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Bone mineral density in girls and boys at different pubertal stages: relation with gonadal steroids, bone formation markers, and growth parameters

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Abstract

Puberty has a key role in bone development. During puberty, several nutritional and hormonal factors play a major role in this process. The aim of this study was to determine the changes in areal bone mineral density (BMD), gonadal steroids, bone formation markers, and growth parameters in healthy Turkish pubertal girls and boys at different pubertal stages. In additional, we aimed to detect the relationship between BMD, sex steroids, and growth parameters, and to reveal the most important determinant of BMD in the pubertal period. BMD of the lumbar spine and total body was performed by dual-energy X-ray absorptiometry (Lunar DPX series) in 174 healthy pubertal children (91 girls, 83 boys), aged 11–15 years. Height and weight were measured. Pubertal stages were assesed. Bone formation markers and gonadal steroids were measured. BMD values significantly increased until stage IV in girls. In boys, BMD values also increased during puberty (P < 0.05), but it was significantly higher in stage IV compared with that in other pubertal stages (P < 0.01). Testosterone levels increased until stage IV in both sexes, particularly in boys. Estrogen levels significantly increased during puberty in girls, whereas it was significantly higher at stage IV in boys (P < 0.001). Bone-specific alkaline phosphatase (BAP) level was higher in early and midpuberty, and decreased in late puberty in girls (P < 0.001). BAP level was higher in stage IV in boys. Osteocalcin level was shown not to change significantly in pubertal stages. There was a modest correlation between BMD values and estrogen and testosterone levels in boys. In girls, there was a correlation between BMD values and estrogen levels only (P < 0.05). Weight was significantly associated with BMD in both sexes (P < 0.05). Estrogen had a significant influence on BMD in boys and girls. In conclusion, bone mass increased throughout puberty in both sexes. Peak bone mass was not achieved in girls, but was obtained at stage IV in boys. Bone formation markers were good predictors of bone mass in girls, but not in boys. Estrogen level made the greatest contribution to bone mineral acquisition in boys and girls. The achievement of peak bone mass was sustained by estrogen in boys. The major independent determinant of BMD in both sexes was weight.

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References

  1. GB Forbes (1988) ArticleTitleSome remarks on bone mineralization J Pediatr 113 167–171 Occurrence Handle3392637

    PubMed  Google Scholar 

  2. RN Southard JD Morris JD Mahan JR Hayes MA Torch A Sommer WB Zipf (1991) ArticleTitleBone mass in healthy children: measurement with quantitative DXA Radiology 179 735–738 Occurrence Handle2027984

    PubMed  Google Scholar 

  3. G Saggese GI Baroncelli S Bertelloni (2000) ArticleTitlePuberty and bone development Best Pract Res Clin Endocrinol Metab 16 53–64 Occurrence Handle10.1053/beem.2001.0180

    Article  Google Scholar 

  4. V Matkovic (1996) ArticleTitleSkeletal development and bone turnover revisited J Clin Endocrinol Metab 81 2013–2016 Occurrence Handle10.1210/jc.81.6.2013 Occurrence Handle8964819

    Article  PubMed  Google Scholar 

  5. G Saggese S Bertelloni GI Baroncelli (1997) ArticleTitleSex steroids and the acquisition of bone mass Horm Res 48 65–71 Occurrence Handle9434047

    PubMed  Google Scholar 

  6. AD Rogol PA Clark JN Roemmich (2000) ArticleTitleGrowth and pubertal development in children and adolescents: effects of diet and physical activity Am J Clin Nutr 72 521–528

    Google Scholar 

  7. O Arisaka M Hoshi S Kanazawa M Numata D Nakajima S Kanno M Negishi K Nishikura A Nitta M Imataka T Kurubayashi K Kano (2001) ArticleTitleEffect of adrenal androgen and estrogen on bone maturation and bone mineral density Metabolism 50 377–379 Occurrence Handle10.1053/meta.2001.21678 Occurrence Handle11288028

    Article  PubMed  Google Scholar 

  8. CW Slemenda TK Reister SL Hui JZ Miller JC Christian CC Johnston (1994) ArticleTitleInfluence on skeletal mineralization in children and adolescents: evidence for varying effects of sexual maturation and physical activity J Pediatr 125 201–207 Occurrence Handle8040762

    PubMed  Google Scholar 

  9. L Dunkel S Wickman (2003) ArticleTitleNovel treatment of short stature with aromatase inhibitors J Steroid Biochem Mol Biol 86 345–356 Occurrence Handle10.1016/S0960-0760(03)00344-3 Occurrence Handle14623531

    Article  PubMed  Google Scholar 

  10. L Del Rio A Carrascosa F Pons M Gusinye D Yeste FM Domenech (1994) ArticleTitleBone mineral density of the lumbar spine in white Mediterranean children, and adolescent changes related to age, sex and puberty Pediatr Res 35 362–366 Occurrence Handle8190528

