Skip to main content
Log in

Bone growth patterns in Chinese children and adolescents: a 6-year follow-up study provides evidence for sexual dimorphism and tracking

  • Original Article
  • Published:
Archives of Osteoporosis Aims and scope Submit manuscript

Abstract

Summary

We prospectively examined bone growth patterns in 894 children aged 6–17 years at the baseline visit, with a 6-year follow-up. Results show bone “tracking” over a six-year interval and sexual dimorphism of bone attained levels and timing of peak bone growth. Our findings underscore childhood and adolescence as critical periods for building bone and developing gender differences.

Introduction

Bone growth patterns were prospectively examined in 894 Chinese children (496 males), aged 6–17 yrs, from a population-based twin cohort. Whole-body bone area (BA), bone mineral content (BMC), and bone mineral density (BMD) were measured by DEXA at baseline and a 6-yr follow-up.

Methods

Graphic smoothing plots and generalized estimating equations were used to model bone attained levels, growth, and “tracking”.

Results

Attained levels of BMC and BA increased curvilinearly with age. Male attained levels were higher than females after age ∼15 yr, but BMD was lower between 13–17 yrs (Tanner stage I to IV). In both genders, peak BMC and BMD growth lagged ∼2 yrs behind peak BA growth, which lagged 2 yrs behind peak height growth. Peak bone growth occurred 1–3 yrs later in males. Over the 6-yr follow-up, all bone measurements “tracked”, but “shifting” across ranks also occurred, and baseline tertile ranking influenced bone growth. Females with early menarche had higher attained levels than females with late menarche at age 12–13 yrs.

Conclusion

Our findings confirm and expand previous studies on peak bone growth conducted in Caucasian cohorts, particularly sexually dimorphic and maturational effects. The significant “tracking” of bone measurements in this 6-yr follow-up study underscores the importance that osteoporosis prevention should begin in childhood and adolescence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

DEXA:

Dual energy X-ray absorptiometry

SD:

Standard deviation

BMC:

Bone mineral content,

BMD:

Bone mineral density

BA:

Bone area

CI:

Confidence interval

References

  1. Lane JM, Serota AC, Raphael B (2006) Osteoporosis: differences and similarities in male and female patients. Orthop Clin North Am 37(4):601–609

    Article  PubMed  Google Scholar 

  2. Cooper C, Campion G, Melton LJ, 3rd (1992) Hip fractures in the elderly: a world-wide projection. Osteoporos Int 2(6):285–289

    Article  PubMed  CAS  Google Scholar 

  3. Lau EM, Cooper C (1996) The epidemiology of osteoporosis. The oriental perspective in a world context. Clin Orthop Relat Res (323):65–74

  4. Bonjour JP, Rizzoli R (1996) Bone acquisition in adolescence In: Marcus R, Feldman DJK (eds) Osteoporosis. Academic, San Diego, CA, pp465–476

    Google Scholar 

  5. Theintz G, Buchs B, Rizzoli R, Slosman D, Clavien H, Sizonenko PC, Bonjour JP (1992) Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 75(4):1060–1065

    Article  PubMed  CAS  Google Scholar 

  6. Krabbe S, Christiansen C, Rodbro P, Transbol I (1979) Effect of puberty on rates of bone growth and mineralisation. Arch Dis Child 54:950–953

    PubMed  CAS  Google Scholar 

  7. Cadogan J, Blumsohn A, Barker ME, Eastell R (1998) A Longitudinal Study of Bone Gain in Pubertal Girls: Anthropometric and Biochemical Correlates. J bone miner res 13(10):1602–1612

    Article  PubMed  CAS  Google Scholar 

  8. Ito M, Yamada M, Hayashi K, Ohki M, Uetani M, Nakamura T (1995) Relation of early menarche to high bone mineral density. Calcif Tissue Int 57(1):11–14

    Article  PubMed  CAS  Google Scholar 

  9. Van Coeverden SC, De Ridder CM, Roos JC, Van’t Hof MA, Netelenbos JC, Delemarre-Van de Waal HA (2001) Pubertal maturation characteristics and the rate of bone mass development longitudinally toward menarche. J Bone Miner Res 16(4):774–781

    Article  PubMed  Google Scholar 

  10. Rauch F, Klein K, Allolio B, Schonau E (1999) Age at menarche and cortical bone geometry in premenopausal women. Bone 25(1):69–73

