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The Journal of Nutrition

Community and International Nutrition

Protein and Micronutrient Intakes Are


Associated with Child Growth and Morbidity
from Infancy to Adulthood in the Philippines1,2

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Alok Bhargava*

University of Maryland School of Public Policy, College Park, MD

Abstract
Background: Interactions between nutrition and infections in developing countries are complex, and analyses of the
interrelations require data from longitudinal studies that span several years and a comprehensive framework facilitating
the formulation of food and health policies.
Objective: The effects of dietary intakes in the Philippines for birth outcomes, heights, weights, and morbidity during ages
2–24 mo; heights and weights during ages 8–19 y; and completed adult heights were analyzed.
Methods: Data on >3000 children from the Cebu Longitudinal Health and Nutrition Survey were modeled in 4 sets of
analyses. Cross-sectional and multilevel models were estimated for length and weight at birth. Dynamic random-effects
models were estimated for childrenÕs heights, weights, and morbidity levels during ages 2–24 mo. ChildrenÕs heights and
weights during ages 8–19 y were modeled by using random-effects models. ChildrenÕs heights at age 22 y were modeled
for investigating the effects of nutritional intakes in early childhood and in adolescence.
Results: Maternal anthropometric indicators, energy intakes, and sociodemographic variables were significantly
associated with childrenÕs length and weight at birth. Dynamic models for childrenÕs heights and weights during ages
2–24 mo showed significant effects of calcium and protein intakes; child morbidity levels were significantly associated
with height and weight. Higher b-carotene intakes were significantly associated with lower morbidity levels. Analyses of
data on children during ages 8–19 y showed significant effects of protein and calcium intakes and of morbidity levels on
heights and weights. Models for childrenÕs heights at age 22 y indicated significant effects of protein and calcium intakes
during early childhood and in adolescence.
Conclusions: The results underscored the need for formulating long-term food and health policies for the Philippines that
enhance childrenÕs physical development and ultimately their adult stature, which is important for physical work capacity
and labor productivity. J Nutr 2016;146:133–41.

Keywords: anthropometric indicators, diet quality, econometric modeling, food policies, longitudinal data,
long-term evaluation, maximum likelihood estimation, morbidity

Introduction
to analyze the factors underlying childrenÕs physical growth and
The importance of interactions between infections and individ-
morbidity that ultimately determine their adult physical work
ualsÕ nutritional status has long been recognized, especially for
capacity (10) and labor productivity (11).
developing countries (1–6). Inadequate protein and micro-
For the design of efficacious food policies, it is important to
nutrient intakes lower the capacity of the body to fight infections, adopt multidisciplinary approaches that incorporate interactions
which, in turn, adversely affects nutritional status by prolonging between nutritional status and infections. For example, weaning
sickness spells. Moreover, absorption rates for nutrients such as programs for breastfed infants may not be effective if they
iron and calcium are often low due to excessive phytate intake inadvertently increase morbidity levels because the mothers failed
from grains (7, 8). In addition, food contamination due to poor to maintain hygiene in preparing the supplements (12). Moreover,
hygiene exacerbates nutrient loss (9). It is therefore important it is important for food policies to match childrenÕs nutritional
requirements with their intakes at various ages. This is an intricate
1
task because childrenÕs requirements depend on their ages and
Supported in part by the Harvest Plus program of the International Food Policy
Research Institute.
growth pattern history (13, 14). It is therefore important to adopt
2
Author disclosures: A Bhargava, no conflicts of interest. a long-term framework for analyzing the effects of childrenÕs
*To whom correspondence should be addressed. E-mail: bhargava@umd.edu. nutritional intakes and morbidity on their physical development.
ã 2016 American Society for Nutrition.
Manuscript received August 20, 2015. Initial review completed October 1, 2015. Revision accepted November 2, 2015. 133
First published online December 9, 2015; doi:10.3945/jn.115.222869.
Furthermore, there has been emphasis in the literature on early May 1983 and April 1984 were invited to enroll in the study, and the refusal
nutritional interventions, especially during the first 2 y of life (15). rate was 4%. The 3080 women in the sample with single births were
Although such interventions may be necessary for undernourished interviewed during pregnancy, at birth, and then bimonthly from ages 2
children growing up in poverty, it is important to adopt a broader to 24 mo (i.e., there were 13 observations on infants in the initial surveys).
Subsequently, mothers and children were interviewed in follow-up surveys
perspective on ‘‘critical windows’’ that may be available for catch-
in 1991, 1994, 1998, 2002, and 2005 when the children were 8, 10, 15,
up growth (16). Thus, for example, heights in the Netherlands 19, and 22 y old, respectively.
surpassed all countries after the Second World War presumably The first survey round conducted during pregnancy measured
due to the school milk programs, which rewarded children for mothersÕ heights and weights around the 30th week of gestation.
daily drinking up to 5 glasses of milk to become ‘‘M-brigadiers’’ MothersÕ food intakes were measured by using the 24-h recall method
(17). The programs were gradually discontinued in the 1980s, and were converted into energy and nutrient intakes with the use of
and some reversion to the mean in Dutch heights is apparent tables for the Philippines (28). MothersÕ food intakes were again
(18). Because childrenÕs requirements for protein and micronu- measured when the infants were born and when they were ;6 and 12 mo

