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Small Birth Weight and Later Body Composition and Fat Distribution in Adolescents: The AVENA Study
Idoia Labayen1, Luis A. Moreno2, Jonatan R. Ruiz3,4, Marcela Gonzlez-Gross5, Julia Wrnberg4,6, Christina Breidenassel7, Francisco B. Ortega3,4, Ascensin Marcos6, Manuel Bueno8; The AVENA Study Group
Objective: To assess the association between birth weight and body composition and fat distribution in adolescents, and to test the possible sex-specific effect in these relationships. Methods and Procedures: A total of 1,223 adolescents 1318.5 years old (553 male adolescents and 670 female adolescents) born at >35 weeks, were selected from a cross-sectional multicenter study conducted in five Spanish cities in 20002002. BMI was calculated from weight and height. Triceps and subscapular skinfold thickness (ST) were measured on the left side, and fat mass (FM) and fat-free mass (FFM) were estimated according to the equations of Slaughter et al. Subscapular skinfold adjusted by tricipital (ST) and waist circumference were used as markers of central adiposity. Results: Birth weight Z-score was positively associated with FFM in female adolescents (P < 0.001), but not in male adolescents, after controlling for age, pubertal stage, gestational age, socioeconomic status, physical activity, and current height (P < 0.001 for interaction between adjusted birth weight Z-score and sex). Adjusted birth weight Z-score was inversely associated with central adiposity in male and female adolescents as measured by ST (P = 0.026). Discussion: These results provide further evidence that gender has an important influence on the programming effect of birth weight on later FFM in adolescents because the effect was only observed in female adolescents. Our results suggest that small size for gestational age at birth could program more central subcutaneous fat deposition in adolescents of both sexes, but further research is needed on this issue.
Obesity (2008) 16, 16801686. doi:10.1038/oby.2008.258

IntroductIon

The term programming has been used for many years to describe the process whereby a stimulus occurring during a critical period of development causes long-term consequences for the health of an individual (1,2). In the last 15 years, epidemiological findings and data from experimental studies in animals have shown that there is a relationship between the early environment in which a child, even a fetus, grows and subsequent development of adult degenerative diseases such as type 2 diabetes (3,4), cardiovascular disease (5), hypertension (6,7), and the metabolic syndrome (8,9). Fetal and neonatal life are critical periods for the development of the physiological and metabolic processes involved in the appearance of

the metabolic syndrome and obesity (1012). In this sense, numerous studies have observed associations between both low weight at birth/born small for gestational age and many adult diseases in humans (13,14). It is well established that central or visceral obesity is a major factor for the clustering of cardiovascular risk factors which defines the metabolic syndrome (hypertension, dyslipidemia, insulin resistance, impaired glucose tolerance, and/or increased waist circumference) (9). In this context, a range of epidemiological, clinical, and experimental studies have shown that there is a relationship between early nutritional environment, patterns of postnatal growth, and the amount and distribution of adipose tissue in adult life (15,16).

1 Department of Nutrition and Food Science, University of the Basque Country, Vitoria, Spain; 2University School of Health Sciences, University of Zaragoza, Zaragoza, Spain; 3Grupo EFFECTS-262, Department of Physiology, University of Granada, Granada, Spain; 4Unit for Preventive Nutrition, Department of Biosciences and Nutrition at NOVUM, Karolinska Institutet, Huddinge, Sweden; 5Faculty of Physical Activity and Sport Sciences, University Polytechnic of Madrid, Madrid, Spain; 6 Immunonutrition Research Group, Department of Metabolism and Nutrition, Spanish Council for Scientific Research (CSIC), Madrid, Spain; 7Department of Nutrition and Food Science, University of Bonn, Bonn, Germany; 8Department of Paediatrics, University of Zaragoza, Zaragoza, Spain. Correspondence: Idoia Labayen Goi (idoia.labayen@ehu.es)

Received 5 April 2007; accepted 29 October 2007; published online 8 May 2008. doi:10.1038/oby.2008.258

