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International Journal of Epidemiology 2008 37(4):902-910; doi:10.1093/ije/dyn133
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Published by Oxford University Press on behalf of the International Epidemiological Association © The Author 2008; all rights reserved.

Association of perinatal factors and obesity in 6- to 8-year-old Chilean children

Francisco Mardones1,*, Luis Villarroel1, Lorena Karzulovic1, Salesa Barja2, Pilar Arnaiz2, Marcela Taibo3 and Francisco Mardones-Restat1

1 Public Health Department, Faculty of Medicine, Pontificia Universidad Católica de Chile, Chile.
2 Pediatrics Department, Faculty of Medicine, Pontificia Universidad Católica de Chile, Chile.
3 National Association for School Assistance (Junta Nacional de Auxilio Escolar y Becas), Ministry of Education, Chile.

* Corresponding author. Marcoleta 434, Postal Code (Código Postal) 833-0073, Santiago, Chile. E-mail: mardones{at}med.puc.cl


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Background It has been reported in Chile that obesity figures in children of 6- to 8-years-old are associated with height for age. We studied the possible influence of perinatal variables on obesity at 6- to 8-years-old controlling for height for age.

Methods All children with 6–8 years of age attending first grade in public primary schools of Chile in year 2005 were included. An historical cohort design was used and perinatal information collected at birth was obtained from the National Registry. Obesity was defined as BMI ≥95th percentile of the CDC reference. Comparisons of obesity prevalence in contingency tables used the chi-squared test. Logistic regression was used to calculate ORs for obesity risk in univariate and multivariate categorical models.

Results Out of 167 494 initial subjects, 153 536 children entered the study. Obesity prevalence was higher in stunted and in tall for age children (20.1 and 26.0%, respectively) compared with those with normal height for age (17.3%) (P < 0.0001). Adjusted odds ratio for perinatal information showed that infants born male, premature and short in length at birth were more prone to obesity than their counterparts. However, birth weight (BW) had a stronger positive influence on obesity risk.

Conclusions Taller and stunted children had higher obesity risk than normal height for age children. This association did not change when controlling for the influence of perinatal data; post-natal influences may be playing an independent role. Although BW was linearly associated with obesity, short and premature babies also had a higher risk of obesity.


Keywords Obesity, children, newborns, cohort study

Accepted 29 May 2008


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
In the past decades obesity has become the leading nutritional concern worldwide. This poses such a threat to public health that the World Health Organization (WHO) has described obesity as a global epidemic.1 An estimated 10% of the world's school-aged children are overweight, and a quarter of these are obese.2

In Chile, this nutrition transition has taken place at a unique rate. In two decades undernutrition has practically disappeared, leaving instead high obesity figures in all age-groups.3 Obesity prevalence in the Chilean adult population was surveyed in year 2003 reaching 23.2% at the national level.4 Chilean children attending first grade primary education in public schools have increased the obesity prevalence estimated with CDC standards from 17% in year 2001 to 19.4% in year 2006.5

Obesity in children entails many health problems during their childhood, such as dyslipidemia, glucose metabolism disorders, hypertension, psychosocial difficulties, eating disorders, orthopaedic problems; among others.6 It also puts them at risk in adulthood. Many studies show that children who are obese tend to be obese when becoming adults, being a major cardiovascular disease risk factor.7,8

Obesity results from a positive energy balance that can be due to increased caloric intake or reduced physical activity, or most commonly both. Also, there is growing evidence for an early origin of chronic adult diseases such as obesity, diabetes and cardiovascular disease.9 Recent reviews have commented that early programming of obesity and cardiovascular disease have been observed mainly in offspring subject to malnutrition during early stages of gestation and which presented early catch-up growth.10 Studies of Finnish children at cardiovascular risk when adults have shown that they had a reduced foetal growth and gained weight rapidly after birth; however, they did not grow in length as fast, being at risk of obesity because of a rapid increase in their body mass index (BMI).11 These possible associations have not been widely studied in different settings, for example in Chile.

Studies in Chilean school-age children have shown that stunted and tall for age children are at greater risk of obesity than normal height for age children;12 it is not known in this population if obesity risk is influenced by early growth.

