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Community and International Nutrition

Filipino Children Exhibit Catch-Up Growth from Age 2 to 12 Years

Department of Nutrition, University of North Carolina at Chapel Hill, Chapel Hill, NC 27516-3997, U.S.

Address correspondence to: Linda S. Adair, Ph.D., Carolina Population Center, University of North Carolina, University Square, CB#8120, Chapel Hill, NC.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Potential for catch-up growth among stunted children is thought to be limited after age 2 y, particularly when they remain in poor environments. We explored the extent to which there were improvements in height status from age 2 to 12 y in a cohort of >2,000 children from the Cebu (The Philippines) Longitudinal Health and Nutrition Survey. At age 2 y, about 63% of sample children were stunted as defined by height-for-age (HAZ) <-2 based on the WHO reference. Of children stunted at age 2, 30% were no longer stunted at 8.5 y, and 32.5% were no longer stunted at 12 y. The mean increase in HAZ among those with such improvements was 1.14 units. The likelihood that children stunted at age 2 y would no longer be stunted at 8.5 y was estimated using logistic regression. Low birth weight, which was associated with more severe stunting in the first 2 y of life, significantly reduced likelihood of catch-up growth in later childhood. In contrast, children with taller mothers, who were first born, longer at birth, less severely stunted in early infancy and those with fewer siblings were more likely to increase HAZ from <-2 to >-2 between ages 2 and 8.5 y. Similar factors predicted the improvement in linear growth from 8.5 to 12 y. These results suggest that there is a large potential for catch-up growth in children into the preadolescent years.

KEY WORDS: • catch-up growth • stunting • height • The Philippines • humans

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Linear-growth retardation is a continuing health problem among children living in poverty in developing countries. It is generally well accepted that most growth retardation occurs during the first 2 y of life, associated primarily with high rates of infection and inadequate nutrition related to poor weaning practices and poor dietary quality. After 2–3 y of age, linear-growth rates of poor children are more similar to those observed in well-nourished children. Thus, deficits in adult height are attributed primarily to linear-growth retardation in infancy and early childhood (Martorell and Habicht 1986 ).

There is a lack of a consensus about the extent to which catch-up growth in later childhood and adolescence reduces the height deficit incurred in early childhood. The biological potential for catch-up growth is well illustrated in studies that evaluate response to clinical intervention with supplementary feeding, treatment of illness or hormone therapy (Golden 1994 ). Tanner (1981) advanced the general hypothesis that when undernourished children are exposed to better environments and good nutrition, the likelihood of catch-up is greater, with the degree of recovery depending on the severity of growth retardation and the timing of exposures. However, the degree to which catch-up occurs in the absence of medical or nutrition intervention is less well documented. Martorell et al. (1994) evaluated the evidence for reversibility of stunting in epidemiologic studies, dividing studies into those cases where children remain in the same poor environments responsible for stunting, vs. those where the child's situation was improved by nutrition supplementation or migration. They concluded that when children remain in the same poor environment, the growth deficits developed in early childhood persist into adulthood, with little catch-up growth. Relatively little is known about the potential for catch-up growth during adolescence. Martorell et al. (1994) suggest that catch-up may depend on whether undernutrition is also associated with delayed maturation, which in turn could allow for a prolonged adolescent growth spurt with greater time for recovery before skeletal growth is complete.

Conclusions about whether, how, and when catch-up occurs are based on limited evidence. First, relatively few longitudinal studies followed children from birth to late childhood or adulthood. Second, in the longitudinal studies that have been done, there are limited observation points with long gaps between measurements, so that changes in the environment and other factors that influence growth are not well documented. Third, epidemiologic studies of catch-up growth tend to compare groups of children or adults by their initial level of stunting (e.g., Martorell et al. 1990 , Satyanarayana et al. 1989 ). These studies tend to show substantial tracking of stature, with groups who were short as young children remaining short as older children or adults. However, with their focus on central tendencies of the groups, they fail to identify individual children who exhibit catch-up growth, and thus cannot contribute substantially to our understanding of the circumstances under which catch-up occurs.

In this paper, we present evidence of catch-up growth based on a longitudinal ecological study of a cohort of Filipino children from Metro Cebu. We focus on growth from age 2 to 12 y, with an intermediate measurement taken at age 8.5 y. We model the overall determinants of height increments, identify children who exhibit catch-up growth, and identify factors associated with recovery from stunting.

