Department of Gastroenterology, University Medical Center Nijmegen, The Netherlands;
UNICEF, New York, NY; and
German Agency for Technical Cooperation, Eschborn, Germany.
2To whom correspondence should be addressed. E-mail: Clive.West{at}staff.nutepi.wau.nl.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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18 wk of pregnancy from 9 rural villages in West Java, Indonesia, were followed until 12–15 mo of age. Weight, length, morbidity, breast-feeding and food intake were assessed monthly. Determinants of length and weight increase and nutritional status reflected by Z-scores were evaluated using multiple linear regression. Neonatal weight (3.2 ± 0.5 kg) and length (49.7 ± 2.2 cm) were reasonable. However, growth started to falter at 6–7 mo of age, resulting in prevalences of 24% stunting and 32% underweight at 12 mo of age. The multiple regression models explained 19–41% of the variation in growth and nutritional status of infants. Neonatal weight (ß = 0.285) and length (ß = 0.492) were the strongest positive predictors of weight-for-age and height-for-age Z-scores, respectively. Fever was negatively associated with weight increase (ß = -0.144) and weight-for-age (ß = -0.142) and weight-for-height Z-scores (ß = -0.255) but not with length increase or height-for-age Z-scores. Intake of complementary foods was positively associated with increases in weight (ß = 0.190) and length (ß = 0.179) and nutritional status of infants (ß = 0.136–0.194). In conclusion, in this rural population in West Java, neonatal weight and especially length, reflecting the prenatal environment, are the most important predictors of infant nutritional status.
KEY WORDS: • infants • growth • nutritional status • feeding • morbidity • determinants
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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,2
). Stunting indicates a public health problem because of its association with an increased risk of morbidity and mortality, delayed motor and mental development, and reduced physical capacity (1
,3
). Most growth faltering, resulting in underweight and stunting, occurs from birth until 2 y of age but may already start during the gestation period (3
).
Prenatal factors, such as maternal nutrition, determine fetal growth during the gestation period, and thus infant weight and length at birth. Infant birth weight and length are determinants of future nutritional status as was shown in Bangladeshi infants who experienced very little catch-up growth after birth (4
). In Indonesian infants, birth weight and length have also been found to be important determinants of infant growth (5
).
During infancy, inadequate intakes of nutrients and frequent or prolonged episodes of infection may exacerbate the effects of fetal and infant growth retardation (1
,6
). However, the severity of the effect of morbidity on growth depends on the pathogens and population involved (7
,8
). Breast-feeding has been found to decrease the risk of morbidity and mortality in infants in developing countries (9
,10
) and morbidity in developed countries (11
). The growth of breast-fed infants differs from that of those who are formula fed; breast-fed infants usually grow faster during the first 3 mo of life but more slowly thereafter (12
). In addition, the effects of the duration of breast-feeding and timely introduction of complementary feeding on growth differ among populations (13
).
To date, most studies have investigated either the effect of birth weight and length (4
,5
) or that of postnatal factors (1
,6
,12
,13
) on growth and nutritional status. In addition, little information has been published on determinants of growth and nutritional status of Indonesian infants. We studied a cohort of Indonesian pregnant women and their newborns until 15 mo of age, which enabled us to assess the relative effect of prenatal and postnatal factors on growth and nutritional status of infants.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Pregnant women from nine rural villages in Leuwiliang subdistrict, Bogor district, West Java, Indonesia were enrolled in six rounds from November 1997 until May 1998; their infants were born between February and November 1998. After birth, all eligible infants were followed up monthly until at least 12 mo of age. Thereafter, infants whose mothers were still willing to participate continued to be measured into childhood until the end of the study period (November 1999). Growth, morbidity, breast-feeding and food intake were assessed monthly. In addition, mothers were interviewed at enrollment for socioeconomic background and pregnancy history, at delivery for infant food intake and other variables and at 13 mo after delivery about the use of contraceptives and pregnancy status. Selected anthropometric measurements of women (14
) were assessed at enrollment, near term and 4 mo postpartum. The data presented in this paper were collected in an intervention trial investigating the effect of vitamin A and iron supplementation during gestation on infant growth. The results of the intervention and details of the study design have been published (14
–17
). Explanation of the study was given to the women at enrollment and all women who participated gave written informed consent. The Ministry of Health Indonesia and the Ethical Committees of the Medical Faculty at the University of Indonesia and Wageningen University approved the research proposal.
