Advertisement

Anisotropic aspects of solubility behavior in the demineralization of cortical bone revealed by XRD analysis

  • Sergei Danilchenko
  • Aleksei KalinkevichEmail author
  • Mykhailo Zhovner
  • Vladimir Kuznetsov
  • He Li
  • Jufang Wang
Original Paper

Abstract

Dissolution of cortical bone mineral under demineralization in 0.1 M HCl and 0.1 M EDTA solutions is studied by X-ray diffraction (XRD). The bone specimens (in the form of planar oriented pieces) were cut from a diaphysial fragment of a mature mammal bone so that a cross-section surface and a longitudinal section surface could be analyzed individually. This permitted to compare the dissolution behavior of bone apatite of different morphologies: crystals having the c-axis of the hexagonal unit-cell generally parallel to the long axis of the bone (major morphology) and those having the c-axis almost perpendicular to the bone axis (minor morphology). For these two types of morphology, the crystallite sizes in two mutually perpendicular directions (namely, [002] and [310]) were estimated by Scherrer formula in the initial and the stepwise-demineralized specimens. The data obtained reveal that the crystals belonging to the minor morphology dissolve faster than the crystals of the major morphological type, despite the fact that the crystallites of the minor morphology seem to be only a little smaller than those of the major morphology; the apatite crystallites irrespective of the morphology type are elongated in the c-axis direction. We hypothesize that the revealed difference in solubility may be caused by diverse chemical modifications of apatite of these two morphological types, since the solubility of apatite is strictly regulated by anionic and cationic substitutions in the lattice. The anisotropy effect in solubility of bone mineral seems to be functionally predetermined and this should be a crucial factor in the resorption and remodeling behavior of a bone. Some challenges arising at XRD examination of partially decalcified cortical bone blocks are discussed, as well as the limitations of estimation of bone crystallite size by XRD line-broadening analysis.

Keywords

Apatite X-ray diffraction Cortical bone Crystal orientation Morphology Demineralization Crystallite size 

