AMERICAN JOURNAL OF HUMAN BIOLOGY 24:633639 (2012)

Original Research Article

Determinants of High Weight Gain and High BMI Status in the First Three Months in Urban Chinese Infants
JIANDUAN ZHANG,1* JINGXIONG JIANG,2 JOHN H. HIMES,3 JING ZHANG,1 GUOYAN LIU,4 XIAONA HUANG,2 YUAN GUO,1 JUNXIN SHI,1 AND SHUHUA SHI1 1 Department of Woman and Childs Care and Adolescence Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology. Wuhan 430030, Hubei, China 2 Department of Child Health, National Center of Women and Childrens Health Care, Chinese Center for Disease Control and Prevention, Beijing 100013, China 3 Department of Epidemiology and Community Health, School of Public Health, University of Minnesota, Minneapolis, Minnesota 55454 4 Department of Preschool Education, Normal College, Shenzhen University, Shenzhen 518060, Guangdong, China

Objectives: Investigate the potential factors associated with high weight gain and high BMI status in the rst three months of life. Methods: Totally, 930 healthy neonates (489 boys and 441 girls) were involved in this community-based, prospective study in China. Data on body weight and length were collected at birth, and the 1st and 3rd months. A self-administered questionnaire was used to collect data regarding social demography, gestational status, delivery, and the feeding patterns of children. Results: Prevalences of high BMI status (BMI = 85th p, re WHO BMI standards) increased over time in both sexes, reaching 24.5% and 12.0% for boys and girls, respectively. General linear mixed models indicate high BMI status at 3 months is signicantly and inversely associated with breastfeeding, as a proportion of feeding occasions [OR 0.74 (95%CI: 0.560.98)] and positively with lower birth weight [OR 2.07 (95%CI: 1.233.49)]. High weight gain (=85th p, re WHO velocity standards) in the rst 3 months is also signicantly associated with breastfeeding [OR 0.76 (95%CI: 0.590.96)] and sex, with boys at a higher risk than girls [OR 1.44 (95%CI: 1.071.97)]. Living in an extended family is associated with both high weight gain and high BMI status, but with marginal statistical signicance. Conclusion: Analyses indicate an increasing trend of high BMI status in early infancy. Breastfeeding provides a protective effect for both high weight gain and high BMI status. The results concerning birth weight suggests a target for intervention. Am. J. Hum. Biol. 24:633639, 2012. ' 2012 Wiley Periodicals, Inc.

Childhood obesity is one of the most important global public health concerns and it has been spreading to many parts of the world (Ogden, et al., 2006; Sanigorski, et al., 2007; Spurgeon, 2002; Stamatakis, et al., 2005). With rapid socioeconomic development since the 1980s, China has been experiencing a signicant transition in life style and nutritional status. Accordingly, the prevalences of childhood overweight and obesity have risen dramatically. In urban areas the prevalence of obesity in preschool children increased from 1.5% in 1989 to 12.6% in 1997, and that of overweight increased from 14.6% to 28.9% in the same period (Luo and Hu, 2002). A recent report indicates that combined overweight and obesity prevalence, and only obesity prevalence among school age children reached 34.2% and 30.3%, respectively, in 2005 (Ji and Cheng, 2009). Concurrent and long-term adverse health outcomes of excessive adiposity in childhood are well documented, including asthma, Type 2 diabetes and elevated cardiovascular disease risks (Brophy, 2009; Dietz and Gortmaker, 2001; WHO, 2000). As these conditions track into adulthood, they are associated with greater middle-age mortality and morbidity (Dietz, 1998; Gunnell et al., 1998). Obese children are more likely to suffer from emotional and social conditions, e.g., depression, low self-esteem, eating disorders, negative body image, and social stigma (Stockton et al., 2009). Infancy is understood as a critical period of developing adiposity and the relative weight gain from birth to 3 months has positive relationships with childhood fat mass (Chomtho et al., 2008). Rapid infancy weight gain is consistently associated with increased subsequent obesity risk
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as well (Ong and Loos, 2006; Vogels et al., 2006; Whitaker 1997). This makes infancy and early childhood an excellent opportunity for obesity prevention and, consequently, it should be a primary focus for intervention against future obesity problems (Birch and Ventura, 2009). Childhood obesity is a multifactorial disorder inuenced by genetic, environmental and cultural factors. Nevertheless, the rapid temporal changes in prevalences of obesity within populations are unlikely to have resulted primarily from genetic factors. Because of the wide variation in environmental and cultural factors that may foster obesity, it is important to examine the particular subset of factors within a country associated with the development of child obesity so that determinants can be understood and appropriate interventions can be tailored. China has several distinctive characteristics that may increase the risk of early development of obesity in

Contract grant sponsor: National Natural Science Fund (NNSF) of China; Contract grant number: 30800917; Contract grant sponsor: The Special Fund for Basic Scientic Research of Central Colleges; Contract grant number: 2011TS017. *Correspondence to: Jianduan Zhang, Department of Woman and Childs Care and Adolescence Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, 13 Hangkong Rd., Wuhan 430030, Hubei, China. E-mail: jd_zh@hotmail.com or jd_zh@mail.hust.edu.cn Received 21 July 2011; Revision received 18 February 2012; Accepted 8 April 2012 DOI 10.1002/ajhb.22284 Published online 24 May 2012 in Wiley Online Library (wileyonlinelibrary. com).

