Skip to main content

Advertisement

SpringerLink
Log in

Effect of Macroanatomic Bone Type and Estrogen Loss on Osteocyte Lacunar Properties in Healthy Adult Women

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

This is the first study to examine clinical human bone specimens by three-dimensional imaging to characterize osteocyte lacunar properties as a function of macroanatomic bone type and estrogen loss. We applied laboratory-based instrumentation [3D X-ray microscope (3DXRM), MicroXCT-200; Carl Zeiss/Xradia, Inc.] that reaches the same resolution as synchrotron microscopy. We used serial transiliac bone biopsy specimens to examine the effect of macroanatomic bone type and estrogen status on osteocyte lacunar properties. These properties include lacunar size (volume, axes lengths of the ellipsoidal lacunar voids), distribution (density, average near-neighbor lacunar distance), and shape factors (sphericity ratio, average eigenvalues, degree of equancy, elongation, and flatness) in both cortical and trabecular bone tissue. The lacunar properties (volume, surface area, density, near-neighbor distance, etc.) and the shape factors (E1, L1, L2, degree of equancy, degree of elongation) were different between cortical and trabecular bone regardless of estrogen status. In cortical bone and trabecular nodes, the lacunar void volume and surface area were either smaller or tended to be smaller in postmenopausal as compared to premenopausal women. The void volume-to-bone volume ratio of cortical bone showed declining trends with estrogen loss. While there were differences between trabecular and cortical bone tissue, the lacunar void sphericity ratio for trabecular struts shows decreasing trends in postmenopausal women. These data suggest that using 3DXRM can provide new insight into osteocyte lacunar properties in transiliac bone biopsies from patients with various skeletal disease/conditions and pharmaceutical treatments.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  1. Buenzli PR, Sims NA (2015) Quantifying the osteocyte network in the human skeleton. Bone 75:144–150

    Article  CAS  PubMed  Google Scholar 

  2. Yeni YN, Vashishth D, Fyhrie DP (2001) Estimation of bone matrix apparent stiffness variation caused by osteocyte lacunar size and density. J Biomech Eng 123:10–17

    Article  CAS  PubMed  Google Scholar 

  3. Schneider P, Meier M, Wepf R, Muller R (2010) Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 47:848–858

    Article  PubMed  Google Scholar 

  4. van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density—is there a role for mechanosensing? Bone 45:321–329

    Article  PubMed  Google Scholar 

  5. 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 

  6. Boyde A, Jones SJ (1996) Scanning electron microscopy of bone: instrument, specimen, and issues. Microsc Res Tech 33:92–120

    Article  CAS  PubMed  Google Scholar 

  7. Qiu 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

    Article  PubMed  Google Scholar 

  8. Rubin MA, Rubin J, Jasiuk I (2004) SEM and TEM study of the hierarchical structure of C57BL/6 J and C3H/HeJ mice trabecular bone. Bone 35:11–20

    Article  PubMed  Google Scholar 

  9. Carter Y, Suchorab JL, Thomas CD, Clement JG, Cooper DM (2014) Normal variation in cortical osteocyte lacunar parameters in healthy young males. J Anat 225:328–336

    Article  PubMed  PubMed Central  Google Scholar 

  10. Carter Y, Thomas CD, Clement JG, Cooper DM (2013) Femoral osteocyte lacunar density, volume and morphology in women across the lifespan. J Struct Biol 183:519–526

    Article  PubMed  Google Scholar 

  11. Carter Y, Thomas CD, Clement JG, Peele AG, Hannah K, Cooper DM (2013) Variation in osteocyte lacunar morphology and density in the human femur—a synchrotron radiation micro-CT study. Bone 52:126–132

    Article  PubMed  Google Scholar 

  12. 12)Britz HM, Carter Y, Jokihaara J, Leppanen OV, Jarvinen TL, Belev G, Cooper DM (2012) Prolonged unloading in growing rats reduces cortical osteocyte lacunar density and volume in the distal tibia. Bone 51:913–919

