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Annals of Biomedical Engineering

, Volume 42, Issue 12, pp 2577–2588 | Cite as

Substrate Concentration Influences Effective Radial Diffusion Coefficient in Canine Cortical Bone

  • Kurt Farrell
  • Daniel O’Conor
  • Mariela Gonzalez
  • Caroline Androjna
  • Ronald J. Midura
  • Surendra N. Tewari
  • Joanne BelovichEmail author
Article
  • 228 Downloads

Abstract

Transport of nutrients and waste across osseous tissue is dependent on the dynamic micro and macrostructure of the tissue; however little quantitative data exists examining how this transport occurs across the entire tissue. Here we investigate in vitro radial diffusion across a section of canine tissue, at dimensions of several hundred microns to millimeters, specifically between several osteons connected through a porous microstructure of Volkmann’s canals and canaliculi. The effective diffusion coefficient is measured by a “sample immersion” technique presented here, in which the tissue sample was immersed in solution for 18–30 h, image analysis software was used to quantify the solute concentration profile in the tissue, and the data were fit to a mathematical model of diffusion in the tissue. Measurements of the effective diffusivity of sodium fluorescein using this technique were confirmed using a standard two-chamber diffusion system. As the solute concentration increased, the effective diffusivity decreased, ranging from 1.6 × 10−7 ± 3.2 × 10−8 cm2/s at 0.3 μM to 1.4 × 10−8 ± 1.9 × 10−9 cm2/s at 300 μM. The results show that there is no significant difference in mean diffusivity obtained using the two measurement techniques on the same sample, 3.3 × 10−8 ± 3.3 × 10−9 cm2/s (sample immersion), compared to 4.4 × 10−8 ± 1.1 × 10−8 cm2/s (diffusion chamber).

Keywords

Transport phenomena Bone tissue engineering Fluorescein disodium salt 

Notes

Acknowledgments

The assistance of Dr. Xiang Zhou, Department of Chemistry at CSU, with use of the spectrofluorometer, is gratefully acknowledged. Funds were provided by the Faculty Research and Development Program and the Undergraduate Summer Research Program at CSU.