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children, e.g., the highest Cesarean-section rate in the world (Li et al., 2006), extended family structure, and a low proportion of exclusive breastfeeding within 46 months (Huang et al., 2009). Yet the understanding of the high weight gain and high BMI status of early childhood is limited in China to ndings from mostly small studies and cross-sectional surveys, and extant studies usually focused on older children (Chen et al., 2006; Yi et al., 2002). Moreover, we are aware of no longitudinal studies available from birth. This study reports results from a longitudinal study of weight gain and BMI status from birth to three months of age in Chinese infants from three cities, where demographic, cultural, and feeding variables were collected for a large sample of children. SUBJECTS AND METHODS A total of 930 infants (489 boys and 441 girls) were recruited through a multistage sampling scheme within the rst month following birth and were followed subsequently at least until three months of age. For the sampling, three cities were selected to represent three distinct administrative and geographic regions of China: Shenyang, capital city of Liaoning province (Northern China); Wuhan, capital city of Hubei Province (Central China) and Guangzhou, capital city of Guangdong Province (Southern China). These are relatively afuent cities and the prevalence of obesity was thought to be relatively high. Within each of the three urban areas Community Health Service Centers/Stations were randomly selected. Finally, the participant infants were then randomly selected from among newborns to local residents that were registered and who would receive health surveillance and routine follow-up. All protocols were standardized across the three eld sites and data collectors were trained and monitored centrally. Informed consent was obtained from the parents. Birth weight and crown-heel length at birth were obtained from the Perinatal Health Booklet (PHB), which was kept by individual parents with health information recorded related to pregnancy from the rst prenatal checkup until 42 days following delivery. These data were collected by consistently trained health staff. Weight and length were measured within 10 days of the exact monthly target ages. Only in Wuhan were children required to be measured at 2 months of age. Body weight was measured to the nearest 50 g with electronic scales and with subjects wearing light indoor clothing. Recumbent length was measured to the nearest 0.1 cm using an infantometer. Both weight and length were taken in duplicate and means of the two measurements were used in the analyses. Socioeconomic and health-related variables were obtained from the PHB and from standardized administered interviews. Maternal weight gain, diseases during pregnancy, and type of delivery were provided by the PHB. Child sex, date of birth, parental age, parental occupations, and education level, as well as family structure and income came from the interviews. The reported occasions of bottle and breast feeding were collected using a specially developed feeding questionnaire at monthly interviews with caregivers. We examined the prevalence of high and very high BMI status, dened as equal to or greater than the 85th and 95th percentiles of the age- and sex-specic standards
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respectively, using the World Health Organization (WHO) Child Growth Standards (2006). High weight gain was dened as weight gain in the rst 3 months = 85th percentile of the WHO velocity standards (2008) specic to sex. Choosing which reference data or standards to use for comparisons, and how to appropriately characterize the children was not straight forward. The WHO standards have been recommended for use in all children (WHO, 2006). Nevertheless, the referent children are all considered healthy even though the standards have been used to characterize overweight and obesity in very young children (Di Onis et al., 2010). The terms overweight and obesity are not customarily applied to children less than 2 years of age, even though early rapid weight gain is a strong predictor of adiposity later in childhood. Z-score cut-offs relative to the WHO standards have been used for BMI and weight-for-length to characterize overweight and obesity in very young children, although conventional criteria have used sex- and age-specic percentiles (WHO, 1995). Our decisions to use BMI percentiles relative to the WHO standards should correctly identify those children with the highest adiposity, and comport with traditional cut-offs and interpretation (WHO, 1995). For the analysis, 3-month weight gains were calculated by linear adjustment of the data at the measured intervals to exactly 3.0 months in duration (91 days). So, for example, for a child who weighed 3.0 kg at birth and 6.0 kg at the 3-month visit at 100 days of age, the adjusted 3-month weight gain 5 (6.03.0 kg) 3 (91/100) 5 2.73 kg. Preterm birth was dened as born prior to 37 weeks of gestation. For analysis, maternal and paternal education levels were recorded into two categories (= middle school; >middle school) because this dichotomy was more discriminating than more complicated schemes or stratifying on university education. The occupations of parents were categorized into those typically reported in Chinese surveys. The monthly household income was recoded into ordinal categories from 1 to 6 (1 5 < 1,000 RMB, 2 5 1,000-<2,000 RMB, 3 5 2,000-< 3,000 RMB, 4 5 3,000-< 5,000 RMB, 5 5 5,000-< 8,000 RMB, 6 5 ! 8,000 RMB). Because of very low percentages of low birth weight and macrosomia, birth weight was categorized into quintiles [quintile cutoffs (kg): 3.0, 3.2, 3.4, and 3.6]. In the general linear mixed models, we used the lowest quintile (3.0 kg) as the cutoff to categorize the participants into two birth weight groups. Breast feeding was originally recorded at each clinic visit by type at each feeding occasion. This allowed categorization as exclusive breast feeding and any breast feeding. Also, we calculated a variable to capture variation in breast feeding as the proportion of total feeding occasions that was only breast feeding, such that no breast feeding 5 0 and exclusive breast feeding 5 1. This measure is less satisfactory than if actual food amounts were obtained but still should be an unbiased estimate of the relative role of breastfeeding practice. For some analyses breast feeding proportion was standardized as a Z-score relative to the mean proportion at that age ( Z XBreastfeedingproprotion meanBreastfeedingproprotion = SDBreastfeedingproprotion ). Although family structure was originally recorded as four nominal categories (1-nuclear family, 2-extended family, 3-joint family, 4-single-parent family), due to very small frequencies of the last two categories (4.6%), only categories of nuclear and extended families were used in the nal regression models. For some variables there are