The study has a number of important strengths. First, it builds on earlier work to identify determinants of incident stunting from birth to age 2 y in the same Cebu Longitudinal Health and Nutrition Survey (CLHNS)¹ sample (Adair and Guilkey 1997 ). Second, the cohort is large (>2,000), and children live in diverse urban and rural environments. Third, we have detailed, repeated measures of socioeconomic and ecological conditions in each household, as well as dietary intake. Finally, by identifying individual children who recover from stunting, we can report the incidence of catch-up growth and, using multivariate methods, report determinants of recovery from stunting.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Subjects are children followed from birth to age 12 y during the CLHNS. This is an ongoing survey in Metro Cebu, the second-largest metropolitan area in The Philippines. Metro Cebu encompasses urban and rural communities within and surrounding Cebu City. The most rapidly growing area of The Philippines, Metro Cebu is characterized by substantial economic development overall, but a high level of income disparity within the population.

From all of the barangays (local administrative units) of Metro Cebu, 17 rural and 16 urban barangays were randomly selected for the study. All pregnant women in these communities who gave birth in a 1-y period from 1983 to 1984 were asked to participate in the CLHNS. The CLHNS child sample is thus a 1-y birth cohort representative of births in Metro Cebu. Home visits were made to collect data during the last trimester of pregnancy, immediately after birth, then bimonthly for 2 y. Follow-up surveys were conducted in 1991–92 and 1994–95 when the children were, on average, ages 8.5 and 11.5 y, respectively.

Infant recumbent length and weight were measured through 24 mo according to standard techniques, and interobserver reliability was routinely assessed. Height, weight and triceps and subscapular skinfold thicknesses were measured during the follow-up surveys. Length (at age 2) or height Z-scores (HAZ) were computed using the WHO reference (Hamill et al. 1979 ). Gestational age was determined from the date of the mother's last menstrual period. When there were pregnancy complications, an uncertain last menstrual period date, or when the infant weighed less than 2500 g at birth, the Ballard method was used to clinically assess gestational age (Ballard et al. 1966 ). Preterm infants were those who completed less than 37 wks gestation.

Detailed in-home interviews with mothers or caretakers, and community surveys with key informants, provided extensive information to characterize family socioeconomic status, demographics, and environment. Dietary intake of mothers, infants, and children was assessed using 24-h dietary recalls or quantitative food frequency questionnaires. Each round of the CLHNS was approved by the University of North Carolina School of Public Health Institutional Review Board for the Protection of Human Subjects.

The present analysis has a focus on three time points: ages 2, 8.5 and 11–12 y. In previous papers (Adair 1989 , Adair et al. 1993a , Adair et al. 1993b , Adair and Guilkey 1997 ), we analyzed data from the first 2 y of life. The present analysis begins with 2-y-old children because this is the age by which most linear growth retardation is thought to occur. Peak incidence of stunting among CLHNS sample children occurred between 6 and 14 mo of age (Adair and Guilkey 1997 ).

The two intervals from age 2–8.5 and 8.5–12 y are treated separately. First, patterns of growth and prevalence of catch-up during each of the two intervals are described, as are characteristics of children who exhibit catch-up growth vs. those who do not. Multivariate linear and logistic regression models are used to identify factors significantly associated with growth increments and catch-up growth.

Sample

The analysis sample includes 2,011 children with complete data from the birth, 24 mo and two follow-up surveys. The original CLHNS birth cohort included 3,080 single live births. Losses to follow-up occurred because of death and migration from the metro Cebu area. Exclusion from the analysis sample occurred because of missing data at one or more time points. As expected, the children lost to follow-up because of death differed significantly from the surviving cohort: they were more likely to be from the poorest households, and to weigh less than 2,500 g at birth. However, children lost to follow-up after 12 mo or who had missing data did not differ significantly in weight or length at 12 mo from those included in the sample.

Characteristics of the sample are shown in Table 1. At the baseline survey, less than half of the sample households had electricity, about 43% of houses were constructed of light, traditional materials, and just over half had only one or two rooms. Only 44% of mothers had more than a sixth-grade education. HAZ-scores for the full sample are presented in Figure 1.