This study aims to report the influence of perinatal variables on obesity risk at 6–8 years of age in Chilean school-age children when controlling for the association of height for age.

We hypothesize that perinatal variables and growth patterns after birth modify the risk for future obesity. In agreement with the developmental origins of health and disease concept, we expect that infants showing intrauterine or post-natal conditions, reflected by variables such as low or high birth weight, prematurity, short length at birth and poor growth in height during childhood, would present higher obesity prevalence at ages 6–8.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Study design and population
Obesity figures at 6- to 8-years-old according to birth data are reported in this historical cohort study. Information at birth for every child was obtained by anonymously linking present files and birth files using the individual identification number; this number serves as the official identification for all purposes during the whole life span. This number was not used in this study either in printed material or any other purpose than the anonymous linking. The study was approved by the Ethical Committee of the School of Medicine, Pontificia Universidad Católica de Chile.

Cross-sectional data from all children attending public schools from Chile and entering first grade in year 2005 were analysed by weight and height using the Annual School Survey collected by the Ministry of Education. The teacher in charge assessed weight and height of the children at the beginning of year 2005.12 Teachers were instructed on how to measure weight and height in a standardized manner with light clothes and without shoes. Weight was recorded to the nearest 0.1 kg and height to the nearest 0.1 cm.

The study obtained perinatal data on all live births born 6–8 years before 2005. The National Registry records the birth files and delivers them to the Statistics Unit of the Ministry of Health where they were obtained.13 Around 250 000 newborns were registered every year using the individual identification number recorded in the birth certificates. Birth weight (BW) and birth length (BL) are determined at maternity hospitals immediately after delivery by trained personnel and standard procedure.14 BW was measured using beam scales accurate to 10 or 20 g. Crown-heel length was measured on a custom-made neonatometer. Gestational age (GA) is estimated by the date of the last menstrual period and for uncertain dates an early ultrasound test allows for correction.15 Ultrasound is available for all pregnant women before 20 weeks of gestation in Chile; when the latter is not performed due to a late pregnancy check-up, a post-natal clinical examination of the newborn done by the physician in charge in the maternity hospital is used to estimate GA at birth.

Chile has instituted various policies and practices that all but eliminated non-registration of live births and infant deaths. For example, in year 2000 99.8% of all live births had deliveries attended by professionals and 99.0% took place in maternity hospitals.15 All public and private hospitals in Chile are required to file a delivery certificate. Death certificates endorsed by medical doctors are also legally required. Both delivery and death certificates must be registered with the Civil Registry Service, generally located within maternity hospitals, thus facilitating immediate registration of births and deaths. In addition, recording of births is encouraged by the monetary and social incentives of the social security system, and registration of death is required before internment of the body. Chile has been reported as having the lowest under registration rate for all deaths in Latin America.16 Thus, the number of unregistered births and deaths is likely to be very small or non-existent.

Only children and live births with complete information on identification number, sex, BW, BL, GA and weight and height at 6- to 8-years-old were included in the study. The validation process at birth and at 6–8 years excluded cases with weight and height measurements outside ± 3 SD of the population values. The initial total population of children for year 2005 reached 167 494 subjects.

Variables
In order to examine our hypothesis, we selected perinatal and post-natal variables that reflect growth and development during early life. Not only BW but other early life events should be considered.17 From the available information we selected BW, BL and GA to represent foetal development, and height at 6–8 years to represent post-natal development. Sex was included as all these variables show a different behaviour according to this factor.

BMI and height for age specific cut-offs by sex and by age of the CDC reference were used to classify each 6- to 8-years-old child nutritional status.18 Obesity was defined as BMI ≥95th percentile and wasting as BMI <5th percentile. Stuntedness was defined as height for age <5th percentile and tallness as height for age >95th percentile.

Maternal years of education, as registered at birth, have been widely used in Chile as a proxy for socio-economic status.19 This variable was included in this study as a possible confounder.