References

  1. 1.
    Albro, M. B., V. Rajan, R. Li, C. T. Hung, and G. A. Ateshian. Characterization of the concentration-dependence of solute diffusivity and partitioning in a model dextran-agarose transport system. Cell Mol. Bioeng. 2:295–305, 2009.PubMedCentralPubMedCrossRefGoogle Scholar
  2. 2.
    An, Y. H., and R. J. Freidman. Animal Models in Orthopaedic Research. Boca Raton, FL: CRC Press, 1998, 624 pp.Google Scholar
  3. 3.
    Androjna, C., J. E. Gatica, J. M. Belovich, and K. A. Derwin. Oxygen diffusion through natural extracellular matrices: implications for estimating “critical thickness” values in tendon tissue engineering. Tissue Eng. Part A 14:559–569, 2008.PubMedCrossRefGoogle Scholar
  4. 4.
    Cardoso, L., S. P. Fritton, G. Gailani, M. Benalla, and S. C. Cowin. Advances in assessment of bone porosity, permeability and interstitial fluid flow. J. Biomech. 46:2253–2265, 2013.CrossRefGoogle Scholar
  5. 5.
    Champe, P. C., R. A. Harvey, and D. R. Ferrier. Biochemistry, 3rd edn. Baltimore: Lippincott, 2005, pp. 235–238.Google Scholar
  6. 6.
    Ciani, C., D. Sharma, S. B. Doty, and S. P. Fritton. Ovariectomy enhances mechanical load-induced solute transport around osteocytes in rat cancellous bone. Bone 59:229–234, 2014.PubMedCrossRefGoogle Scholar
  7. 7.
    Cussler, E. L. Diffusion: Mass Transfer in Fluid Systems. Cambridge: Cambridge University Press, p. 647, 2009.CrossRefGoogle Scholar
  8. 8.
    Dirksen, T. R., and G. V. Marinetti. Lipids of bovine enamel and dentin and human bone. Tissue Res. 6:1–10, 1970.CrossRefGoogle Scholar
  9. 9.
    Eriksen, E. F. Cellular mechanisms of bone remodeling. Rev. Endocr. Metab. Disord. 11:219–227, 2010.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Fernandez-Seara, M. A., S. L. Wehrli, and F. W. Wehrli. Diffusion of exchangeable water in cortical bone studied by nuclear magnetic resonance. Biophys. J. 82:522–529, 2002.PubMedCentralPubMedCrossRefGoogle Scholar
  11. 11.
    Geankoplis, C. Transport Processes and Separation Process Principles (Includes Unit Operations). Upper Saddle River NJ: Prentice Hall Press, 2003; (1056 pp).Google Scholar
  12. 12.
    Hollis, A. Vitamin D: Synthesis, Metabolism, and Clinical Measurement. Disorders of Bone and Mineral Metabolism. Philadelphia: Lippincott Williams and Wilkins, 2002, 159 pp.Google Scholar
  13. 13.
    Jilka, R. L. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40:1434–1446, 2007.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Knothe Tate, M. L., P. Niederer, and U. Knothe. In vivo tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone 22:107–117, 1998.Google Scholar
  15. 15.
    Knothe Tate, M. L., and U. Knothe. An ex vivo model to study transport processes and fluid flow in loaded bone. J. Biomech. 33:247–254, 2000.Google Scholar
  16. 16.
    Knothe Tate, M. L., U. Knothe, and P. Niederer. Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and functional adaptation. Am. J. Med. Sci. 316:189–195, 1998.Google Scholar
  17. 17.
    Lang, S. B., N. Stipanich, and E. A. Soremi. Diffusion of glucose in stressed and unstressed canine femur in vitro. Ann. N. Y. Acad. Sci. 238:139–148, 1974.PubMedCrossRefGoogle Scholar
  18. 18.
    Lemaire, T., J. Kaiser, S. Naili, and V. Sansalone. Textural versus electrostatic exclusion-enrichment effects in the effective chemical transport within the cortical bone: a numerical investigation. Int. J. Numer. Methods Biomed. Eng. 11:1223–1242, 2013.CrossRefGoogle Scholar
  19. 19.
    Li, W., L. You, M. B. Schaffler, and L. Wang. The dependency of solute diffusion on molecular weight and shape in intact bone. Bone 45:1017–1023, 2009.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    McCauley, L. K., and T. J. Martin. Twenty-five years of PTHrP progress: from cancer hormone to multifunctional cytokine. J. Bone Miner. Res. 27:1231–1239, 2012.PubMedCrossRefGoogle Scholar
  21. 21.
    Montermini, D., C. P. Winlove, and C. Michel. Effects of perfusion rate on permeability of frog and rat mesenteric microvessels to sodium fluorescein. J. Physiol. 543:959–975, 2003.CrossRefGoogle Scholar
  22. 22.
    Morris, M. A., J. A. Lopez-Curto, S. P. Hughes, K. N. An, J. B. Bassingthwaighte, and P. J. Kelly. Fluid spaces in canine bone and marrow. Microvasc. Res. 2:188–200, 1982.CrossRefGoogle Scholar
  23. 23.
    Oliva, A., J. Farina, and M. Llabres. Development of two high-performance liquid chromatographic methods for the analysis and characterization of insulin and its degradation products in pharmaceutical preparations. J. Chromatogr. B Biomed. Sci. Appl. 749:25–34, 2000.PubMedCrossRefGoogle Scholar
  24. 24.
    Patel, R. B., J. M. O’Leary, S. J. Bhatt, A. Vasnja, and M. L. Knothe Tate. Determining the permeability of cortical bone at multiple length scales using fluorescence recovery after photobleaching techniques. Proceedings of the 51st Annual Meeting of the Orthopaedic Research Society, Washington D.C., 2004.Google Scholar
  25. 25.
    Piekarski, K., and M. Munro. Transport mechanism operating between blood supply and osteocytes in long bones. Nature 269:80–82, 1977.PubMedCrossRefGoogle Scholar
  26. 26.
    Pietrzak, W. S., and J. Woodell-May. The composition of human cortical allograft bone derived from FDA/AATB-screened donors. J. Craniofac. Surg. 16:579–585, 2005.PubMedCrossRefGoogle Scholar
  27. 27.
    Potts, J. T. Parathyroid hormone: past and present. J. Endocrinol. 187:311–325, 2005.PubMedCrossRefGoogle Scholar
  28. 28.
    Price, C., X. Zhou, W. Li, and L. Wang. Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J. Bone Miner. Res. 26:277–285, 2011.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Qui, S., D. P. Fyhrie, S. Palnitkar, and D. S. Rao. Histomorphometric assessment of haversian canal and osteocyte lacunae in different-sized osteons in human rib. Anat. Rec. 272A:520–525, 2003.CrossRefGoogle Scholar
  30. 30.
    Schaffler, M. B., and D. B. Burr. Stiffness of compact bone: effects of porosity and density. J. Biomech. 21:13–16, 1988.PubMedCrossRefGoogle Scholar
  31. 31.
    Truskey, G. A., F. Yuan, and D. F. Katz. Transport Phenomena in Biological Systems. Upper Saddle River, NJ: Pearson/Prentice Hall, 2004; (888 pp).Google Scholar
  32. 32.
    Wang, X., J. D. Mabrey, and C. M. Agrawal. An interspecies comparsion of bone fracture properties. Bio-Med. Mater. Eng. 8:1–9, 1998.Google Scholar
  33. 33.
    Wang, X., and Q. Ni. Determination of cortical bone porosity and pore size distribution using a low field pulsed NMR approach. J. Orthop. Res. 21:312–319, 2009.CrossRefGoogle Scholar
  34. 34.
    Wang, L., Y. Wang, Y. Han, S. C. Henderson, R. J. Majeska, S. Weinbaum, and M. B. Schaffler. In situ measurement of solute transport in the bone lacunar-canalicular system. Proc. Natl Acad. Sci. U.S.A. 102:11911–11916, 2005.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Wang, X. Fundamental biomechanics in bone tissue engineering. In: Synthesis Lectures on Tissue Engineering. San Rafael, CA: Morgan & Claypool Publishers, 2010, 225 pp.Google Scholar
  36. 36.
    Wen, D., C. Androjna, A. Vasanji, J. Belovich, and R. J. Midura. Lipids and collagen matrix restrict the hydraulic permeability within the porous compartment of adult cortical bone. Ann. Biomed. Eng. 3:558–569, 2010.CrossRefGoogle Scholar
  37. 37.
    Yang, S., K. F. Leong, Z. Du, and C. K. Chua. The design of scaffolds for use in tissue engineering. Part II. Rapid prototyping techniques. Tissue Eng. 8:1–11, 2002.PubMedCrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2014

Authors and Affiliations

  • Kurt Farrell
    • 1
  • Daniel O’Conor
    • 1
  • Mariela Gonzalez
    • 1
  • Caroline Androjna
    • 2
  • Ronald J. Midura
    • 2
  • Surendra N. Tewari
    • 1
  • Joanne Belovich
    • 1
    Email author
  1. 1.Department of Chemical and Biomedical EngineeringCleveland State UniversityClevelandUSA
  2. 2.Department of Biomedical EngineeringCleveland Clinic Lerner Research InstituteOhioUSA

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