Skip to main content

Advertisement

Log in

A Comparison of the Physical and Chemical Differences Between Cancellous and Cortical Bovine Bone Mineral at Two Ages

  • Published:
Calcified Tissue International Aims and scope Submit manuscript

An Erratum to this article was published on 11 March 2009

Abstract

To assess possible differences between the mineral phases of cortical and cancellous bone, the structure and composition of isolated bovine mineral crystals from young (1–3 months) and old (4–5 years) postnatal bovine animals were analyzed by a variety of complementary techniques: chemical analyses, Fourier transform infrared spectroscopy (FTIR), X-ray diffraction (XRD), and 31P solid-state magic angle spinning nuclear magnetic resonance spectroscopy (NMR). This combination of methods represents the most complete physicochemical characterization of cancellous and cortical bone mineral completed thus far. Spectra obtained from XRD, FTIR, and 31P NMR all confirmed that the mineral was calcium phosphate in the form of carbonated apatite; however, a crystal maturation process was evident between the young and old and between cancellous and cortical mineral crystals. Two-way analyses of variance showed larger increases of crystal size and Ca/P ratio for the cortical vs. cancellous bone of 1–3 month than the 4–5 year animals. The Ca/(P + CO3) remained nearly constant within a given bone type and in both bone types at 4–5 years. The carbonate and phosphate FTIR band ratios revealed a decrease of labile ions with age and in cortical, relative to cancellous, bone. Overall, the same aging or maturation trends were observed for young vs. old and cancellous vs. cortical. Based on the larger proportion of newly formed bone in cancellous bone relative to cortical bone, the major differences between the cancellous and cortical mineral crystals must be ascribed to differences in average age of the crystals.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Glimcher MJ (1998) The nature of the mineral phase in bone: biological and clinical applications. In: Alvioli L, Krane S (eds) Metabolic bone disease. Academic Press, New York, pp 23–50

    Chapter  Google Scholar 

  2. LeGeros RZ (1991) Calcium phosphates in oral biology and medicine. Karger, Basel, p 110

    Google Scholar 

  3. Roufosse AH, Landis WJ, Sabine WK, Glimcher MJ (1979) Identification of brushite in newly deposited bone mineral from embryonic chicks. J Ultrastruct Res 68:235–255

    Article  PubMed  CAS  Google Scholar 

  4. Bonar LC, Grynpas MD, Glimcher MJ (1984) Failure to detect crystalline brushite in embryonic chick and bovine bone by X-ray diffraction. J Ultrastruct Res 86:93–99

    Article  PubMed  CAS  Google Scholar 

  5. Biltz RM, Pellegrino ED (1971) The hydroxyl content of calcified tissue mineral. Calcif Tissue Res 36:259–263

    Article  Google Scholar 

  6. Rey C, Miquel JL, Facchini L, Legrand AP, Glimcher MJ (1995) Hydroxyl groups in bone mineral. Bone 16:583–586

    Article  PubMed  CAS  Google Scholar 

  7. Loong C-K, Rey C, Kuhn LT, Combes C, Wu Y, Chen S-H, Glimcher MJ (2000) Evidence of hydroxyl-ion deficiency in bone apatites: an inelastic neutron scattering study. Bone 26:599–602

    Article  PubMed  CAS  Google Scholar 

  8. Cho G, Wu Y, Ackerman JL (2003) Detection of hydroxyl ions in bone mineral by solid-state NMR spectroscopy. Science 300:1123–1127

    Article  PubMed  CAS  Google Scholar 

  9. Wilson EE, Awonusi A, Morris MD, Kohn DH, Tecklenburg MM, Beck LW (2005) Highly ordered interstitial water observed in bone by nuclear magnetic resonance. J Bone Miner Res 20:625–634

    Article  PubMed  CAS  Google Scholar 

  10. Wu Y, Glimcher MJ, Rey C, Ackerman JL (1994) A unique protonated phosphate group in bone mineral not present in synthetic calcium phosphates. J Mol Biol 244:423–435

    Article  PubMed  CAS  Google Scholar 

  11. Roufosse AH, Aue WP, Roberts JE, Glimcher MJ, Griffin RG (1984) Investigation of the mineral phases of bone by solid-state phosphorus-31 magic angle sample spinning nuclear magnetic resonance. Biochemistry 23:6115–6120

    Article  PubMed  CAS  Google Scholar 

  12. Legros R, Bonel G, Montel G, Balmain-OLigo N, Juster M (1977) Systematic study of the variations in mineral composition of different bones from various animals according to their localization [in French]. C R Acad Sci Hebd Seances Acad Sci D 285:1519–1522

    PubMed  CAS  Google Scholar 

  13. Bigi A, Cojazzi G, Panzavolta S, Ripamonti A, Roveri N, Romanello M, Noris Suarez K, Moro L (1997) Chemical and structural characterization of the mineral phase from cortical and trabecular bone. J Inorg Chem 68:45–51

    CAS  Google Scholar 

  14. Mokrzynski S (1994) Analysis of mineral composition of femoral bones in the human fetus [in Polish]. An Acad Med Stetin 40:23–35

