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Differences in Osteocyte Density and Bone Histomorphometry Between Men and Women and Between Healthy and Osteoporotic Subjects

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Abstract

Bone defects related to osteoporosis develop with increasing age and differ between males and females. It is currently thought that the bone remodeling process is supervised by osteocytes in a strain-dependent manner. We have shown an altered response of osteocytes from osteoporotic patients to mechanical loading, and osteocyte density is reduced in osteoporotic patients, which might relate to imperfect bone remodeling, leading to lack of bone mass and strength. Hence, information on osteocyte density will contribute to a better understanding of bone biology in males and females and to the assessment of osteoporosis. Osteocyte density as well as conventional histomorphometric parameters of trabecular bone were determined in cancellous iliac crest bone of healthy postmenopausal women and men and of osteoporotic women and men. Osteocyte density was higher in healthy females than in healthy males and lower in osteoporotic females than in healthy females. Bone mass was reduced in osteoporotic patients, both male and female. In females, trabecular number was reduced, whereas in males, trabecular thickness was reduced and eroded surface was increased. There were no correlations between the parameter groups bone architecture, bone formation, bone resorption, and osteocyte density. These results are consistent with impaired osteoblast function in osteoporotic patients and with a different mechanism of bone loss between men and women, in which osteocyte density might play a role. The reduced osteocyte numbers in female osteoporotic patients might relate to imperfect bone remodeling leading to lack of bone mass and strength.

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References

  1. Skerry TM, Bitensky L, Chayen J, Lanyon LE (1989) Early strain-related changes in enzyme activity in osteocytes following bone loading in vivo. J Bone Miner Res 4:783–788

    PubMed  CAS  Google Scholar 

  2. Klein-Nulend J, Van der Plas A, Semeins CM, Ajubi NE, Frangos JA, Nijweide PJ, Burger EH (1995) Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9:441–445

    PubMed  CAS  Google Scholar 

  3. Knothe Tate ML, Adamson JR, Tami AE, Bauer TW (2004) The osteocyte. Int J Biochem Cell Biol 36:1–8

    Article  PubMed  CAS  Google Scholar 

  4. Marotti G, Cané V, Palazzini S, Palumbo C (1990) Structure-function relationships in the osteocyte. Ital J Miner Electrolyte Metab 4:93–106

    Google Scholar 

  5. Cowin SC, Moss-Salentijn L, Moss ML (1991) Candidates for the mechanosensory system in bone. J Biomech Eng 113:191–197

    PubMed  CAS  Google Scholar 

  6. Lanyon LE (1993) Osteocytes, strain detection, bone modeling and remodeling. Calcif Tissue Int 53:S102–S106

    Article  PubMed  Google Scholar 

  7. Mullender MG, Huiskes R (1995) A proposal for the regulatory mechanism of Wolff’s law. J Orthop Res 13:503–512

    Article  PubMed  CAS  Google Scholar 

  8. Aarden EM, Nijweide PJ, van der Plas A, Albas MJ, Mackie EJ, Horton MA, Helfrich MH (1996) Adhesive properties of isolated chick osteocytes in vitro. Bone 18:305–313

    Article  PubMed  CAS  Google Scholar 

  9. Parfitt AM (1996) Skeletal heterogeneity and the purposes of bone remodeling. In: Marcus R, Feldman D, Kelsey J (eds), Osteoporosis. Academic Press, San Diego, pp 315–329

    Google Scholar 

  10. Bakker A, Klein-Nulend J, Burger E (2004) Shear stress inhibits while disuse promotes osteocyte apoptosis. Biochem Biophys Res Commun 320:1163–1168

    Article  PubMed  CAS  Google Scholar 

  11. Mullender MG, Huiskes R (1995) A proposal for the regulatory mechanism of Wolff’s law. J Orthop Res 13:503–512

    Article  PubMed  CAS  Google Scholar 

  12. Rodan GA (1997) Bone mass homeostasis and bisphosphonate action. Bone 20:1–4

    Article  PubMed  CAS  Google Scholar 

  13. Sterck JG, Klein-Nulend J, Lips P, Burger EH (1998) Response of normal and osteoporotic human bone cells to mechanical stress in vitro. Am J Physiol 274:E1113–E1120

    PubMed  CAS  Google Scholar 

  14. Rodan GA (1991) Mechanical loading, estrogen deficiency, and the coupling of bone formation to bone resorption. J Bone Miner Res 6:527–530

    PubMed  CAS  Google Scholar 

  15. Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM (1985) The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tissue Int 37:594–597

    PubMed  CAS  Google Scholar 

  16. Parfitt AM (1984) Age-related structural changes in trabecular and cortical bone: cellular mechanisms and biomechanical consequences. Calcif Tissue Int 36:S123–S128