Study population.
Of 366 women recruited at 18 wk of pregnancy, 318 infants were eligible for follow-up after birth. Loss of subjects occurred because of withdrawal from supplementation (n = 18), moving outside the research area (n = 15), stillbirth or twins (n = 13), or neonatal death (n = 2) (14
,16
). During the follow-up period from birth to 12 mo, 16 infants moved outside the research area and 12 infants died. Neonatal weight or length (in mo 1 of life) and gender ratio did not differ between infants who left the study and infants who were followed up to 12 mo (n = 290). All 318 infants experienced at least one anthropometric assessment. Infants who were measured 1–9 (n = 46), 10–13 (n = 100) or 14–19 (n = 172) times did not differ with respect to neonatal weight or length, weight gain or length increase during the first 6 mo of life and gender ratio. The mean number of measurements was 13.2 ± 3.6.
Assessment of infants.
Weight and length of infants were measured and mothers interviewed for morbidity and food intake of their infants during their monthly visit to their neighborhood health post (Posyandu). In principle, visits for each health post were planned on the same date of each month. However, in practice, visits were made within 1 wk of the planned date. We attempted to reach individual mothers who were not able to attend by visiting their homes.
Anthropometry.
Two pairs of trained field assistants measured weight and length of infants using standardized methods (18
). Weight was measured to the nearest 50 g using a baby weighing scale (Misaki baby scale, Japan), which was tared each time before use. Calibration with a standard weight (5 kg) at regular intervals showed that all scales were stable and precise. Recumbent length was measured to the nearest 0.1 cm using a wooden length board (19
). Infants were measured with light clothing. Birth or neonatal weight and length had been measured by two of the authors (M.K.S. and S.M.) during a postnatal home visit (16
). All field assistants had received training and were supervised every month by the two authors mentioned above. Independent measurements performed in random subsample of 5% of the infants showed a technical SD of 44 g and 0.70 cm for weight and length, respectively (17
).
Morbidity.
At the time of the anthropometric assessment, the same field assistants interviewed the caretaker (the mother in all but 2 cases) of the infant about symptoms of morbidity in the 14 d preceding the visit. More specifically, mothers were asked to recall the following: diarrhea, defined as 
3 stools in 1 d that were more liquid than usual; fever, mother’s evaluation of infant’s body temperature above normal (hot to the touch; "panas"); running nose ("pilek"), nasal discharge; cough, persistent coughing; difficulty breathing, breathing with severe noise or wheezing or difficulty inhaling; ear discharge, fluid or pus draining from at least one ear; and vomiting. Questions were asked in Bahasa Indonesia or in the local language (Sundanese) if the mother did not understand the term. First the interviewer asked the mother for any symptoms and then asked her specifically for each category and for how many days the infant suffered from that specific symptom. Episodes were defined as a period of sickness separated by at least 3 d. Mortality of infants was recorded at a home visit after death had been reported.
Breast-feeding and food intake.
