Skip to main content
SpringerLink
Log in

A Delay in Pubertal Onset Affects the Covariation of Body Weight, Estradiol, and Bone Size

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

The skeletal system functions as a locomotive organ and a mineral reservoir and combinations of genetic and environmental factors affect the skeletal system. Although delayed puberty is associated with compromised bone mass, suppression of estrogen should be beneficial to cortical strength. The purpose was to employ path analysis to study bone strength and delayed puberty. Forty-five female rats were randomly assigned to a control group (n = 15) and an experimental group (n = 30) that received injections of gonadotropin releasing hormone antagonist (GnRH-a). Causal models were constructed by specifying directed paths between bone traits. The first model tested the hypothesis that the functional relationships between bone traits and body weight were altered by a delay in pubertal onset. GnRH-a injections during puberty altered the covariation between body weight and bone size. The second model was constructed to test the hypothesis that variability in stiffness was causally related to variability in body weight. The model also tested the relationship between the periosteal and endocortical surfaces and their relationship to stiffness. There was no change in the relationship between the surfaces in the GnRH-a group. The third model determined the effect of estradiol on both total area and relative cortical area in both groups. The relationship between periosteal surface and serum estradiol levels was only significant during estrogen suppression. These data suggest that increases in body weight during or prior to puberty may not be protective of bone strength.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Jepsen KJ, Hu B, Tommasini SM et al (2009) Phenotypic integration of skeletal traits during growth buffers genetic variants affecting the slenderness of femora in inbred mouse strains. Mammal Genome 20:21–33

    Article  Google Scholar 

  2. Kitano H (2002) Systems biology: a brief overview. Science 295:1662–1664

    Article  PubMed  CAS  Google Scholar 

  3. Golden NH (2000) Osteoporosis prevention: a pediatric challenge. Arch Pediatr Adolesc Med 154:542–543

    PubMed  CAS  Google Scholar 

  4. Bailey DA (1997) The Saskatchewan pediatric bone mineral accrual study: bone mineral acquisition during the growing years. Int J Sports Med 18(Suppl 3):S191–S194

    Article  PubMed  Google Scholar 

  5. Bailey DA, Martin AD, McKay HA, Whiting S, Mirwald R (2000) Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 15:2245–2250

    Article  PubMed  CAS  Google Scholar 

  6. Drinkwater BL, Nilson K, Chesnut CHIII, Bremner WJ, Shainholtz S, Southworth MB (1984) Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311:277–281

    PubMed  CAS  Google Scholar 

  7. Pettersson U, Stalnacke B, Ahlenius G, Henriksson-Larsen K, Lorentzon R (1999) Low bone mass density at multiple skeletal sites, including the appendicular skeleton in amenorrheic runners. Calcif Tissue Int 64:117–125

    Article  PubMed  CAS  Google Scholar 

  8. Warren MP, Brooks-Gunn J, Fox RP, Lancelot C, Newman D, Hamilton WG (1991) Lack of bone accretion and amenorrhea: evidence for a relative osteopenia in weight-bearing bones. J Clin Endocrinol Metab 72:847–853

    Article  PubMed  CAS  Google Scholar 

  9. Warren MP, Brooks-Gunn J, Fox RP, Holderness CC, Hyle EP, Hamilton WG (2002) Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: a longitudinal study. J Clin Endocrinol Metab 87:3162–3168

    Article  PubMed  CAS  Google Scholar 

  10. Carbon R, Sambrook PN, Deakin V et al (1990) Bone density of elite female athletes with stress fractures. Med J Aust 153:373–376

    PubMed  CAS  Google Scholar 

  11. Loud KJ, Gordon CM, Micheli LJ, Field AE (2005) Correlates of stress fractures among preadolescent and adolescent girls. Pediatrics 115:e399–e406

    Article  PubMed  Google Scholar 

  12. Myerson M, Gutin B, Warren MP, Wang J, Lichtman S, Pierson RN Jr (1992) Total body bone density in amenorrheic runners. Obstet Gynecol 79:973–978

    PubMed  CAS  Google Scholar 

  13. Warren MP, Stiehl AL (1999) Exercise and female adolescents: effects on the reproductive and skeletal systems. J Am Med Womens Assoc 54:115–120, 138