View larger version (15K): [in this window] [in a new window]   Figure 1. Mean height-for-age Z-scores of Cebu Longitudinal Health and Nutrition Survey sample males and female children from age 2 to 12 y. Data from the 1994 survey are cross-sectional by age, but linked with earlier longitudinal data for each child.

    Catch-up growth. While there is considerable clinical and epidemiologic literature on catch-up growth, there is no standard definition of "catch-up growth." In general, the term refers to acceleration in growth after a period of growth retardation. The assumption is that accelerated growth will return the individual to his or her genetically determined growth trajectory (Ashworth and Milward 1986 ). However, sometimes catch-up is used to refer to complete recovery or restoration of growth to normal levels. In other cases, catch-up is considered to be an acceleration in growth rates which may or may not result in stature within normal limits for age and sex. For the present analysis, we define catch-up growth with and without reference to an external reference. "Recovery from stunting" is defined as a HAZ-score <-2 at age 2 y, but -2 at age 8.5 or 11–12 y. Use of a variable representing a change in Z-score may be problematic because a Z-score has a different meaning at different ages (Tanner 1986 ). Z-scores among older children may misclassify those whose pre-adolescent and early adolescent growth pattern differs from the WHO reference population. Of concern for the present study is the likelihood of later sexual maturation relative to the reference population, and thus apparent inflation of the magnitude of growth retardation relative to the reference. To avoid the use of an external reference, we also assess height increments in the two age intervals (2 to 8.5 and 8.5 to 12 y). The increment from age 2 to 8.5 y is a slight underestimate of the actual height increment, since the measurement at age 2 was of recumbent length. Finally, we regress height at time t on height at time t-1, sex, and duration of the interval from t-1 to t, and calculate residuals. Children are then grouped according to their studentized residuals, and catch-up growth is defined as a residual >1 (14.3% of the sample). This method identifies children with greater than expected growth, irrespective of their starting length (Esrey et al. 1990 ).

    Independent variables. Covariates were specified as continuous variables in linear regression models. For ease of interpretation of relative risk ratios from logistic regression analysis, covariates were defined as categorical variables (described below).

    Biological factors. Mother's height partially accounts for genetic growth potential. However, mothers in developing countries may not have reached their genetic potential for growth because of undernutrition and infection during their own childhood. Short maternal stature was defined as height <145 cm, a level acknowledged to represent risk of poor reproductive outcomes (WHO 1994 ). Tall mothers were those with a height greater than 154.75 cm, which represents the 75^th percentile of height for adult Filipinas. Infants were considered long at birth if their recumbent length was above the 75^th percentile of the Filipino reference (Florentino et al. 1992 ). Low ponderal index, an indicator of asymmetric fetal growth restriction, was defined as weight/length below the 10th percentile of the Lubchenco et al. (1966) reference. Severe stunting at age 2 was defined as a HAZ score below -3, while those not severely stunted had a HAZ between -2 and -3. Child age is relevant only for the analysis of the 8–12 y time period. During the 1991–92 survey, children were measured in their birth month, with the result that all children are of the same age (mean ± SD = 102 ± 1 mo). Because of survey logistical considerations, the age range during the 1994 follow-up was greater (mean ± SD = 138 ± 5 mo). Girls were asked during the 1994 survey whether and when they had begun menstrual periods. Only 7% of girls were post-menarchal.

For the logistic regression analyses, birth weight and gestational age were represented by a set of dichotomous variables representing low birth weight (LBW)-preterm, LBW-full term, and normal birth weight-preterm infants, with normal birth weight-full term infants as the reference category. In the length increment models, birth weight was entered as a continuous variable.

    Socioeconomic measures. Socioeconomic status is represented by total household income at each survey; ownership of selected assets (television, refrigerator, air conditioner, any motor vehicle); presence of electricity and piped water; house construction (light weight, traditional materials such as nipa palm vs. solid construction with cinder block); and a general rating of cleanliness of the area around the house. We focus on level of the indicator at the beginning of each interval, as well as change in each indicator over the study intervals.

Demographic variables include mother's age and education (<6th grade, >12th grade), index child's birth order and number of younger siblings at the time of measurement.