Statistical analysis
SPSS version 15.0 was used for statistical analysis. Student's t-tests for independent samples and chi-square tests were used to calculate the P-values of the differences between means, respectively. Odds ratios (OR) with 95% CI were calculated to estimate obesity risks using multiple logistic regression after adjustment for sex, GA, BW, BL, education and height for age at 6–8 years age. The test for collinearity used was the variance inflation factor.20


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
Children 6–8 years of age at 2005 and their corresponding live births that had complete information on the required variables were 153, 536 subjects. Excluded cases were those with ages out of range and/or no birth date information (4.6% from the total of 167 494), with height and weight measurements outside ± 3 SD (1.3%) and also those children lacking any perinatal variable (0.9%) or either weight or height at 6–8 years (1.5%). In this population males were 51.32%. Table 1 shows mean values of other included variables for all the children entering the study.


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Table 1 Mean ± SD of study variables from 153 536 children attending first grade of public primary education (Chile, 2005)

 
Obesity prevalence reached 17.9%. Other indicators of nutritional status for children 6–8 years had the following prevalence: 5.2% for wasting; 6.4% for stuntedness and 5.7% for tallness.

BW, BL, GA, height, weight and BMI at 6- to 8-years-old, and education, were all correlated with each other to varying degrees (Table 2); many of the associations were positive (P < 0.0001). Weight at 6–8 years was correlated with BW and BL to an almost equal degree. Height at 6–8 years was positively correlated with BW and BL but the latter was slightly larger than the former. As expected, BMI at 6–8 years had a high r-value when correlated to present weight but all other associations had a rather low correlation coefficient. Interestingly, education had very weak associations with all other variables.


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Table 2 Matrix of bivariate correlation coefficients of independent variables for 153 536 children attending first grade of public primary education (Chile, 2005)

 
Table 3 presents obesity figures according to categories of the study variables. Obesity prevalence was higher for males and increased with higher BW and BL. GA at birth showed similar values between categories. Stunted and tall for age children of 6–8 years have a higher obesity risk than normal height for age children; the former being lower than the latter.


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Table 3 Obesity prevalence at 6–8 years of age according to categories of study variables: 153 536 children attending first grade of public primary education (Chile, 2005)

 
BW, BL and GA were plotted against obesity and a linear association was apparent in the three cases.

Table 4 shows non-adjusted and adjusted ORs for obesity risk. Non-adjusted ORs in model 1 maintained a similar trend among the categories of each variable than the results observed for obesity prevalence: it was lower for girls and ORs increased with higher BW or BL.


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Table 4 Relation of perinatal variables and height for age at 6–8 years to obesity risk

 
Other models presented in Table 4 progressively included a higher number of variables for obesity risk. Model 2 which included adjustments for sex and BL had similar ORs than model 1. The inclusion of adjustment for GA in model 3 showed a preventive effect for term deliveries. Model 4, which included adjustment for BW, resulted in a higher preventive effect for term deliveries and also in a new inverse association of BL for obesity risk. On the other hand, ORs for BW categories in model 4 continued to be positively associated but stronger than OR values in model 1. Model 5, that included adjustment for height for age at 6–8 years categories, showed similar ORs for height for age at 6–8 years categories as model 1, and also resulted in similar obesity risks for sex, BL, GA and BW as in model 4. Findings described above were also observed in another non-presented logistic regression model that included just continuous independent variables. In that model there was no evidence of collinearity; the variance inflation factor values ranged between 1 and 3.20


    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
This study examined early life conditions that may predispose to obesity. The main results of this study showed that indicators of perinatal growth (BW, BL and GA) had a strong association with obesity risk: the strongest association was positive and for BW meanwhile BL and GA had an inverse association. In addition, the indicator of post-natal growth (height for age) maintained a U-shaped effect that was present before adjusting for the effect of the indicators of perinatal growth. What about after adjustment?