INFANT BMI STATUS AND WEIGHT GAIN IN CHINA TABLE 1. Categorical variables describing the study subjects and

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feeding status

their families
Categorical variable Sex Boys Girls Gestational age Preterm Non-preterm Delivery method C-section Vaginal Birth weight (g) <2,500 2,5004,000 >54,000 Single-child family Yes No Maternal education level Middle school or less High school/technical secondary school University/college Master degree or higher Paternal education level Middle school or less High school/technical secondary school University/college Master degree or higher Maternal occupations White-collar Intellectual Self-employed laborer Service staff On-the-job worker Cadre/civil servant Unemployment Unknown Paternal occupations White-collar Intellectual Self-employed laborer Service staff On-the-job worker Cadre/civil servant Unemployment Unknown Monthly household income (RMB) <1,000 1,000<2,000 2,000-<3,000 3,000<5,000 5,000<8,000 !8,000 Family structure Nuclear family Extended family Joint family Single-parent family N %

TABLE 2. Continuous variables describing the study subjects and Variable Maternal age [mean (SD), y] Paternal age [mean (SD), y] Exclusive breastfeeding at 1st month (n, %) Exclusive breastfeeding at 3rd month (n, %) Any breastfeeding at 1st month (n, %) Any breastfeeding at 3rd month (n, %) Breastfeeding as a proportion of feeding occasions at 3rd month [mean (SD)] Breastfeeding as a proportion of feeding occasions at 1st month [mean (SD)] N 930 930 877 905 877 905 877 905 28.3 (3.7) 30.8 (4.5) 344 (39.23) 365 (40.36) 761 (86.74) 709 (78.34) 0.63 (0.40) 0.69 (0.36)

489 441 56 867 623 306 14 861 55 812 118 195 231 457 45 162 255 445 67 143 146 92 60 52 42 264 131 171 92 166 56 126 102 71 146 22 117 223 291 173 88 549 339 36 6

52.6 47.4 6.1 93.9 67.1 32.9 1.5 92.6 5.9 87.3 12.7 21.0 24.9 49.2 4.9 17.4 27.5 47.9 7.2 15.4 15.7 9.9 6.4 5.6 4.5 28.4 14.1 18.4 9.9 17.8 6.0 13.6 11.0 7.6 15.7 2.4 12.8 24.4 31.9 18.9 9.6 59.0 36.4 3.9 0.7

RESULTS Tables 1 and 2 summarize socio-demographic, perinatal status and feeding patterns of the infants and their families. Some of these highlight distinctive aspects of Chinese populations, e.g., high proportion of delivery by C-section (67%) and single-child families (87.3%); a very low prevalence of low birth weight (1.5%), and about 40% of children living in an extended family. The parents tend to be rather young and well educated with over half of mothers and fathers having university or advanced degrees. The rates of exclusive breastfeeding at the 1st and 3rd month are 39.2% and 40.4%, respectively. Table 3 presents the means and standard deviations of body weight and length by monthly clinic visit and sex. The age-specic means exceed the medians of the WHO growth standards and approximate the 60th to 70th percentiles for each measurement. The increasing prevalences of high and very high BMI status at each age are presented in Figure 1. Prevalences of high BMI status rises from 9.6% to 24.5% for boys and 2 increases from 7.7% to 20.9% for girls (Xcmn1 5 86.7, P < 0.0001); likewise those with very high BMI status start at 1.6% for both sexes and end up with 12.1% for boys and 2 7.9% for girls, respectively (Xcmn1 5 74.1, P < 0.0001). No signicant sex difference was observed in prevalences within age groups except for the prevalence of very high BMI status at the 3rd month, with boys exceeding that of girls (12.1% vs. 7.9%, x2 5 4.35, P < 0.05). Boys had signicantly greater mean weight gains than girls during the rst three months (t 5 11.40, P < 0.001), with the average weight gains for boys and girls being 3.48 6 0.66 kg and 3.00 6 0.60 kg, respectively. Of these 3-month weight gains 42.2% in boys and 33.8% in girls exceeded the 85th percentile of the WHO growth velocity standard; this sex difference was statistically signicant (x2 5 6.83, P 5 0.009). All the variables in Tables 1 and 2 were considered as potential determinants of high BMI status at 3 months and of high weight gains. The nal reduced logistic models retained only those variables that proved statistically signicant in the crude models or that were theoretically important to include. Interaction between birth weight and feeding proportion, education level and feeding proportions, household income and feeding proportion were investigated and none was found to be statistically signicant. Table 4 presents the crude and adjusted odds ratios from the general mixed logistic model estimating high BMI status at 3 months. The crude analyses suggest
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small amounts of missing data so the actual number of cases may vary slightly in some descriptive summaries. Chi-square tests were used to evaluate the differences between prevalences, and the differences of mean weight gains between groups were compared by t-tests. Age prevalences in the gure were smoothed across ages using cubic splines in Excel software. To accommodate inter-city differences and intra-class correlations among cities, general linear mixed models were used via the SAS procedure PROC MIXED to examine factors associated with high weight gain and BMI status at 3 months, with city as a random effect. The resulting odds ratios (OR) and 95% condence intervals are presented. All data were analyzed using SAS v9.2.