    Dietary intake. Daily energy intake was calculated from 24-h dietary recalls during the surveys from birth to 2 y and at age 11–12 y. During the 1991–92 survey, intake was assessed using a quantitative food frequency questionnaire, with items derived from a list based on 24-h food recalls from sample women. While these two methods are not directly comparable, they are useful for ranking individual's intakes. Dichotomous variables represented an increase in energy intake at or above the sample 75th percentile, or below the 25th percentile during the relevant interval.

Multivariate models

We use several different multivariate analysis methods, depending on the form of the dependent variable. Data were analyzed using Stata Release 5 (StataCorp 1997 ). Logistic regression is used to estimate the likelihood of recovery from stunting at time t among those who were stunted at time t-1, and to differentiate those with greater than expected growth from those with average or less than expected growth. The analysis sample for the recovery from stunting model includes only children who were stunted at age 2 y. Ordinary least squares linear regression is used to model height increments in the full sample, irrespective of stunting status at age 2 y.

In all of these models, the dependent variable represents a change from one age to the next. First difference models have the advantage of controlling for the potential bias related to unobserved heterogeneity.

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
HAZ-scores of sample children at ages 2–12 y are shown in Figure 1 . The 1994 data are stratified by age in half-year intervals to show the cross-sectional differences in height by age. There were no significant differences in earlier height measures among children measured at different ages in 1994–95. The lower HAZ scores of older girls most likely represent delayed maturity in the Filipinas relative to the U.S. reference population.

The prevalence of stunting in Cebu children is quite high when judged relative to the WHO reference. Nearly two-thirds of females and about 60% of males were stunted at age 2 y. Using the Filipino national reference data and suggested cutoff of length below the 5^th percentile (Florentino et al. 1992 ), 15.6% of males and 10.8% of females were "underheight," suggesting that stunting is more prevalent in the Cebu sample than in the country as a whole.

Recovery from stunting.

Of the 1,252 children stunted at 2 y of age, 379 (30.3%) were not stunted at age 8.5 y, and 407 (32.5%) were not stunted at age 11–12 y. Of those who recovered from stunting by age 8.5, 63% were girls. To what extent does this "recovery" mean only small changes in HAZ around the -2 SD cutoff? The mean change in HAZ from age 2 to 8.5 y among those who recovered from stunting was 1.14 SD. Only seven of these children had a change in HAZ of less than 0.2 SD, suggesting that improvements in linear growth were substantial. Of the 379 who recovered by age 8.5 y, 11% could be considered "fully recovered," that is, their HAZ at 8.5 y was within normal limits for their age and sex (HAZ >-1) using the WHO reference. All of the children in the recovery group had a height at age 8.5 y that fell above the Philippines 25^th percentile.

Of the 1022 children stunted at age 8.5 y, 191 (18.2%) were not stunted by age 11–12 y. Of the children with late recovery, 39.3% were girls.

Recovery from stunting is strongly associated with severity and timing of stunting. Table 2 defines groups of children by when during the first 2 y they first became stunted, then shows the mean HAZ of each group at subsequent ages, and the percentage who recovered from stunting by age 8.5. The children with the most severe stunting at 2 y were those who were stunted early in infancy. In turn, those with early stunting were also more likely to have been LBW infants (see Adair and Guilkey 1997 for further discussion of the determinants of stunting in the first 2 y). While LBW occurred in only 2.7% of infants who were never stunted by age 2 y, over 30% of infants stunted in the first 6 mo were LBW. Overall, LBW infants were 3.56 times more likely than infants weighing 2,500 g or more to be stunted at age 2 [95% confidence interval (CI) 2.41–5.25, t = 6.4]. Children with early, severe stunting had much lower rates of recovery from stunting by age 8.5.

The likelihood of recovery from stunting in the sample of 1,252 children who were stunted at age 2 was estimated using logistic regression. Results are presented in Tables 3 and 4. Initial models included independent variables representing the change in risk factors from one time period to the next (income, assets, housing quality, sanitary conditions, water and electricity, younger siblings born in the interval, energy intake) as well as constant maternal factors (height, parity at birth of the index child, education), and child characteristics (birth weight and length, preterm status, sex, maturity for girls only). In examining the effects of parity, it was apparent that most of the difference in growth related to first vs. higher order births. Thus, a dummy variable indicating that the child was firstborn was included in the models. For simplicity, variables were dropped from the model when their T-statistic was <1, and their exclusion had no effect on other variables or the overall fit of the model.

