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Mineral maturity and crystallinity index are distinct characteristics of bone mineral

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Abstract

The purpose of this study was to test the hypothesis that mineral maturity and crystallinity index are two different characteristics of bone mineral. To this end, Fourier transform infrared microspectroscopy (FTIRM) was used. To test our hypothesis, synthetic apatites and human bone samples were used for the validation of the two parameters using FTIRM. Iliac crest samples from seven human controls and two with skeletal fluorosis were analyzed at the bone structural unit (BSU) level by FTIRM on sections 2–4 μm thick. Mineral maturity and crystallinity index were highly correlated in synthetic apatites but poorly correlated in normal human bone. In skeletal fluorosis, crystallinity index was increased and maturity decreased, supporting the fact of separate measurement of these two parameters. Moreover, results obtained in fluorosis suggested that mineral characteristics can be modified independently of bone remodeling. In conclusion, mineral maturity and crystallinity index are two different parameters measured separately by FTIRM and offering new perspectives to assess bone mineral traits in osteoporosis.

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References

  1. Green J (1994) The physicochemical structure of bone: cellular and noncellular elements. Miner Electrolyte Metab 20:7–15

    CAS  PubMed  Google Scholar 

  2. Cazalbou S (2000) Ph.D. thesis. University of Toulouse, France

  3. 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 

  4. Barry AB, Baig AA, Miller SC, Higuchi WI (2002) Effect of age on rat bone solubility and crystallinity. Calcif Tissue Int 71:167–171

    Article  CAS  PubMed  Google Scholar 

  5. Ager JW, Nalla RK, Breeden KL, Ritchie RO (2005) Deep-ultraviolet Raman spectroscopy study of the effect of aging on human cortical bone. J Biomed Opt 10:034012

    Article  CAS  PubMed  Google Scholar 

  6. Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB (2003) Aging of microstructural compartments in human compact bone. J Bone Miner Res 18:1012–1019

    Article  CAS  PubMed  Google Scholar 

  7. 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  CAS  PubMed  Google Scholar 

  8. Legeros RZ (1981) Apatites in biological systems. Prog Crystal Growth Charact 4:1–45

    Article  CAS  Google Scholar 

  9. 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 ν(4) PO4 3− vibration. Biochim Biophys Acta 1527:11–19

    CAS  PubMed  Google Scholar 

  10. 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

    CAS  PubMed  Google Scholar 

  11. Pleshko N, Boskey A, Mendelsohn R (1991) Novel infrared spectroscopic method for the determination of crystallinity of hydroxyapatite minerals. Biophys J 60:786–793

    Article  CAS  PubMed  Google Scholar 

  12. 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. I. Investigations in the upsilon 4 PO4 domain. Calcif Tissue Int 46:384–394

    Article  CAS  PubMed  Google Scholar 

  13. Rey C, Shimizu M, Collins B, Glimcher MJ (1991) Resolution-enhanced Fourier transform infrared spectroscopy study of the environment of phosphate ion in the early deposits of a solid phase of calcium phosphate in bone and enamel and their evolution with age. 2. Investigations in the ν3PO4 domain. Calcif Tissue Int 49:383–388

    Article  CAS  PubMed  Google Scholar 

  14. Akkus O, Adar F, Schaffler MB (2004) Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone (NY) 34:443–453

    CAS  Google Scholar 

  15. Morris MD, Finney WF, Rajachar RM, Kohn DH (2004) Bone tissue ultrastructural response to elastic deformation probed by Raman spectroscopy. Faraday Discuss 126:159–168 discussion 169–183

    Article  CAS  PubMed  Google Scholar 

  16. Tarnowski CP, Ignelzi MA Jr, Wang W, Taboas JM, Goldstein SA, Morris MD (2004) Earliest mineral and matrix changes in force-induced musculoskeletal disease as revealed by Raman microspectroscopic imaging. J Bone Miner Res 19:64–71