Notes

Acknowledgements

This work was partially supported by grants from the International Science & Technology Cooperation Program of China (ISTCP, NO. 2015DFR30940), Special Program from Chinese Academy of Science in Cooperation with Russia, Ukraine and the Republic of Belarus (2015, 2017) and the Introduced Intelligence project from the State Administration of Foreign Experts Affairs P.R. China (2016).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    LeGeros, R.Z.: Apatites in biological systems. Prog. Cryst. Growth Charact. Mater. 4(1), 1–45 (1981)Google Scholar
  2. 2.
    Rey, C., Combes, C., Drouet, C., Glimcher, M.J.: Bone mineral: update on chemical composition and structure. Osteoporos. Int. 20(6), 1013–1021 (2009)CrossRefGoogle Scholar
  3. 3.
    Combes, C., Cazalbou, S., Rey, C.: Apatite biominerals. Minerals 6(2), 34 (2016).  https://doi.org/10.3390/min6020034 CrossRefGoogle Scholar
  4. 4.
    Robinson, R.A.: An electron-microscopic study of the crystalline inorganic component of bone and its relationship to the organic matrix. J. Bone Joint Surg. Am. 34(2), 389–476 (1952)CrossRefGoogle Scholar
  5. 5.
    Eppell, S.J., Tong, W., Katz, J.L., Kuhn, L., Glimcher, M.J.: Shape and size of isolated bone mineralites measured using atomic force microscopy. J. Orthop. Res. 19(6), 1027–1034 (2001)CrossRefGoogle Scholar
  6. 6.
    Carlström, D., Glas, J.E.: The size and shape of the apatite crystallites in bone as determined from line-broadening measurements on oriented specimens. Biochim. Biophys. Acta 35, 46–53 (1959)CrossRefGoogle Scholar
  7. 7.
    Handschin, R.G., Stern, W.B.: X-ray diffraction studies on the lattice perfection of human bone apatite (Crista iliaca). Bone 16(4), S355–S363 (1995)CrossRefGoogle Scholar
  8. 8.
    Rindby, A., Voglis, P., Engström, P.: Microdiffraction studies of bone tissues using synchrotron radiation. Biomaterials 19(22), 2083–2090 (1998)CrossRefGoogle Scholar
  9. 9.
    Sakae, T., Kono, T., Okada, H., Nakada, H., Ogawa, H., Tsukioka, T., Kaneda, T.: X-ray micro-diffraction analysis revealed the crystallite size variation in the neighboring regions of a small bone mass. J. Hard Tissue Biol. 26(1), 103–107 (2017)CrossRefGoogle Scholar
  10. 10.
    Lees, S.: A model for the distribution of HAP crystallites in bone—an hypothesis. Calci. Tissue Int. 27(1), 53–56 (1979)CrossRefGoogle Scholar
  11. 11.
    Matsushima, N., Akiyama, M., Terayama, Y.: Quantitative analysis of the orientation of mineral in bone from small-angle X-ray scattering patterns. Jpn. J. Appl. Phys. 21(1), 186–189 (1982)ADSCrossRefGoogle Scholar
  12. 12.
    Fratzl, P., Schreiber, S., Klaushofer, K.: Bone mineralization as studied by small-angle X-ray scattering. Connect. Tissue Res. 34(4), 247–254 (1996)CrossRefGoogle Scholar
  13. 13.
    Wenk, H.R., Heidelbach, F.: Crystal alignment of carbonated apatite in bone and calcified tendon: results from quantitative texture analysis. Bone 24(4), 361–369 (1999)CrossRefGoogle Scholar
  14. 14.
    Sasaki, N., Matsushima, N., Ikawa, T., Yamamura, H., Fukuda, A.: Orientation of bone mineral and its role in the anisotropic mechanical properties of bone: transverse anisotropy. J. Biomech. 22(2), 157–164 (1989)CrossRefGoogle Scholar
  15. 15.
    Sasaki, N., Sudoh, Y.: X-ray pole figure analysis of apatite crystals and collagen molecules in bone. Calcif. Tissue Int. 60(4), 361–367 (1997)CrossRefGoogle Scholar
  16. 16.
    Klug, H., Alexander, L.: X-Ray Diffraction Procedure for Polycrystallite and Amorphous Materials. Wiley, New York (1974)Google Scholar
  17. 17.
    Boskey, A.: Bone mineral crystal size. Osteoporos. Int. 14, S16–S21 (2003)CrossRefGoogle Scholar
  18. 18.
    Horvath, A.L.: Solubility of structurally complicated materials: II. Bone. J. Phys. Chem. Ref. Data 35(4), 1653–1668 (2006)ADSMathSciNetCrossRefGoogle Scholar
  19. 19.
    Figueiredo, M., Cunha, S., Martins, G., Freitas, J., Judas, F., Figueiredo, H.: Influence of hydrochloric acid concentration on the demineralization of cortical bone. Chem. Eng. Res. Des. 89(1), 116–124 (2011)CrossRefGoogle Scholar
  20. 20.
    Castro-Ceseña, A.B., Novitskaya, E.E., Chen, P.Y., Hirata, G.A., McKittrick, J.: Kinetic studies of bone demineralization at different HCl concentrations and temperatures. Mat. Sci. Eng. C 31(3), 523–530 (2011)CrossRefGoogle Scholar
  21. 21.
    Danilchenko, S.N., Moseke, C., Sukhodub, L.F., Sulkio-Cleff, B.: X-ray diffraction studies of bone apatite under acid demineralization. Cryst. Res. Technol. 39(1), 71–77 (2004)CrossRefGoogle Scholar