Socioeconomic and environment effects on growth are hypothesized to operate through more proximate variables such as nutrition and morbidity. A lack of sufficient increase in dietary energy intake with age was associated with decreased chances of recovery, but was not significant at the 0.05 level (P = 0.11). We have only poor information about morbidity, and thus some of the underlying socioeconomic variables in the model may serve as proxies for such unmeasured or poorly measured proximate biological factors. An increase in the number of common household assets, an overall indicator of improvement in household wealth, increased the likelihood of recovery from stunting. To assess the effects of initial level of assets vs. change in assets, we compared the effects of (a) having few assets initially, but improvement over time; (b) more initial assets with no change or a decline; or (c) more initial assets with an improvement, to a reference category of low assets and no improvement. The likelihood of recovery from stunting was doubled with higher initial assets and improvements during the study interval. However, in interpreting this result, it is important to note the low percentage of households in which these conditions held. Paradoxically, improvement in the general cleanliness around the household was marginally associated with a decrease in the likelihood of recovery from stunting. Being firstborn and having fewer younger siblings at age 8.5 significantly increased the likelihood of recovery.

There were fewer significant predictors of recovery from stunting between age 8.5 and 12 y. Less severe stunting at age 8.5 y, being firstborn, and having fewer younger siblings enhanced the likelihood of recovery. Males and post-menarchal girls were more likely than pre-menarchal girls to recover from stunting. Socioeconomic factors significantly associated with an increased likelihood of recovery were modernization marked by acquisition of water or electricity in the house (irrespective of initial status), and higher levels of maternal education. There were no significant effects of dietary change between 8.5 and 12 y.

Growth increments.

The mean height increment from 2 to 8.5 y was 39.1 ± 4.0 cm in girls, and 37.7 ± 3.8 cm in boys. A rough comparison can be made by examining the difference in median height in the WHO reference at these ages, which is 42.5 cm in girls and 38.9 cm in boys. The 67 early maturers in the sample (i.e., girls who reported menarche prior to the 1994–95 survey) had significantly higher growth increments (42.3 ± 4.6 cm) than those who had not had menarche by the 1994–95 survey (38.9 ± 3.8 cm) (ANOVA, P < 0.001). A similar trend is seen from 8.5 to 12 y. Boys had a mean increment of 14.5 ± 3.8 cm, pre-menarchal girls grew on average 17.3 ± 4.2 cm and menarchal girls grew 23.2 ± 3.0 cm.

Linear regression models of height increments were specified with variables similar to those included in the initial logit models. Results presented in Table 5 are generally consistent with those from the recovery from stunting models. Initial height was included in the models to account for regression to the mean. There was a tendency for children who were longer at age 2 y to grow slightly less in the interval (P = 0.13). Larger increments from age 2 to 8.5 y were associated with having a taller, more educated mother, longer length but lower weight at birth, and with being female (particularly an early maturer). Children who were firstborns, and who had fewer younger siblings at age 8.5 y grew significantly more, as did those with larger increases in dietary energy intake. Improvements in socioeconomic indicators, with the exception of neighborhood cleanliness, had positive effects on growth increments. Prematurity alone or in combination with categories of birth weight did not significantly affect height increments in this interval.

The last analysis defined catch-up growth using the residual method described above. This method identified a group of 292 children, about half of whom also recovered from stunting. The remaining children were either not initially stunted (n = 117) or their higher than expected growth was still not sufficient to bring their HAZ above -2 at age 8.5 (n = 33). The children with greater than expected growth in height from age 2 to 8.5 y did not differ significantly from the rest of the sample children in HAZ, nor were they more or less likely to be stunted at age 2 y. Their mean height increment was 44.78 cm compared to 38.29 cm in children with expected growth (residual between -1 and +1). The logistic regression model comparing children exhibiting this definition of catch-up to the rest of the sample (Table 6 )shows some results similar to the recovery from stunting model: having a taller mother, being firstborn, having fewer younger siblings and high initial household assets with improvements in assets during the interval each increased the likelihood of catch-up growth. In addition, the residual model shows an effect of improvements in assets even among those with lower initial assets (T = 1.89), as well as a significant effect of increased energy intake on the likelihood that a child would have a greater than expected growth rate from age 2 to 8.5 y. In contrast to the recovery from stunting model, birth characteristics (weight, length, prematurity and ponderal index) had no significant effects.