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trients such as calcium and iron are also high during adolescence old. ChildrenÕs intakes from weaning were assessed by using 24-h recalls
(3), an exclusive focus on early interventions can lead to a from ages 4 to 24 mo. Infants were weighed at birth by using Salter dial-
faced scales, and birth length was measured with the use of locally made
misallocation of scarce resources.
boards. Infant lengths and weights and mothersÕ weights were subse-
For the analyses of longitudinal data on children that span quently measured at 2-mo intervals in 12 time periods.
several years, it is important to tackle 2 sets of issues. First, growth Demographic and socioeconomic variables were compiled for the
spurts, especially around puberty, are affected by the secretion of households. For example, the childÕs gender and birth order and the
hormones that depend on childrenÕs nutritional status, including number of persons in the household were recorded. The highest grade
dietary intakes such as that of protein (19, 20). Moreover, there is completed by the mother was also recorded. The socioeconomic status of
considerable variation in growth spurts during adolescence and in the household was assessed via several questions during the first 2 y.
the dynamics of body composition, such as leg growth, which Because of missing observations on some items, a socioeconomic status
peaks a few months earlier than trunk growth (14). Thus, in index was constructed on the basis of 7 items: whether the family owned
addition to factors such as length and weight at birth, it is useful the house and/or owned the land, types of vehicles owned, number of
appliances owned, number of rooms, number of furniture items owned,
to account for childrenÕs dietary intakes during adolescence in
and if the family owned other houses.
models for their completed heights. Furthermore, information was compiled on mother and infant
Second, inferences from data analyses critically depend on morbidities and immunizations in the surveys when children were
the models postulated for the interrelations between childrenÕs between 2 and 24 mo old. For mothers, the morbidity index was based
diets, morbidity, and growth. Previous research has computed on 6 items for the past 24 h—namely, if mothers had been ill or had
simple correlations or associations between childrenÕs length and diarrhea, cold or congestion, cough, fever, and other illnesses; this index
weight at birth and completed heights by using data from several ranged from 0 to 6. For children, morbidity index 1 covered 6 symptoms
countries (21). Such formulations largely ignore the nutritional in the past 24 h: cough, fever, nasal discharge, ear discharge, sore throat,
factors affecting child growth during the in-between years; the and other illnesses. ChildrenÕs morbidity index 2 covered the past week
estimated coefficients are likely to be ‘‘upward biased’’ due to the and inquired about 7 items: cough, nasal congestion, ear discharge, fever,
number of days of diarrhea, other illnesses, and measles; this index
omission of positively correlated explanatory variables.
ranged from 0 to 13. The childrenÕs diarrhea index was based on the
This article analyzed the data from 21 survey rounds of the number of days the child had diarrhea and was doubled if there was
Cebu Longitudinal Health and Nutrition Survey conducted from blood in the stool; this index ranged from 0 to 24. Last, childrenÕs
1983 to 2005 involving >3000 Filipino children from birth to immunizations against diphtheria, pertussis, and tetanus, tuberculosis,
adulthood (22). First, models were estimated for childrenÕs measles, polio, cholera, and other illnesses were recorded at different
lengths and weights at birth that were explained by socioeco- time points. The total number of vaccinations received before the age of
nomic variables and mothersÕ nutritional status. Second, chil- 2 y was used as an index for immunizations.
dren heights and weights were modeled in the period 2–24 mo of Finally, follow-up surveys were conducted when children were 8, 10,
age by estimating dynamic random-effects models (23) and the 15, 19, and 22 y old. MothersÕ and childrenÕs heights and weights were
effects of nutrient intakes were investigated; protein intakes are measured in the survey rounds. ChildrenÕs food intakes were measured at
ages 10, 15, and 19 y by using 24-h recalls and were converted into
important for growth, especially where the diets are lacking in
energy and nutrient intakes. ChildrenÕs total morbidities and number of
animal products (2), and calcium intakes are essential for bone immunizations they received during the ages of 2–24 mo were included
growth (24). ChildrenÕs morbidity levels in the previous 24 h and in the longitudinal database for analyzing growth patterns when the
7 d and diarrheal morbidity were modeled by using indexes that children were 8–19 y old.
reflected the intensity and duration of sicknesses (25, 26);
b-carotene intakes were included as explanatory variables (4, Empirical models. The availability of longitudinal data from Cebu
27). Third, random-effects models were estimated by using data enabled 4 sets of interdependent analyses. First, the cross-sectional
at ages 8, 10, 15, and 19 y on childrenÕs heights and weights. model for childrenÕs birth length (and weight) is given in Equation 1:
Fourth, childrenÕs heights when they turned 22 y were explained lnðLengthÞi ¼ a0 þ a1 ðGenderÞi þ a2 ðBirth orderÞI
by using early anthropometric measurements and protein and 2
þa3 ðBirth orderÞi þ a4 ðNumber of persons in householdÞi
calcium intakes during the ages of 2–24 mo and from 10–19 y. þa5 ðNumber of persons in householdÞi
2

