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Journal of Clinical Endocrinology & Metabolism Vol. 73, No. 3 555-563
doi:10.1210/jcem-73-3-555
Copyright © 1991 by the Endocrine Society.
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Critical Years and Stages of Puberty for Spinal and Femoral Bone Mass Accumulation during Adolescence*

JEAN-PHILIPPE BONJOUR, GÉRALD THEINTZ, BERTRAND BUCHS, DANIEL SLOSMAN and RENÉ RIZZOLI{dagger}

Division of Clinical Pathophysiology, Department of Medicine Geneva, Switzerland
The Division of Biology of Growth and Reproduction, Department of Pediatrics and Genetics Geneva, Switzerland
The Division of Nuclear Medicine, Department of Radiology, University Hospital Geneva, Switzerland

Address all correspondence and requests for reprints to: J.-P. Bonjour, M.D., Division of Clinical Pathophysiology, Department of Medicine, University Hospital, CH-1211 Geneva 4, Switzerland.

Maximizing peak bone mass is advocated as a way to prevent osteoporosis. As a prerequisite to the elaboration of any preventive program aimed at maximizing peak bone mass, it is important to determine how the rate of skeletal growth at clinically relevant sites, such as lumbar spine and femoral neck, proceeds in relation to age and pubertal stages in both sexes. Bone mass was assessed in 207 healthy Caucasian boys and girls, aged 9–18 yr. Bone mineral density (BMD; grams per cm2) and content (BMC; grams) were determined in lumbar spine (L2- L4), femoral neck (FN), and midfemoral shaft (FS), using dual energy x-ray absorptiometry. Bone variables were correlated with both chronological age and pubertal stage, and compared with young adult (20–35 yr) reference values. The main results are: 1) in males, compared to females, there was a marked agerelated delay in L2-L4 BMD or BMC increase, but no delay was observed in relation to pubertal stages; 2) at the end of the rapid growth spurt, trends for higher mean values in males were observed for L2-L4 BMC, FN BMD, and particularly FS BMD, but no sex difference was observed for L2-L4 BMD; 3) in females, but not in males, a dramatic reduction in bone mass growth was observed after 15 yr of age, particularly for L2-L4 BMD/BMC and FN BMD. This sharp reduction occurred between the second and fourth years after menarche. In the 14- to 15-yr-old female group, BMD in L2-L4, FN, and FS corresponded to 99.2%, 105.1%, and 94.1%, respectively, and BMC in L2-L4 to 97.6% of the mean values recorded in 20- to 35-yrold women. In conclusion, this cross-sectionnal study indicates that during pubertal development, major differences are observed in bone mass growth according to sex and skeletal site. Whereas in males bone mass at different skeletal sites continues to increase substantially between 15–18 yr, skeletal mass growth appears to dramatically slow down at the levels of both lumbar spine and FN at 15–16 yr of age in female adolescents. This suggests that the generally accepted notion that in both males and females bone mass continues to substantially accumulate at all skeletal sites until the fourth decade may not be a constant in human physiology.

* This work was supported by Nestle SA and the National Swiss Foundation (Grant 3200.27-720). The bone densitometer used for this investigation was acquired thanks to a substantial contribution from Sandoz-Wander, Switzerland.

{dagger} Recipient of a Max Cloetta career development award.

Received December 10, 1990.




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Long-Term Outcome after Depot Gonadotropin-Releasing Hormone Agonist Treatment of Central Precocious Puberty: Final Height, Body Proportions, Body Composition, Bone Mineral Density, and Reproductive Function
J. Clin. Endocrinol. Metab., December 1, 1999; 84(12): 4583 - 4590.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
Estrogen Receptor Gene Polymorphism, But Not Estradiol Levels, Is Related to Bone Density in Healthy Adolescent Boys: A Cross-Sectional and Longitudinal Study
J. Clin. Endocrinol. Metab., December 1, 1999; 84(12): 4597 - 4601.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
V. Gilsanz
Importance of Technique for Determination of Phenotype
J. Clin. Endocrinol. Metab., November 1, 1999; 84(11): 4294 - 4295.
[Full Text]


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EndocrinologyHome page
K. Wiren, E. Keenan, X. Zhang, B. Ramsey, and E. Orwoll
Homologous Androgen Receptor Up-Regulation in Osteoblastic Cells May Be Associated with Enhanced Functional Androgen Responsiveness
Endocrinology, July 1, 1999; 140(7): 3114 - 3124.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
S. Ferrari, D. Manen, J.-P. Bonjour, D. Slosman, and R. Rizzoli
Bone Mineral Mass and Calcium and Phosphate Metabolism in Young Men: Relationships with Vitamin D Receptor Allelic Polymorphisms
J. Clin. Endocrinol. Metab., June 1, 1999; 84(6): 2043 - 2048.
[Abstract] [Full Text]


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Am. J. Clin. Nutr.Home page
D. Teegarden, R. M Lyle, W. R Proulx, C C. Johnston, and C. M Weaver
Previous milk consumption is associated with greater bone density in young women
Am. J. Clinical Nutrition, May 1, 1999; 69(5): 1014 - 1017.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
J. Sainz, J. M. Van Tornout, J. Sayre, F. Kaufman, and V. Gilsanz
Association of Collagen Type 1 {alpha}1 Gene Polymorphism with Bone Density in Early Childhood
J. Clin. Endocrinol. Metab., March 1, 1999; 84(3): 853 - 855.
[Abstract] [Full Text]