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A series of studies have shown that there is a J-shaped or U-shaped relationship between birth weight and adult BMI, with a higher prevalence of adult obesity occurring at both low and high birth weights (17). However, the association between birth weight and BMI contradicts considerably evidences that a high birth weight programs less susceptibility to cardiovascular disease risk factors (18). BMI is frequently used as a marker of obesity because it is widely available and is correlated with direct measures of adiposity. Nevertheless, BMI mainly reflects fat-free mass (FFM) and it is more difficult to interpret when the relative proportions of fat, muscle, bone, and organ mass are changing, e.g., during childhood and adolescence. Several recent studies supported one hypothesis that could explain this paradox: low birth size would increase the risk of cardiovascular disease by programming a truncal fat deposition and/or a small proportion of lean mass later in life (19,20). Fat distribution independently of fat mass (FM) and percentage of body fat also predicts the risk of cardiovascular disease and type 2 diabetes, and it is possible that early programming of body composition affects fat distribution. Several studies have been conducted on the relation between birth weight and later lean body mass, body FM, and body fat distribution (16,2124). They have shown positive associations between lean body mass and birth weight, whereas associations with adiposity and body fat distribution were more variable. Although both sexes are susceptible to programming stimuli during pregnancy, recent studies have provided important new insights identifying marked sex differences. The sex-specific association between birth weight and later blood pressure (25,26), glucose homeostasis (27), dyslipidemia (28), or the risk of developing hypertension or renal disease has been investigated in children, adolescents, and young adults. Sex differences have also been reported in animal studies (29,30). There are few studies examining the programming effect on body composition and fat distribution in adolescents, which is a critical period in the development of obesity. These studies were small and/or had limited ability to look at confounding factors and possible sex differences. The aim of this study was to examine the relation between birth weight, for a given gestational age, and FM, body fat percentage, and FFM. The relationships between birth weight and body fat distribution were also studied. In addition, we explored the hypothesis that the programming effect of birth weight on body composition and body fat distribution would have differential effects in male and female adolescents.
Methods And Procedures Subjects included in this analysis belonged to the AVENA (Alimentacin y Valoracin del Estado Nutricional en Adolescentes) Study population. The AVENA Study was designed to evaluate the nutritional status, dietary and leisure time habits, and physical activity and fitness of Spanish adolescents, in order to identify risk factors for chronic diseases in adulthood. The complete methodology of this multicenter cross-sectional survey from five Spanish cities (Santander, Granada, Murcia, Zaragoza, and Madrid) has been described previously (31,32). For the purpose of this analysis, we identified 1,223 healthy Caucasian adolescents whose data on birth weight, socioeconomic status, gestational age, physical activity, and anthropometric measurements were
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available. To be born at >35 weeks of gestation (94.2%) was an additional inclusion criterion. Written informed consent was obtained from parents or guardians and subjects, and the complete study protocol was approved by the Ethical Committee of the Hospital Universitario Marqus de Valdecilla (Santander).
socioeconomic status In accordance with the recommendations of the Spanish Society of Epidemiology, the socioeconomic status was assessed using the educational level and the type of occupation of the father. Taking into account this information, the adolescents were classified into five categories: low, medium-low, medium, medium-high, and high socioeconomic status (33). neonatal data Birth weight and gestational age at birth were obtained from health booklets records that are issued at birth and where childs pediatricians records birth weight, charts the infants growth, vaccinations, etc. Birth weight was expressed as the individual birth weight observations less the expected birth weight for each gestational age and sex, according to population-specific reference values described previously for this population (34). Gestational age was coded as 1 (from 35 to 40 weeks of gestation) or 2 (>40 weeks of gestation). Physical examination Trained anthropometrists performed all the measurements following the methods described below; one measured weight, height, and circumferences and the other one, skinfolds (35). Height (cm) was measured using a stadiometer to the nearest 0.1 cm (SECA, Vogel & Halke GmbH & CO. KG, Hamburg, Germany). Body weight was measured without shoes and with light clothing to the nearest 0.05 kg using a beam balance (SECA, Vogel & Halke GmbH & CO. KG, Hamburg, Germany). BMI was calculated as weight in kilograms divided by square of height in meters (kg/m2) and overweight and obesity percentages were calculated using the criteria proposed by Cole et al. (36). Waist circumference was measured horizontally midway between the lowest rib margin and the iliac crest, near the level of the umbilicus, at the end of gentle expiration, with an inelastic tape to the nearest 0.1 cm in triplicate and the mean value was obtained. Triceps and subscapular skinfold thickness (ST) were measured on the left side (37) in triplicate with the use of a skinfold caliper (Holtain, Crymych, UK) and the mean values were calculated (3840). Previously, we have reported the standardization process and reliability of anthropometric measures to assess body composition in this multicenter survey (35). Thus, for all the ST measurements, intraobserver technical errors of measurements were <1 mm, and reliability >95%. Interobserver reliability for ST ranged from 83.05% for biceps skinfold to 96.38% for calf skinfold. For waist circumference, intraobserver technical errors of measurements were <1 cm, and reliability >95%. Interobserver reliability for this measurement was >95%. ST measurements were used to estimate FM (and hence body fat percentage) using the equations of Slaughter et al. (41). This equation has been proposed as the most accurate for estimation of body fat percentage from ST in this particular population of adolescents (42). FFM (kg) was derived by subtracting FM from total body weight. The subscapular adjusted by triceps ST and waist circumference were used as markers of central adiposity (43,44). Pubertal status was classified according to the method of Tanner (45). Physical activity A physical activity index was calculated using four quantitative variables estimated by questionnaires, metabolic equivalents values of: (i) activities pointed out on the summer period questionnaires, (ii) daily physical activity for week days, and (iii) Saturday, and (iv) Sunday
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physical activities considering the academic course period. Using factorial analysis of principal components, it was identified a single factor with an autovalue >1 and which accounted for the 55.9% of the variance. Therefore, in order to establish higher validity to physical activity index calculation, the subjects answered to another questionnaire with the question about the practice of regular physical activity (yes or no). This last value was compared with physical activity index variable. The procedure for the physical activity index calculation has been reported in detail elsewhere (46).
statistical analysis Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) software 13.0 (SPSS, Chicago, IL). Physical characteristics of the study sample by sex are presented as means and s.d., unless otherwise stated. Variables with skewed distribution, i.e., body FM, subscapular and tricipital STs and waist circumference were log transformed to obtain a more symmetrical distribution. Regression analysis was used to assess associations between FFM, FM, or subcutaneous fat distribution and the Z-score for birth weight, when controlling for age, pubertal status, gestational age, socioeconomic status, and physical activity level. The regression analysis examining the association between subscapular ST and birth weight Z-score was additionally controlled for tricipital ST. Moreover, the analysis studying the association between waist circumference and birth weight Z-score were also additionally controlled for total FM. The Tanner stage categorical variable was transformed in four Dummy variables to perform the regression analysis. The association between birth weight Z-score and body composition was also adjusted for variation in body size by adjusting for height (47,48). We also tested the interaction effect between sex and birth weight Z-score. As evidence existed that the strength of the association between birth size and body composition measurements differed, then the results for males and females are presented separately. Some data regarding pubertal status interaction are shown in the Results section. results
table 1 characteristics of the subjects
Variable Age (years) Tanners puberty stage IIIa Tanners puberty stage IIIIVa Tanners puberty stage Va Birth weight (kg) (Z-score) Weight (kg) Height (cm) BMI (kg/m2) Waist circumference (cm) Triceps SFT (mm) Subscapular SFT (mm) Body compositionb Fat-free mass (kg) Fat mass (kg) Body fat percentage (%) 50.2 7.93 13.1 9.38 19.4 9.95 41.6 4.63 14.6 5.87 25.2 5.93 <0.001 <0.001 <0.001 3.45 0.535 0.08 0.544 63.3 12.76 170.6 8.52 21.7 3.63 76.4 9.14 12.4 6.15 11.5 6.30 3.31 0.506 0.06 0.504 56.3 9.19 161.8 6.10 21.5 3.20 70.9 7.66 16.8 5.31 13.1 5.24 <0.001 <0.001 <0.001 <0.001 0.3621 <0.001 <0.001 <0.001 Males (n = 553) 15.1 1.26 30 (5.4%) 268 (48.5%) 255 (46.1%) Females (n = 670) 15.3 1.35 4 (0.6%) 398 (59.4%) 268 (40%) P 0.076

