The Relationship of Rapid Weight Gain in Infancy to Obesity and Skeletal Maturity in Childhood
Department of Human Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU, United Kingdom. E-mail: N.Cameron@lboro.ac.uk
Objective: Children with birth weight appropriate for gestational age (AGA) who also demonstrate rapid weight gain in infancy have a greater risk of being overweight or obese during childhood. A concurrent advancement in skeletal maturity would account for their greater size and would, therefore, not necessarily pose a threat of greater risk during adolescence and early adulthood. This study aims to determine whether children with rapid weight gain during infancy have advanced skeletal maturity during childhood.
Research Methods and Procedures: One hundred and ninety-three African children (boys = 108; girls = 85) of normal birth weight and gestational age were assessed from birth to 9 years. Body composition was assessed at 9 years of age by whole-body DXA, and skeletal maturity was assessed using the Tanner-Whitehouse II technique. Rapid weight gain in infancy was defined as a +0.67 change in weight-for-age Z-score between birth and 2 years.
Results: Rapid weight gain was experienced by over 20% of the sample. Children with rapid weight gain were significantly lighter at birth and significantly taller, heavier, and fatter throughout childhood. Chronological age and Tanner-Whitehouse II technique skeletal ages at 9 years were not significantly different between groups or between sexes within groups.
Discussion: Because AGA children with rapid weight gain have a greater risk of overweight and obesity but are not advanced in skeletal maturity, later adolescent adjustments toward average weight and fatness values are unlikely. The identification and monitoring of such children is of importance in reducing their risk of morbidity.
The ability of children to demonstrate catch-up growth has been recognized for almost four decades (1) and is characterized by an increased growth velocity in height and/or weight after the removal of some constraint on normal growth. This increased velocity brings the child's height-for-age or weight-for-age status back toward the normal centiles, and in the best-case scenario, actually returns the child's growth pattern to its preinsult status (2). In addition to catch-up growth occurring after the removal of an insult in childhood and adolescence, catch-up growth also occurs during infancy. In this scenario, the rationale is that the growth of the fetus had been constrained, and when freed from this constraint, the affected infant demonstrates rapid growth to reach its genetically determined growth canal (3). The focus of previous research on catch-up growth in infancy has generally been on children who were small for gestational age (SGA)1 at birth and who were thus thought to have suffered from intrauterine growth retardation as a result of factors other than maternal size.
Rapid growth during infancy in children who have not been suffering from intrauterine insult and are not SGA has been the focus of more recent research (4, 5, 6, 7). These authors have identified that rapid growth in infancy, which they term catch-up growth, is associated with an increase in childhood risk factors for overweight and obesity. Such children had significantly greater weights, heights, and fatness later in childhood and a more centralized fat distribution (6). Cameron (4), in an analysis of South African urban children, was able to conclude that the majority of such children were overweight by 2 years of age and more likely to be classified as obese by 9 years of age.
Although SGA children who demonstrate rapid weight gain in infancy are known to enter puberty earlier (8, 9, 10), no such information is yet available on children who had birthweights that were appropriate for gestational age (AGA) and absolutely no information is available on skeletal maturity. Obesity and overweight are associated with advanced maturity, both sexual and skeletal, in normal children (11, 12). Such advancement in AGA children with rapid weight gain in infancy would account for their greater size during childhood and thus not necessarily pose a threat of greater risk during adolescence and early adulthood.
This paper reports on the skeletal maturity of normal South African urban African children who demonstrate rapid weight gain during infancy.