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Arch. Dis. Child.Home page
C. Tao, T. Yu, S. Garnett, J. Briody, J. Knight, H. Woodhead, C. T Cowell;, and Z. MUGHAL
Vitamin D receptor alleles predict growth and bone density in girls • Commentary
Arch. Dis. Child., December 1, 1998; 79(6): 488 - 494.
[Abstract] [Full Text]


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J. Am. Coll. Nutr.Home page
T. L. Duff and S. J. Whiting
Calciuric Effects of Short-Term Dietary Loading of Protein, Sodium Chloride and Potassium Citrate in Prepubescent Girls
J. Am. Coll. Nutr., April 1, 1998; 17(2): 148 - 154.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
S. Ferrari, R. Rizzoli, D. Slosman, and J.-P. Bonjour
Familial Resemblance for Bone Mineral Mass Is Expressed before Puberty
J. Clin. Endocrinol. Metab., February 1, 1998; 83(2): 358 - 361.
[Abstract] [Full Text]


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J. Clin. Endocrinol. Metab.Home page
A. M. Boot, S. M. P. F. d. M. Keizer-Schrama, H. A. P. Pols, E. P. Krenning, and S. L. S. Drop
Bone Mineral Density and Body Composition before and during Treatment with Gonadotropin-Releasing Hormone Agonist in Children with Central Precocious and Early Puberty
J. Clin. Endocrinol. Metab., February 1, 1998; 83(2): 370 - 373.
[Abstract] [Full Text]


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NEJMHome page
J. Sainz, J. M. Van Tornout, M. L. Loro, J. Sayre, T. F. Roe, and V. Gilsanz
Vitamin D-Receptor Gene Polymorphisms and Bone Density in Prepubertal American Girls of Mexican Descent
N. Engl. J. Med., July 10, 1997; 337(2): 77 - 82.
[Abstract] [Full Text] [PDF]


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NEJMHome page
C. Carani, K. Qin, M. Simoni, M. Faustini-Fustini, S. Serpente, J. Boyd, K. S. Korach, and E. R. Simpson
Effect of Testosterone and Estradiol in a Man with Aromatase Deficiency
N. Engl. J. Med., July 10, 1997; 337(2): 91 - 95.
[Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
A. A. Toogood, J. E. Adams, P. A. O'Neill, and S. M. Shalet
Elderly Patients with Adult-Onset Growth Hormone Deficiency Are Not Osteopenic
J. Clin. Endocrinol. Metab., May 1, 1997; 82(5): 1462 - 1466.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
V. Gilsanz, A. Kovanlikaya, G. Costin, T. F. Roe, J. Sayre, and F. Kaufman
Differential Effect of Gender on the Sizes of the Bones in the Axial and Appendicular Skeletons
J. Clin. Endocrinol. Metab., May 1, 1997; 82(5): 1603 - 1607.
[Abstract] [Full Text] [PDF]


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NEJMHome page
Y. Zhang, D. P. Kiel, B. E. Kreger, L. A. Cupples, R. C. Ellison, J. F. Dorgan, A. Schatzkin, D. Levy, and D. T. Felson
Bone Mass and the Risk of Breast Cancer among Postmenopausal Women
N. Engl. J. Med., February 27, 1997; 336(9): 611 - 617.
[Abstract] [Full Text] [PDF]


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Arch. Dis. Child.Home page
C. Mølgaard, B. L. Thomsen, A. Prentice, T. J Cole, and K. F. Michaelsen
Whole body bone mineral content in healthy children and adolescents
Arch. Dis. Child., January 1, 1997; 76(1): 9 - 15.
[Abstract] [Full Text]


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CLIN PEDIATRHome page
M. D. Lonzer, R. Imrie, D. Rogers, D. Worley, A. Licata, and M. Secic
Effects of Heredity, Age, Weight, Puberty, Activity, and Calcium Intake on Bone Mineral Density in Children
Clinical Pediatrics, April 1, 1996; 35(4): 185 - 189.
[Abstract] [PDF]


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BMJHome page
M J Valimaki, M Karkkainen, C Lamberg-Allardt, K Laitinen, E Alhava, J Heikkinen, O Impivaara, P Makela, J Palmgren, R Seppanen, et al.
Exercise, smoking, and calcium intake during adolescence and early adulthood as determinants of peak bone mass
BMJ, July 23, 1994; 309(6949): 230 - 235.
[Abstract] [Full Text]


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JAMAHome page
T. Lloyd, M. B. Andon, N. Rollings, J. K. Martel, J. R. Landis, L. M. Demers, D. F. Eggli, K. Kieselhorst, and H. E. Kulin
Peak Bone Mineral Density in Young Women-Reply
JAMA, December 22, 1993; 270(24): 2926 - 2927.
[Abstract] [PDF]


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JAMAHome page
T. Lloyd, M. B. Andon, N. Rollings, J. K. Martel, J. R. Landis, L. M. Demers, D. F. Eggli, K. Kieselhorst, and H. E. Kulin
Calcium Supplementation and Bone Mineral Density in Adolescent Girls
JAMA, August 18, 1993; 270(7): 841 - 844.
[Abstract] [PDF]


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JAMAHome page
R. R. Recker, K. M. Davies, S. M. Hinders, R. P. Heaney, M. R. Stegman, and D. B. Kimmel
Bone Gain in Young Adult Women
JAMA, November 4, 1992; 268(17): 2403 - 2408.
[Abstract] [PDF]


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Arch Pediatr Adolesc MedHome page
Bones of Today, Bones of Tomor014
Arch Pediatr Adolesc Med, January 1, 1992; 146(1): 22 - 25.
[Abstract] [PDF]




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