Together with the morbidity interview, the mother was asked whether the infant was still breast-fed and whether the infant received any other liquid or food in the 14 d preceding the visit. Breast-feeding and food intake data, including food given to the infant before or at the time of starting the breast-feeding i.e., prelacteal feeding, had been collected at the postnatal home visit. The type of liquid or food was recorded using a precoded questionnaire. For breast-feeding status, infants were categorized as exclusively breast-fed, predominantly breast-fed (i.e., receiving breast milk plus water, tea, coffee or fruit juices, but no artificial milk), complementary fed, or nonbreast-fed (20
). Here, we refer to infants breast-fed exclusively as those infants who were exclusively breast-fed regardless of whether they received prelacteal feeding. For data analysis, infant food intake was categorized as follows, animal products: meat (beef or chicken), liver, egg, fish; biscuits: biscuit, bread, noodles, porridge (bean or wheat-flour); fruit: banana and other; rice: rice, rice porridge, rice steamed in banana leaves ("lontong"); tempeh: tempeh or tofu ("tahu"); vegetables: carrot, dark green leafy vegetables, cabbages, (French) beans, potato and other; snacks: fried (sweet) potato or cassava (in small quantities not with the meal), bakso (flour and meat balls), cookies (other than biscuit), chips, krupuk, agar-agar, candies; milk: milk, infant formula, fortified infant food; liquids: water, tea and/or coffee with or without sugar, honey, fruit or vegetable juice.
Data analysis.
Data from 318 infants eligible for follow-up were pooled for analysis irrespective of the treatment that their mothers had received during pregnancy. Growth, morbidity, iron status and feeding mode of infants did not differ from 0 to 12 mo of age among the three treatment groups, although serum retinol concentrations were improved by vitamin A plus iron supplementation (16
,17
). In addition, no differences in growth were found among groups up to 18 mo of age (unpublished data). Therefore we consider that pooling of the data of all infants to analyze the determinants of growth faltering is justified. Weight and length were converted into Z-scores using the NCHS/WHO reference data incorporated in the Epi-Info software (Epi Info2000 version 1.0.5. CDC, Atlanta). Stunting was defined as a height-for-age Z-score of less than -2, underweight as weight-for-age Z-score less than -2 and wasting as weight-for-height Z-score less than -2. For analysis, follow-up data of infants were grouped into monthly age groups of 0 (0 until 0.99 mo, neonatal) to 18 (18 until 18.99 mo). However, we considered that only up to 15 mo of age there was a reasonable amount of follow-up (anthropometric) data available for analysis (n = 128); therefore, descriptive data are presented for infants up to that age. For further analysis, we present the follow-up data up to 12 mo to reduce the risk of selection bias and to have higher power by having more infants in the analysis. Because only some of the infants could be reached within 72 h to measure birth weight and length (16
), we took weight and length measured during mo 1 (neonatal weight and length) as the starting point of our growth measurements. For infants who had two measurements in mo 1 of life (90%), the means were used.
For the analysis of association of symptoms of morbidity or food groups with growth, nutritional status or feeding practices and for multiple linear regression, morbidity symptoms and food intake were converted into a ratio correcting for compliance with the assessments as follows: the total number of episodes of a symptom or the total number of interviews in which a certain food group was reported to be consumed by the infant from 0 to 12 mo of age was divided by the total number of assessments this infant had during this follow-up period.
Comparisons of continuous, normally distributed data between groups were done using t test or ANOVA if correction for other variables was necessary. Comparisons of continuous, nonnormally distributed data and categorical data between groups were done using Mann Whitney U test and 
2 test, respectively. Associations of normally and nonnormally distributed data were evaluated using Pearson’s correlation and Spearman rank correlation, respectively. For correction of gender in the association between growth and morbidity or food intake, partial correlation was applied. Determinants of growth and nutritional status of infants were evaluated using backward multiple linear regression (threshold 0.1). Three types of variables were considered in the analysis, i.e., prenatal factors such as those reflecting socioeconomic status (education, work, housing), maternal height and nutritional status (weight, mid-upper arm circumference) during pregnancy and infant neonatal weight and length; postnatal factors such as duration of breast-feeding, food practices and morbidity; and covariants such as gender, birth order and age of the infants. All variables presented in Table 1
were included and entered as dichotomous or continuous. Occupation of the father was entered as dichotomous (0 = daily worker, 1 = monthly worker or trader) variable but was not a significant determinant in the model. Mid-upper arm circumference of mothers was not included in any model because it was highly correlated with maternal weight (r > 0.8).