  22. 22.
    El-Bassyouni, G.T., Guirguis, O.W., Abdel-Fattah, W.I.: Morphological and macrostructural studies of dog cranial bone demineralized with different acids. Curr. Appl. Phys. 13(5), 864–874 (2013)ADSCrossRefGoogle Scholar
  23. 23.
    Lewandrowski, K.U., Tomford, W.W., Michaud, N.A., Schomacker, K.T., Deutsch, T.F.: An electron microscopic study on the process of acid demineralization of cortical bone. Calcif. Tissue Int. 61(4), 294–297 (1997)CrossRefGoogle Scholar
  24. 24.
    Walsh, W.R., Christiansen, D.L.: Demineralized bone matrix as a template for mineral-organic composites. Biomaterials 16(18), 1363–1371 (1995)CrossRefGoogle Scholar
  25. 25.
    Teitelbaum, S.L.: Bone resorption by osteoclasts. Science 289(5484), 1504–1508 (2000)ADSCrossRefGoogle Scholar
  26. 26.
    Akbay, A., Bozkurt, G., Ilgaz, O., Palaoglu, S., Akalan, N., Benzel, E.C.: A demineralized calf vertebra model as an alternative to classic osteoporotic vertebra models for pedicle screw pullout studies. Eur. Spine J. 17(3), 468–473 (2008)CrossRefGoogle Scholar
  27. 27.
    Lee, C.Y., Chan, S.H., Lai, H.Y., Lee, S.T.: A method to develop an in vitro osteoporosis model of porcine vertebrae: histological and biomechanical study: laboratory investigation. J. Neurosurg. Spine 14(6), 789–798 (2011)CrossRefGoogle Scholar
  28. 28.
    Ehrlich, H., Koutsoukos, P.G., Demadis, K.D., Pokrovsky, O.S.: Principles of demineralization: modern strategies for the isolation of organic frameworks: part II. Decalcification. Micron 40(2), 169–193 (2009)CrossRefGoogle Scholar
  29. 29.
    Bish, D.L., Post, J.E. (eds.): Modern powder diffraction. In: Ribbe, P.H. (ed.) Reviews in Mineralogy, 20. Mineralogical Society of America, Washington, DC (1989)Google Scholar
  30. 30.
    Langford, J.I., Wilson, A.J.C.: Scherrer after sixty years: a survey and some new results in the determination of crystallite size. J. Appl. Crystallogr. 11(2), 102–113 (1978)CrossRefGoogle Scholar
  31. 31.
    Danilchenko, S.N., Kukharenko, O.G., Moseke, C., Protsenko, I.Y., Sukhodub, L.F., Sulkio-Cleff, B.: Determination of the bone mineral crystallite size and lattice strain from diffraction line broadening. Cryst. Res. Technol. 37(11), 1234–1240 (2002)CrossRefGoogle Scholar
  32. 32.
    Doi, Y., Moriwaki, Y., Aoba, T., Takahashi, J., Joshin, K.: ESR and IR studies of carbonate-containing hydroxyapatites. Calcif. Tissue Int. 34(1), 178–181 (1982)CrossRefGoogle Scholar
  33. 33.
    Rogers, K., Beckett, S., Kuhn, S., Chamberlain, A., Clement, J.: Contrasting the crystallinity indicators of heated and diagenetically altered bone mineral. Palaeogeogr. Palaeoclimatol. Palaeoecol. 296(1), 125–129 (2010)CrossRefGoogle Scholar
  34. 34.
    Pan, H., Tao, J., Yu, X., Fu, L., Zhang, J., Zeng, X., Tang, R.: Anisotropic demineralization and oriented assembly of hydroxyapatite crystals in enamel: smart structures of biominerals. J. Phys. Chem. B 112(24), 7162–7165 (2008)CrossRefGoogle Scholar
  35. 35.
    Tseng, W.J., Lin, C.C., Shen, P.W., Shen, P.: Directional/acidic dissolution kinetics of (OH, F, Cl)-bearing apatite. J. Biomed. Mater. Res. A 76(4), 753–764 (2006)CrossRefGoogle Scholar
  36. 36.
    Turunen, M.J., Kaspersen, J.D., Olsson, U., Guizar-Sicairos, M., Bech, M., Schaff, F., Isaksson, H.: Bone mineral crystal size and organization vary across mature rat bone cortex. J. Struct. Biol. 195(3), 337–344 (2016)CrossRefGoogle Scholar
  37. 37.
    Kaspersen, J.D., Turunen, M.J., Mathavan, N., Lages, S., Pedersen, J.S., Olsson, U., Isaksson, H.: Small-angle X-ray scattering demonstrates similar nanostructure in cortical bone from young adult animals of different species. Calcif. Tissue Int. 99, 76–87 (2016)CrossRefGoogle Scholar
  38. 38.
    Weiner, S., Wagner, H.D.: The material bone: structure-mechanical function relations. Annu. Rev. Mater. Sci. 28(1), 271–298 (1998)ADSCrossRefGoogle Scholar
  39. 39.
    Baig, A.A., Fox, J.L., Young, R.A., Wang, Z., Hsu, J., Higuchi, W.I., Otsuka, M.: Relationships among carbonated apatite solubility, crystallite size, and microstrain parameters. Calcif. Tissue Int. 64(5), 437–449 (1999)CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sergei Danilchenko
    • 1
  • Aleksei Kalinkevich
    • 1
    Email author
  • Mykhailo Zhovner
    • 1
  • Vladimir Kuznetsov
    • 1
  • He Li
    • 2
  • Jufang Wang
    • 2
  1. 1.Institute for Applied Physics, NAS of UkraineSumyUkraine
  2. 2.Institute of Modern Physics, CASLanzhouChina

Personalised recommendations