þa6 ðSocioeconomic indexÞi þ a7 ðMothers highest gradeÞi


þa8 lnðMothers heightÞi þ a9 lnðMothers weightÞi
Methods þa10 lnðMothers energy intake=dÞi þ ui ði ¼ 1; 2; .; NÞ ð1Þ
The Cebu Longitudinal Health and Nutrition Survey was conducted in
metropolitan Cebu, the Philippines, from 1983 to 2005 (22); data on The model in Equation 1 postulates nonlinearities between childÕs birth
maternal and infant health indicators and sociodemographic variables order and number of persons in the household and the natural logarithm
are available from 21 survey rounds. At baseline, a clustering-sampling of length (or weight) at birth. Moreover, mothersÕ heights and weights
procedure was used to randomly select 17 urban and 16 rural ‘‘barangays’’ are likely to be positively associated with birth size, so that it would be
representing ;28,000 households. Pregnant women giving birth between inappropriate to combine them as the BMI in this model (26, 29, 30). In

134 Bhargava
addition, mothersÕ energy and nutrient intakes are important for during the 2- to 24-mo period and was included as an explanatory
intrauterine development (31). The correlation between mothersÕ highest variable in the models. In addition, data on dietary intakes were compiled at
grade and socioeconomic index was 0.41, and it did not present any 3 time points, and protein and calcium intakes were averaged to produce
difficulties for the estimation of model parameters. figures for 10–19 y; averaging was helpful in reducing the impact of
Second, the dynamic random-effects model for childrenÕs heights within-child variations in intakes (36). In alternative versions of the
with the use of bimonthly observations in the period from 2 to 24 mo is model, 2 indicator variables for time periods were included as explan-
given in Equation 2: atory variables to account for the trends underlying the dietary intakes.
Dynamic and static random-effects models were also estimated for
lnðHeightÞit ¼ b0 þ b1 ðGenderÞi þ b2 ðBirth orderÞi
childrenÕs weights. Last, 4 specifications were estimated for investi-
þb3 ðNumber of persons in householdÞi gating the effects of childrenÕs heights at age 2 y on their completed
þb4 ðSocioeconomic indexÞi þ b5 ðMothers highest gradeÞi heights.
þb6 ðMothers morbidity indexÞit
þb7 lnðMothers energy intake=dÞit Statistical methods and test statistics. The statistical estimation