    Article  PubMed  Google Scholar 

  17. Carden A, Rajachar RM, Morris MD, Kohn DH (2003) Ultrastructural changes accompanying the mechanical deformation of bone tissue: a Raman imaging study. Calcif Tissue Int 72:166–175

    Article  CAS  PubMed  Google Scholar 

  18. Miller LM, Little W, Schirmer A, Sheik F, Busa B, Judex S (2007) Accretion of bone quantity and quality in the developing mouse skeleton. J Bone Miner Res 22:1037–1045

    Article  PubMed  Google Scholar 

  19. Carden A, Morris MD (2000) Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt 5:259–268

    Article  CAS  PubMed  Google Scholar 

  20. Fratzl P, Gupta HS, Paschalis EP, Roschger P (2004) Structure and mechanical quality of the mineral quality of the collagen-mineral nano-composite in bone. J Mater Chem 14:2115–2123

    Article  CAS  Google Scholar 

  21. Paschalis EP, Glass EV, Donley DW, Eriksen EF (2005) Bone mineral and collagen quality in iliac crest biopsies of patients given teriparatide: new results from the fracture prevention trial. J Clin Endocrinol Metab 90:4644–4649

    Article  CAS  PubMed  Google Scholar 

  22. Miller LM, Novatt JT, Hamerman D, Carlson CS (2004) Alterations in mineral composition observed in osteoarthritic joints of cynomolgus monkeys. Bone (NY) 35:498–506

    CAS  Google Scholar 

  23. Huang RY, Miller LM, Carlson CS, Chance MR (2003) In situ chemistry of osteoporosis revealed by synchrotron infrared microspectroscopy. Bone (NY) 33:514–521

    CAS  Google Scholar 

  24. 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 

  25. Gee A, Dietz VR (1955) Pyrophosphate formation upon ignition of precipitated basic calcium phosphate. J Am Chem Soc 77:2961–2965

    Article  CAS  Google Scholar 

  26. Shemesh A (1990) Crystallinity and diagenesis of sedimentary apatites. Geochim Cosmochim Acta 54:2433–2438

    Article  CAS  Google Scholar 

  27. Termine JD, Posner AS (1966) Infra-red determination of the percentage of crystallinity in apatitic calcium phosphates. Nature (Lond) 211:268–270

    Article  CAS  Google Scholar 

  28. Frazier PD, Little MF, Casciani FS (1967) X-ray diffraction analysis of human enamel containing different amounts of fluoride. Arch Oral Biol 12:35–42

    Article  CAS  PubMed  Google Scholar 

  29. Bohic S, Heymann D, Pouezat JA, Gauthier O, Daculsi G (1998) Transmission FT-IR microspectroscopy of mineral phases in calcified tissues. C R Acad Sci III 321:865–876

    CAS  PubMed  Google Scholar 

  30. Gadaleta SJ, Paschalis EP, Betts F, Mendelsohn R, Boskey AL (1996) Fourier transform infrared spectroscopy of the solution-mediated conversion of amorphous calcium phosphate to hydroxyapatite: new correlations between X-ray diffraction and infrared data. Calcif Tissue Int 58:9–16

    Article  CAS  PubMed  Google Scholar 

  31. 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 (NY) 25:287–293

    CAS  Google Scholar 

  32. Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL (1997) FTIR microspectroscopic analysis of human iliac crest biopsies from untreated osteoporotic bone. Calcif Tissue Int 61:487–492

    Article  CAS  PubMed  Google Scholar 

  33. 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  CAS  PubMed  Google Scholar 

  34. Glimcher MG (1998) The nature of the mineral phase in bone: biological and clinical implications. In: Avioli LV, Krane SM (eds) Metabolic bone disease. Academic Press, San Diego, pp 23–50

    Google Scholar 

  35. Jager C, Welzel T, Meyer-Zaika W, Epple M (2006) A solid-state NMR investigation of the structure of nanocrystalline hydroxyapatite. Magn Reson Chem 44:573–580