The data reported in this historical cohort study are based on Chilean registers of first graders in public primary education and their corresponding live birth registers. Obesity prevalence in this study was similar to the figure reported by the Chilean Association for School Assistance of the Ministry of Education for first graders in 2005.5 Mean values of perinatal variables presented in Table 1 were also similar to those presented in recent reports of national figures.15,21

Excluded cases in this historical cohort study were 8.3% and were mostly due to out of range information in school-age children files (4.6%), similarly to a previous report on the Chilean school-age children files.12 The excluded cases that lacked information on weight and height or had height and weight measurements outside ± 3 SD were 2.8%, a figure that is slightly lower than another national report that used data from previous years.12 Just 0.9% of the total subjects lacked information on perinatal variables; this very low observed proportion is also congruent with another national report.15

There might be errors in weight and height values determined at 6–8 years of age due to the fact that teachers in charge only practise this kind of determination once year. In addition, the scales and stadiometers that are available at the more than 9000 schools around the country are not always well-calibrated. However, the very large size of the study and the precaution of eliminating height and weight measurements outside ± 3 SD may have kept some of the possible positive and negative errors cancelled out or at a very low level. Moreover, mean height and weight at 6–8 years found in this study closely approximate to those mean values for boys and girls of the CDC standard.18

Although there were eight cases weighing ≤13 kg, value below the 5th percentile of the weight/age CDC standard (Table 1),18 their height values were accordingly short and their BMI values were also close to the 5th percentile of the BMI/age CDC standard.18

Measurement errors of perinatal variables are considered negligible because health professionals are regularly in charge of this kind of determinations using well-standardized procedures and instruments.15,21

The use of the CDC standard seems justified in the Chilean setting by arguments that are presented ahead. Mean height and weight at 6–8 years found in this study closely approximate to those mean values for boys and girls of the CDC standard.18 That standard in turn seems to measure an intermediate prevalence of obesity at 6- to 8-years-old as compared with other standards.22 In that recent publication, quite close values of obesity prevalence were ascertained by the new International standard23 and by the 1994 NCHS growth chart from the USA.24

Obesity prevalence and obesity risk in 6–8 years females were consistently lower than in males in univariate and multivariate models; this observation was in agreement with already reported information of primary public schools in Chile for previous years.12 The observed association with height for age was also quite similar to models already reported.12

Obesity risk at 6–8 years was inversely associated with GA, for a given BL and a given BW. Children of 6–8 years who were born at term (38–42 weeks) had a reduced obesity risk when compared with those born preterm (≤37 weeks). There have been some recent reports of an increased risk of obesity for preterm infants.25 Studies have also looked at body composition in preterm infants later in life and have found increased measures of central adiposity that are associated with obesity and the metabolic syndrome.25–28 Other studies have shown inverse associations of GA with blood pressure and/or insulin resistance at different ages.29–32 For example, a recent study has found that adults who were born moderately preterm have increased blood pressure and insulin resistance at 30 years of age.29 The authors stated that as the proportion of preterm births is increasing, and increasing numbers of preterm infants are now surviving into adulthood, it is likely that those survivors will contribute an increasing proportion of the overall burden of cardiovascular disease in developed countries. The proportion of preterm births and their survival are also increasing in Chile.15,33

Obesity risk was also inversely associated with BL for a given BW to a similar degree as GA. As discussed by Leon et al., the pattern of linear bone growth is different from that of weight.30,34,35 Average BL at 35 weeks gestation in Chilean newborns is over 90% of length at 40 weeks, in contrast to BW, which at this stage is only 69% of weight at 40 weeks.21 BL is thus going to be less affected by impaired foetal nutrition in late gestation than is BW.30 Therefore, short BL seems to be related to a short GA but still maintained an independent inverse effect on obesity risk in this study. Of the various studies of the possible effect of BL on obesity risk during childhood or adulthood, none have reached the strength of the association observed in this study, most likely because the sample size was not big enough for the rather small obesity prevalence in the studied populations.36–38 An inverse association of BL with risk of type 2 diabetes has been observed in 7-year-old children; this risk was increased by high growth rates after 7 years of age;39 another study has confirmed this association in children of 8 years of age.40