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þb8 lnðMothers BMIÞit theory assumed that the number of children (N) was large but the
þb9 ðChildren immunizations totalÞi number of time periods (T) was small. Thus, previous observations on
dependent variables, such as childrenÕs heights and weights, were treated
þb10 ðChildren morbidity indexÞit-1
as correlated with the errors (‘‘endogenous’’) (23). Realizations of certain
þb11 ðChildren diarrhea indexÞit-1 time-varying explanatory variables in different survey rounds were
þb12 lnðChildren protein=energy intake=dÞit-1 assumed to be uncorrelated with the errors (‘‘exogenous’’). The errors
þb13 lnðChildren calcium=energy intake=dÞit-1 (u1it) were assumed to be independent across children but correlated over
þb14 lnðHeightÞit-1 time with a positive definite variance-covariance matrix. A numerical
þu1it ði ¼ 1; 2; .; N; t ¼ 2; .; 11Þ ð2Þ optimization routine (E04 JBF) (37) was used in a FORTRAN program
to compute the maximum likelihood estimates. Asymptotic SEs of the
u1i t represents random-error terms that can be decomposed in a random- parameters were computed by numerically approximating second
effects fashion as follows: derivatives of the maximized log-likelihood functions. For static models,
stepwise procedures were used to compute the efficient instrumental
u1it ¼ di þ v1it ð3Þ variable estimates (35).
Furthermore, certain explanatory variables in the models in Equa-
where di represents child-specific random effects that were assumed to tions 2 and 4 were likely to be correlated with the errors, especially the
be distributed with zero mean and constant variance, and v1it were random effects (di). In the model estimated for childrenÕs weights during
distributed with zero mean and constant variance (32). The estima- ages 2–24 mo, for example, morbidity levels could be correlated with
tion techniques treated previous observations on childrenÕs heights as child-specific random effects. Maximum likelihood methods were used
‘‘endogenous’’ variables, i.e., correlated with the errors u1it (23) (see to consistently estimate the model variables and to test the ‘‘exogeneity’’
below). null hypothesis for childrenÕs morbidity levels.
The dynamic model in Equation 2 contained previous measurement Last, in the model explaining childrenÕs completed heights at age
on height as an explanatory variable, thereby enabling a distinction 22 y, previous height at age 2 y was likely to be correlated with the error
between short- and long-run effects of explanatory variables. Moreover, terms. Specification 1 postulated cross-sectional type regressions that
previous levels of morbidities and protein and calcium intakes were treated childrenÕs heights at age 2 y as uncorrelated with error terms. In
postulated to affect current heights. Because the data were available at specification 2, childrenÕs height at age 2 y was treated as correlated with
2-mo intervals, the model in Equation 2 expressed nutrient intakes as the error terms in instrumental variable estimation. Specification 3
ratios to energy intakes (33, 34). Such ratios reflect diet quality and estimated a dynamic random-effects model by using the data for 2 time
obviate the need for separately including childrenÕs energy intakes, which periods and treating height at age 2 y as an exogenous variable. In
are influenced by anthropometric measures and energy expenditures specification 4, childrenÕs height at age 2 y was treated as an endogenous
(33). It was appropriate to combine mothersÕ heights and weights as the variable in the maximum likelihood estimation.
BMI with the use of a statistical test (26).
The models for childrenÕs weights and morbidity levels during the
ages of 2–24 mo were similar to the model in Equation 2, although there
were some differences. For example, current morbidity levels were Results
introduced as explanatory variables in the model for weight. This can Table 1 reports sample means and SDs of salient variables used
induce correlations between the errors affecting the model for weight
in the analyses. The sample consisted of a similar proportion of
and morbidity levels and is discussed below. The models for childrenÕs
morbidity levels included explanatory variables such as householdÕs
boys and girls. Mean child birth order was ;3 and number of
access to piped water and flush toilets, hygiene condition, and childrenÕs persons in the household was 5.6. Maternal highest grade was a
intakes of b-carotene expressed as ratios to energy intakes. Third, the mean of 7.6 and socioeconomic index was 7.25; this index
dynamic random-effects model for childrenÕs heights (and weights) with ranged from 1 to 26. MothersÕ mean height was 150.8 cm and
the use of data at ages 8, 10, 15, and 19 y is given in Equation 4: weight when the child was 1 y was 46.1 kg; the corresponding
mean BMI (in kg/m2) was 20.4. The mean morbidity index for
lnðHeightÞit ¼ c0 þ c1 ðGenderÞi þ c2 ðSocioeconomic indexÞi
þc3 ðMothers highest gradeÞi þ c4 lnðMothers heightÞi
mothers was 0.58. The mean energy intake was 3144 kcal/d during
þc5 lnðMothers weightÞit the pregnancy and declined to 2333 kcal/d when the child was 1 y.
þc6 ðChildren immunizations totalÞi Mean morbidity indexes 1 and 2, corresponding to the
þc7 ðChildren morbidity index totalÞi previous 24 h and 7 d when the children were 1 y, were 0.91 and
þc8 lnðChildren protein intake=dÞi 1.03, respectively; the respective values at age 2 y were 0.79
þc9 lnðChildren calcium intake=dÞi and 0.95, which represented a slight decline. The mean number
þc10 lnðHeightÞit-1 þ u2it ði ¼ 1; 2; .; N; t ¼ 2; 3; 4Þ ð4Þ of child immunizations was 1.38; 63% of the children did
not receive any immunizations. ChildrenÕs heights and weights
Because the observations were available at unequally spaced intervals, showed steady increases. ChildrenÕs energy, protein, calcium,
static versions of the models (35) that excluded previous heights were and b-carotene intakes increased over time. For example, mean
also estimated for assessing the robustness of the estimated parameters. protein and calcium intakes at age 19 y were 70.9 g/d and 520 mg/d,
The index for childrenÕs total morbidity levels summed up all morbidities respectively.
Growth and morbidity patterns of children in Cebu 135
TABLE 1 Characteristics of children in the Cebu Longitudinal Health and Nutrition Survey from birth to
age 19 y1

Age
Variable Birth 1y 2y 8y 10 y 15 y 19 y

Girls, % 47 — — — — — —
Birth order 3.14 6 2.0 — — — — — —
Number of persons in household 5.57 6 2.8 — — — — — —
Socioeconomic status index 7.25 6 4.0 — — — — — —
MothersÕ — — — — — — —
Highest grade 7.56 6 3.7 — — — — — —

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Morbidity index — 0.58 6 1.1 0.56 6 1.1 — — — —
Height, cm 150.8 6 5.1 — — — — — —
Weight, kg 50.1 6 6.9 46.1 6 7.3 47.1 6 7.6 52.2 6 9.5 52.7 6 10.0 53.8 6 10.4 55.2 6 10.8
Energy intake, kcal/d 3144 6 1781 2333 6 1521 — — — — —
ChildrenÕs — — — — — — —
Morbidity index 12 — 0.91 6 1.3 0.79 6 1.2 — — — —
Morbidity index 22 — 1.03 6 1.5 0.95 6 1.3 — — — —
Diarrhea index — 0.25 6 1.0 0.18 6 0.8 — — — —
Total number of immunizations3 — — 1.38 6 2.1 — — — —
Height, cm 49.3 6 2.1 70.7 6 3.0 79.1 6 3.7 117.7 6 5.6 133.8 6 7.5 154.0 6 7.8 157.1 6 8.1
Weight, kg 2.99 6 0.5 7.9 6 1.1 9.8 6 1.2 20.6 6 3.1 28.5 6 6.1 44.5 6 7.9 49.8 6 8.7
Energy intake, kcal/d — 434 6 350 727 6 404 — 1201 6 570 1688 6 875 1883 6 1064
Protein intake, g/d — 12.3 6 12.1 21.6 6 15.6 — 38.4 6 19.7 51.6 6 32.2 70.9 6 45.0
Calcium intake, mg/d — 256 6 350 282 6 333 — 322 6 239 364 6 231 520 6 113
b-Carotene intake, μg/d — 132 6 373 350 6 800 — 526 6 906 708 6 1195 758 6 1610
1
Values are means 6 SDs, n = 3080 children.
2
Morbidity index 1 covered the past 24 h, whereas morbidity index 2 covered the past 7 d.
3
Total number of vaccinations received by the age 2 y.