    PubMed  Google Scholar 

  17. Parfitt AM, Mathews CHE, Villanueva AR, Kleerekoper M (1983) Relationships between surface, volume, and thickness of iliac trabecular bone in aging and osteoporosis. J Clin Invest 72:1396–1409

    PubMed  CAS  Google Scholar 

  18. Recker RR, Kimmel DB, Parfitt AM, Davies M, Keshawarz N, Hinders S (1988) Static and tetracycline-based bone histomorphometric data from 34 normal postmenopausal females. J Bone Miner Res 3:133–144

    PubMed  CAS  Google Scholar 

  19. Steiniche T, Christiansen P, Vesterby A, Hasling C, Ullerup R, Mosekilde L, Melsen F (1994) Marked changes in iliac crest bone structure in postmenopausal osteoporotic patients without any signs of disturbed bone remodeling or balance. Bone 15:73–79

    Article  PubMed  CAS  Google Scholar 

  20. Aaron JE, Makins NB, Sagreiya K (1987) The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop 215:260–271

    PubMed  Google Scholar 

  21. Batra GS, Hainey L, Freemont AJ, Andrew G, Saunders PT, Hoyland JA, Braidman IP (2003) Evidence for cell-specific changes with age in expression of oestrogen receptor (ER) alpha and beta in bone fractures from men and women. J Pathol 200:65–73

    Article  PubMed  CAS  Google Scholar 

  22. Oursler MJ, Kassem M, Turner R, Riggs BL, Spelsberg TC (1996) Regulation of bone cell function by gonadal steroids. In: Marcus R, Feldman D, Kelsey J (eds), Osteoporosis. Academic Press, San Diego, pp 237–260

    Google Scholar 

  23. Palumbo C, Palazzini S, Marotti G (1990) Morphological study of intercellular junctions during osteocyte differentiation. Bone 11:401–406

    Article  PubMed  CAS  Google Scholar 

  24. Marotti G, Ferretti M, Muglia MA, Palumbo C, Palazzini S (1992) A quantitative valuation of osteoblast-osteocyte relationships on growing endosteal surface of rabbit tibiae. Bone 13:363–368

    Article  PubMed  CAS  Google Scholar 

  25. Qui S, Rao DS, Palnitkar S, Parfitt AM (2003) Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. J Bone Miner Res 18:1657–1663

    Google Scholar 

  26. Hernandez CJ, Majeska RJ, Schaffler MB (2004) Osteocyte density in woven bone. Bone 35:1095–1099

    Article  PubMed  CAS  Google Scholar 

  27. Mullender MG, Van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18:109–113

    Article  PubMed  CAS  Google Scholar 

  28. Chappard D, Alexandre C, Camps M, Montheard JP, Riffat G (1983) Embedding iliac bone biopsies at low temperature using glycol and methyl methacrylates. Stain Technol 58:299–308

    PubMed  CAS  Google Scholar 

  29. Chappard D, Alexandre C, Riffat G (1983) Histochemical identification of osteoclasts. Review of current methods and reappraisal of a simple procedure for routine diagnosis on undecalcified human iliac bone biopsies. Basic Appl Histochem 27:75–85

    PubMed  CAS  Google Scholar 

  30. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. J Bone Miner Res 2:595–610

    PubMed  CAS  Google Scholar 

  31. Ornoy A, Giron S, Aner R, Goldstein M, Boyan BD, Schwartz Z (1994) Gender dependent effects of testosterone and 17beta-estradiol on bone growth and modelling in young mice. Bone Miner 24:43–58

    Article  PubMed  CAS  Google Scholar 

  32. Cheng MZ, Zaman G, Rawlinson SCF, Suswillo RFL, Lanyon LE (1995) Oestrogen amplifies bone’s osteogenic responses to load-bearing in female rat ulna in vitro. Calcif Tissue Int 56:428

    Google Scholar 

  33. Cheng MZ, Zaman G, Lanyon LE (1994) Estrogen enhances the stimulation of bone collagen synthesis by loading and exogenous prostacyclin, but not prostaglandin E2, in organ cultures of rat ulnae. J Bone Miner Res 9:805–816

    PubMed  CAS  Google Scholar 

  34. Cheng MZ, Zaman G, Rawlinson SC, Suswillo RF, Lanyon LE (1996) Mechanical loading and sex hormone interactions in organ cultures of rat ulna. J Bone Miner Res 11:502–511

    PubMed  CAS  Google Scholar 

  35. Vashishth D, Verborgt O, Divine G, Schaffler MB, Fyhrie DP (2000) Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 26:375–380