The descriptive data, anthropometric variables, and body composition measurements of the 1,223 study subjects are shown in Table 1. The mean birth weight in males (3.45 0.535 kg) was higher (P < 0.001) than in females (3.31 0.506 kg). There were no sex-related statistically significant differences in the socioeconomic status; the percentage of subjects distribution in the five socioeconomic status levels considered in males and females, respectively were as follows: 6.5% vs. 6.4% low, 25.7% vs. 23.1% low-medium, 32.4% vs. 38.7% medium, 26.0% vs. 26.0% medium-high and 9.4% vs. 5.8% at high level. The physical activity level was greater (P < 0.001) in males (0.32 0.05) than in females (0.26 0.03). In boys, overweight and obesity percentages (18.6 and 6.5%, respectively) were higher, (P = 0.001), than in girls (overweight 15.7% and obesity 2.7%). The relationships between birth weight and anthropometric and body composition measures in male and female adolescents are shown in Tables 2 and 3 (unadjusted and adjusted models, respectively). The relationship between birth weight Z-score and FFM strongly differed between the two sexes. FFM was significantly associated with birth weight Z-score in the unadjusted model among both males and females (P = 0.001 and P < 0.001, respectively), but this association remained significant after adjustment for several potential confounding factors
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All values are mean s.d., unless otherwise indicated. SFT, skinfold thickness. a Values are n and sample percentage. bCalculated from skinfold thickness measurements.