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J. ZHANG ET AL. TABLE 3. Mean weight and length by sex at birth and 1, 2, and 3 months of age Boys Weight Length Z
D

Girls Weight Z
D

Length Z
D

Age (month) Birth 1 2a 3

n 489 472 192 489

Mean (SD, kg) 3.38 (0.42) 4.61 (0.51) 5.92 (0.65) 6.85 (0.77)

Mean (SD, cm) 50.6 (1.6) 55.2 (1.9) 59.2 (2.2) 62.6 (2.1)

n 441 426 153 441

Mean (SD, kg) 3.25 (0.39) 4.28 (0.50) 5.48 (0.53) 6.25 (0.69)

Mean (SD, cm) 49.9 (1.5) 54.1 (1.8) 57.9 (1.6) 60.9 (2.1)

ZD 0.41 0.22 0.41 0.46

0.08 0.18 0.43 0.54

0.38 0.26 0.34 0.43

0.04 0.13 0.43 0.48

ZD: Referring to WHO child growth standards, the sex-specic weight- for- age, length- for- age, and BMI- for- age, respectively. This is a mean Z-score just for comparison purposes. a Only in Wuhan children were measured at the 2-month visit.

Fig. 1. Prevalences of high and very high BMI status over time from 0 to 3 months. [Color gure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

increased risk of high BMI status at 3 months for infants with birth weights < 3.0 kg and for those living in an extended family. Also, the proportion of feeding occasions at three months (but not at 1 month) that were breastfeeding is protective in the crude analysis. After adjustment for child sex, maternal education level, household economic status, and rst month breastfeeding proportion, high BMI status at 3 months remains signicantly associated with birth weight and breastfeeding proportion at 3 months. Children from the lowest birth weight quintile (<3.0 kg) are, on average, more than twice as likely to reach high BMI status at 3 months than those with higher birth weight, and breastfeeding proportion at month 3 concurrently reduced 25% risk of developing high BMI status per 1 SD difference. Table 5 presents the crude and adjusted odds ratios from the general mixed logistic model estimating high 3month weight gains. The crude analyses suggest an increased risk of high weight gains among boys and those living in extended families. In the fully adjusted model, sex remains statistically signicant [OR, 1.44 (95% CI, 1.07, 1.97)] and Z-score of breastfeeding as a proportion of total feeding occasions at 3 months is protective against high 3-month weight gains [OR, 0.76 (95% CI, 0.59, 0.96)]. DISCUSSION With its prevalence being doubled or even tripled within one decade (Chen, 2008), childhood overweight and obesity are becoming serious public health issues in China. The prevalence of metabolic syndrome (MS) in severely obese children and adolescents in the Zhejiang area has reached a high level and insulin resistance and hypoadiponectinemia were found in the MS children (Fu et al., 2007), indicating they share with those living in more afuent Western countries similar risks of metabolic synAmerican Journal of Human Biology

drome associated with excessive weight. According to the latest National Population Sampling Survey in 2006, up to 20% of the population in mainland China was under 14 years old, i.e., 26.5 million Chinese children. The sheer magnitude of the potential problem of an epidemic of childhood obesity in China is overwhelming (Ji, 2008). The current prospective study aims at a better understanding of the early predictors of high BMI status at 3 months and high weight gain in the same period. Participants of this study are community-based Chinese infants from three cities. Their mean birth weights and lengths are almost identical to those of the national Chinese city Children Growth Reference (birth weight within 50 g, length within 2 mm) (Coordinating Study Group of Nine Cities on the Physical Growth and Development of Children Capital Institute of Pediatrics, 2007). Weight-for-length percentile charts have been used to describe childrens weight relative to their length and to categorize them as normal, underweight, or overweight (Gibson, 2005). This compares a childs weight to that of children of similar length but not necessarily the same age (Nash, 2008). In 2006, the WHO released the WHO Child Growth Standards (WHO Multicentre Growth Reference Study Group, 2006) based on a multicountry study involving breastfed infants and young children from six geographically distinct sites (Brazil, Ghana, India, Norway, Oman and the United States). Thereafter BMI-forage is available and in contrast with weight-for-length, it combines weight and length as well as age of children together. These newly released standards depict normal early childhood growth under optimal environmental conditions and can be used to assess children everywhere, regardless of ethnicity, socioeconomic status and type of feeding (WHO Multicentre Growth Reference Study Group, 2006). By using weight-for-height and BMI as the indicators for weight status referring to above standards, de Onis et al. compared the prevalence and trends of overweight and obesity among children aged 0 to 5 from 144 countries (de Onis, 2010). Furthermore, this study also showed that the prevalences of overweight estimates on the basis of weight-for-height and BMI-for-age are alike in both developed and developing countries (de Onis, 2010). Similarly, to obtain internationally comparable results, BMI was adopted as the indicator of childrens weight status in our study. So far no guidance exists in regard to appropriate BMI cutoffs for children younger than 2 years, and some concerns remain that the WHO standards are based on children who were exclusively breastfed and this nature might relate to low risk of obesity. However, according to Gibson, Waterlow, etc. (Dietitians of Canada, 2004; Gibson, 2005; Mei, 2002; Waterlow, 1977),