Results for infant lengths and weights at birth. Table 2 test indicated that the variance of random effects was statisti-
presents the results for natural logarithms of lengths and weights cally greater than zero. The main findings from these models
of infants at birth with the use of 2 specifications. The model was were, first, that childrenÕs birth order and number of persons in
first estimated by using ordinary least squares; ‘‘barangay’’-level the household were associated in a nonlinear fashion with their
random effects were included in the second specification and the lengths and weights at birth. The estimated coefficients showed
variables were estimated by maximum likelihood (38, 39). The that infant lengths and weights significantly (P < 0.05) increased
results from the 2 models were very close, although a statistical with birth order, although at a declining rate; lengths and

TABLE 2 Ordinary least-squares and maximum likelihood estimates of models for childrenÕs lengths and weights at birth in Cebu,
Philippines1

Dependent variable
ln (Length), cm ln (Weight), kg
Explanatory variables Ordinary least squares Maximum likelihood2 Ordinary least squares Maximum likelihood2

Constant 3.017 6 0.122 3.028 6 1.171 21.488 6 0.420 21.490 6 0.42


Indicator for girls, 0–1 20.009* 6 0.002 20.009* 6 0.002 20.017* 6 0.005 20.017* 6 0.0004
Birth order 0.005* 0.005* 6 0.001 0.028* 6 0.004 0.028* 6 0.004
(Birth order)2 20.0004* 6 0.0002 20.0004* 6 0.0001 20.002* 6 0.0004 20.002* 6 0.0003
Number of persons in household 20.003* 6 0.001 20.003* 6 0.001 20.008* 6 0.004 20.008* 6 0.004
(Number of persons in household)2 0.0002* 6 0.0001 0.0002* 6 0.0001 0.001* 6 0.0005 0.0005* 6 0.0002
Socioeconomic index 0.001* 6 0.0003 0.001* 6 0.0002 0.003* 6 0.001 0.003* 6 0.001
MothersÕ
Highest grade 0.0005* 6 0.0002 0.0005* 6 0.0003 0.002* 6 0.001 0.001 6 0.001
ln Height, cm 0.130* 6 0.027 0.128* 6 0.027 0.299* 6 0.091 0.301* 6 0.091
ln Weight, kg 0.050* 6 0.007 0.051* 6 0.007 0.252* 6 0.023 0.253* 6 0.023
Energy intake, kcal/d 0.004* 6 0.001 0.004* 6 0.001 0.007 6 0.005 0.005 6 0.005
Chi-square (1) test, multilevel random effects 10.63* 30.07*
R2 0.095* 0.111*
1
Values are regression coefficients 6 SEs, n = 2990 children. *P , 0.05.
2
Multilevel models with random effects for ‘‘barangay.’’

136 Bhargava
weights declined with respect to household size at an increasing the previous time period was also negative and significant.
rate. Girls were shorter and lighter than boys at birth. Although childrenÕs intake of protein expressed as a ratio to
Second, the coefficients of mothersÕ highest grade and socio- energy intake was not significantly associated, the coefficient of
economic index were positive and significant. This was also calcium intake was positive and significantly associated with
true for mothersÕ heights and weights. The ‘‘elasticity’’ of infant childrenÕs heights. The coefficient of the lagged dependent
length with respect to mothersÕ height (percentage change in variable was 0.88, implying large long-run effects of explanatory
infant length resulting from a 1% change in mothersÕ height) was variables on childrenÕs heights. For example, whereas the short-
0.13; the elasticity with respect to mothersÕ weight was 0.05. The run elasticity of childrenÕs heights with respect to the calcium
elasticities of infant birth weight with respect to mothersÕ heights to energy intake ratio was 0.001, the long-run elasticity was
and weights were 0.30 and 0.25, respectively. Third, mothersÕ ;0.01.
energy intakes were significantly associated with infant lengths; The results for childrenÕs weights in Table 3 are presented for
the coefficients were positive but not significant in the model for 2 specifications—namely, where childrenÕs height was excluded

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weight. from the model and where height was an explanatory variable
(40). In both models, socioeconomic index and mothersÕ highest
Results for childrenÕs heights, weights, and morbidity grade, BMI, and energy intakes were positively and significantly
indexes during ages 2–24 mo. Table 3 presents the results associated with weights. By contrast, birth order and number of
from dynamic random-effects models for childrenÕs heights and persons in the household were negatively associated. Moreover,
weights estimated by using data at bimonthly intervals; results childrenÕs number of immunizations and protein to energy
for childrenÕs morbidity indexes are shown in Table 4. In the intake ratio were positively and significantly associated with
model for childrenÕs heights, socioeconomic index and mothersÕ weights. ChildrenÕs combined morbidity index and the diarrhea
highest grade were positively and significantly associated, index were estimated with negative coefficients that were
whereas birth order and number of persons in the household significant. Moreover, there was evidence of correlations be-
were negatively associated. MothersÕ BMI and energy intakes tween child-specific random effects (di) and morbidity indexes
were positively and significantly associated with childrenÕs and childrenÕs heights. The likelihood ratio statistics for exogeneity
heights. By contrast, mothersÕ morbidity index was negatively hypotheses in the 2 models for weights were 53.8 and 485.2,
associated with childrenÕs heights. respectively; these statistics were distributed in large samples as
The number of childrenÕs immunizations was positively and chi-square variables with 33 and 44 df and rejected the null
significantly associated with height, although the coefficients hypotheses.
were small. Moreover, coefficients of childrenÕs morbidity The results for childrenÕs morbidity indexes in Table 4 were
indexes 1 and 2 in the previous time period were negative and similar across the models and underscored the importance of
significant and were very close in magnitudes. Thus, the 2 socioeconomic, environmental, and dietary variables. Girls were
morbidity indexes were combined partly to reduce the number less often sick than boys; socioeconomic index was negatively
of variables in the model. The coefficient of the diarrhea index in and significantly associated with the first 2 morbidity indexes