    PubMed  CAS  Google Scholar 

  14. Hogler W, Blimkie CJ, Cowell CT et al (2008) Sex-specific developmental changes in muscle size and bone geometry at the femoral shaft. Bone 42:982–989

    Article  PubMed  CAS  Google Scholar 

  15. Garn SM, Nagy JM, Sandusky ST (1972) Differential sexual dimorphism in bone diameters of subjects of european and african ancestry. Am J Phys Anthropol 37:127–129

    Article  PubMed  CAS  Google Scholar 

  16. Tommasini SM, Nasser P, Jepsen KJ (2007) Sexual dimorphism affects tibia size and shape but not tissue-level mechanical properties. Bone 40:498–505

    Article  PubMed  Google Scholar 

  17. Turner RT, Vandersteenhoven JJ, Bell NH (1987) The effects of ovariectomy and 17 beta-estradiol on cortical bone histomorphometry in growing rats. J Bone Miner Res 2:115–122

    PubMed  CAS  Google Scholar 

  18. Turner RT, Wakley GK, Hannon KS (1990) Differential effects of androgens on cortical bone histomorphometry in gonadectomized male and female rats. J Orthop Res 8:612–617

    Article  PubMed  CAS  Google Scholar 

  19. Kim BT, Mosekilde L, Duan Y et al (2003) The structural and hormonal basis of sex differences in peak appendicular bone strength in rats. J Bone Miner Res 18:150–155

    Article  PubMed  CAS  Google Scholar 

  20. Jiang Y, Zhao J, Genant HK, Dequeker J, Geusens P (1997) Long-term changes in bone mineral and biomechanical properties of vertebrae and femur in aging, dietary calcium restricted, and/or estrogen-deprived/-replaced rats. J Bone Miner Res 12:820–831

    Article  PubMed  CAS  Google Scholar 

  21. Katsumata T, Nakamura T, Ohnishi H, Sakurama T (1995) Intermittent cyclical etidronate treatment maintains the mass, structure and the mechanical property of bone in ovariectomized rats. J Bone Miner Res 10:921–931

    PubMed  CAS  Google Scholar 

  22. Peng Z, Tuukkanen J, Vaananen HK (1994) Exercise can provide protection against bone loss and prevent the decrease in mechanical strength of femoral neck in ovariectomized rats. J Bone Miner Res 9:1559–1564

    Article  PubMed  CAS  Google Scholar 

  23. Yingling VR, Khaneja A (2006) Short-term delay of puberty causes a transient reduction in bone strength in growing female rats. Bone 38:67–73

    Article  PubMed  Google Scholar 

  24. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge

    Google Scholar 

  25. Jepsen KJ, Hu B, Tommasini SM et al (2007) Genetic randomization reveals functional relationships among morphologic and tissue-quality traits that contribute to bone strength and fragility. Mammal Genome 18:492–507

    Article  Google Scholar 

  26. Sharkey NA, Lang DH (2007) Genes in context: probing the genetics of fracture resistance. Exerc Sport Sci Rev 35:86–96

    Article  PubMed  Google Scholar 

  27. Bower AL, Lang DH, Vogler GP et al (2006) QTL analysis of trabecular bone in BXD F2 and RI mice. J Bone Miner Res 21:1267–1275

    Article  PubMed  Google Scholar 

  28. Li R, Svenson KL, Donahue LR, Peters LL, Churchill GA (2008) Relationships of dietary fat, body composition, and bone mineral density in inbred mouse strain panels. Physiol Genomics 33:26–32

    Article  PubMed  CAS  Google Scholar 

  29. Yingling VR, Taylor G (2008) Delayed pubertal development by hypothalamic suppression causes an increase in periosteal modeling but a reduction in bone strength in growing female rats. Bone 42:1137–1143

    Article  PubMed  CAS  Google Scholar 

  30. Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608

    Article  PubMed  CAS  Google Scholar 

  31. Brodt MD, Ellis CB, Silva MJ (1999) Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res 14:2159–2166

    Article  PubMed  CAS  Google Scholar 

  32. Zebaze RM, Jones A, Knackstedt M, Maalouf G, Seeman E (2007) Construction of the femoral neck during growth determines its strength in old age. J Bone Miner Res 22:1055–1061