INFANT BMI STATUS AND WEIGHT GAIN IN CHINA TABLE 4. Crude and adjusted odds ratios (OR) and 95% condence intervals (CI) for high BMI status at 3 months Effects Sex Birth weight (kg) Family structure Maternal education level Monthly household income (RMB) Breastfeeding proportion at 1 mo (Z) Breastfeeding proportion at 3 mo (Z) 0,Girls (ref.); 1,Boys 0,!3.0 (ref.); 1,<3.0 0,Nuclear family(ref.) 1,Extended family 0>Middle school (ref.) 1 Middle school Crude Odds Ratio (95% CI) 1.23 (0.91, 1.68) 2.10 (1.49, 2.97) 1.54 (1.11, 2.15) 0.96 (0.66, 1.40) 1.03 (0.91, 1.17) 0.78 (0.50, 1.21) 0.63 (0.42, 0.95)

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Adjusted Odds Ratio (95% CI) 1.16 (0.83, 1.63) 2.07 (1.23, 3.49) 1.33 (0.93, 1.89) 0.90 (0.59, 1.39) 1.04 (0.93, 1.89) 1.13 (0.85, 1.49) 0.74 (0.56, 0.98)

Notes: Adjusted for gestational age, maternal weight gain during pregnancy, paternal education level.

TABLE 5. Crude and adjusted odds ratios (OR) and 95% condence intervals (CI) for high weight gains in the rst three month Effects Sex Birth weight (kg) Family structure Maternal education level Monthly household income (RMB) Breastfeeding proportion at 1 mo (Z) Breastfeeding proportion at 3 mo (Z) 0,Girls (ref.); 1,Boys 0, !3.0(ref.); 1,<3.0 0, Nuclear family(ref.) 1, Extended family 0, >Middle school(ref.) 1, Middle school Crude Odds Ratio (95% CI) 1.43 (1.09, 1.86) 0.91 (0.69, 1.20) 1.46 (1.10, 1.94) 1.49 (1.07, 2.09) 1.00 (0.90, 1.12) 0.99 (0.87, 1.13) 0.71 (0.50, 1.01) Adjusted Odds Ratio (95% CI) 1.44 (1.07, 1.97) 1.05 (0.70, 1.58) 1.25 (0.92, 1.70) 1.23 (0.83, 1.23) 1.08 (0.95, 1.23) 1.18 (0.93, 1.50) 0.76 (0.59, 0.96)

Adjusted for gestational age, maternal weight gain during pregnancy, paternal education level. Because of the measurements at 2 months were only obtained in one center (Wuhan), they were not included in this gure.

BMI-for-age percentile scores between 85th to 94th percentile were used as criteria for overweight, and 95th percentile was cutoff of obese to correspond to similar cut-offs at older ages. Whereas, in line with WHO recommendations (WHO, 1995) in de Oniss report, proportion of BMI values > 1 SD and 2SDs from the median among children aged 0 to 5 with were calculated (de Onis, 2010). Given the normal distribution of weight status, the values of 1 SD approximately equal to 85th percentile. Therefore, in our nal regression models, 85th percentile was adopted as the criteria to distinguish children with high weight gain and with high BMI status from the overall participants. By using the above criteria, the prevalence of high BMI status in our study at 3 months reaches 24.5% for boys and 20.9% for girls, and 12.1% boys and 7.9% girls reached or surpassed 95th percentile of BMI-for-age, that is, with very high BMI status. These levels clearly exceed those expected using the WHO standards, however, are lower than the 15.8% reported for a recent combined-sex sample of infants less than 4 months of age from Yunnan, China (Li et al., 2007), where obesity" was dened as at least 20% heavier than the older WHO reference of weight for height. We found a pattern of signicant and progressive increase in prevalence of high BMI in both sexes. There are few data available for direct comparisons at these early ages. A similar pattern of increasing overweight and obesity was observed in Iranian infants from birth to 6 months of age (Heidari et al., 2008). Certainly, in older children prevalences often increase with age (Hillier et al., 2007; Rudolf et al., 2006; Sanigorski et al., 2007). Thus, the development of high BMI status in our sample appears to be primarily a postnatal phenomenon. Infants with birth weight less than 3 kg had approximately twice the risk of having high BMI status at 3 months compared with those born at larger birth weights. This pattern of lower birth weight and subsequent higher