    Article  PubMed  CAS  Google Scholar 

  11. Wang X, Wang B, Zhang F, Chen C, Yang J, Fang Z, Zhang X, Christiani DC, Weiss, ST et al (1998) Blood pressure at age 3–24 years in a rural community in Anhui, China. Ann Epidemiol 8(8):504–512

    Article  PubMed  CAS  Google Scholar 

  12. Wang Y, Ge K, Popkin BM (2000) Tracking of body mass index from childhood to adolescence: a 6-y follow-up study in China. Am J Clin Nutr 72(4):1018–1024

    PubMed  CAS  Google Scholar 

  13. Bundak R, Darendeliler F, Gunoz H, Bas F, Saka N, Neyzi O (2006) Analysis of puberty and pubertal growth in healthy boys. Journal article Eur J Pediatr DOI 10.1007/s00431-006-0293-y [Epub ahead of print]

  14. Ferrari S, Rizzoli R, Slosman D, Bonjour JP (1998) Familial resemblance for bone mineral mass is expressed before puberty. J Clin Endocrinol Metab 83:358–361

    Article  PubMed  CAS  Google Scholar 

  15. Ferrari SL, Chevalley T, Bonjour JP, Rizzoli R (2006) Childhood fractures are associated with decreased bone mass gain during puberty: an early marker of persistent bone fragility? J Bone Miner Res 21(4):501–507

    Article  PubMed  Google Scholar 

  16. Magarey AM, Boulton TJ, Chatterton BE, Schultz C, Nordin BE, Cockington RA (1999) Bone growth from 11 to 17 years: relationship to growth, gender and changes with pubertal status including timing of menarche. Acta Paediatr 88(2):139–146

    Article  PubMed  CAS  Google Scholar 

  17. Ruff C (2005) Growth tracking of femoral and humeral strength from infancy through late adolescence. Acta Paediatr 94(8):1030–1037

    Article  PubMed  Google Scholar 

  18. Loro ML, Sayre J, Roe TF, Goran MI, Kaufman FR, Gilsanz V (2000) Early identification of children predisposed to low peak bone mass and osteoporosis later in life. J Clin Endocrinol Metab 85(10):3908–3918

    Article  PubMed  CAS  Google Scholar 

  19. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM (1993) Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet 341(8837):72–75

    Article  PubMed  CAS  Google Scholar 

  20. Heaney RP (2005) BMD: The problem. Osteoporos Int 16:1013–1015

    Article  PubMed  Google Scholar 

  21. Wu XP, Yang YH, Zhang H, Yuan LQ, Luo XH, Cao XZ, Liao EY (2005) Gender differences in bone density at different skeletal sites of acquisition with age in Chinese children and adolescents. J Bone Miner Metab 23(3):253–260

    Article  PubMed  Google Scholar 

  22. Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA (1999) A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the university of Saskatchewan bone mineral accrual study. J Bone Miner Res 14(10):1672–1679

    Article  PubMed  CAS  Google Scholar 

  23. Bailey DA, Wedge JH, McCulloch RG, Martin AD, Bernhardson SC (1989) Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am 71(8):1225–1231

    PubMed  CAS  Google Scholar 

  24. Blimkie CJ, Lefevre J, Beunen GP, Renson R, Dequeker J, Van Damme P (1993) Fractures, physical activity, and growth velocity in adolescent Belgian boys. Med Sci Sports Exerc 25(7):801–808

    Article  PubMed  CAS  Google Scholar 

  25. Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–303

    Article  PubMed  CAS  Google Scholar 

  26. Marshall WA, Tanner JM (1970) Variations in pattern of pubertal changes in boys. Arch Dis Child 45:13–23

    PubMed  CAS  Google Scholar 

  27. Cleveland WS (1979) Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74:829–836

    Article  Google Scholar 

  28. Rodriguez RN, Strokes ME (1998) Recent enhancements and new directions in SAS/STAT Software, Part II. Nonparametric modeling procedure 1262–1270

  29. SAS Institute (1997) SAS/STAT Software: Changes and Enhancements through Release 6.12. Cary, NC

    Google Scholar 

  30. Lu PW, Briody JN, Ogle GD, Morley K, Humphries IR, Allen J, Howman-Giles R, Sillence D, Cowell CT (1994) Bone mineral density of total body, spine, and femoral neck in children and young adults: a cross-sectional and longitudinal study. J Bone Miner Res 9(9):1451–1458