only in females (Table 3). There was a significant interaction effect of puberty stage on the relationship between birth weight Z-score and later FFM (P < 0.001). Indeed, this relationship was not significant at the stages II and III, and became significant in the stages IV (B = 2.248; P < 0.001) and V (B = 3.810; P < 0.001). In males, the relationship between birth weight Z-score and FFM was diminished after controlling for the potential cofounders and became not significant (Table 3). There were no statistical differences in the strength of this relationship among all puberty maturation stages. There was no evidence that the associations between birth weight and FM differed between the sexes (Table 2). Body FM was positively correlated with birth weight Z-score in the unadjusted regression model in both sexes (P < 0.001) and this association persisted after controlling for age, pubertal status, socioeconomic status, gestational age, physical activity, and height among both males and females (P = 0.001). The association between birth weight Z-score and subsequent body fat percentage differed between males and females (Table 2). This relationship was only significant in males in the unadjusted model (P = 0.018), which was strengthened after controlling for age, pubertal status, socioeconomic status, gestational age, physical activity, and current height (P = 0.001) (Table 3).
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table 2 unstandarized regression coefficients (B) and s.e. showing the association between birth weight Z-score and body composition variables in males and females adolescents
All adolescents (n = 1,223) Variable Weight (kg) Height (cm) BMI (kg/m )
2

Males (n = 553) B 2.527 2.527 2.004 1.838 2.786 s.e. 0.658 0.658 0.615 0.775 0.705 P <0.001 <0.001 0.001 0.018 <0.001 B

Females (n = 670) s.e. 0.688 0.455 0.343 0.454 0.584 P <0.001 <0.001 <0.001 0.105 0.004 3.942 2.793 2.378 0.737 1.692

Interaction between birth weight and sex P <0.001 <0.001 0.361 <0.001 0.542 <0.001 <0.001 0.153

B 3.969 3.678 0.728 3.125 1.547 0.550 2.864 0.012

a

s.e. 0.986 0.609 0.449 0.404 0.415 0.462 0.471 0.009

P <0.001 <0.001 <0.001 <0.001 <0.001 0.234 <0.001 0.206

Fat-free mass (kg) Fat mass (kg) % Body fat Waist circumference (cm) Subscapular SFT (mm)
a

Birth weight Z-score controlling also for tricipital SFT. SFT, skinfold thickness.

table 3 unstandarized regression coefficients (B) and s.e. showing the association between birth weight Z-score and body composition variables in males and females adolescents after controlling for age, pubertal stage, socioeconomic status, gestational age, physical activity, and height
All adolescents (n = 1,223) Variable Fat-free mass (kg) Fat mass (kg) %Body fat Waist circumference (cm) Subscapular SFT (mm)a
a

Males (n = 553) P B 0.538 2.561 2.023 s.e. 0.642 0.800 0.737 P 0.402 0.001 0.006

Females (n = 670) B 1.432 0.650 0.840 s.e. 0.360 0.468 0.604 P <0001 0.165 0.165

Interaction between adjusted birth weight and sex P <0.001 0.475 <0.001 <0.001 0.144

B 0.474 1.487 1.587 1.421 0.022

s.e. 0.431 0.433 0.479 0.496 0.010

0.272 0.001 0.001 0.004 0.026

Birth weight Z-score controlling also for tricipital skinfold thickness. SFT, skinfold thickness.