weight in infancy has been observed elsewhere (McMillen and Robinson, 2005; Oken and Gillman, 2003; Stettler et al., 2002). Our results indicate that those lower BW children must have experienced a period of relative catching-up, although not all of their weight gains exceeded the 85 percentile of the WHO velocity standard, because the association with lower birth weights was not signicant in the analysis of high weight gains. It is interesting that our sample of Chinese infants exceeded the expected frequencies above the cut-offs for BMI relative to the WHO standards, given that breastfeeding was less than ubiquitous at these early ages. The proportion of feeding occasions that were breastfeeding at 3 months showed signicant protective effects in our study for both excessive 3-month weight gains and high BMI status at 3 months. In the preliminary analysis we found neither consistent nor signicant associations between exclusive breastfeeding or ever breastfeeding and high weight gains or BMI status at 3 months, presumably because of the relatively high breastfeeding rate. Accordingly, we constructed the continuously distributed variable to capture the proportion of feeding occasions that were breast fed. Our ndings are consistent with many studies of breast feeding and infant growth (WHO, 2002), and the associations of breastfeeding with increased obesity, fatness, and metabolic syndrome later in childhood and in adults (Bergmann et al., 2003; Bogen et al., 2004; GrummerStrawn and Mei, 2004). We did not nd signicant associations between our breastfeeding measure at 1 month and either high BMI status at 3 months or excessive 3-month weight gains. We have speculated that the potential impact of breastfeeding at 1 month may be diminished in our population because of the very high proportion of C-section deliveries (67%). In practice, the immediate initiation of breastfeeding in the hospital is made more difcult and is delayed because
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of the surgical procedure. Moreover, the postoperative pain also increases the difculty in breastfeeding practices (de Armas et al., 2009). We nd it encouraging that even if immediate breast feeding cannot be initiated, persistence with breastfeeding until 3 months can still have a protective effect on high weight gains and BMI status at 3 months of age. In the unadjusted analyses, family structure was found to be a signicant determinant of both high weight gains and BMI status. Even though these associations did not remain statistically signicant in the fully adjusted models, we believe it is informative to comment about this aspect of the ndings because they depart from the family patterns often found in many Western countries. Three-generation families or extended families are a common family structure in China, especially when the children are still very young. For example, it is estimated that 5070% of urban Chinese children live with their parents and grandparents (Li, 2005; Zheng et al., 2008). This is considered a traditional pattern and it is becoming less common, especially in urban areas during the recent period of social transition. In our research, 36% of the children lived in an extended family. Given that 87% of the children had no siblings because of the persistent family planning policy instituted in the 1980s, one child is usually surrounded" by at least four adults, who tend to be over-caring, over-concerned, and over-feeding the only child. According to Jiangs qualitative research, grandparents tended to urge children to eat more meals and larger portion at served meals for preschool children (Jiang, 2007). Our analyses did not indicate signicant effects of measures related to socioeconomic status like maternal education or income. Nevertheless, we chose to leave these variables in the nal models to ensure that these theoretically important covariates were accounted for. Lower socioeconomic status has been shown elsewhere to be a strong independent risk factor of overweight and obesity in children (Lu, 2004). The lack of associations of socioeconomic factors with overweight at 3 months or excessive 3-month weight gains may be due to the young ages of infants involved and the relative homogeneity of diets at that age. Because of the one-child policy most Chinese parents value their children highly and spare no expense in picking the best brands of infant formula and foods so income may not be very discriminating especially during infancy. Finally, the validity of the household income data is not clear and the closeness of the OR to 1.00 in the logistic models may simply reect less than optimal quality of the data. We are aware that high BMI status during infancy might not be strikingly predictive of overweight status later in childhood and adulthood because of the rapidly changing growth and shifting of percentiles, especially during the rst year of life. Nevertheless, given the established longitudinal trajectories for weight growth and impacts on later obesity of excessive weight gains in infancy (Danielzik et al., 2004; Dennison, et al., 2006; Ong and Loos, 2006), and the increasing prevalences of overweight and obesity in the preschool years (Demerath et al., 2009; Luo and Hu, 2002), we believe it is important to understand the natural history of overweight from the earliest ages. This large and well-controlled communitybased study in this cohort of Chinese infants provides new insights regarding probable determinants in this important and rapidly changing population.
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LIMITATIONS In this study, we used BMI as a measure of weight status in infancy which is not universally well tested. However, BMI-for-age comparing a childs weight, adjusted for length, among children of a similar age, is an acceptable summary measure and is becoming more commonly used by researchers to study early weight status (Himes, 2009) and was used in a recently published article (de Onis, 2010). The WHO Growth Standard does not contain any East Asian populations which might affect the results to the degree that genetic or population-specic factors may play roles in early growth patterns. Nevertheless, it is recommended by the WHO for universal use although it includes data from six countries only. The birth weight and crown-heel length were obtained from the Perinatal Health Booklet which might not be as precise as the data obtained under more carefully controlled research settings. There is no reason to suspect, however, that such data are biased even though they may be less reliable. To the degree that measurement reliability contributed additional random error, our ndings should be relatively conservative. ACKNOWLEDGMENTS The authors extend their sincere thanks to the health staffs from Maternal and Child Health Centre/Hospital and the Community Health Service Centers in Shenyang, Qiaokou and Jianghan districts in Wuhan, and Panyu and Haizhu districts in Guangzhou who provided support in the project through data collection and services on the front lines. Last but not least, they greatly appreciate the parents who have been willing to be involved in this research project. LITERATURE CITED
hm O, Richter R, DudenBergmann KE, Bergmann RL, von Kries R, Bo hausen JW, Wahn U. 2003. Early determinants of childhood overweight and adiposity in a birth cohort study: Role of breastfeeding. Int J Obes Relat Metab Disord 27:162172. Birch LL, Ventura AK. 2009. Preventing childhood obesity: what works? Int J of Obes 33:S74S81. Bogen DL, Hanusa BH, Whitaker RC. 2004. The effect of breast-feeding with and without formula use on the risk of obesity at 4 years of age. Obes Res 12:15271535. Brophy S, Cooksey R, Gravenor MB, et al. 2009. Risk factors for childhood obesity at age 5: Analysis of the Millennium Cohort Study. BMC Public Health 9:467473. Chen C M. 2008. Overview of obesity in Mainland China. Obes Rev 9:14 21. Chen X, Qiu X, Yang S, et al. 2006. Risk factors of Obesity among Children Under 7 Years Old. Chin J Child Health Care 14:9394. Chomtho S, Wells JCK, Williams JE, et al. 2008. Infant growth and later body composition: evidence from the 4-component model. Am J Clin Nutr 87:17761784. Coordinating Study Group of Nine Cities on the Physical Growth and Development of Children Capital Institute of Pediatrics. 2007. A national survey on growth of children under 7 years of age in nine cities of China, 2005. Chin J Pediatr 45:609614 (in Chinese). se K, Dilba B, Mu Danielzik S, Czerwinski-Mast M, Langna ller MJ. 2004. Parental overweight, socioeconomic status and high birth weight are the major determinants of overweight and obesity in 57 y-old children: baseline data of the Kiel Obesity Prevention Study (KOPS). Int J Obes Relat Metab Disord 28:14941502. as SM, Modino SC, Bolan os PI, Guardiola PD, Alvarez de Armas MG, Meg TM. 2009. Importance of breastfeeding in the prevalence of metabolic syndrome and degree of childhood obesity. Endocrinol Nutr 56:400403. Demerath EW, Reed D, Choh AC, et al. 2009. Rapid postnatal weight gain and visceral adiposity in adulthood: the FELS longitudinal study. Obesity 17:20602066.