    CAS  Google Scholar 

  15. Boskey AL, Gadaleta S, Gundberg C, Doty SB, Ducy P, Karsenty G (1998) Fourier transform infrared microspectroscopy analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone 23:187–196

    Article  PubMed  CAS  Google Scholar 

  16. Legros R, Balmain N, Bonel G (1987) Age-related changes in mineral of rat and bovine cortical bone. Calcif Tissue Int 41:137–144

    Article  PubMed  CAS  Google Scholar 

  17. Rey C, Renugopalakrishnan V, Collins B, Glimcher MJ (1991) Fourier transform infrared spectroscopic study of the carbonate ions in bone mineral during aging. Calcif Tissue Int 49:251–258

    Article  PubMed  CAS  Google Scholar 

  18. Boskey AL, DiCarlo E, Paschalis E, West P, Mendelsohn R (2005) Comparison of mineral quality and quantity in iliac crest biopsies from high- and low-turnover osteoporosis: an FT-IR microspectroscopic investigation. Osteoporos Int 16:2031–2038

    Article  PubMed  CAS  Google Scholar 

  19. Tarnowski CP, Ignelzi MA Jr, Morris MD (2002) Mineralization of developing mouse calvaria as revealed by Raman microspectroscopy. J Bone Miner Res 17:1118–1126

    Article  PubMed  Google Scholar 

  20. Miller LM, Vairavamurthy V, Chance MR, Mendelsohn R, Paschalis EP, Betts F, Boskey AL (2001) In situ analysis of mineral content and crystallinity in bone using infrared micro-spectroscopy of the nu4 PO4 3− vibration. Biochim Biophys Acta 1527:11–19

    PubMed  CAS  Google Scholar 

  21. Bonar LC, Roufosse AH, Sabine K, Grynpas MD, Glimcher MJ (1983) X-ray diffraction studies of the crystallinity of bone mineral in newly synthesized and density fractionated bone. Calcif Tiss Res 35:202–209

    Article  CAS  Google Scholar 

  22. Grynpas MD (1976) The crystallinity of bone mineral. J Mater Sci 11:1691–1696

    Article  Google Scholar 

  23. Bonar LC, Roufosse AN, Sabine WK, Grynpas MD, Glimcher MJ (1983) X-ray diffraction studies of the crystallinity of bone mineral in newly synthesized and density fractionated bone. Calcif Tissue Int 35:202–209

    Article  PubMed  CAS  Google Scholar 

  24. Matsushima N, Hikichi K (1989) Age changes in the crystallinity of bone mineral and in the disorder of its crystal. Biochim Biophys Acta 992:155–159

    PubMed  CAS  Google Scholar 

  25. Rey C, Shimizu M, Collins B, Glimcher MJ (1990) Resolution enhanced Fourier transform infrared spectroscopy study of the environment of phosphate ions in the early deposits of a solid phase of calcium phosphate in bone and enamel and their evolution with age. 1: Investigations in the υ4 PO4 domain. Calcif Tissue Int 46:384–394

    Article  PubMed  CAS  Google Scholar 

  26. Rey C, Shimizu M, Collins B, Glimcher MJ (1991) Resolution enhanced Fourier transform infrared spectroscopy study of the environment of phosphate ions in the early deposits of a solid phase of calcium phosphate in bone and enamel and their evolution with age. 2: Investigations in the υ3 PO4 domain. Calcif Tissue Int 49:383–388

    Article  PubMed  CAS  Google Scholar 

  27. Rey C, Hina A, Tofighi A, Glimcher MJ (1995) Maturation of poorly crystalline apatites: chemical and structural aspects in vivo and in vitro. Cells Mater 5:345–356

    CAS  Google Scholar 

  28. Rey C, Glimcher MJ (1992) Short range organization of the Ca-P mineral phase in bone and enamel: changes with age and maturation. In: Slavkin H, Price P (eds) Chemistry and biology of mineralized tissues. Elsevier, San Diego, pp 5–18

    Google Scholar 

  29. Cazalbou S, Combes C, Eichert D, Rey C, Glimcher MJ (2004) Poorly crystalline apatites: evolution and maturation in vitro and in vivo. J Bone Miner Metab 22:310–317

    Article  PubMed  Google Scholar 

  30. Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL (1997) FTIR microspectroscopic analysis of normal human cortical and trabecular bone. Calcif Tissue Int 61:480–486

    Article  PubMed  CAS  Google Scholar 

  31. Handschin RG, Stern WB (1992) Crystallographic lattice refinement of human bone. Calcif Tissue Int 51:111–120

    Article  PubMed  CAS  Google Scholar 

  32. Simmons ED Jr, Pritzker KPH, Grynpas MD (1991) Age-related changes in the human femoral cortex. J Orthop Res 9:155–167

    Article  PubMed  Google Scholar 

  33. Lundon K, Dumitriu M, Grynpas MD (1997) Supraphysiologic levels of testosterone affect cancellous and cortical bone in the young female cynomolgus monkey. Calcif Tissue Int 60:54–62

