Skip to main content
SpringerLink
Log in

The Pathway of Bone Fluid Flow as Defined by In Vivo Intramedullary Pressure and Streaming Potential Measurements

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

The pathway for intracortical fluid flow response to a step-load was identified in vivo using intramedullary pressure (ImP) and streaming potential (SP) measurements, and allowed the development of a load-induced flow mechanism which considers mechanotransduction and mechanoelectrotransduction phenomena. An avian model was used for monitoring, simultaneously, ImP and SP under axial loading which generated peak strains of approximately 600 microstrain (με). ImP response to step-load decayed more quickly than SP relaxation, in which multiple time constants were observed during the relaxations. While the initial relaxation of SP showed a decay on the order of 200 ms, ImP decayed on the order of approximately 100 ms. After the initial decay (∼200 ms after loading), ImP quickly relaxed to base line, while SP continued to dominate relaxation. It appears that the decay of ImP is indicative of resistive fluid flow occurring primarily in the vasculature and other intraosseous channels such as lacunar-canalicular pores, and that SP represents the fluid flow in the smaller porosities, i.e., lacunar-canalicular system or even microspores. These results suggest that SP and ImP decays are determined by a hierarchical interdependent system of multiple porosities, and that the temporal dynamics of load-bearing define the manner in which the fluid patterns and pressures are distributed. © 2002 Biomedical Engineering Society.

PAC2002: 8719Tt, 8719Rr, 8719Nn

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Chole, R. A., and S. P. Tinling. Incomplete coverage of mammalian bone cell matrix by lining cells. Ann. Otol. Rhinol. Laryngol. 102:543–550, 1993.

    Google Scholar 

  2. Cochran, G. V., M. W. Johnson, M. P. Kadaba, F. Vosburgh, M. W. Ferguson-Pell, and V. R. Palmieri. Piezoelectric internal fixation devices: A new approach to electrical augmentation of osteogenesis. J. Orthop. Res. 3:508–513, 1985.

    Google Scholar 

  3. Cowin, S. C. Bone poroelasticity. J. Biomech. 32:217–238, 1999.

  4. Cowin, S. C., S. Weinbaum, and Y. Zeng. A case for bone canaliculi as the anatomical site of strain generated potentials. J. Biomech. 28:1281–1297, 1995.

    Google Scholar 

  5. Dillaman, R. M. Movement of ferritin in the 2-day-old chick femur. Anat. Rec. 209:445–453, 1984.

    Google Scholar 

  6. Dillaman, R. M., R. D. Roer, and D. M. Gay. Fluid movement in bone: Theoretical and empirical. J. Biomech. 24:163–177, 1991.

    Google Scholar 

  7. Doty, S. D., and B. H. Schofield. Metabolic and structural changes with osteocytes of rat bone. In Calcium Parathyroid Hormone and the Calcitonins, edited by Talmage and Munson. Amsterdam: Excerpta Medica, 1972, pp. 353–364.

    Google Scholar 

  8. Frangos, J. A., T. Y. Huang, and C. B. Clark. Steady shear and step changes in shear stimulate endothelium via independent mechanisms-superposition of transient and sustained nitric oxide production. Biochem. Biophys. Res. Commun. 224:660–665, 1996.

    Google Scholar 

  9. Gross, D., and W. S. Williams. Streaming potential and the electromechanical response of physiologically moist bone. J. Biomech. 15:277–295, 1982.

    Google Scholar 

  10. Hillsley, M. V., and J. A. Frangos. Review: bone tissue engineering: The role of interstitial fluid flow. Biotechnol. Bioeng. 43:573–581, 1994.

    Google Scholar 

  11. Iannacone, W., E. Korostoff, and S. R. Pollack. Microelectrode study of stress-generated potentials obtained from uniform and nonuniform compression of human bone. J. Biomed. Mater. Res. 13:753–763, 1979.

    Google Scholar 

  12. Jacobs, C. R., C. E. Yellowley, B. R. Davis, Z. Zhou, J. M. Cimbala, and H. J. Donahue. Differential effect of steady versus oscillating flow on bone cells. J. Biomech. 31:969–976, 1998.