    PubMed  CAS  Google Scholar 

  31. Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus R (1999) Bone mineral acquisition in healthy Asian, Hispanic, black, and Caucasian youth: a longitudinal study. J Clin Endocrinol Metab 84(12):4702–4712

    Article  PubMed  CAS  Google Scholar 

  32. Fournier PE, Rizzoli R, Slosman DO, Theintz G, Bonjour JP (1997) Asynchrony between the rates of standing height gain and bone mass accumulation during puberty. Osteoporos Int 7(6):525–532

    Article  PubMed  CAS  Google Scholar 

  33. Molgaard C, Thomsen BL, Michaelsen KF (1999) Whole body bone mineral accretion in healthy children and adolescents. Arch Dis Child 81(1):10–15

    PubMed  CAS  Google Scholar 

  34. Braillon PM (2003) Annual changes in bone mineral content and body composition during growth. Horm Res 60(6):284–290

    Article  PubMed  CAS  Google Scholar 

  35. van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, de Muinck Keizer-Schrama SM (2002) Reference data for bone density and body composition measured with dual energy x ray absorptiometry in white children and young adults. Arch Dis Child 87(4):341–347

    Article  PubMed  Google Scholar 

  36. Vanderschueren D, Bouillon R (1995) Androgens and bone. Calcif Tissue Int 56:341–346

    Article  PubMed  CAS  Google Scholar 

  37. Bonjour JP, Theintz G, Buchs B, Slosman D, Rizzoli R (1991) Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab 73(3):555–563

    Article  PubMed  CAS  Google Scholar 

  38. Ho AY, Kung AW (2005) Determinants of peak bone mineral density and bone area in young women. J Bone Miner Metab 23(6):470–475

    Article  PubMed  Google Scholar 

  39. Guo Y, Zhao LJ, Shen H, Guo Y, Deng HW (2005) Genetic and environmental correlations between age at menarche and bone mineral density at different skeletal sites. Calcif Tissue Int 77(6):356–360

    Article  PubMed  CAS  Google Scholar 

  40. Rice S, Blimkie CJ, Webber CE, Levy D, Martin J, Parker D, Gordon CL (1993) Correlates and determinants of bone mineral content and density in healthy adolescent girls. Can J Physiol Pharmacol 71(12):923–930

    PubMed  CAS  Google Scholar 

  41. Boot AM, de Ridder MA, Pols HA, Krenning EP, de Muinck Keizer-Schrama SM (1997) Bone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity. J Clin Endocrinol Metab 82(1):57–62

    Article  PubMed  CAS  Google Scholar 

  42. Rosenthal DI, Mayo-Smith W, Hayes CW, Khurana JS, Biller BMK, Neer RM, Klibanski A (1989) Age and bone mass in premenopausal women. J Bone Miner Res 4:533–538

    PubMed  CAS  Google Scholar 

  43. Sowers MFR, Clark MK, Hollis B, Wallace RB, Jannausch M (1992) Radial bone mineral density in pre- and perimenopausal women: a prospective study of rates and risk factors for loss. J Bone Miner Res 7:647–657

    Article  PubMed  CAS  Google Scholar 

  44. Rizzoli R, Bonjour JP (1999) Determinants of peak bone mass and mechanisms of bone loss. Osteoporos Int 9(2):S17–S23

    Article  PubMed  Google Scholar 

  45. Bass S, Pearce G, Bradney M, Hendrich E, Delmas PD, Harding A, Seeman E (1998) Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts.J Bone Miner Res 13(3):500–507

    Article  PubMed  CAS  Google Scholar 

  46. Kumar R, Wang B, Wang X, Chen C, Yang J, Fu L, Xu X (2006) Bronchodilator responses in Chinese children from asthma index families and the general population. J Allergy Clin Immunol 117(6):1257–1263

    Article  PubMed  Google Scholar 

Download references

Conflict of interest statement

None of the authors have a conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaobin Wang.

Additional information

Fengxiu Ouyang and Binyan Wang contributed equally to this article.

Source(s) of support: This study is supported in part by grant R01 HD049059, R01 HL0864619 and R01 AR045651 from the National Institute of Health and by the Food Allergy Project.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ouyang, F., Wang, B., Arguelles, L.M. et al. Bone growth patterns in Chinese children and adolescents: a 6-year follow-up study provides evidence for sexual dimorphism and tracking. Arch Osteoporos 2, 29–43 (2007). https://doi.org/10.1007/s11657-007-0015-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11657-007-0015-8

Keywords

Navigation