TABLE 3 Maximum likelihood estimates of dynamic random-effects models for heights and weights of
children in Cebu, Philippines, ages 2–24 mo1

Dependent variable
Explanatory variables ln (Height), cm ln (Weight), kg ln (Weight),2 kg

Constant 0.576 6 0.002 0.527 6 0.022 21.045 6 0.030


Indicator for girls, 0–1 20.002* 6 0.0003 20.009* 6 0.001 20.021* 6 0.001
Socioeconomic index 0.003* 6 0.0004 0.001* 6 0.0001 0.002* 6 0.002
Birth order 20.0004* 6 0.0001 20.001* 6 0.0002 20.001* 6 0.0003
Number of persons in household 20.0002* 6 0.0001 20.001* 6 0.0002 20.001* 6 0.0003
MothersÕ
Highest grade 0.0002* 6 0.0001 0.0004* 6 0.0001 0.001* 6 0.0002
ln BMI 0.006* 6 0.001 0.031* 6 0.003 0.057* 6 0.004
ln Energy intake, kcal/d 0.0005* 6 0.0001 0.002* 6 0.001 0.002* 6 0.001
Morbidity index 20.0002* 6 0.0001 20.0001 6 0.0003 20.0004 6 0.0003
ChildrenÕs
Number of total immunizations 0.0002* 6 0.0001 0.0003* 6 0.0001 0.001* 6 0.0002
Morbidity indexes 1 and 23 20.0003* 6 0.0001 20.003* 6 0.0003 20.004* 6 0.0002
Diarrhea index3 20.0003* 6 0.0001 20.004* 6 0.0003 20.004* 6 0.001
ln protein/energy intake, g/(kcal  d) 0.0004 6 0.0003 0.004* 6 0.001 0.004* 6 0.001
ln calcium/energy intake, mg/(kcal  d) 0.001* 6 0.0001
ln height, cm 0.561* 6 0.004
Lagged dependent variable 0.880* 6 0.0001 0.867* 6 0.003 0.550* 6 0.004
Chi-square test for exogeneity4 (df) 53.8* (33) 485.2* (44)
1
Values are regression coefficients 6 SEs, n = 2076 children repeatedly observed in 11 periods. *P , 0.05.
2
First model for weight did not include childrenÕs height.
3
ChildrenÕs lagged morbidity and nutrient intakes were included in the model for height; current morbidity and intakes were included in the
model for weight.
4
Test if childrenÕs morbidity and diarrhea indexes were correlated with random effects.

Growth and morbidity patterns of children in Cebu 137


TABLE 4 Maximum likelihood estimates of dynamic random-effects models for morbidity indexes of children in Cebu, Philippines,
ages 2–24 mo1

Dependent variable
Explanatory variables ChildrenÕs morbidity index 1 ChildrenÕs morbidity index 2 ChildrenÕs diarrhea index

Constant 2.977 6 0.037 5.516 6 0.040 1.740 6 0.486


Indicator for girls, 0–1 20.068* 6 0.019 20.097* 6 0.019 20.027* 6 0.014
Socioeconomic index 20.008* 6 0.003 0.007* 6 0.002 20.003 6 0.002
Birth order 20.027* 6 0.005 0.004 6 0.005 20.007* 6 0.003
Number of persons in household 0.009* 6 0.004 20.006 6 0.003 0.002 6 0.002
MothersÕ

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Highest grade 20.014* 6 0.002 20.006* 6 0.003 20.002* 6 0.001
Morbidity index 0.137* 6 0.008 0.062* 6 0.009 0.031* 6 0.008
Household
Piped water, 0–1 20.025 6 0.061 20.037 6 0.069 0.012 6 0.026
Flush toilet, 0–1 20.068 6 0.076 20.039 6 0.087 20.013 6 0.031
General hygiene condition,2 1–4 20.052* 6 0.009 20.049* 6 0.009 0.006 6 0.004
ChildrenÕs
Total number of immunizations 20.015* 6 0.006 0.002 6 0.007 20.002 6 0.002
ln Height, cm 20.388* 6 0.008 20.956* 6 0.008 20.373* 6 0.101
ln b-Carotene/energy intake, μg/(kcal  d) 20.025* 6 0.003 20.009* 6 0.004 20.008* 6 0.003
Lagged dependent variable 0.051* 6 0.008 0.042* 6 0.008 0.582* 6 0.154
Between/within variance ratio 0.086* 6 0.006 0.050* 6 0.005
Chi-square (22) test for exogeneity3 20.9 27.0 42.4*
1
Values are regression coefficients 6 SEs, n = 2065 children repeatedly observed in 11 time periods. *P , 0.05.
2
Higher scores on general hygiene conditions reflect greater cleanliness.
3
Test for whether childrenÕs height and b-carotene to energy intake ratio were correlated with the random effects.