Research Methods and Procedures
The sample for analysis was obtained from the Birth—to– Twenty birth cohort study set in the urban conurbation of Soweto-Johannesburg, South Africa (13). Participants were assessed at birth, 3 months, 6 months, and at 1, 2, 4, 5, 8, 9, and 10 years of age. Not all children were assessed on all measurement occasions, resulting in a mixed-longitudinal study design. On each assessment occasion, measurements of height, weight, head and arm circumferences, and skinfolds at the triceps and subscapular sites were taken. At 9 years, a subsample of the participants was enrolled into a bone health study to investigate factors affecting the acquisition of peak bone mass. In addition to the standard anthropometric measurements and pubertal status using Tanner stage, these children also had whole body DXA scans using an Hologic 4500A (Hologic, Inc., Waltham, MA) and, thus, assessments of bone densities and body composition. Skeletal maturity was also assessed by a single trained observer using the Tanner-Whitehouse II technique (TWII) (14) to determine bone age using 20 bones (TWII 20), the radius, ulna, metacarpals, and phalanges, and the carpal bones. The radiation exposure involved in obtaining hand-wrist radiographs is typically 0.01 milliSieverts (mSv) per radiograph. Background radiation dosage in the UK, i.e., the dosage to which everyone is exposed, is 2.2 mSv per annum. Thus, a hand-wrist radiograph exposes the child to the radiation dosage that he/she would naturally receive in 1.7 days in the UK and is one-fiftieth of the World Health Organization's recommended maximum dosage to children involved in research projects (0.5 mSv) (15).
The subsample for the current analysis was constrained by ethnicity, birth weight, gestational age, and completeness of both DXA and hand-wrist radiograph data. One hundred and ninety-three children (boys = 108; girls = 85) were identified with African ethnicity, complete weight data at birth and 2 years, birthweights within the sample mean ±2 Z-scores (2187 to 4082 g), normal gestational ages (36 to 40 weeks), and complete DXA and bone age data. There were no significant differences between the main sample and the subsample of DXA participants for any anthropometric variable throughout the 9 years of the study apart from triceps skinfold at 2 years that differed on average by 0.65 mm (t = −2.67, p = 0.01) and maternal heights that differed by 1.6 cm (t = −2.56; p = 0.01). Neither difference was thought to be germane to the current analysis. One hundred and fifty-two children were in Tanner stage 1 for both pubic hair (PH) and genitalia or breast (G/B), 22 were in Tanner stages PH1/GB2, 6 were in Tanner stages PH2/GB1, and 13 in Tanner stages PH2/GB2. All girls were premenarcheal. Thus, all participants were either prepubertal or in early puberty, and in view of the well-recognized lack of association between skeletal and sexual maturity (16, 17), it was not thought appropriate to consider pubertal status in the current analysis.
Rapid growth was defined by a change in Z-score of weight-for-age between birth and 2 years >0.67 (6). This change was equivalent to a change of one centile band within the UK reference data, i.e., from the 25th to 50th centiles, 50th to 75th centiles, and so on. Statistical analysis was carried out using CSS:Statistica software (Statsoft, Tulsa, OK). All procedures were approved by the Human Ethics Committees of the Faculty of Health Sciences of the University of the Witwatersrand, South Africa and Loughborough University, UK.
Rapid weight gain was experienced by 42 children (21.8%; boys = 23; girls = 19) and normal weight gain by 151 (78.2%; boys = 85; girls = 66). The proportions of boys and girls within the groups were not significantly different (χ2 = 0.02; p = 0.88). No significant differences between these groups were observed for gravidity, parity, maternal age, maternal height, maternal weight, or socio-economic status. In common with previous analyses (6), the children with rapid weight gain were significantly lighter at birth (2982 vs. 3206 g; t = 3.39; p = 0.00) and significantly taller and heavier from age 1 to 9 years in the study and fatter (greater subcutaneous skinfolds) from 5 years of age. At 9 years, they were 3.8 cm taller and 3.8 kg heavier with 3.7% greater body fat (Table 1). Differences in DXA values and anthropometric variables were not significant when controlled for height and weight. When controlling for body mass index (BMI), however, significant differences persisted in the sum of subcutaneous skinfolds (F = 5.03, p = 0.026), fat weight (F = 8.21, p = 0.005), and lean tissue mass (F = 5.93, p = 0.016). Thus, the rapid weight gain group had significantly greater subcutaneous fat, total body fat, and lean tissue for equivalent BMIs.
