Ethnic and sex differences in skeletal maturation among the Birth to Twenty cohort in South Africa

Tim J Cole, Emily K Rousham, Nicola L Hawley, Noel Cameron, Shane A Norris, John M Pettifor, Tim J Cole, Emily K Rousham, Nicola L Hawley, Noel Cameron, Shane A Norris, John M Pettifor

Abstract

Aim: To examine ethnic and sex differences in the pattern of skeletal maturity from adolescence to adulthood using a novel longitudinal analysis technique (SuperImposition by Translation And Rotation (SITAR)).

Setting: Johannesburg, South Africa.

Participants: 607 boys and girls of black as well as white ethnicity from the Birth to Twenty bone health study, assessed annually from 9 to 20 years of age.

Outcome measure: Bone maturity scores (Tanner-Whitehouse III radius, ulna, and short bones (TW3 RUS)) assessed longitudinally from hand-wrist radiographs were used to produce individual and mean growth curves of bone maturity and analysed by the SITAR method.

Results: The longitudinal analysis showed that black boys matured later by 7.0 SE 1.6 months (p<0.0001) but at the same rate as white boys, whereas black girls matured at the same age but at a faster rate than white girls (by 8.7% SE 2.6%, p=0.0007). The mean curves for bone maturity score consistently showed a midpubertal double kink, contrasting with the quadratic shape of the commonly used reference centile curves for bone maturity (TW3).

Conclusions: Skeletal maturity was reached 1.9 years earlier in girls than boys, and the pattern of maturation differed between the sexes. Within girls, there were no ethnic differences in the pattern or timing of skeletal maturity. Within boys, however, skeletal maturity was delayed by 7 months in black compared with white ethnicity. Skeletal maturation, therefore, varies differentially by sex and ethnicity. The delayed maturity of black boys, but not black girls, supports the hypothesis that boys have greater sensitivity to environmental constraints than girls.

Keywords: Adolescent Health; Growth.

Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions.

Figures

Figure 1
Figure 1
Individual and mean curves of radius, ulna and short bones (RUS) bone maturity score in boys by ethnicity analysed by SuperImposition by Translation And Rotation. (A) White boys: individual unadjusted curves. (B) White boys: individual curves adjusted for tempo and velocity, with the mean adjusted curve. (C) Black boys: individual unadjusted curves. (D) Black boys: individual curves adjusted for tempo and velocity, with the mean adjusted curve.
Figure 2
Figure 2
Individual and mean curves of radius, ulna and short bones (RUS) bone maturity score in girls by ethnicity analysed by SuperImposition by Translation And Rotation. (A) White girls: individual unadjusted curves. (B) White girls: individual curves adjusted for tempo and velocity, with the mean adjusted curve. (C) Black girls: individual unadjusted curves. (D) Black girls: individual curves adjusted for tempo and velocity, with the mean adjusted curve.
Figure 3
Figure 3
Mean curves by sex and ethnicity of radius, ulna and short bones (RUS) bone maturity score in the Birth to Twenty subsample compared with the Tanner–Whitehouse III (TW3) reference (25th, 50th and 75th centiles). V indicates the median age of attaining adult bone maturity (RUS bone maturity score of 1000) in each group.