    Article  PubMed  Google Scholar 

  33. Ferretti JL, Capozza RF, Mondelo N, Montuori E, Zanchetta JR (1993) Determination of femur structural properties by geometric and material variables as a function of body weight in rats. Evidence of a sexual dimorphism. Bone 14:265–270

    Article  PubMed  CAS  Google Scholar 

  34. Reid IR (2006) Obesity and osteoporosis. Ann Endocrinol (Paris) 67:125–129

    CAS  Google Scholar 

  35. Rosen CJ, Ackert-Bicknell CL, Adamo ML et al (2004) Congenic mice with low serum IGF-I have increased body fat, reduced bone mineral density, and an altered osteoblast differentiation program. Bone 35:1046–1058

    Article  PubMed  CAS  Google Scholar 

  36. Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646

    Article  PubMed  CAS  Google Scholar 

  37. Riggs BL, O’Fallon WM, Muhs J, O’Connor MK, Kumar R, Melton LJ 3rd (1998) Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women. J Bone Miner Res 13:168–174

    Article  PubMed  CAS  Google Scholar 

  38. Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003) Bone loss and bone size after menopause. N Engl J Med 349:327–334

    Article  PubMed  Google Scholar 

  39. Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD (2006) Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21:1856–1863

    Article  PubMed  Google Scholar 

  40. Tseng KF, Bonadio JF, Stewart TA, Baker AR, Goldstein SA (1996) Local expression of human growth hormone in bone results in impaired mechanical integrity in the skeletal tissue of transgenic mice. J Orthop Res 14:598–604

    Article  PubMed  CAS  Google Scholar 

  41. Silva MJ, Brodt MD, Ettner SL (2002) Long bones from the senescence accelerated mouse SAMP6 have increased size but reduced whole-bone strength and resistance to fracture. J Bone Miner Res 17:1597–1603

    Article  PubMed  Google Scholar 

  42. Bonadio J, Jepsen KJ, Mansoura MK, Jaenisch R, Kuhn JL, Goldstein SA (1993) A murine skeletal adaptation that significantly increases cortical bone mechanical properties. Implications for human skeletal fragility. J Clin Invest 92:1697–1705

    Article  PubMed  CAS  Google Scholar 

  43. Khosla S (2008) Estrogen and bone: insights from estrogen-resistant, aromatase-deficient, and normal men. Bone 43:414–417

    Article  PubMed  CAS  Google Scholar 

  44. Rauch F, Travers R, Glorieux FH (2006) Cellular activity on the seven surfaces of iliac bone: a histomorphometric study in children and adolescents. J Bone Miner Res 21:513–519

    Article  PubMed  Google Scholar 

  45. Rauch F, Travers R, Glorieux FH (2007) Intracortical remodeling during human bone development—a histomorphometric study. Bone 40:274–280

    Article  PubMed  Google Scholar 

  46. Warden SJ, Fuchs RK, Castillo AB, Nelson IR, Turner CH (2006) Exercise when young provides lifelong benefits to bone structure and strength. J Bone Miner Res 22(2):251–259

    Article  Google Scholar 

  47. Price C, Herman BC, Lufkin T, Goldman HM, Jepsen KJ (2005) Genetic variation in bone growth patterns defines adult mouse bone fragility. J Bone Miner Res 20:1983–1991

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

I thank Mona Al-Amin of the Social Science Data Library, Temple University, for her statistical expertise in path analysis.

Author information

Authors and Affiliations

  1. Department of Kinesiology, Temple University, 121 Pearson Hall, 3307 North Broad Street, Philadelphia, PA, 19140, USA

    Vanessa R. Yingling

  2. Department of Anatomy and Cell Biology, Temple University, 121 Pearson Hall, 3307 North Broad Street, Philadelphia, PA, 19140, USA

    Vanessa R. Yingling

Authors
  1. Vanessa R. Yingling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vanessa R. Yingling.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yingling, V.R. A Delay in Pubertal Onset Affects the Covariation of Body Weight, Estradiol, and Bone Size. Calcif Tissue Int 84, 286–296 (2009). https://doi.org/10.1007/s00223-009-9231-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-009-9231-0

Keywords

Search

Navigation