Poor foetal growth, estimated by BW, was associated with a lower obesity risk; at each positive change in BW of 500 g the OR for obesity progressively increased at the following rates: 25, 34, 43 and 57%. Similar results were found in two recent studies of Brazilian children.41,42 In our study, adjustments for other perinatal variables increased the strength of this association, an observation that was also seen in a Danish study.36 Therefore, it seems from the most recent studies in Latin America that obesity risk in children is to some extent determined by or shares determinants with BW. Previous studies showed also mostly positive associations between BW and BMI, which in turn is associated with a higher prevalence of chronic diseases, especially cardiovascular and type-2 diabetes.9,33 Following a study published in 1992,33 very recent studies have consistently shown an inverse association between BW and central obesity in children, adolescents and adults.43–45 Unfortunately, we did not perform fat distribution measures in our study.43 As recently concluded by Oken and Gillman,46 there is a seeming paradox of increased adiposity at both ends of the BW spectrum: higher BMI with higher BW and increased central obesity with lower BW; the combination of lower BW and higher attained BMI is most strongly associated with later disease risk.46

Adjustments performed using perinatal variables showed that the direction of GA and BL effects on obesity risk changed, especially after adjusting for BW.

The reversals in coefficients in Table 4 indicates that being long at birth is positively associated with subsequent BMI, while being long at birth for a given BW is negatively associated with later BMI. Similarly, being born at term is positively associated with subsequent BMI, while being born at term for a given BW is negatively associated with later BMI.

No further changes were apparent for obesity risks adjusted for BW, BL, sex, GA, education and height for age were done. Because adjustments for later stature at 6–8 years are equivalent to a measure of the effect of post-natal growth,47,48 this indicates that there is a specific effect of the four studied perinatal factors on obesity risk, which is still very important at 6–8 years of age. In addition, there is an independent effect of post-natal growth on obesity risk. A similar view has been recently included in the analysis of the association between size at birth and blood pressure in early adolescence.49

BL was protective against obesity because most probably from birth on body composition was highly influenced by non-fat mass rather than fat mass, as can be expected from a higher linear growth during gestation.

Post-natal linear growth had a U-shaped association with obesity, implying that there is a protective effect for normal height for age 6- to 8-year-old children compared with stunted cases. Although various studies have suggested that stunted children have a higher obesity risk than their normal counterparts, their results are inconclusive.50 Our results confirm the importance of post-natal growth effects on obesity risk.51 Tall for age children had a higher obesity risk than children with normal height for age. There may be at least two possible explanations for this association. First, due to their higher linear growth, implicating higher bone and muscle mass, some of the tall for age cases may have had a higher non-fat mass that may explain the higher BMI diagnosed as obesity.52 Second, excess of fat mass raises insulin levels53 and insulin and other growth factors induce intense anabolism contributing to growth in infancy and childhood possibly leading to a higher linear growth.54 More research on growth curves, hormones, growth factors and body composition is needed.

Mean maternal education in this study reached 9.7 years, almost two more years than previously published data from a similar population of women performed 20 years ago.55 This improvement in the number of education reveals a positive impact of the educational programmes. Nevertheless, education was not correlated with BW (Table 2), possibly due to the fact that the higher income population is not included in this study design. Maternal education was positively associated with obesity risk. This association did not change after adjusting for the other study variables.

We did not adjust for other potential confounders that may be relevant for obesity risk such as parental weight.56 This factor may be important in the Chilean setting where the obesity epidemic began specially for the adult population in the 1980s3 and at the end of the 1990s the parents of these children began to procreate. Another important factor is gestational diabetes that is highly associated with obesity during pregnancy;56 obesity during pregnancy has importantly increased in the last two decades57 and so has diabetes prevalence, which is increasing in all age-groups, including in women of childbearing age.58

A general conclusion of this study is that both pre- and post-natal preventive measures are needed when dealing with the obesity epidemics in the Chilean setting. Attributable risk calculations for any of the perinatal variables and for post-natal growth seem to need fat distribution studies, as well as adequacy of BW for GA.59 Knowledge on individual central adiposity is needed given the above mentioned influences of BW and attained BMI, allowing for the effect of height at any age.


    Acknowledgements
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
We gratefully acknowledge both the Chilean Association for School Assistance of the Ministry of Education, and the Statistics Unit of the Chilean Ministry of Health, for providing us the national files that were analysed in this study. This study did not have support from external sources.

Conflict of interest: None declared


    References
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Acknowledgements
 References
 
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