but was not significant in the model for diarrhea index. Whereas corresponding estimate, 0.35, from the static model. In contrast,
mothersÕ highest grade was significantly negatively associated, the estimated long-run elasticity of childrenÕs weights with
mothersÕ morbidity index was positively associated with all 3 respect to mothersÕ heights was 0.47, which was very close to the
indexes. Moreover, greater hygiene in the house was associated corresponding estimate from the static model.
with lower child morbidity levels. This was also true for number Third, the number of immunizations received by children
of immunizations that the children received and for the ratio of during the ages of 2–24 mo was significantly associated with
b-carotene to energy intakes. height. Moreover, childrenÕs morbidity levels during the ages of
Finally, the lagged dependent variables were estimated with 2–24 mo were negatively associated with height and weight in
small coefficients of 0.05 and 0.04 in the models for morbid- later years; the coefficients were significant in the static versions
ity indexes 1 and 2, respectively, and were significant. The co- of the models. Last, coefficients of childrenÕs average intakes of
efficient of the lagged dependent variable in the model for protein and calcium during the ages of 10–19 y were significant
diarrhea index was larger (0.58), indicating longer persistence in the model for height; coefficients of protein intakes were
in the effects of explanatory variables on diarrhea index. positive and significant in the model for weight. Coefficients of
Coefficients of previous heights were negative, indicating that lagged dependent variables were lower in Table 5 than those in
taller children were sick less often and with lower intensity. The Table 3 because the models were estimated by using observa-
exogeneity hypothesis for previous heights could not be tions separated by several years.
rejected in the models for morbidity indexes 1 and 2; the
exogeneity hypothesis was rejected in the model for diarrhea Results from models for childrenÕs heights at 22 y
index. explained by current and early variables. Table 6 reports
the results from 4 specifications for childrenÕs completed
Results for childrenÕs heights and weights during ages heights at 22 y with the use of data on heights at age 2 y. The
8–19 y. Table 5 reports the estimates from dynamic and static results from specification 1 showed that the coefficients of
random-effects models for childrenÕs heights and weights with mothersÕ height and childrenÕs calcium intakes in adoles-
the use of data at 8, 10, 15, and 19 y. First, the coefficient of the cence were positive and significantly associated with completed
socioeconomic index was significant only in the dynamic model heights at age 22 y. However, the coefficient of calcium intakes
for childrenÕs heights; this coefficient was positive but was not at 2 y was estimated with an unexpected minus sign, which was
significant in the static version of the model. The coefficient of significant. The coefficient of height at age 2 y was 0.43, which
mothersÕ highest grade was significant in all models except the was large and significant. In specification 2, estimated by using
dynamic model for weights. instrumental variables, this coefficient decreased to 0.14 and
Second, the coefficient of mothersÕ height was estimated to be was no longer significant. The instrumental variables used for
large and significant in the models for childrenÕs heights and heights at age 2 y were mothersÕ highest grade and weight. A
weights. Whereas the short-run elasticity of childrenÕs heights test for exogeneity (41) showed that there was likely to be a
with respect to mothersÕ heights was 0.30 in the dynamic model, correlation between errors affecting this model and childrenÕs
the long-run elasticity was 0.76, which was larger than the heights at age 2 y.
138 Bhargava
TABLE 5 Efficient estimates of dynamic and static random-effects models for heights and weights of
children in Cebu, Philippines, by using data at ages 8, 10, 15, and 19 y1

Dependent variable
ln (Height), cm ln (Weight), kg
Explanatory variables Dynamic model2 Static model2 Dynamic model Static model

Constant 1.645 6 0.002 2.904 6 0.147 0.050 6 0.219 20.006 6 0.471


Indicator for girls, 0–1 20.044* 6 0.001 20.025* 6 0.002 20.070* 6 0.004 20.068* 6 0.007
Socioeconomic index 0.0001* 6 0.0001 0.0003 6 0.0003 20.0001 6 0.0004 0.0004 6 0.0009
MothersÕ
Highest grade 0.0003* 6 0.0001 0.001* 6 0.0003 20.0003 6 0.0004 0.002* 6 0.001

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ln Height, cm 0.298* 6 0.001 0.352* 6 0.030 0.272* 6 0.046 0.474* 6 0.097
ln Weight, kg 20.0003 6 0.002 0.040* 6 0.004 0.055* 6 0.008 0.240* 6 0.015
ChildrenÕs
Total number of immunizations 0.0003* 6 0.0001 0.001* 6 0.0004 0.001* 6 0.0006 0.003* 6 0.001
Total morbidity index 20.0001 6 0.0001 20.0002* 6 0.0001 20.0001 6 0.0002 20.0008* 6 0.0004
ln Protein intake,3 g/d 0.004* 6 0.001 0.009* 6 0.003 0.019* 6 0.004 0.035* 6 0.008
ln Calcium intake,3 mg/d 0.002* 6 0.001 0.005* 6 0.002
Lagged dependent variable 0.391* 6 0.002 0.619* 6 0.008
1
Values are regression coefficients 6 SEs, n = 1700 children repeatedly observed in 4 time periods. *P , 0.05.
2
Dynamic models were estimated by maximum likelihood, whereas static models used a stepwise estimation procedure.
3
Nutrient intakes at ages 10, 15, and 19 y were averaged.