    PubMed  CAS  Google Scholar 

  36. Jordan GR, Loveridge N, Power J, Clarke MT, Parker M, Reeve J (2003) The ratio of osteocytic incorporation to bone matrix formation in femoral neck cancellous bone: an enhanced osteoblast work rate in the vicinity of hip osteoarthritis. Calcif Tissue Int 72:190–196

    Article  PubMed  CAS  Google Scholar 

  37. McCreadie BR, Hollister SJ, Schaffler MB, Goldstein SA (2004) Osteocyte lacuna size and shape in women with and without osteoporotic fracture. J Biomech 37:563–572

    Article  PubMed  Google Scholar 

  38. Burger EH, Klein-Nulend J, Smit TH (2003) Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon – a proposal. J Biomech 36:1453–1459

    Article  PubMed  Google Scholar 

  39. Parfitt AM (1993) Bone age, mineral density and fatigue damage. Calcif Tissue Int 53:S82–S85

    PubMed  Google Scholar 

  40. Dunstan CR, Somers NM, Evans RA (1993) Osteocyte death and hip fracture. Calcif Tissue Int 53:S113–S116

    Article  PubMed  Google Scholar 

  41. Parfitt AM, Villanueva AR, Foldes J, Rao DS (1995) Relations between histologic indices of bone formation: implications for the pathogenesis of spinal osteoporosis. J Bone Miner Res 10:466–473

    Article  PubMed  CAS  Google Scholar 

  42. Roholl PJM, Blauw E, Zurcher C, Dormans JAMA, Theuns HM (1994) Evidence for a diminished maturation of preosteoblasts into osteoblasts during aging in rats: an ultrastructural analysis. J Bone Miner Res 9:355–366

    PubMed  CAS  Google Scholar 

  43. Gohel AR, Hand AR, Gronowicz GA (1995) Immunogold localization of beta1-integrin in bone: effects of glucocorticoids and insulin-like growth factor I on integrins and osteocyte formation. J Histochem Cytochem 43:1085–1096

    PubMed  CAS  Google Scholar 

  44. Li KC, Zernicke RF, Barnard RJ, Li AFY (1991) Differential response of rat limb bones to strenuous exercise. J Appl Physiol 70:554–560

    PubMed  CAS  Google Scholar 

  45. Recker RR (1993) Architecture and vertebral fracture. Calcif Tissue Int 53:S139–S142

    Article  PubMed  Google Scholar 

  46. Arlot ME, Delmas PD, Chappard D, Meunier PJ (1990) Trabecular and endocortical bone remodeling in postmenopausal osteoporosis: comparison with normal postmenopausal women. Osteoporos Int 1:41–49

    Article  PubMed  CAS  Google Scholar 

  47. Parfitt AM (1992) Implications of architecture for the pathogenesis and prevention of vertebral fracture. Bone 13:S41–S47

    PubMed  Google Scholar 

  48. Brockstedt H, Kassem M, Eriksen EF, Mosekilde L, Melsen F (1993) Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone 14:681–691

    Article  PubMed  CAS  Google Scholar 

  49. Nijweide PJ, Burger EH, Klein-Nulend J (2002) The osteocyte. In: Bilezikian JP, Raisz LG, Rodan GA (eds), Principles of bone biology, 2nd ed, vol 1. Academic Press, San Diego, pp 93–108

    Google Scholar 

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Acknowledgments

We thank Dorien van der Meer for assisting with the measurement of osteocyte density. We thank V. Everts for valuable comments on the manuscript. The Netherlands Institute for Dental Sciences supported the work of S.D.T. The University of Nijmegen (The Netherlands) supported the work of M.G.M.

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Authors and Affiliations

  1. Department of Oral Cell Biology, Academic Centre for Dentistry Amsterdam, Universiteit van Amsterdam and Vrije Universiteit, Amsterdam, The Netherlands

    M. G. Mullender, S. D. Tan & J. Klein-Nulend

  2. Faculté de Médecine, Laboratoire de Biologie du Tissu Osseux, Saint-Etienne Cedex 02, 42023, France

    L. Vico & C. Alexandre

Authors
  1. M. G. Mullender
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  2. S. D. Tan
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  3. L. Vico
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  4. C. Alexandre
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  5. J. Klein-Nulend
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Correspondence to J. Klein-Nulend.

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M. G. Mullender and S. D. Tan contributed equally to this work.

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Mullender, M.G., Tan, S.D., Vico, L. et al. Differences in Osteocyte Density and Bone Histomorphometry Between Men and Women and Between Healthy and Osteoporotic Subjects. Calcif Tissue Int 77, 291–296 (2005). https://doi.org/10.1007/s00223-005-0043-6

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  • DOI: https://doi.org/10.1007/s00223-005-0043-6

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