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. The number of boys and girls was not different; 27% of the infants were first-borns. Birth weight of infants was reasonable (Table 2
); 6% of the infants had low birth weight (<2500 g). Most of the increase in length and weight of infants occurred during the first 6 mo (Table 2)
. At the neonatal assessment, only 7% of the infants were stunted, 5% were underweight and none were wasted. At 6 mo of age, nutritional status of infants had returned to the same level as at the neonatal assessment. However, at 12 mo of age, 24% were stunted, 32% underweight and 4% wasted, and at 15 mo, these proportions had increased to 32, 40 and 6%, respectively. Growth faltering started at 3–4 mo of age; however, when compared with neonatal nutritional status, this was 6 to 7 mo of age (Fig. 1
). Wasting was less prevalent than stunting and underweight throughout the period of follow-up. Boys had greater weight and length than girls from 0 to 15 mo (data not shown). This difference was due mainly to the greater birth weight and length of boys, and greater increases in weight [0.39 (0.20–0.57) kg, mean (95% confidence interval), P < 0.0001)] and length [0.7 (0.2–1.2) cm, P < 0.01)] during the first 6 mo of life. Height-for-age, weight-for-age and weight-for-height Z-scores from 0 to 15 mo did not differ between boys and girls. Compared with the 12-mo breast-fed pooled data set of WHO (12
), length and weight of boys and girls started to falter from the reference curve at 6–7 mo of age. At 12 mo of age, mean weight-for-age and height-for-age Z-scores were -1.25 and -1.17 for boys and -1.12 and -1.13 for girls, respectively.
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). The mean period of exclusive breast-feeding was 1.96 ± 1.95 mo. Almost all women continued breast-feeding their infants during the study follow-up (Fig. 2)
. The small proportion of mothers that breast-fed exclusively or predominantly after 6 mo postpartum were mostly those who had returned to exclusive or predominant breast-feeding after having tried unsuccessfully to introduce food to their infants. Most infants were first introduced to liquids, fruit (often banana) and biscuits, whereas foods such as rice, vegetables, tempeh and snacks were introduced at a later age. From 4 mo of age, intake of foods increased rapidly (data not shown). At 4 mo of age, 15% of the infants did not have a good appetite as reported by their mothers and this increased gradually to 50% at 12 mo of age.
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60% for running nose, 45% for fever and 30% for cough. About 10% of the infants suffered from diarrhea and/or vomiting during the follow-up period. Prevalence of ear discharge was rare. Morbidity prevalence was not significantly related to season or gender.
The multiple regression models explained 19–41% of the variation in growth and nutritional status of infants, with the models for length increase and height-for-age Z-scores performing the best (Table 3
). In each model, neonatal weight and especially neonatal length were the strongest positive predictors of nutritional status of infants. These two variables were also the strongest negative predictors of increases in weight and length of infants. Prenatal variables such as maternal weight and height at 18 wk of pregnancy and postnatal variables such as fever and intakes of fruit, biscuits or snacks were of similar strength in predicting increases in length and weight and nutritional status of infants. Fever was negatively associated with weight increase and weight-for-age and weight-for-height Z-scores but not with length increase and height-for-age Z-scores. Intake of complementary foods was positively associated with increases in weight and length and nutritional status of infants (Table 3)
. Prelacteal feeding, colostrum intake and number of months the infant was "exclusively" breast-fed were excluded from all models by the regression procedure; the last-mentioned was included in the weight-for-height model although it was not significant (P = 0.059).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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,21
). Other factors reflecting prenatal environment, such as maternal weight, and postnatal factors, such as intake of certain complementary food groups and morbidity, were associated to lesser extents with infant nutritional status. This suggests that prenatal environment is a more important determinant of infant nutritional status than postnatal factors.
The negative association between neonatal length and length increase and between neonatal weight and weight increase shows that infants who are born short and light can still catch up to some extent with their longer and heavier counterparts during y 1 of life. However, they will not achieve the same weight or length at 12 mo of age as infants born longer and heavier (22
,23
); thereafter, the chances of recovery are small (24
,25
).