In specification 3, the dynamic model was estimated by using when height was treated as an endogenous variable and remained
data at ages 2 and 22 y and by treating height at 2 y as an significant.
exogenous variable. However, coefficients of childrenÕs protein
and calcium intakes were not statistically different from zero. In
Discussion
specification 4, which treated previous height as an endogenous
variable, the estimated coefficients of protein and calcium This article presented 4 sets of comprehensive analyses for
intakes were 0.006 and 0.003, respectively, and were significant. growth and morbidity patterns of children in Cebu, Philippines,
The likelihood ratio test statistic for the exogeneity hypothesis and tackled the conceptual and methodologic aspects. First, the
for heights at 2 y was 13.6 and indicated that child-specific results for infant lengths and weights at birth underscored the
random effects were correlated with previous heights. Moreover, importance of mothersÕ nutritional status reflected in height,
the coefficient of childrenÕs heights at 2 y decreased to 0.025 weight, and energy intakes. Moreover, in alternative models for

TABLE 6 Efficient estimates of models for completed heights of children in Cebu, Philippines, at age 22 y
explained by variables including heights at age 2 y1

Dependent variable (ln height at age 22 y): estimation method, cm


Explanatory variables Specification 12 Specification 23 Specification 34 Specification 45

Constant 1.609 6 0.107 2.341 6 0.250 1.704 6 0.024 2.671 6 0.001


Indicator for girls, 0–1 20.067* 6 0.001 20.071* 6 0.002 20.067* 6 0.024 20.073* 6 0.001
Socioeconomic index 0.0001 6 0.001 0.0002 6 0.0002 20.0001 6 0.024 0.0004* 6 0.0001
MothersÕ ln height, cm 0.331* 6 0.021 0.439* 6 0.041 0.320* 6 0.024 0.471* 6 0.001
ChildrenÕs ln
Protein intakes at age 2 y, g/d 0.001 6 0.002 0.001 6 0.001
Calcium intakes at age 2 y, mg/d 20.003* 6 0.001 20.0016 6 0.0014
Protein intake in adolescence,6 g/d 0.0004 6 0.002 0.0041 6 0.003
Calcium intake in adolescence, mg/d 0.002* 6 0.002 0.0024 6 0.002
Time-varying protein intake, g/d 20.002 6 0.024 0.006* 6 0.0002
Time-varying calcium intake, mg/d 0.002 6 0.023 0.003* 6 0.001
Height at age 2 y, cm 0.431* 6 0.016 0.137 6 0.092 0.424* 6 0.024 0.025* 6 0.0002
Chi-square (1) test for overidentification 0.08
Chi-square (1) test exogeneity height at age 2 y 13.1* 13.6*
1
Values are regression coefficients 6 SEs, n = 1692 children repeatedly observed in 2 time periods. *P , 0.05.
2
ChildrenÕs height at age 2 y was treated as an exogenous variable and the model was estimated by ordinary least squares.
3
ChildrenÕs height at age 2 y was treated as an endogenous variable with mothersÕ highest grade and weight used as instrumental
variables.
4
ChildrenÕs height at age 2 y was treated as an exogenous variable and the model was estimated by maximum likelihood.
5
ChildrenÕs height at age 2 y treated as an endogenous variable and the model was estimated by maximum likelihood.
6
Nutrient intakes at ages 10, 15, and 19 y were averaged.

Growth and morbidity patterns of children in Cebu 139


infant birth lengths and weights, mothersÕ energy intakes from linear growth, which, in turn, determines their adult physical
fat were estimated with coefficients 0.004 and 0.007, respec- work capacity and labor productivity.
tively; the coefficient was significant in the model for length. It is
often difficult to assess the effects of mothersÕ diet quality on Acknowledgments
birth outcomes, partly because limited information is avail- While retaining responsibility for the views, I thank L Adair,
able on dietary intakes during pregnancy trimesters (31). Future A Bas, E Birol, H Bouis, L Howard, I Larenas, N Lee, and
research compiling data on mothersÕ food intakes during M Zeller for their valuable help. This article is dedicated to the
pregnancy at regular intervals could shed light on these issues. memory of Nevin S Scrimshaw, who selflessly spent his valuable
Second, the analyses of childrenÕs growth and morbidity time educating AB regarding the nutrition-infection interac-
patterns during the ages of 2–24 mo provided several insights. tions. AB had responsibility for all parts of the manuscript and
Although it is recognized that catch-up growth in developing read and approved the final manuscript.
countries critically depends on morbidity levels (42), children

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