PEDIATRIC ORIGINAL ARTICLE

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1 PEDIATRIC ORIGINAL ARTICLE Macrosomia is associated with high weight-for-height in children aged 1 3 years in Shanghai, China ZYu 1, JQ Sun 2, JD Haas 3,YGu 4,ZLi 4 and X Lin 1 1 Institute for Nutritional Sciences, Shanghai Institutes for Biologic Sciences, Chinese Academy of Sciences, Shanghai, P.R. China; 2 Department of Nutrition, Huadong Hospital, Shanghai, P.R. China; 3 Division of Nutritional Sciences, Cornell University, Ithaca, NY, USA and 4 Huangpu Hospital on Women s and Children s Health, Shanghai, P.R. China Objective: To investigate the association between macrosomia and high weight-for-length/height in 1 3 years old Chinese infants. Design: A retrospective longitudinal study. Subjects: 918 children aged 1 3 years in Shanghai, China. Measurements: Body weight and length/height, illness status and feeding modalities were obtained during follow-up. Macrosomia was defined as birth weight X90th percentile of sex specific birth weight distribution. High weight-for-length/ height was defined as a weight-for-length/height z-score X1.68 using the WHO growth reference. Results: The odds ratios (ORs) for high weight-for-length/height were 3.60 (95% confidence interval (CI), ) for boys and 1.39 (95% CI, ) for girls who were macrosomic compared with the nonmacrosomic counterparts after adjustment for age. The ORs were attenuated to 3.48 (95% CI, ) for boys and were still nonsignificant for girls (OR, 1.38; 95% CI, ) after further controlling for illness status, the age of breast-feeding cessation and the age at introduction of complementary foods. From the analysis of boys and girls combined, the ORs were 2.48 (95% CI, ) with adjustment for age and sex and 2.33 (95% CI, ) with all covariates. Conclusion: Macrosomia is an important predictor for high weight-for-length/height in Chinese children aged 1 3 years. (2008) 32, 55 60; doi: /sj.ijo ; published online 27 November 2007 Keywords: infant obesity; macrosomia; China; birth weight; infant growth (2008) 32, & 2008 Nature Publishing Group All rights reserved /08 $ Introduction The obesity epidemic is currently a critical global concern, in part because obese individuals are at increased risk of developing type 2 diabetes mellitus (T2DM), cardiovascular disease (CVD) and cancer. 1 3 Obese children are more likely to have impaired glucose tolerance 4 and to become obese adults. 5 A study by Vanhala et al. 6 reported that individuals who are both obese as a child and as an adult have a high probability having metabolic syndrome, that is, abdominal obesity, hypertension, dyslipidaemia and insulin resistance, a clustering of CVD risk factors. Higher birth weights have been shown to be associated with higher levels of body weight and body mass index Correspondence: Dr X Lin, Institute for Nutritional Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 294 Tai Yuan Lu, Shanghai , P.R. China. xlin@sibs.ac.cn and Dr JQ Sun, Department of Nutrition, Huadong Hospital, 221 Yan An Xi Lu, Shanghai , P.R. China. jianqins@gmail.com Received 28 December 2006; revised 14 October 2007; accepted 21 October 2007; published online 27 November 2007 (BMI) in childhood A rapidly increased rate of newborn macrosomia (birth weight X4000 g) has been documented since last two decades. For instant, In Yantai, China, the percentages of newborn macrosomia increased from 2.6% in the 1970s to 13.2% in the 1990s. 11 In Shanghai, the percentages of newborn macrosomia increased by 50 percent from 1989 to with the greatest increase being observed in urban areas. 13 Similar trends were also observed for the prevalence of childhood overweight and obesity in the same period of time. From 1985 to 2000, the prevalence of overweight increased 28-fold and the prevalence of obesity increased fourfold among Chinese children aged 7 18 years with the most marked increase being apparent for boys. 14 However, few studies have been made into the relationship of newborn macrosomia and body weight in earlier years of life in the Chinese children. The aim of the present study was to investigate whether macrosomia is associated with high weightfor-length/height in children 1 3 years of age in Shanghai, China. In addition, we estimated the influence of illness status and infant feeding modalities on this association.