    Article  PubMed  CAS  Google Scholar 

  34. Kim H-M, Rey C, Glimcher MJ (1995) Isolation of calcium-phosphate crystals of bone by non-aqueous methods at low temperature. J Bone Miner Res 10:1589–1601

    Article  PubMed  CAS  Google Scholar 

  35. Boskey AL, Mendelsohn R (2005) Infrared spectroscopic characterization of mineralized tissues. Vib Spectrosc 38:107–114

    Article  PubMed  CAS  Google Scholar 

  36. Ou-Yang H, Paschalis EP, Mayo WE, Boskey AL, Mendelsohn R (2001) Infrared microscopic imaging of bone: spatial distribution of CO 2-3 . J Bone Miner Res 16:893–900

    Article  PubMed  CAS  Google Scholar 

  37. Ouyang H, Sherman PJ, Paschalis EP, Boskey AL, Mendelsohn R (2004) Fourier transform infrared microscopic imaging: effects of estrogen and estrogen deficiency on fracture healing in rat femurs. Appl Spectrosc 58:1–9

    Article  PubMed  CAS  Google Scholar 

  38. Awonusi A, Morris MD, Tecklenburg MM (2007) Carbonate assignment and calibration in the Raman spectrum of apatite. Calcif Tissue Int 81:46–52

    Article  PubMed  CAS  Google Scholar 

  39. Paschalis EP, DiCarlo E, Betts F, Sherman P, Mendelsohn R, Boskey AL (1996) FTIR microspectroscopic analysis of human osteonal bone. Calcif Tissue Int 59:480–487

    PubMed  CAS  Google Scholar 

  40. Camacho NP, Rinnerthaler S, Paschalis EP, Mendelsohn R, Boskey AL, Fratzl P (1999) Complementary information on bone ultrastructure from scanning small angle X-ray scattering and Fourier-transform infrared microspectroscopy. Bone 25:287–293

    Article  PubMed  CAS  Google Scholar 

  41. Boskey AL, Moore DJ, Amling M, Canalis E, Delany AM (2003) Infrared analysis of the mineral and matrix in bones of osteonectin-null mice and their wildtype controls. J Bone Miner Res 18:1005–1011

    Article  PubMed  CAS  Google Scholar 

  42. Wu Y, Ackerman JL, Strawich ES, Rey C, Kim HM, Glimcher MJ (2003) Phosphate ions in bone: identification of a calcium-organic phosphate complex by 31P solid-state NMR spectroscopy at early stages of mineralization. Calcif Tissue Int 72:610–626

    Article  PubMed  CAS  Google Scholar 

  43. Kaflak A, Chmielewski D, Górecki A, Kolodziejski W (1998) Kinetics of 1H–31P cross polarization in human trabecular bone. Solid State Nucl Magn Reson 10:191–195

    Article  PubMed  CAS  Google Scholar 

  44. Wu Y, Ackerman JL, Kim H-M, Rey C, Barroug A, Glimcher MJ (2002) Nuclear magnetic resonance spin–spin relaxation of the crystals of bone, dental enamel and synthetic hydroxyapatites. J Bone Miner Res 17:472–480

    Article  PubMed  CAS  Google Scholar 

  45. Engleman EE, Jackson LL, Norton DR (1985) Determination of carbonate carbon in geological materials by coulometric titration. Chem Geol 53:125–128

    Article  CAS  Google Scholar 

  46. Klug HP, Alexander LE (1974) X-ray diffraction procedures for polycrystallite and amorphous materials, 2nd edn. Wiley, New York

    Google Scholar 

  47. Rey C, Collins B, Goehl T, Dickson IR, Glimcher MJ (1989) The carbonate environment in bone mineral: a resolution enhanced Fourier transform infrared spectroscopy study. Calcif Tissue Int 45:157–164

    Article  PubMed  CAS  Google Scholar 

  48. Kuhn LT, Wu Y, Rey C, Gerstenfeld LC, Grynpas MD, Ackerman JL, Kim HM, Glimcher MJ (2000) Structure, composition and maturation of newly deposited calcium-phosphate crystals in chicken osteoblast cell cultures. J Bone Miner Res 15:1301–1309

    Article  PubMed  CAS  Google Scholar 

  49. Repo MA, Bockman RS, Betts F, Boskey AL, Alcock NW, Warrel RP Jr (1988) Effect of gallium on bone mineral properties. Calcif Tissue Int 43:300–306

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. Adele Boskey for her review of this manuscript and Dr. Jon Goldberg for his help with the statistical analysis. Supported in part by National Institutes of Health grants R01-AR34081, R01-AG14701, R01-AR42258, and T32-AR07112; a grant from the Peabody Foundation; the American Foundation for Aging Research; and the Orthopaedic Research and Education Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liisa T. Kuhn.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s00223-009-9234-x

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuhn, L.T., Grynpas, M.D., Rey, C.C. et al. A Comparison of the Physical and Chemical Differences Between Cancellous and Cortical Bovine Bone Mineral at Two Ages. Calcif Tissue Int 83, 146–154 (2008). https://doi.org/10.1007/s00223-008-9164-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-008-9164-z

Keywords

Navigation