INFANT BMI STATUS AND WEIGHT GAIN IN CHINA Dennison BA, Edmunds LS, Stratton HH, Pruzek RM. 2006. Rapid infant weight gain predicts childhood overweight. Obesity 14:491499. Dietitians of Canada, Canadian Pediatric Society, The College of Family Physicians of Canada, Community Health Nurses Association of Canada. 2004. A health professionals guide to using growth charts. Paediatr Child Health 9:174176. ssner M, Borghi E. 2010. Global prevalence and trends of De Onis M, Blo overweight and obesity among preschool children. Am J Clin Nutr 92:12571264. Dietz WH. 1998. Childhood weight affects adult morbidity and mortality. J Nutr 128:411414. Dietz WH, Gortmaker SL. 2001. Preventing obesity in children and adolescents. Annu Rev Public Health 22:337353. Fu JF, Liang L, ZOU CC, Hong F, Wang CL, Wang XM, Zhao ZY. 2007. Prevalence of the metabolic syndrome in Zhejiang Chinese obese children and adolescents and the effect of metformin combined with lifestyle intervention. Int J Obes 31:1522. Gibson R. 2005. Principles of nutritional assessment. 2nd ed. New York, NY: Oxford University Press. Grummer-Strawn LM, Mei Z. 2004. Does breastfeeding protect against pediatric overweight? Analysis of longitudinal data from the Centers for Disease Control and Prevention Pediatric Nutrition Surveillance System. Pediatr 113:e81e86. Gunnarsdottir I, Thorsdottir I. 2003. Relationship between growth and feeding in infancy and body mass index at the age of 6 years. Int J Obes 27:15231527. Gunnell DJ, Frankel SJ, Nanchahal K, Peters TJ, Smith GD. 1998. Childhood obesity and adult cardiovascular mortality: A 57-y follow-up study based on the Boyd Orr cohort. Am J Clin Nutr 67:11111118. Heidari ST, Vakili MA Emamghorashi F. 2008. Longitudinal pattern and reference values of obesity indices of infants in Jahrom (Southern Region of ), Iran. Iran J Pediatr 18:3846. Hillier TA, Teresa, Pedula KL, Schmidt MM, Mullen JA, Charles M-A, Pettitt, DJ. 2007. Childhood obesity and metabolic imprinting. Diab Care 30:22872292. Himes J. 2009. Challenges of accurately measuring and using BMI and other indicators of obesity in children. Pediatrics 124:S3S22. Huang Q, Chen L, Ruan H, Liang J, Gu Y. 2009. Feeding status of 0$ 2 years infants in suburb of Guangzhou. Int Med Health Guidance News 15:58. Ji CY. 2008. The prevalence of childhood overweight/obesity and the epidemic changes in 1985-2000 for Chinese school-age children and adolescents. Obes Rev 9:7881. Ji Ch, Cheng TO. 2009. Epidemic increase in overweight and obesity in Chinese children from 1985 to 2005. Int J Cardiol 132:110. Jiang J, Urban R, Wang H, et al. 2007. Inuence of grandparents on eating behaviors of young children in Chinese three-generation families. Appetite 48:377383. Kimberly KM, Marlene BH, Hatim AO. 2009. Overweight children and adolescents: impact on psychological and social development. Int J Child Health Hum Dev 1:377384. Krebs NF, Jacobson MS. 2003. Prevention of pediatrics overweight and obesity. Pediatrics 112:424430. rvelin MR. 2001. Family social class, maternal Laitinen J, Power C, Ja body mass index, childhood body mass index, and age at menarche as predictors of adult obesity. Am J Clin Nutr 74:287294. Li H. 2005. How grandparents educated children in three-generation family. Preschool Res 6:2830 (in Chinese). Li L, Zhao A, Xu R. 2007. The association between birth weight and obesity of infants and toddlers. Chin Maternal Child Health 22:12051206 (in Chinese). Li XY, Wu Z, Wang T, Xu L, Gao J. 2006. Caesarean section rate and its inuence factors in China. Chin J Public Health 22:12 (in Chinese). Lu L. 2004. Advantage and disadvantage for grandparents caring. Child Family Education 10:68 (in Chinese).