    Article  PubMed  CAS  Google Scholar 

  36. Boskey A, Maresca M, Appel J (1989) The effects of noncollagenous matrix proteins on hydroxyapatite formation and proliferation in a collagen gel system. Connect Tissue Res 21:171–176 discussion 177–178

    Article  CAS  PubMed  Google Scholar 

  37. Boskey AL (1989) Noncollagenous matrix proteins and their role in mineralization. Bone Miner 6:111–123

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  39. Dziak KL, Akkus O (2008) Effects of polyelectrolytic peptides on the quality of mineral crystals grown in vitro. J Bone Miner Metab 26:569–575

    Article  CAS  PubMed  Google Scholar 

  40. Rey C, Beshah K, Griffin R, Glimcher MJ (1991) Structural studies of the mineral phase of calcifying cartilage. J Bone Miner Res 6:515–525

    Article  CAS  PubMed  Google Scholar 

  41. Pucéat E, Reynard B, Lécuyer C (2004) Can crystallinity be used to determine the degree of chemical alteration of biogenic apatites? Chem Geol 205:83–97

    Article  CAS  Google Scholar 

  42. Runt J, Kanchanasopa M. Crystallinity determination. In: Encyclopedia of polymer science and technology, vol 9. Wiley, New York, pp 446–464

  43. Ferrari AC, Robertson J (2004) Raman spectroscopy of amorphous nanostructured, diamond-like carbon, and nanodiamond. Philos Trans R Soc Lond A 362:2477–2512

    Article  CAS  Google Scholar 

  44. Fitzer EG E, Rozploch F, Steinert D (1987) Application of laser-Raman spectroscopy for characterization of carbon fibres. High Temp High Press 19:537–544

    Google Scholar 

  45. Nasdala L, Pidgeon RT, Wolf D (1996) Heterogeneous metamictization of zircon on a microscale. Geochim Cosmochim Acta 60:1091–1097

    Article  CAS  Google Scholar 

  46. Bala Y, Farlay D, Delmas PD, Meunier PJ, Boivin G (2009) Time sequence of secondary mineralization and microhardness in cortical and cancellous bone from ewes. Bone. doi:10.1016/j.bone.2009.11.032

  47. Grynpas MD (1990) Fluoride effects on bone crystals. J Bone Miner Res 5(suppl 1):S169–S175

    Article  Google Scholar 

  48. Posner AS, Eanes ED, Harper RA, Zipkin I (1963) X-ray diffraction analysis of the effect of fluoride on human bone apatite. Arch Oral Biol 168:549–570

    Article  Google Scholar 

  49. Bang S, Boivin G, Gerster JC, Baud CA (1985) Distribution of fluoride in calcified cartilage of a fluoride-treated osteoporotic patient. Bone (NY) 6:207–210

    CAS  Google Scholar 

  50. Fratzl P, Roschger P, Eschberger J, Abendroth B, Klaushofer K (1994) Abnormal bone mineralization after fluoride treatment in osteoporosis: a small-angle X-ray-scattering study. J Bone Miner Res 9:1541–1549

    Article  CAS  PubMed  Google Scholar 

  51. Boivin G, Chavassieux P, Chapuy MC, Baud CA, Meunier PJ (1989) Skeletal fluorosis: histomorphometric analysis of bone changes and bone fluoride content in 29 patients. Bone (NY) 10:89–99

    CAS  Google Scholar 

  52. Faibish D, Ott SM, Boskey AL (2006) Mineral changes in osteoporosis: a review. Clin Orthop Relat Res 443:28–38

    Article  PubMed  Google Scholar 

  53. Landis WJ (1995) The strength of a calcified tissue depends in part on the molecular structure and organization of its constituent mineral crystals in their organic matrix. Bone (NY) 16:533–544

    CAS  Google Scholar 

  54. Chachra D, Turner CH, Dunipace AJ, Grynpas MD (1999) The effect of fluoride treatment on bone mineral in rabbits. Calcif Tissue Int 64:345–351