There was no evidence that the associations between birth weight and subcutaneous fat distribution as estimated by ST differed between males and females (P = 0.153 for interaction between birth weight and sex). When the influence of birth weight on fat distribution was tested, the results showed that birth weight Z-score was not significantly associated with subscapular ST when controlling for tricipital skinfold (B = 0.012; P = 0.206). This relationship turned to be statistically significant after controlling for age, pubertal status, socioeconomic status, gestational age, physical activity, and current height (B = 0.022; P = 0.026). The association of birth weight Z-score with waist circumference was positive and statistically significant in both sexes (P < 0.001 in males and P = 0.004 in females) in the unadjusted model and it remained significant only in males when adjusting with potential confounders (Table 3). However, this relationship disappeared in both sexes when FM was included in the regression model (B = 0.299, P = 0.689; and B = 0.153, P = 0.801; in males and females, respectively).
dIscussIon

In this study, we showed that a greater birth weight Z-score was associated with a higher FFM in females but not in males, which confirms the sex-related differences in the programming effect on body composition. In addition, the results suggest that
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small size for gestational age at birth could program more subcutaneous central fat deposition in adolescents of both sexes. Before adjustment, birth weight Z-score was significantly and positively related to later body size measurements (weight, height, and BMI) in accordance with the results of previous studies in children, adolescents and adults. Moreover, unadjusted birth weight Z-score was significantly associated with both FM and FFM among males and females (Table 2). However, in males the relationship between birth weight and FFM turned not to be significant after controlling for possible confounding factors including current body height. Our data suggest that the associations found with BMI may not adequately reflect the many effects of influences on different body compartments. This provides further evidence indicating that a high birth weight may programs higher FFM rather than simply predisposing to greater body size in a sex-specific manner. The literature relating birth size to subsequent body FM is not consistent. The results of several studies performed in children (49), young adults (50), and older adults (21,51), have indicated that after controlling for a range of confounders, including measures of current body size, decreases in birth weight were not associated with increases in FM. Our findings are in agreement with the study performed by Rogers et al. (52). They have shown that increased weight or ponderal index at birth
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resulted in increased adiposity at 910 years measured using dual-energy X-ray absorptiometry in a large sample of 3,006 boys and 3,080 girls. The programming of less lean mass by suboptimal fetal growth has been observed in previous published reports in which body composition measurements were obtained using dualenergy X-ray absorptiometry (21,22), anthropometric methods (51,53), or bioelectrical impedance (20). Unfortunately, the influence of sex on the relationship between size at birth and later body composition has not been examined in detail because of the small number of subjects. To the best of our knowledge, our study is the only one performed in adolescents with an adequate sample size for the ability to look at confounding factors and possible sex differences. We have previously reported a sex-specific effect of birth weight Z-score on lean body mass and bone mass measured using dual-energy X-ray absorptiometry independent of height in a more reduced group of female, but not male, adolescents (54). Recently published results of a large study performed in children showed that the relationship between both length and ponderal index at birth with lean body mass differed between the sexes, being these associations stronger in girls after adjustment for stage of puberty (52). Our findings are in agreement with other observations published in the literature, in which the adjustment for stage of puberty had a major effect on many of the observations (55). Sex-specific programming, only observed in females, has also been reported for blood pressure (25), insulin action (56), and pulse pressure (26) either in human or in animal studies (30), but the reasons for the differences between male and female subjects remain unexplained. It is not possible from data of these studies to determine whether the association of birth weight with FFM in females reflects neither an association with muscle, bone, organ mass, nor a combination of all three. However, some epidemiological studies have confirmed that both bone and muscle growth may be programmed by genetic and/or environmental influences during intrauterine life (18,51,57). The results of this investigation showed several interesting results concerning birth weight association with central body fat distribution in adolescents. Birth weight Z-score after controlling for potential confounders, was inversely associated with a more truncal subcutaneous body fat distribution in both males and females, as showed by the subscapular adjusted by tricipital skinfold. These findings are consistent with previous studies in which low birth weight was found to be associated with a more central fat distribution as measured using the same anthropometric methods in children (23,58), adolescents (59), and adults (16,60). However, although these STs ratios have been widely used as indices of central adiposity, they have several limitations and their interpretation can be problematic (44). Both nuclear magnetic resonance and computed tomography are the reference methods to the assessment of central body fat and visceral FM. Nevertheless, as these methods are costly and the techniques used expose the subjects to ionizing radiation, for the studies that involve large numbers of subjects, skinfolds and waist circumference have been proposed
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as reliable alternatives for the measurement of total and distribution of FM (43,61). Our results are in agreement with several reports showing an inverse association between birth weight and central fat deposition in children (24), adolescents (62), and adults (63) as measured using dual-energy X-ray absorptiometry. However, the results concerning the relationship between birth weight and waist circumference seem to be contradictories. Therefore, in our study, birth weight was associated with an increased waist circumference in both the unadjusted and adjusted models, but this relationship disappeared when controlling for total FM. One possible explanation could be that the subscapular adjusted by the triceps skinfolds and waist circumference might reflect different aspects of body fat distribution. Further research with more direct measurements of central fat is needed on this issue to be certain about the association between low birth weight and central fat deposition. In conclusion, the programming effect of low birth body size on FFM is sex-specific, observed only in females, and in the presence of high-energy diets could predispose these children to an unhealthy body composition in adult life. In addition, this study suggests that a low birth weight, for a given gestational age, could be independently associated with a higher subcutaneous truncal fat distribution in the studied male and female adolescents. These observations could have important implications in the adult life, as increased central fat deposition is associated with insulin resistance and an increased risk of cardiovascular diseases.
AcknowledgMents
Sources of financial support: the AVENA-Study was supported by the Spanish Ministry of Health (FIS 00/0015), and grants from Panrico S.A., Madaus S.A. and Procter and Gamble S.A. J.R.R. and F.B.O. were supported by CSD grants (109/UPB31/03; 13/UPB20/04) and Spanish Ministry of Education grants (AP2003-2128; AP-2004-2745).