    Article  PubMed  Google Scholar 

  13. Recker RR, Saville PD, Heaney RP (1977) Effect of estrogens and calcium carbonate on bone loss in postmenopausal women. Ann Intern Med 87:649–655

    Article  CAS  PubMed  Google Scholar 

  14. Recker R, Lappe J, Davies K, Heaney R (2000) Characterization of perimenopausal bone loss: a prospective study. J Bone Miner Res 15:1965–1973

    Article  CAS  PubMed  Google Scholar 

  15. Finkelstein JS, Brockwell SE, Mehta V, Greendale GA, Sowers MR, Ettinger B, Lo JC, Johnston JM, Cauley JA, Danielson ME, Neer RM (2008) Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J Clin Endocrinol Metab 93:861–868

    Article  CAS  PubMed  Google Scholar 

  16. Akhter MP, Lappe JM, Davies KM, Recker RR (2007) Transmenopausal changes in the trabecular bone structure. Bone 41:111–116

    Article  CAS  PubMed  Google Scholar 

  17. Mullender MG, Huiskes R, Versleyen H, Buma P (1996) Osteocyte density and histomorphometric parameters in cancellous bone of the proximal femur in five mammalian species. J Orthop Res 14:972–979

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  19. Dunstan CR, Somers NM, Evans RA (1993) Osteocyte death and hip fracture. Calcif Tissue Int 53:S116–117.

    Article  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. Wong SY, Kariks J, Evans RA, Dunstan CR, Hills E (1985) The effect of age on bone composition and viability in the femoral head. J Bone Joint Surg Am 67:274–283

    Article  CAS  PubMed  Google Scholar 

  22. Baud CA, Auil E (1971) Osteocyte differential count in normal human alveolar bone. Acta Anat 78:321–327.

    Article  CAS  PubMed  Google Scholar 

  23. Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, Muller R (2007) Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 22:1557–1570

    Article  PubMed  Google Scholar 

  24. Recker R, Lappe J, Davies KM, Heaney R (2004) Bone remodeling increases substantially in the years after menopause and remains increased in older osteoporosis patients. J Bone Miner Res 19:1628–1633

    Article  PubMed  Google Scholar 

  25. Christiansen C, Christensen MS, McNair P, Hagen C, Stocklund KE, Transbol I (1980) Prevention of early postmenopausal bone loss: controlled 2-year study in 315 normal females. Eur J Clin Invest 10:273–279

    Article  CAS  PubMed  Google Scholar 

  26. Genant HK, Ettinger B, Cann CE, Reiser U, Gordan GS, Kolb FO (1985) Osteoporosis: assessment by quantitative computed tomography. Orthop Clin North Am 16:557–568

    CAS  PubMed  Google Scholar 

  27. Moore RJ, Durbridge TC, Woods AE, Vernon Roberts B (1989) Variation in histomorphometric estimates across different sites of the iliac crest. J Clin Pathol 42:814–816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Akhter MP, Candell S, Recker R, Fong T, Coats J, Kimmel DB (2010) Characterization of osteocyte lacunae in adult human bone by 3D X-ray microscopy. J Bone Miner Res 26:229–238.

    Google Scholar 

  29. Feser M, Gelb J, Chang H, Cui H, Duewer F, Lau S, Tkachuk A, Yun W (2008) Sub-micron resolution CT for failure analysis and process development. Microsc Microanal 16:327–336

    Google Scholar 

  30. Dong P, Haupert S, Hesse B, Langer M, Gouttenoire PJ, Bousson V, Peyrin F (2014) 3D Osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone 60:172–185

    Article  PubMed  Google Scholar 

  31. Wadell H (1935) Volume, shape, and roundness of quartz particles. J Geol 43:250–280

    Article  Google Scholar 

  32. Blott SJ, Pye K (2008) Particle shape: a review and new methods of characterization and classification. Sedimentology 55:31–63