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

To study determinants of catch-up growth, we analyzed overall growth increments, recovery from stunting and greater than expected growth rates irrespective of attained size at the beginning of the interval under study. Results from these three different analyses were similar in most respects, but differed in the importance of birth characteristics as determinants of growth patterns in older children.

Catch-up growth represents an interaction of the child's biological growth potential with environmental factors that enhance growth, among which optimal nutrition and low morbidity are most prominent. The recovery from stunting models only analyze children whose poor linear growth left them stunted at age 2 y. Some of these stunted children, despite growth-retarding influences early in life (such as poor infant feeding and high morbidity), were able to catch-up later. The recovery from stunting model suggests that those who recovered had greater growth potential at birth, evidenced by taller maternal stature, higher birth length and low ponderal index. In later childhood, with improvements in socioeconomic conditions and diet, these children show catch-up in linear growth to more closely approximate their growth potential.

Other children appear to have more limited growth potential from birth onward. This lower growth potential is in evidence among full-term LBW infants, those with an adequate ponderal index (evidence of proportionate intrauterine growth restriction) and those with intergenerational or genetic effects represented by short maternal stature. When coupled with poor growth during the first 2 y of life, this results in the lowest likelihood of later catch-up growth. Mean HAZ scores of children stunted by age 2 y were significantly lower among those who were LBW compared to those with normal birth weight (-3.36 ± 0.92 vs -3.00 ± 0.73, ANOVA, P < 0.001). The absence of strong effects of prematurity may reflect the birth-weight distribution among surviving preterm infants, only 12 of whom weighed less than 2,000 g at birth. The combination of pre- and postnatal growth retardation is most likely the result of a continuum of adverse environmental factors from the prenatal period through infancy. In a previous analysis of determinants of stunting in the CLHNS sample, we found that low birth weight, lack of breast-feeding, early introduction of weaning foods and increased diarrheal morbidity increased the incidence of stunting in the first year of life (Adair and Guilkey 1997 ). These findings emphasize the importance of attention to maternal nutrition and health during pregnancy, and to optimal feeding and preventive health practices during infancy.

The lack of persistent effects of birth characteristics in the residual model most likely reflects the fact that this analysis characterizes catch-up growth without respect to stunting status. Birth characteristics may play a greater role in recovery from stunting, largely because they are so important as determinants of early stunting.

The CLHNS sample shows evidence of improvements in socioeconomic conditions over time. Mean household income levels rose (accounting for the effects of inflation), more households acquired electricity and piped water, and the average number of common assets increased. The effects of such improvements on child health are likely to operate through improved nutrition and decreased morbidity from infectious diseases. We assessed only one dimension of change in nutrition (energy intake), but found that between age 2 and 8.5 y, height increments were increased by bigger increases in dietary energy intake. The lack of a significant effect of increased energy intake on recovery from stunting or on height increments from age 8.5 to 12 y may reflect imprecise measurement of diet or the importance of other aspects of dietary quality or nutrient intake. Other measures of dietary quality were not taken into account in the present analysis. A weakness of the study is the lack of dietary and morbidity data during the intervals from ages 2 to 8.5 and 8.5 to 12 y.

In general, when socioeconomic status improves, children grow more. The stronger effect of assets vs. income in the 2–8.5 y interval likely represents the fact that assets are measured with less error than income. The effects of increased assets were restricted to households with higher initial assets in the recovery from stunting model, but in the residual model, acquisition of assets was a stronger determinant of higher than expected growth among households with lower initial assets. This suggests a possible threshold effect, with greater improvements needed for a child to recover from stunting.

The effect of birth order and younger siblings most likely represents competition for limited resources within the household. At all ages, first-born children have higher mean HAZ than children of higher birth order, and within CLHNS families, firstborns are taller and have higher IQ scores than their next younger sibling (Adair 1998 ). When household income and assets are held constant, having more siblings is likely to mean that each child gets less of the needed resources, including food, nurturing and health care. This result emphasizes the importance of family planning and reduced family size as a means to improve child growth.