AvenA study grouP

Coordinator A. Marcos, Madrid. Local coordinators M.J. Castillo, Granada. A. Marcos, Madrid. S. Zamora, Murcia. M. Garca Fuentes, Santander. M. Bueno, Zaragoza, Spain. Granada: M.J. Castillo, M.D. Cano, R. Sola (Biochemistry); A. Gutirrez, J.L. Mesa, J. Ruiz (Physical fitness); M. Delgado, P. Tercedor, P. Chilln (Physical activity), M. Martn, F. Carreo, F. Ortega, G.V. Rodrguez, R. Castillo, F. Arellano (Collaborators). Universidad de Granada, E-18071 Granada. Madrid: A. Marcos, M. Gonzlez-Gross, J. Wrnberg, S. Medina, F. Snchez Muniz, E. Nova, A. Montero, B. de la Rosa, S. Gmez, S. Samartn, J. Romeo, R. lvarez, (Coordination, immunology) A. lvarez (Cytometric analysis) L. Barrios (Statistical analysis) A. Leyva, B. Pay (Psychological assessment). L. Martnez, E. Ramos, R. Ortiz, A. Urzanqui (Collaborators). Instituto de Nutricin y Bromatologa, Consejo Superior de Investigaciones Cientficas (CSIC). E-28040 Madrid. Murcia: S. Zamora, M. Garaulet, F. Prez-Llamas, J.C. Baraza, J.F. Marn, F. Prez de Heredia, M.A. Fernndez, C. Gonzlez, R. Garca, C. Torralba, E. Donat, E. Morales, M.D. Garca, J.A. Martnez, J.J. Hernndez, A. Asensio, F.J. Plaza, M.J. Lpez (Diet analysis). Dpto. Fisiologa, Universidad de Murcia, E-30100 Murcia. Santander: M. Garca Fuentes, D. Gonzlez-Lamuo, P. de Rufino, R. Prez-Prieto, D. Fernndez, T. Amigo (Genetic study). Dpto. Pediatra, Universidad de Cantabria, E-19003 Santander.
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The authors declared no conflict of interest.
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