Table 1. Comparisons of the means ± SD of anthropometric and body composition values at 9 years of age between children exhibiting normal weight increments (n = 151) and those with rapid weight gain in infancy (n = 42)
|Birthweight (g)||3206 ± 362||2982 ± 433||3.39||0.001|
|Weight (kg)||28.6 ± 4.43||32.4 ± 7.10||−4.24||0.000|
|Height (cm)||132.0 ± 5.6||135.8 ± 5.0||−3.87||0.000|
|BMI (kg/m2)||16.39 ± 2.45||17.47 ± 3.12||−2.39||0.018|
|Waist circumference (cm)||56.63 ± 5.29||59.70 ± 7.37||−3.03||0.003|
|Hip circumference (cm)||63.38 ± 7.15||66.77 ± 9.24||−2.55||0.012|
|Sum skinfolds* (mm)||54.06 ± 19.11||65.41 ± 22.96||−3.30||0.001|
|BMC (g)||902.73 ± 132.95||959.36 ± 149.31||−2.38||0.019|
|Fat weight (kg)||7.31 ± 3.34||9.76 ± 5.43||−3.62||0.000|
|LTM (kg)||20.16 ± 2.47||21.58 ± 2.63||−3.22||0.002|
|Percentage fat||24.99 ± 7.94||28.74 ± 9.08||−2.62||0.010|
|Chronological age (years)||9.51 ± 0.27||9.50 ± 0.25||0.43||0.666|
|TWII (20) skeletal age (years)||9.38 ± 0.94||9.50 ± 1.04||−0.84||0.403|
|RUS skeletal age (years)||9.44 ± 1.07||9.56 ± 1.04||−0.70||0.485|
|CARP skeletal age (years)||9.37 ± 0.97||9.52 ± 1.15||−0.83||0.409|
Chronological age and TWII skeletal ages at 9 years were not significantly different. They were also not significantly different between the sexes in either rapid weight gain or normal weight gain groups.
The significantly greater sizes of AGA birth weight children who demonstrate rapid weight gain do not seem to be caused by advanced skeletal maturity in late childhood. Rapid growth in infancy would be consistent with skeletal delay, but as no measures of skeletal maturity are available for that time, it can only be stated that any such delay, if it occurred, was not apparent by 9 years of age.
It should be emphasized that AGA children with rapid weight gain are not simply demonstrating regression to the mean. Regression to the mean would require mean anthropometric values to be close to the mean, and that is not the case. The heights, weights, and measures of body composition of children with rapid weight gain approximate the 75th centiles of reference data (18), whereas those of the normal weight gain group are on or near the 50th centile. The greater size of AGA rapid weight gain children does not seem to be genetically determined, because maternal height was similar for both rapid weight gain and normal weight gain children. No information is available on paternal statures.
AGA children with rapid weight gain in infancy are characterized by normal to lower birthweights, significantly greater height and weight during childhood, and significantly greater subcutaneous fat, total body fat, and lean tissue at equivalent BMIs. Their skeletal maturity is consistent with chronological age in late childhood and with the skeletal maturities of their peers who did not demonstrate rapid growth in infancy. Because these children have a greater risk of overweight and obesity (4, 5, 6, 7) but are not advanced in skeletal maturity, later adolescent adjustments toward relatively lower weight and fatness values are unlikely. The identification and monitoring of such children is, therefore, of importance in reducing their risk of morbidity.
The Birth-to-Twenty birth cohort study receives financial and logistic support from the Urbanization and Health Program of the Medical Research Council of South Africa; Anglo-American Chairman's Fund; Child, Youth and Family Development of the Human Sciences Research Council of South Africa; and the University of the Witwatersrand. The Bone Health study is financially supported by the Wellcome Trust (UK).
Nonstandard abbreviations: SGA, small for gestational age; AGA, appropriate for gestational age; TWII, Tanner-Whitehouse II technique; PH, pubic hair; G/B, genitalia or breast; BMI, body mass index.