    Google Scholar 

  33. Bonewald LF (2011) The amazing osteocyte. J Bone Miner Res 26:229–238

    Article  CAS  PubMed  Google Scholar 

  34. Mullender MG, Tan SD, Vico L, Alexandre C, Klein Nulend J (2005) Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 77:291–296

    Article  CAS  PubMed  Google Scholar 

  35. Qiu S, Rao DS, Palnitkar S, Parfitt AM (2002) Age and distance from the surface but not menopause reduce osteocyte density in human cancellous bone. Bone 31:313–318

    Article  CAS  PubMed  Google Scholar 

  36. Qiu S, Rao DS, Palnitkar S, Parfitt AM (2002) Relationships between osteocyte density and bone formation rate in human cancellous bone. Bone 31:709–711

    Article  CAS  PubMed  Google Scholar 

  37. Sharma D, Ciani C, Marin PA, Levy JD, Doty SB, Fritton SP (2012) Alterations in the osteocyte lacunar-canalicular microenvironment due to estrogen deficiency. Bone 51:488–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3(Suppl 3):S131–S139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Jilka RL, Noble B, Weinstein RS (2013) Osteocyte apoptosis. Bone 54:264–271

    Article  PubMed  Google Scholar 

  40. Bonewald LF, Johnson ML (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42:606–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S (2013) Mechanosensation and transduction in osteocytes. Bone 54:182–190

    Article  CAS  PubMed  Google Scholar 

  42. Verborgt O, Tatton NA, Majeska RJ, Schaffler MB (2002) Spatial distribution of Bax and Bcl-2 in osteocytes after bone fatigue: complementary roles in bone remodeling regulation? J Bone Miner Res 17:907–914

    Article  CAS  PubMed  Google Scholar 

  43. Hannah KM, Thomas CD, Clement JG, De Carlo F, Peele AG (2010) Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 47:866–871

    Article  CAS  PubMed  Google Scholar 

  44. Mader KS, Schneider P, Muller R, Stampanoni M (2013) A quantitative framework for the 3D characterization of the osteocyte lacunar system. Bone 57:142–154

    Article  PubMed  Google Scholar 

  45. Qiu S, Rao DS, Palnitkar S, Parfitt AM (2006) Differences in osteocyte and lacunar density between Black and White American women. Bone 38:130–135

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This project was partially funded by Merck, Inc. The bone biopsies were obtained in a project originally supported by NIH Grants AR39221 and AG04275 (Dr. Recker, PI). Purchase of the 3D X-Ray Microscope (MicroXCT-200; Carl Zeiss X-Ray Microscopy; Pleasanton, CA) was funded by NIH-SIG (1S10OD016333-01, Dr. Akhter, PI). Thanks to Mr. Brad Hugenroth for his input and editing.

Author information

Authors and Affiliations

  1. Osteoporosis Research Center (ORC), Creighton University of School of Medicine, Suite #4820, 601 North 30th Street, Omaha, NE, 68131, USA

    Mohammed P. Akhter, D. B. Kimmel, J. M. Lappe & R. R. Recker

Authors
  1. Mohammed P. Akhter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. B. Kimmel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. M. Lappe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. R. Recker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohammed P. Akhter.

Ethics declarations

Conflict of interest

Dr. Mohammed Akhter, Dr. Don Kimmel, Dr. Joan Lappe, and Dr. Robert Recker have no conflict of interests to disclose.

Human and Animal Rights and Informed Consent

Analyses were performed on bone biopsies collected in an already completed study. No patient’s informed consent was needed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akhter, M.P., Kimmel, D.B., Lappe, J.M. et al. Effect of Macroanatomic Bone Type and Estrogen Loss on Osteocyte Lacunar Properties in Healthy Adult Women. Calcif Tissue Int 100, 619–630 (2017). https://doi.org/10.1007/s00223-017-0247-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-017-0247-6

Keywords

Search

Navigation