    Google Scholar 

  13. Johnson, M. W. Behavior of fluid in stressed bone and cellular stimulation. Calcif. Tissue Int. 36:S72-S76, 1984.

    Google Scholar 

  14. Johnson, M. W., D. A. Chakkalakal, R. A. Harper, J. L. Katz, and S. W. Rouhana. Fluid flow in bone in vitro. J. Biomech. 15:881–885, 1982.

    Google Scholar 

  15. Kelly, P. J., K. N. An, E. Y. S. Chao, and J. A. Rand. Fracture healing: Biomechanical, fluid dynamic and electrical considerations. Bone Mineral Research. New York: Elsevier, 1985, pp. 295–319.

    Google Scholar 

  16. Li, G. P., J. T. Bronk, K. N. An, and P. J. Kelly. Permeability of cortical bone of canine tibiae. Microvasc. Res. 34:302–310, 1987.

    Google Scholar 

  17. Mak, A. F., D. T. Huang, J. D. Zhang, and P. Tong. Deformation-induced hierarchical flows and drag forces in bone canaliculi and matrix microporosity. J. Biomech. 30:11–18, 1997.

    Google Scholar 

  18. Mak, A. F., L. Qin, L. K. Hung, C. W. Cheng, and C. F. Tin. A histomorphometric observation of flows in cortical bone under dynamic loading. Microvasc. Res. 59:290–300, 2000.

    Google Scholar 

  19. Montgomery, R. J., B. D. Sutker, J. T. Bronk, S. R. Smith, and P. J. Kelly. Interstitial fluid flow in cortical bone. Microvasc. Res. 35:295–307, 1988.

    Google Scholar 

  20. 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. 23:188–200, 1982.

    Google Scholar 

  21. Neuman, M. W. Blood:Bone equilibrium. Calcif. Tissue Int. 34:117–120, 1982.

    Google Scholar 

  22. Otter, M. W., and G. V. Cochran. Comments on "fluid movement in bone: Theoretical and empirical." J. Biomech. 25:1495, 1992.

    Google Scholar 

  23. Otter, M. W., V. R. Palmieri, and G. V. Cochran. Transcortical streaming potentials are generated by circulatory pressure gradients in living canine tibia. J. Orthop. Res. 8:119–126, 1990.

    Google Scholar 

  24. Otter, M. W., V. R. Palmieri, D. D. Wu, K. G. Seiz, L. A. MacGinitie, and G. V. Cochran. A comparative analysis of streaming potentials in vivo and in vitro. J. Orthop. Res. 10:710–719, 1992.

    Google Scholar 

  25. Otter, M. W., Y. X. Qin, C. T. Rubin, and K. J. McLeod. Does bone perfusion/reperfusion initiate bone remodeling and the stress fracture syndrome? Med. Hypotheses 53:363–368, 1999.

    Google Scholar 

  26. Otter, M. W., D. D. Wu, W. A. Bieber, and G. V. Cochran. Intraarterial protamine sulfate reduces the magnitude of streaming potentials in living canine tibia. Calcif. Tissue Int. 53:411–415, 1993.

    Google Scholar 

  27. Piekarski, K., and M. Munro. Transport mechanism operating between blood supply and osteocytes in long bones. Nature (London) 269:80–82, 1977.

    Google Scholar 

  28. Pienkowski, D., and S. R. Pollack. The origin of stressgenerated potentials in fluid-saturated bone. J. Orthop. Res. 1:30–41, 1983.

    Google Scholar 

  29. Pollack, S. R., N. Petrov, R. Salzstein, G. Brankov, and R. Blagoeva. An anatomical model for streaming potentials in osteons. J. Biomech. 17:627–636, 1984.

    Google Scholar 

  30. Pollack, S. R., R. Salzstein, and D. Pienkowski. Streaming potential in fluid filled bone. Ferroelectrics 60:297–309, 1984.

    Google Scholar 

  31. Qin, Y. X., K. McLeod, M. W. Otter, and C. T. Rubin. The interdependent role of loading frequency, intracortical fluid pressure and pressure gradients in guiding sitespecific bone adaptation. 44th Ann. Mtg. Orthop. Res. Soc. 23:544, 1998.