2 56 Materials and methods Study population Children who were singletons and born between 1 January 1998 to 31 May 2001, lived in Huangpu District, Shanghai, China and who received routine health care at one of eight local health centers in the district were included in this study. As a part of routine health care, trained public health workers provided guidance on infant feeding practices, performed physical examinations and anthropometric measurements of children during the first 3 years. All of the newborn infants attend their local health center for routine health care according to the population registration system in China. Thus, this study includes the complete population of singleton live births who remained alive during the study period. Children were presented at the local health centers with their parents and/or grandparents during the first and second month after the delivery. Thereafter during the first year they attended the center every 2 months followed by semiannual visits until the age of 3 years. A total of 1978 children (1011 boys and 966 girls) participated in the study. Of them, 918 children (471 boys and 447 girls) were older than 1 year by 31 May 2001 and were included as subjects for this investigation. Anthropometric measurements Birth weight and crown-heel length were obtained from the birth certificates. As mean birth weight in boys was significantly higher than that of girls (3424±489 g vs 3283±442 g, Po0.001), macrosomia was defined as birth weight X90th percentile of the sex specific birth weight distribution. This corresponds to a birth weight greater than 3995 g for boys and 3840 g for girls. Body weight and length measurements were taken at each postnatal physical examination. Body weight was measured with a beam balance scale with subjects wearing light indoor clothing without shoes. Body length was measured as recumbent length by a neonatometer if children were younger than 2 years of age or as standing height by a stadiometer if children were 2 years or older. Weight was measured to the nearest 0.1 kg and height to the nearest 0.1 cm. The children were classified as having high weight-for-length/height when his/her weightfor-length/height z-score at the last physical examination was more than the 90th percentile of the participants weight-for-length/height z-scores using the WHO growth reference. 15 The cut-off point was Health status and feeding style Information on health status and feeding mode was recorded for each physical examination. This information included self-reported illness during the previous month, if the mother was currently breastfeeding the infant, and when the infant was introduced to any of the following complementary foods: cereals, eggs, vegetables, fruits and soybean products. According to the responses, health status was dichotomized as (a) ill or (b) not ill, breastfeeding as (a) never and less than 6 months or (b) more than 6 months, introduction of each complimentary food as (a) before or (b) after the sixth month. Introduction of soybean products was classified as (a) never, as well as (b) before or (c) after 6 months. Statistical analysis We tested the differences in weight, height, z-scores for weight-for-age, length/height-for-age and weight-for-length/ height, illness status and feeding modalities between nonmacrosomic and macrosomic children by univariate analysis of variance for the continuous variables and logistic regression for the categorical variables while controlling for age and sex. Multiple logistical regression models were employed to assess the odds ratios (ORs) of macrosomic infants having high weight-for-length/height at the last physical examination compared with their counterparts who were not macrosomic. The analyses were done separately for each sex and then were combined for both sexes as there was no statistically significant interaction for the risk of high weight-for-length/height between sex and macrosomic status in both the simple and multiple adjusted models. The analyses were also repeated by excluding infants with a low birth weight (birth weight o2500 g, 20 boys and 18 girls) and by defining macrosomia as birth weight X4000 g. The statistical inference was made when Po0.05 (two sided). Statistics were analyzed with the SPSS (version 14.0) and SAS (version 9.1). Results Macrosomic newborns were significantly heavier and taller than nonmacrosomic infants (Table 1). Infants who were macrosomic at birth had significantly higher body weight and length or height than nonmacrosomic infants at 1 3 years of age. At the last physical examination, z-scores of weight-for-age, length/height-for-age and weight-for-length/ height were significantly higher in infants who were macrosomic at birth than those who were nonmacrosomic. Children who were macrosomic at birth were more likely to be fed cereals at a relatively younger age. The age adjusted ORs were 3.60 (95% confidence interval (CI), ) for macrosomic boys and 1.39 (95% CI, ) for macrosomic girls for high weight-for-length/ height compared with the nonmacrosomic boys and girls, respectively (Table 2). The ORs were attenuated to 3.48 (95% CI, ) for boys after further controlling for illness status, the timing of cessation of breastfeeding, the timing of the introduction of cereals, eggs, vegetables, fruits and soybeans; whereas the association remained nonsignificant for girls (OR, 1.38; 95% CI, ) after the multivariate adjustment. When data for boys and girls were combined,

