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Transport in HaroldFrostLand: A Metaphor for Fluid Movement to and through BMUs
H. Winet
Departments of Orthopaedic Surgery and Bioengineering, University of California Los Angeles, Los Angeles, California USA

 

The concept that fluid percolating through bone matrix is the basis for mechanotransduction of stress stimuli to modeling and remodeling has proved challenging4. Traditional solid mechanical models in which piezoelectricity is the mechanotransduction process are more intuitive to orthopaedic practitioners nurtured on the fundamentalism of Wolff’s “Law”. However, the scientific evidence from Anderson and Ericksson1, Piekarski and Munro5, and Hillsley and Frangos3 strongly support a bone fluid flow (BFF) paradigm, which, when coupled with the Utah paradigm of Frost2 forms the most scientifically validated explanation to date of osteon response to mechanical stress in vivo.

In order to make this explanation more intuitive we have developed a metaphorical rendering of the model. The rendering adds an extension to include our current model for the effects of skeletal muscle contraction on the basic multicellular unit (BMU). In the metaphor, cortical bone is the continent nation HaroldFrostland. Its cities are fed by waterways which serve as metaphors for each of the fluid transporting pathways from arteries to inter-collagen spaces of bone matrix.

Bounding the continent are oceans wherein underwater earthquakes—metaphors for skeletal muscle contractions—generate solitary pressure waves (tsunamis) and a ripple effect in continental waterways. Critical for penetration by and effectiveness of such solutions is that flow resistance in the waterways must allow pressure buildup. Locks/valves serve to provide this resistance. When pressure is sufficient filtration at transfer points—metaphors for where nutrient exchange occurs--is enhanced. By this means, muscle contraction enhances delivery of fluid not only to bone cells; but around them as well, stimulating mechanotransduction.

  1. Anderson JC ,C Eriksson (1970) Piezoelectric properties of dry-wet bone Nature 277: 167-169.
  2. Frost HM (1963) Bone Remodeling Dynamics. Springfield, Ill: Charles C. Thomas.
  3. Hillsley MV ,JA Frangos (1994) Review: Bone tissue engineering: The role of interstitial fluid flow Biotechn. Bioeng. 43: 573-581.
  4. Kaplan FS, WC Hayes, TM Keaveny, A Boskey, TA Einhorn ,JP Iannotti (1994) Form and function of bone in Simon SR (ed.) Orthopaedic Basic Science Rosemont: American Academy of Orthopaedic Surgeons. pp. 127-184.
  5. Piekarski K ,M Munro (1977) Transport mechanism operating between blood supply and osteocytes in long bones Nature 269: 80-82.