Results from several intervention studies demonstrate the potential for catch-up growth in children, but also point to the importance of sustained intervention. Perez-Escamilla et al. (1994) found that supplementation, education and health care provided for a period of 9 mo benefits children irrespective of the age at which supplementation is initiated. However, they found that improvements in growth of Cali, Colombia, children were not sustained once the intervention ceased. Similarly, Walker et al. (1996) reported benefits of a 2-y nutrition supplementation program for stunted children, but found that children returned to their pre-supplementation trajectory when supplementation ceased. Like the CLHNS children, the Jamaican children studied by Walker et al. gained in height relative to the WHO reference, as shown by increasing HAZ scores. Results from the Cebu study suggest that more comprehensive, sustainable improvements in socioeconomic status may contribute to improved child growth.

The Cebu study leaves important questions unanswered about the ultimate effects of catch-up growth on adult height. Further follow-up of these children is necessary to document what happens during the adolescent growth spurt. It remains to be seen whether there will be further improvements in growth during adolescence. In other settings, researchers observed a prolonged growth spurt, resulting in a reduction of the adult height deficit (Cameron and Kgamphe 1993 ). This is possible since pubertal delay provides an opportunity for more catch-up growth prior to skeletal maturity. However, Martorell et al. (1994) expressed the concern that improvements in health and nutrition may result in earlier maturation and therefore limited potential for catch-up growth during adolescence.

There is evidence that maturation is delayed in Cebu sample girls relative to U.S. girls. Only 1.3% of Cebu 11-y-old girls, and 5.1% of 12-y-old girls reported menarche. In contrast, based on data from the U.S. National Longitudinal Survey of Adolescent Health, about 31% of 11-y-old girls and 63% of 12-y-old girls were postmenarchal. The HAZ scores of U.S. reference sample girls reflect this pattern of earlier maturation. The later maturing Cebu girls show a deviation in height, even from the WHO 10^th percentile at age 11 y. When we examine HAZ-scores by age using cross-sectional age-specific CLHNS 1994–95 data, we see lower HAZ scores in older girls. Among Cebu girls with earlier menarche, there is more apparent catch-up growth. Early menarche was a very strong determinant of greater than expected growth in height in the residual model. Further follow-up of these earlier maturing girls to determine final adult height will be of particular interest. The 1998–99 round of the CLHNS will provide further insights into the effects of maturation.

In summary, this community-based nonintervention study demonstrates a considerable degree of catch-up growth from age 2 y to later childhood in a cohort of Filipino children. The potential for catch-up growth is greatest among children with increased growth potential, marked by taller mothers, longer length and lower ponderal index at birth, and less severe stunting during early infancy. Children at greatest risk of long-term height deficits are LBW infants who are also severely stunted during infancy. The persistent effects on later childhood growth of birth characteristics and growth during infancy strongly support optimal maternal health and nutrition before and during pregnancy as well as optimal infant feeding and health-care practices. The demonstrated potential for catch-up growth in later childhood emphasizes the importance of sustained attention to the health and nutrition of the older child. Improvements in maternal education, family planning and income-earning opportunities are important social changes that would ultimately support this goal.

	ACKNOWLEDGMENTS

 
Funding for the collection and analysis of the CLHNS follow-up data was provided by the National Institutes of Health, The World Bank, The Asian Development Bank, Family Health International and the Thrasher Research Fund. This paper was presented at Experimental Biology 97. Adair, L. S. (1997) Filipino children exhibit catch-up growth between ages 2 and 11. FASEB J. 11: A574.

	FOOTNOTES

 
¹ Abbreviations used: CI, confidence interval; CLHNS, Cebu Longitudinal Health and Nutrition Survey; HAZ, height-for-age Z-score determined from the WHO growth reference; LBW, low birth weight, <2500 g.

Manuscript received September 7, 1998. Initial review completed December 3, 1998. Revision accepted February 23, 1999.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Adair L. S. Growth of Filipino infants who differ in body proportion at birth. Am. J. Human Biology 1989;1:673-682

2. Adair L. S. Sibling resemblance in height, fatness and IQ is affected by SES and environment (Abstract). FASEB J 1998;12:A344

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