3 Table 1 Characteristics of the study participants Nonmacrosomia Macrosomia P-values 57 Number of participants Age at last physical examination (mean (s.d.), in years) 1.4 (0.5) 1.5 (0.5) Female sex (no. (%)) 401 (49) 46 (49) Birth-weight a (mean (s.d.), in g) 3268 (410) 4121 (204) o0.001 Birth-recumbent length a (mean (s.d.), in cm) 49.6 (1.5) 50.9 (1.2) o0.001 Later body weight b (mean (s.d.), in kg) 11.2 (1.6) 12.2 (1.7) o0.001 Later body length or height b (mean (s.d.), in cm) 81.5 (6.1) 83.6 (6.0) o0.001 Later BMI b (mean (s.d.), in kg m 2 ) 16.9 (1.4) 17.5 (1.7) o0.001 z-scores at last physical examination Weight-for-age b (mean (s.d.)) 0.65 (0.81) 1.34 (0.85) o0.001 Length/height-for-age b (mean (s.d.)) 0.52 (0.98) 1.18 (0.93) o0.001 Weight-for-length/height b (mean (s.d.)) 0.55 (0.83) 1.09 (0.96) o0.001 Having any current illness c (no. (%)) 140 (17) 10 (11) Breastfeeding p6 months or never a (no. (%)) 413 (50) 49 (52) Introduced cereal foods before 6 months a (no. (%)) 300 (37) 45 (49) Introduced eggs before 6 months a (no. (%)) 329 (41) 42 (46) Introduced vegetables before 6 months a (no. (%)) 43 (5) 7 (8) Introduced fruits before 6 months a (no. (%)) 206 (25) 29 (32) Introduced soybean products before 6 months a (no. (%)) 111 (14) 17 (18) Abbreviations: BMI, body mass index; no., number; s.d., standard deviation. a Adjusted for sex. b The last measurements of body weight and length/height, and adjusted for age and sex. c Having any illness during the past month of the last physical examination and adjusted for age and sex. Table 2 Odds ratios (ORs) and 95% confidence intervals (CIs) for high weight-for-length/height according to macrosomic status Nonmacrosomia Macrosomia Boys Number of cases/total participants 42/423 13/ ( ) (OR (95% CI)) a (OR (95% CI)) b ( ) Girls Number of cases/total participants 31/401 5/ ( ) (OR (95% CI)) a, ( ) (OR (95% CI)) b Boys and girls combined Number of cases/total participants 73/894 18/ ( ) (OR (95% CI)) c (OR (95% CI)) c ( ) a Adjusted for age. b Adjusted for age, illness status, the timing of cessation of breastfeeding, the timing of introduction of eggs, cereal foods, vegetables, fruits and soybean products. c Further adjusted for sex. and adjustments were made for age and sex in one model and then the addition of other diet and health covariates in a second model, the ORs were 2.48 (95% CI, ) and 2.33 (95% CI, ), respectively. Excluding children with a low birth weight, the ORs were 2.39 (95% CI, ) after adjusting for age and sex, and 2.23 (95% CI, ) after adjusting further for other covariates. Defining macrosomia as birth weight X4000 g, the ORs were 3.64 (95% CI, ) with adjustment for age and sex and 3.25 (95% CI, ) after further controlling for the covariates, respectively. With sexes combined, the multivariate adjusted relationships were significant in children without any reported illness in the previous month (OR, 2.33; 95% CI, ) and in those who were breastfed more than 6 months (OR, 2.45; 95% CI, ). Significant associations were also presented in children who were introduced to cereals or fruits before the age of 6 months (OR, 3.58; 95% CI, for earlier cereal food introduction and OR, 4.24; 95% CI, for earlier fruit introduction). The association was also apparent among infants who were introduced to eggs at the age of 6 months or more (OR, 2.33; 95% CI, ). Among boys, those who were macrosomic at birth or introduced to cereal foods before 6 months were more likely to have high weight-for-length/height compared with those who were nonmacrosomic and introduced to cereals at the age of 6 months or more (P for trend ¼ ; Table 3). Discussion In the present study, we found that children who had a higher birth weight were associated with high weight-forlength/height at 1 3 years of age. Controlling for illness status and feeding styles attenuated slightly the strength of the association, especially for boys. To our knowledge, this is the first study reporting the association between macrosomia and high weight-for-length/height in earlier years of life in

4 58 Table 3 Odds ratios (ORs) and 95% confidence intervals (CIs) for high weight-for-length/height according to macrosomic status and the timing of cereal foods introduction a (OR (95% CI)) Boys Girls Nonmacrosomia and introduced to cereals X6 months (boys/girls, 258/254) b Nonmacrosomia and introduced 1.88 ( ) 0.85 ( ) to cereals o6 months (boys/girls, 161/139) b Macrosomia and introduced to 2.83 ( ) 0.63 ( ) cereals X6 months (boys/girls, 27/20) b Macrosomia and introduced to 8.03 ( ) 1.81 ( ) cereals o6 months (boys/girls, 20/25) b P for trend P for interaction c a Adjusted for age, illness status, the timing of cessation of breastfeeding, the timing of introduction of eggs, vegetables, fruits and soybean products. b Number of participants in each category by sex. There are 14 subjects having missing data on the timing of cereal food introduction (5 boys and 9 girls). c Interaction between sex, macrosomic status and the timing of cereal food introduction. Chinese infants. Our data are in agreement with other studies Tanaka et al. 7 reported that there is a positive association between birth weight and BMI at 3 years of age in Japan. A case-control study by Takahashi and colleagues 8 suggested that children who were obese at 3 years of age had higher birth weights compared with their normal weight counterparts. In the study of Whitaker, 9 American children with a large birth weight (X90th percentile) had the higher percentages of obese children at 2 4 years of age, which is more apparent in boys than that in girls. A longitudinal study by Parsons et al. 10 indicated that the association between higher birth weight and higher levels of BMI may persist into adulthood among the participants of a British birth cohort. In our study, the association between prenatal and postnatal development at 1 3 years of age was attenuated after controlling for postnatal illness status and feeding modalities. However, a significant association was only