The importance of neonatal length relative to the other variables in the models for length increase and height-for-age Z-scores was greater than that of neonatal weight in the models for weight increase and weight-for-age Z-scores. This was shown by the higher ß relative to the other variables in the models and the greater percentage of variation explained by the models including neonatal length. The apparent greater association of neonatal length with length increase in comparison to neonatal weight with weight increase is probably due in part to the higher measurement error of neonatal length. Any measurement error induces a negative association because the neonatal measure is included in the calculation of the increase. In addition, fever was associated with weight gain and weight-for-age Z-scores but not with length increase and height-for-age Z-scores. Therefore, prenatal environment seems to play a larger role in the prediction of linear growth and stunting than in weight gain and underweight. Genetic background probably plays a limited role in this because Indonesian preschool children from high socioeconomic class families have been found to have the same growth potential as an American reference population (26
). Although changes may occur slowly over generations, the underlying causes may be nutritional (27
).
This study contributes to the understanding of the complex pattern of determinants in infant growth and the relative contribution of prenatal and postnatal factors; however, there are two limitations. First, we used neonatal length and weight instead of birth weight and length. Therefore, the environment during the first days of life of the infants may have already affected neonatal weight and length. On the other hand, we did not find an association between feeding practices in the first days after birth, such as partly discarding colostrum or prelacteal feeding, and neonatal weight or length of infants. Second, we can explain only about one third of the variation in growth and nutritional status of infants during y 1 of life with our models. This means that there might be other important factors that we did not assess that play a role in infant growth. In addition, adaptations of the fetus to limitations in nutrient supply, for example of certain micronutrients, may not be reflected in neonatal weight and length but may influence later child health (27
).
Growth faltering during the second half of infancy is often seen in Asian populations (5
,25
). Although stunting was highly prevalent at 12 and 15 mo of age, the proportion of stunting in the present study was lower than reported earlier in Madurese infants (6
). The figure at 15 mo could be an underestimation. Because participation after 12 mo of age depended on the willingness of the mothers to come to the Posyandu for the monthly measurements, a selection bias could have occurred. Likely the mothers who still attended were more health conscious and this was reflected in a better nutritional status of their children.
The positive association between intake of certain complementary foods and growth suggests that part of the growth faltering, especially in the second half of y 1 of life, was due to inadequate food intake. Earlier, Kusin et al. (22
) reported that food given to infants might have insufficient energy density, but also the micronutrient content may have been inadequate (13
,28
). In addition, decreased appetite of infants as reported by mothers in our study may have been due to anorexia as a result of morbidity or insufficient micronutrient intake (6
,29
). Morbidity as reflected by fever indeed had a negative effect on weight gain and nutritional status of infants, and the period in which growth started to falter coincided with the period in which the prevalence of morbidity had increased maximally.
Exclusive breast-feeding for 4 mo (30
) did not show an advantage above complementary or predominantly breast-feeding in terms of growth or morbidity. However, it should be noted that almost none of the infants were really exclusively breast-fed and that there was little variation in breast-feeding practices. It is likely, however, that breast milk intake protected infants from more severe growth faltering (29
).
Our study shows that neonatal length is the strongest predictor of infant nutritional status; therefore, it is very important to ensure that women enter pregnancy in good health and with adequate nutritional status. However, infancy is still considered to be a period in which growth and nutritional status can be improved by reducing morbidity and ensuring good nutrition.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Manuscript received 5 September 2001. Initial review completed 5 November 2001. Revision accepted 11 April 2002.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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26. Droomers, M., Gross, R., Schultink, W. & Sastroamidjojo, S. (1995) High socioeconomic class preschool children from Jakarta, Indonesia are taller and heavier than NCHS reference population. Eur. J. Clin. Nutr. 49:740-744.[Medline]
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29. Brown, K. H., Stallings, R. Y., de-Kanashiro, H. C., Lopez-de Romana, G. & Black, R. E. (1990) Effects of common illnesses on infants’ energy intakes from breast milk and other foods during longitudinal community-based studies in Huascar (Lima), Peru. Am. J. Clin. Nutr. 52:1005-1013.
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