    Google Scholar 

  32. Qin, Y. X., K. McLeod, and C. T. Rubin, Intracortical fluid flow is induced by dynamic intramedullary pressure independent of matrix deformation. 46th Ann. Mtg. Orth. Res. Soc. 25:740, 2000.

    Google Scholar 

  33. Qin, Y. X., C. T. Rubin, and K. J. McLeod, Nonlinear dependence of loading intensity and cycle number in the maintenance of bone mass and morphology. J. Orthop. Res. 16:482–489, 1998.

    Google Scholar 

  34. Rubin, C. T., and L. E. Lanyon. Osteoregulatory nature of mechnaical stimuli: function as a determinant for adaptive remodeling in bone. J. Orthop. Res. 5:300–310, 1987.

    Google Scholar 

  35. Salzstein, R. A., and S. R. Pollack. Electromechanicall potentials in cortical bone—II. Experimental analysis. J. Biomech. 20:271–280, 1987.

    Google Scholar 

  36. Salzstein, R. A., S. R. Pollack, A. F. Mak, and N. Petrov, Electromechanical potentials in cortical bone-I. A continuum approach. J. Biomech 20:261–270, 1987.

    Google Scholar 

  37. Scher, H., M. F. Shlesinger, and J. T. Bendler, Time-scale invariance in transport and relaxation. Phys. Today 44:26–34, 1991.

    Google Scholar 

  38. Scott, G. C., and E. Korostoff, Oscillatory and step response electromechanical phenomena in human and bovine bone. J. Biomech. 23:127–143, 1990.

    Google Scholar 

  39. Seliger, W. G. Tissue fluid movement in compact bone. Anat. Rec. 166:247–255, 1970.

    Google Scholar 

  40. Smit, T. H., J. M. Huyghe, and S. C. Cowin. Estimation of the poroeleastic parameters of cortical bone. J. Biomech. (in press).

  41. Soares, A. M., V. E. Arana-Chavez, A. R. Reid, and E. Katchburian, Lanthanum tracer and freeze-fracture studies suggest that compartmentalisation of early bone matrix may be related to initial mineralisation. J. Anat. 181 (Pt 2):345–356, 1992.

    Google Scholar 

  42. Starkebaum, W., S. R. Pollack, and E. Korostoff. Microelectrode studies of stress-generated potentials in four-point bending of bone. J. Biomed. Mater. Res. 13:729–751, 1979.

    Google Scholar 

  43. Tanaka, T., and A. Sakano. Differences in permeability of microperoxidase and horseradish peroxidase into the alveolar bone of developing rats. J. Dent. Res. 64:870–876, 1985.

    Google Scholar 

  44. 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 

  45. 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 2:107–117, 1998.

    Google Scholar 

  46. Wang, L., S. P. Fritton, S. C. Cowin, and S. Weinbaum. Fluid pressure relaxation depends upon osteonal microstructure: Modeling an oscillatory bending experiment. J. Biomech. 32:663–672, 1999.

    Google Scholar 

  47. Weinbaum, S., S. C. Cowin, and Y. Zeng. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J. Biomech. 27:339–360, 1994.

    Google Scholar 

  48. Weinbaum, S., P. Guo, and L. You. A new view of mechanotransduction and strain amplification in cells with microvilli and cell processes. Biorheology 38:119–142, 2001.

    Google Scholar 

  49. Zeng, Y., S. C. Cowin, and S. Weinbaum. A fiber matrix model for fluid flow and streaming potentials in the canaliculi of an osteon. Ann. Biomed. Eng. 22:280–292, 1994.

    Google Scholar 

  50. Zhang, D., and S. C. Cowin. Oscillatory bending of a poroelastic beam. J. Mech. Phys. Solids 42:1575–1579, 1994.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, State University of New York at Stony Brook, Stony Brook, NY

    Yi-Xian Qin, Wei Lin & Clinton Rubin

Authors
  1. Yi-Xian Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Clinton Rubin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qin, YX., Lin, W. & Rubin, C. The Pathway of Bone Fluid Flow as Defined by In Vivo Intramedullary Pressure and Streaming Potential Measurements. Annals of Biomedical Engineering 30, 693–702 (2002). https://doi.org/10.1114/1.1483863

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1114/1.1483863

Search

Navigation