    PubMed  Google Scholar 

  11. H Plotkin M Nunez ML Alvarez Filgueira JR Zanchetta (1996) ArticleTitleLumbar spine bone density in Argentine children Calcif Tissue Int 58 144–149 Occurrence Handle10.1007/s002239900025 Occurrence Handle8852568

    Article  PubMed  Google Scholar 

  12. AM Boot AJ de Ridder APH Pols (1997) ArticleTitleBone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity J Clin Endocrinol Metab 82 57–62 Occurrence Handle10.1210/jc.82.1.57 Occurrence Handle8989233

    Article  PubMed  Google Scholar 

  13. J Bonjour G Theintz B Buchs D Slosman R Rizzoli (1991) ArticleTitleCritical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence J Clin Endocrinol Metab 73 555–563 Occurrence Handle1874933

    PubMed  Google Scholar 

  14. G Theintz B Buschs R Rizzoli D Slosman H Clavien PC Sizonenko JP Bonjour (1992) ArticleTitleLongitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the level of lumbar spine and femoral neck in female subjects J Clin Endocrinol Metab 75 1060–1065 Occurrence Handle10.1210/jc.75.4.1060 Occurrence Handle1400871

    Article  PubMed  Google Scholar 

  15. M Gilsanz DT Gibbens TF Roe M Carlson MO Senac MI Boechat HK Huang EE Schulz CR Libanati CC Cann (1988) ArticleTitleVertebral bone density in children: effect of puberty Radiology 166 847–850 Occurrence Handle3340782

    PubMed  Google Scholar 

  16. C Glastre P Braillon L David P Cochat PJ Meunier PD Delmas (1990) ArticleTitleMeasurement of bone mineral content of the lumbar spine by dual-energy X-ray absorptiometry in normal children: correlations with growth parameters J Clin Endocrinol Metab 705 1330–1333

    Google Scholar 

  17. C Ohlsson BA Bengtsson OG Isaksson TT Andreassen MC Slootweg (1998) ArticleTitleGrowth hormone and bone Endocr Rev 19 55–79 Occurrence Handle10.1210/er.19.1.55 Occurrence Handle9494780

    Article  PubMed  Google Scholar 

  18. GR Frank (1995) ArticleTitleThe role of estrogen in pubertal skeletal physiology: epiphyseal maturation and mineralization of the skeleton Acta Paediatr 846 627–630

    Google Scholar 

  19. L Audi A Carrascosa A Ballabriga (1984) ArticleTitleAndrogen metabolism by human fetal epiphyseal cartilage and its chondrocytes in primary culture J Clin Endocrinol Metab 585 819–825

    Google Scholar 

  20. MT Corvol A Carrascosa L Tsagris O Blanchard R Rappaport (1987) ArticleTitleEvidence for a direct in vitro action of sex steroids on rabbit cartilage cells during skeletal growth: influence of age and sex Endocrinology 120 1422–1429 Occurrence Handle3830056

    PubMed  Google Scholar 

  21. A Carrascosa L Audi MA Ferrandez A Ballabriga (1990) ArticleTitleBiological effects of androgens and identification of specific dihydrotestosterone-binding sites in cultured human fetal epiphyseal chondrocytes J Clin Endocrinol Metab 70 134–140 Occurrence Handle2294127

    PubMed  Google Scholar 

  22. M Ernst C Schmid ER Froesch (1988) ArticleTitleEnhanced osteoblast proliferation and collagen gene expression by estradiol Proc Natl Acad Sci USA 85 2307–2310 Occurrence Handle3353379

    PubMed  Google Scholar 

  23. SR Cummings WS Browner D Bauner K Stone K Ensrud S Jamal B Ettinger (1998) ArticleTitleEndogenous hormones and the risk of hip and vertebral fractures among older women. Study of Osteoporotic Fractures Research Group N Engl J Med 339 733–738 Occurrence Handle10.1056/NEJM199809103391104 Occurrence Handle9731089

    Article  PubMed  Google Scholar 

  24. D Bonofiglio C Garofalo S Catalano S Marsico S Aquila S Ando (2004) ArticleTitleLow calcium intake is associated with decreased adrenal androgens and reduced bone age in premenarcheal girls in the last pubertal stages J Bone Mineral Metab 22 64–70 Occurrence Handle10.1007/s00774-003-0451-5

    Article  Google Scholar 

  25. J Bilezikian A Morishima J Bell MM Grumbach (1998) ArticleTitleBrief report: increased bone mass as a result of estrogen therapy in a man with aromatase deficiency N Engl J Med 339 599–603 Occurrence Handle10.1056/NEJM199808273390905 Occurrence Handle9718379

    Article  PubMed  Google Scholar 

  26. RL Jilka G Hangoc G Girasole G Passeri DC Williams JS Abrams B Boyce H Broxmeyer SC Manolagas (1992) ArticleTitleIncreased osteoclast development after estrogen loss: mediation by interleukin-6 Science 257 88–91 Occurrence Handle1621100