References

    1. Eveleth PB, Tanner JM. Worldwide variation in human growth. 2nd edn Cambridge: Cambridge University Press, 1990:1–395.
    1. Tanner JM, Healy MJR, Goldstein H, et al. Assessment of skeletal maturity and prediction of adult height (TW3 method). 3rd edn London: W B Saunders Ltd., 2001:1–110.
    1. Hawley NL, Rousham EK, Johnson W, et al. Determinants of relative skeletal maturity in South African children. Bone 2012;50:259–64.
    1. Cole TJ, Cole AJL. Bone age, social deprivation, and single parent families. Arch Dis Child 1992;67:1281–5.
    1. Pathmanathan G, Raghaven P. Bone age based linear growth and weight of underprivileged North-West Indian children compared with their well-off North-West Indian peers. J Anat Soc India 2006;55:34–42.
    1. Hawley NL, Rousham EK, Norris SA, et al. Secular trends in skeletal maturity in South Africa: 1962–2001. Ann Hum Biol 2009;22:353–9.
    1. Freitas D, Malina RM, Maia J, et al. Short-term secular change in height, body mass and Tanner-Whitehouse 3 skeletal maturity of Madeira youth, Portugal. Ann Hum Biol 2012;39:195–205.
    1. Tanner JM, Landt KW, Cameron N, et al. Prediction of adult height from height and bone-age in childhood. Arch Dis Child 1983;58:767–76.
    1. Richter L, Norris S, Pettifor J, et al. Cohort profile: Mandela's children: the 1990 Birth to Twenty study in South Africa. Int J Epidemiol 2007;36:504–11.
    1. Richter L, Norris SA, de Wet T. Transition from Birth to Ten to Birth to Twenty: the South African cohort reaches 13 years of age. Paediatr Perinat Epidemiol 2004;18:290–301.
    1. Cole TJ, Donaldson MD, Ben-Shlomo Y. SITAR—a useful instrument for growth curve analysis. Int J Epidemiol 2010;39:1558–66.
    1. Cole TJ, Pan H, Butler GE. A mixed effects model to estimate timing and intensity of pubertal growth from height and secondary sexual characteristics. Ann Hum Biol 2014;41:76–83.
    1. Schwartz G. Estimating the dimension of a model. Ann Statist 1978;6:461–4.
    1. Merrell M. The relationship of individual growth to average growth. Hum Biol 1931;3:37–70.
    1. Cole TJ, Cortina Borja M, Sandhu J, et al. Nonlinear growth generates age changes in the moments of the frequency distribution: the example of height in puberty. Biostatistics 2008;9:159–71.
    1. Cole TJ. Sympercents: symmetric percentage differences on the 100 loge scale simplify the presentation of log transformed data. Stat Med 2000;19:3109–25.
    1. Stinson S. Sex differences in environmental sensitivity during growth and development. Yearbook Phys Anthropol 1985;28:12–148.
    1. McCance RA, Widdowson EM. Review lecture- determinants of growth and form. Proc Royal Soc B Biol Sci 1974;185:1–17.
    1. Jones LL, Griffiths PL, Norris SA, et al. Is puberty starting earlier in urban South Africa? Am J Hum Biol 2009;21:395–7.
    1. Jones LL, Griffiths PL, Norris SA, et al. Age at menarche and the evidence for a positive secular trend in urban South Africa. Am J Hum Biol 2009;21:130–2.
    1. Biro FM, Greenspan LC, Galvez MP, et al. Onset of breast development in a longitudinal cohort. Pediatrics 2013;132:1019–27.
    1. Herman-Giddens ME, Steffes J, Harris D, et al. Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings Network. Pediatrics 2012;130:e1058–68.
    1. Whitehouse WA, Tanner JM. Variations in the pattern of pubertal changes in girls. Arch Dis Child 1969;44:291–303.
    1. Whitehouse WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child 1970;45:13–23.
    1. Tanner JM, Whitehouse RH, Takaishi M. Standards from birth to maturity for height, weight, height velocity, and weight velocity: British children, 1965 Part I. Arch Dis Child 1966;41:454–71.
    1. Tanner JM, Whitehouse RH, Takaishi M. Standards from birth to maturity for height, weight, height velocity, and weight velocity: British children, 1965 Part II. Arch Dis Child 1966;41:613–35.
    1. Peto R. The horse-racing effect. Lancet 1981;2:467–8.
    1. Rousham EK. Gender bias in South Asia: effects on child growth and nutritional status. In: Pollard TM, Hyatt SB. eds. Sex, gender and health. Cambridge: Cambridge University Press, 1999:37–52.

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