639

Luo J, Hu FB. 2002. Time trends of obesity in pre-school children in China from 1989 to 1997. Int J Obes Relat Metab Disord 26:553558. McMillen C, Robinson JS. 2005. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Phys Rev 85:571633. Mei Z, Grummer-Strawn LM, Pietrobelli A, Goulding A, Goran M, Dietz W. 2002. Validity of body mass index compared with other body composition screening indexes for the assessment of body fatness in children and adolescents. Am J Clin Nutr 75:978985. Nash A, Secker D, Corey M, Dunn M, OConnor DL. 2008. Field testing of the 2006 World Health Organization growth charts from birth to 2 years: Assessment of hospital undernutrition and overnutrition rates and the usefulness of BMI. JPEN J Parenter Enteral Nutr 32:145153. Neeltje Vogels, Danielle LA Posthumus, Edwin CM, Mariman, et al. 2006. Determinants of overweight in a cohort of Dutch children. Am J Clin Nutr 84:717724. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. 2006. Prevalence of overweight and obesity in the United States, 1999 2004. JAMA 295:15491555. Oken E, Gillman MW. 2003. Fetal origins of obesity. Obes Res 11:496506. Ong KK, Loos RJF. 2006. Rapid infancy weight gain and subsequent obesity: Systematic reviews and hopeful suggestions. Acta Paediatrica 95:904908. Rudolf MCJ, Levine R, Feltbower R, Connor A, Robinson M. 2006. The TRENDS Project: Development of a methodology to reliably monitor the obesity epidemic in childhood. Arch Dis Child 91:309311. Sanigorski AM, Bell AC, Kremer PJ, Swinburn BA. 2007. High childhood obesity in an Australian population. Obesity 15:19081912. Spurgeon D. 2002. Childhood obesity in Canada has tripled in past 20 years. BMJ 324:1416. Stamatakis E, Primatesta P, Chinn S, Rona R, Falascheti E. 2005. Overweight and obesity trends from 1974 to 2003 in English children: What is the role of socioeconomic factors? Arch Dis Child 90:9991004. Stettler N, Zemel BS, Kumanyika S, Stallings VA. 2002. Infant weight gain and childhood overweight status in a multi-center, cohort study. Pediatr 109:194199. Stockton MB, Lanctot JQ, McClanahan BS, Klesges LM, Klesges RC, Kumanyika S, Sherrill-Mittleman D. 2009. Self-perception and body image associations with body mass index among 8-10-year-old African American girls. J Pediatr Psychol 34:11441154. Waterlow J, Buzina R, Keller W, Lane J, Nichaman M, Tanner J. 1977. The presentation and use of height and weight data for comparing the nutritional status of groups of children under the age of 10 years. Bull World Health Organ 55:489498. Whitaker C, Wright JA, Pepe MS, Seidel KD, Dietz WH. 1997. Prediction obesity in young adulthood from childhood and parental obesity. N Engl J Med 37:869873. WHO Working Group on the Growth Reference Protocol and the WHO Task Force on Methods for the Natural Regulation of Fertility. 2002. Growth of healthy infants and the timing, type, and frequency of complementary foods. Am J Clin Nutr 76:620627. WHO. 1995. Physical status: The use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser, 854. WHO. 2000. Obesity: Preventing and Managing the Global Epidemic. World Health Organization Technical Support Series No. 894. Geneva, Switzerland: World Health Organization. WHO Multicentre Growth Reference Study Group, 2006. WHO child growth standards based on length/height, weight and age. Acta Paediatr Suppl 450:7685. Yi M, Sun D, Zhou X. 2002. A Case-control Study on Association between Infant Breastfeeding and Obesity Preschool Children. Acta Academica Med Qingdao Univ 38:206208. Zheng K, Zhang X, Li L, Shu Y, Qiu L. 2008. Impact factors of breastfeeding during hospital stay after neonate birth in Hangzhou city. Chin J of Child Health Care 16:716718 (in Chinese).

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