    PubMed  Google Scholar 

  27. G Girasole RL Jilka G Passeri S Boswell G Boder DC Williams SC Manolagas (1992) ArticleTitle17-Beta-estradiol inhibits interleukin-6 production by bone marrow-derived stromal cells and osteoblasts in vitro: a potential mechanism for the antiosteoporotic effect of estrogens J Clin Invest 89 883–891 Occurrence Handle1541679

    PubMed  Google Scholar 

  28. S Mora P Pitukcheewanont FR Kaufman JC Nelson V Gilsanz (1999) ArticleTitleBiochemical markers of bone turnover and the volume and the density of bone in children at different stages of sexual development J Bone Miner Res 14 1664–1671 Occurrence Handle10491213

    PubMed  Google Scholar 

  29. H Tobiume S Kanzaki S Hida T Ono T Moriwake S Yamauchi H Tanaka Y Seino (1997) ArticleTitleSerum bone alkaline phosphatase isoenzyme levels in normal children and children with growth hormone (GH) deficiency: a potential marker for bone formation and response to growth hormone therapy J Clin Endocrinol Metab 82 2056–2061 Occurrence Handle10.1210/jc.82.7.2056 Occurrence Handle9215272

    Article  PubMed  Google Scholar 

  30. M van Coeverden JC Netelenbos CM de Ridder JC Roos C Popp-Snijders HA Dellemarre-van de Waal (2002) ArticleTitleBone metabolism markers and bone mass in healthy pubertal boy and girls Clin Endocrinol 57 107–116 Occurrence Handle10.1046/j.1365-2265.2002.01573.x

    Article  Google Scholar 

  31. AD Rogol JN Roemmich AP Clark (2002) ArticleTitleGrowth at puberty J Adolesc Health 31 192–200 Occurrence Handle10.1016/S1054-139X(02)00485-8 Occurrence Handle12470915

    Article  PubMed  Google Scholar 

  32. BJ Riis S Krabbe C Christiansen BD Catherwood LJ Deftos (1985) ArticleTitleBone turnover in male puberty: a longitudinal study Calcif Tissue Int 37 213–217 Occurrence Handle3926271

    PubMed  Google Scholar 

  33. A Blumsohn RA Hannon R Wrate J Barton AW al-Dehaimi A Colwell R Eastell (1994) ArticleTitleBiochemical markers of bone turnover in girls during puberty Clin Endocrinol 40 663–670

    Google Scholar 

  34. JZ Ilich NH Badenhop T Jelic (1997) ArticleTitleCalcitriol and bone mass accumulation in females during puberty Calcif Tissue Int 61 104–109 Occurrence Handle10.1007/s002239900304 Occurrence Handle9312397

    Article  PubMed  Google Scholar 

  35. K Kruse U Kracht (1986) ArticleTitleEvaluation of serum osteocalcin as an index of altered bone metabolism Eur J Pediatr 145 27–33 Occurrence Handle10.1007/BF00441848 Occurrence Handle3015628

    Article  PubMed  Google Scholar 

  36. S Wickman E Kajantie L Dunkel (2003) ArticleTitleEffects of suppression of estrogen action by the P450 aromatase inhibitor letrozole on bone mineral density and bone turnover in pubertal boys J Clin Endocrinol Metab 88 3783–3793 Occurrence Handle10.1210/jc.2002-021643

    Article  Google Scholar 

  37. C Moolgard BL Thomsen KF Michaelsen (1999) ArticleTitleWhole-body bone mineral accretion in healthy children and adolescence Arch Dis Child 81 10–15 Occurrence Handle10373125

    PubMed  Google Scholar 

  38. JA DePriester TJ Cole NJ Bishop (1991) ArticleTitleBone growth and mineralisation in children aged 4 to 10 years Bone Miner 12 57–65 Occurrence Handle10.1016/0169-6009(91)90121-F Occurrence Handle2001501

    Article  PubMed  Google Scholar 

  39. JR Zanchetta H Plotkin M Nunez ML Alvarez Filguira R Glancszpigel (1994) ArticleTitleDeterminant of femoral neck, lumbar spine and whole-body mineral density in the 2–20 age population Bone Mineral 25 IssueID2 43

    Google Scholar 

  40. S Bertelloni GI Baroncelli G Frederico (1998) ArticleTitleAltered bone mineral density in patients with complete androgen sensitivity syndrome Horm Res 50 309–314 Occurrence Handle10.1159/000023296 Occurrence Handle9973670

    Article  PubMed  Google Scholar 

Download references

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Correspondence to Betül Ersoy.

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Yilmaz, D., Ersoy, B., Bilgin, E. et al. Bone mineral density in girls and boys at different pubertal stages: relation with gonadal steroids, bone formation markers, and growth parameters. J Bone Miner Metab 23, 476–482 (2005). https://doi.org/10.1007/s00774-005-0631-6

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  • DOI: https://doi.org/10.1007/s00774-005-0631-6

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