    Article  CAS  PubMed  Google Scholar 

  55. Turner CH, Garetto LP, Dunipace AJ, Zhang W, Wilson ME, Grynpas MD, Chachra D, McClintock R, Peacock M, Stookey GK (1997) Fluoride treatment increased serum IGF-1, bone turnover, and bone mass, but not bone strength, in rabbits. Calcif Tissue Int 61:77–83

    Article  CAS  PubMed  Google Scholar 

  56. Turner CH, Hasegawa K, Zhang W, Wilson M, Li Y, Dunipace AJ (1995) Fluoride reduces bone strength in older rats. J Dent Res 74:1475–1481

    Article  CAS  PubMed  Google Scholar 

  57. Turner CH, Boivin G, Meunier PJ (1993) A mathematical model for fluoride uptake by the skeleton. Calcif Tissue Int 52:130–138

    Article  CAS  PubMed  Google Scholar 

  58. Li Y, Liang C, Slemenda CW, Ji R, Sun S, Cao J, Emsley CL, Ma F, Wu Y, Ying P, Zhang Y, Gao S, Zhang W, Katz BP, Niu S, Cao S, Johnston CC Jr (2001) Effect of long-term exposure to fluoride in drinking water on risks of bone fractures. J Bone Miner Res 16:932–939

    Article  CAS  PubMed  Google Scholar 

  59. Yerramshetty JS, Akkus O (2008) The associations between mineral crystallinity and the mechanical properties of human cortical bone. Bone (NY) 42:476–482

    CAS  Google Scholar 

  60. Tadano S, Giri B, Sato T, Fujisaki K, Todoh M (2008) Estimating nanoscale deformation in bone by X-ray diffraction imaging method. J Biomech 41:945–952

    Article  PubMed  Google Scholar 

  61. Giri B, Tadano S, Fujisaki K, Sasaki N (2009) Deformation of mineral crystals in cortical bone depending on structural anisotropy. Bone (NY) 44:1111–1120

    Google Scholar 

  62. Durchschlag E, Paschalis EP, Zoehrer R, Roschger P, Fratzl P, Recker R, Phipps R, Klaushofer K (2006) Bone material properties in trabecular bone from human iliac crest biopsies after 3- and 5-year treatment with risedronate. J Bone Miner Res 21:1581–1590

    Article  CAS  PubMed  Google Scholar 

  63. Hanschin RG, Stern WB (1995) X-ray diffraction studies on the lattice perfection of human bone apatite (crista iliaca). Bone (NY) 16:355S–363S

    CAS  Google Scholar 

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Acknowledgments

The authors express their gratitude to Ruben Vera (Centre de Diffractométrie Henri Longchambon, Université de Lyon, France) for performing the XRD analyses, and to Monique Arlot for her help in statistical analysis. This work was supported in part by an unrestricted educational grant from Eli Lilly to INSERM.

Conflict of interest statement

The authors have no conflict of interest.

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Authors and Affiliations

  1. Faculté de Médecine R. Laennec, INSERM Unité 831, Université de Lyon, Rue Guillaume Paradin, 69372, Lyon Cedex 08, France

    Delphine Farlay & Georges Boivin

  2. CECOMO, Université de Lyon, Campus de la Doua, Villeurbanne, France

    Gérard Panczer

  3. ENSIACET, Toulouse, France

    Christian Rey

Authors
  1. Delphine Farlay
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  2. Gérard Panczer
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  3. Christian Rey
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  4. Pierre D. Delmas
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  5. Georges Boivin
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Corresponding author

Correspondence to Delphine Farlay.

Additional information

Pierre Delmas deceased July 23, 2008.

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Farlay, D., Panczer, G., Rey, C. et al. Mineral maturity and crystallinity index are distinct characteristics of bone mineral. J Bone Miner Metab 28, 433–445 (2010). https://doi.org/10.1007/s00774-009-0146-7

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  • DOI: https://doi.org/10.1007/s00774-009-0146-7

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