apparent for the timing of cereal food introduction among boys in the multivariate adjusted analyses. Boys who were introduced to cereal foods at the age of 6 months or more were less likely to have high weight-for-length/height later (OR, 0.49; 95% CI, ) compared with those who were introduced to cereals before the age of 6 months, regardless of the weight status at birth. Infants who were macrosomic at birth were more likely to have an earlier introduction to cereal food than nonmacrosomic infants in this study. There was also a synergistic effect of newborn macrosomia and earlier introduction to cereal foods on the development of high weight-for-length/height in boys. In the Danish National Birth Cohort, 16 infants who had earlier introduction to complementary food had significantly more weight gain from birth to 1 year compared with those who had later introduction to complementary food. It has also been reported that early introduction to solid foods is associated with increased BMI and percentage of body fat in infants of a prospective study in the UK. 17 Study by Ong and colleagues 18 reported that energy intake is significantly higher among infants who were given weaning foods earlier. These infants have higher body weight compared with those who were fed weaning foods later. Our data along with previous studies suggest the important role of the feeding style in the etiology of childhood obesity and its implication for the body composition development in later life. There is evidence suggesting that intrauterine development as indicated by birth weight is a determinant of morbidity and mortality in adulthood. 19 However, environmental factors and lifestyles adopted throughout life may play an important role in adult diseases occurrence. 20,21 Limited studies have reported postnatal environment factors accounting for the association of birth weight and childhood obesity. Although the effects of the complementary foods introduction contributing to childhood obesity have not been fully estimated, the duration and exclusivity of breastfeeding seems to be a protective factor in some studies, but not all. 25 Our data seem to indirectly support that prolonged exclusivity of breastfeeding might help maintain a normal body weight among infants in the earlier years of life. Some reports suggest that higher birth weight may be a risk factor of both type 1 diabetes and T2DM in children. There is evidence indicating that birth weight may have a J-shape relationship with T2DM during adulthood, adult women who had either low or high birth weight have an increased relative risk of having T2DM in the Nurses Health Study. 29 In the Bogalusa Heart Study, overweight is associated with various cardiovascular risk factors and cardiovascular risk factor clustering even in the children as young as 5 10 years of age. 30 Although there is little evidence that higher levels of childhood BMI associated with higher birth weights may lead to the occurrence of certain diseases, it appears likely that children with higher levels of BMI tend to have an increased risk of being obese in adolescence 31 and adulthood. 4 In this study, to enhance statistical power, we defined macrosomia as birth weight X90th percentile of the sex specific birth weight distribution. However, the 90th percentile for boys was 3995 g that is really close to the classic cut-off point (4000 g); and defining macrosomia as birth weight X4000 g yielded comparable results. Gestational age of our study subjects was not included in this analysis, as the duration of gestation does not seem to have any influence on later infant body weight. 10 Because data was collected at the first postpartum month, the data of maternal prenatal or preconception anthropometric measurements was not available for the current analyses. Maternal prenatal body weight

5 and weight gain was previously reported to influence children s body weight. 9 Understanding the relationship between maternal prenatal nutritional status to children s birth weight and later body weight may help elucidate the natural history of the association between birth weight and body weight during childhood and perhaps in later life. One limitation of this study is that quantitative data on dietary intakes were not available, so we could not assess postnatal dietary differences between the macrosomic and nonmacrosomic infants. We analyzed the data controlling for both illness status and feeding styles in the same models since these two factors are highly correlated. 17 However, the synergistic effects of earlier introduction of cereal foods on high body weight development among macrosomic boys imply that infant feeding modalities might be important modifiable factors for the association between birth weight and body weight during the earlier years of life in Chinese infants. In addition, we do not have data on postnatal physical activity, which might confound the influence of food intake on the association between macrosomia and high weight-for-length/height among infants. In conclusion, our data suggest that high birth weight is an important predictor of excess body weight at the 1 3 years of age in this study population. Postnatal environmental factors, such as illness and especially infant feeding styles, are important confounding factors of the association. Understanding the effect of intrauterine and pediatric nutrition on body weight during infancy may help design targeted intervention for the early prevention of obesity. Acknowledgements This study was supported by Ministry of Science and Technology of China (973 Program, Grant No. 2006CB503900) and Science and Technology Commission of Shanghai Municipality (Grants No. 04DZ14007). 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