Idealization of pericellular fluid space geometry and dimension results in a profound underprediction of nano-microscale stresses imparted by fluid drag on osteocytes

Journal of Biomechanics

Volumn 41, Issue 8, 2008, Pages 1736-1746

  Anderson, Eric J ^a   Knothe Tate, Melissa L ^a,b  

^a Case Western Reserve University   (United States)

^b Case Western Reserve University   (United States)

Author keywords

Cell mechanics; Mechanical loading; Mechanotransduction; Osteocytes; Stress strain

Indexed keywords

COMPUTATIONAL FLUID DYNAMICS; DRAG COEFFICIENT; MATHEMATICAL MODELS; TRANSMISSION ELECTRON MICROSCOPY;

CELL MECHANICS; MECHANICAL LOADING; MECHANOTRANSDUCTION; OSTEOCYTES;

CELLS;

ANIMAL EXPERIMENT; ARTICLE; BODY FLUID COMPARTMENT; CELL ACTIVITY; CELL STRESS; CELL SURFACE; COMPUTATIONAL FLUID DYNAMICS; FLUID FLOW; GEOMETRY; NONHUMAN; OSTEOCYTE; PERICELLULAR FLUID SPACE; PRIORITY JOURNAL; RAT; SHEAR STRENGTH; STATISTICAL ANALYSIS;

BIOMECHANICS; BONE MATRIX; COMPUTER SIMULATION; EXTRACELLULAR FLUID; MECHANOTRANSDUCTION, CELLULAR; MICROFLUIDICS; OSTEOCYTES; STRESS, MECHANICAL;

EID: 43549108732     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2008.02.035     Document Type: Article

References (37)

1. Almekinders L.C., Banes A.J., and Ballenger C.A. Effects of repetitive motion on human fibroblasts. Medicine and Science in Sports and Exercise 25 (1993) 603-607
2. Anderson E.J., and Knothe Tate M.L. Open access to novel dual flow chamber technology for in vitro cell mechanotransduction, toxicity and pharamacokinetic studies. Biomedical Engineering Online 6 (2007) 46 10.1186/1475-925x-6-46
3. Anderson E.J., Kaliyamoorthy S., Alexander J.I.D., and Knothe Tate M.L. Nano-microscale models of periosteocytic flow show differences in stresses imparted to cell body and processes. Annals of Biomedical Engineering 33 (2005) 52-62
4. Anderson E.J., Falls T.D., Sorkin A.M., and Knothe Tate M.L. The imperative for controlled mechanical stresses in unraveling cellular mechanisms of mechanotransduction. Biomedical Engineering Online 5 (2006) 27 10.1186/1475-925x-5-27
5. Anderson E.J., Kreuzer S., Small O., and Knothe Tate M.L. Pairing computational and scaled physical models to determine permeability as a measure of cellular communication in micro-and nano-scale pericellular spaces. Microfluidics and Nanofluidics 4 (2008) 193-204 10.1007/s10404-007-0156-5
6. Burger E.H., and Veldhuijzen J.P. Influence of mechanical factors on bone formation, resorption and growth in vitro. In: Hall B.K. (Ed). Bone vol. 7 (1993), CRC Press, Boca Raton, FL, USA 37-56
7. Donahue S.W., Donahue H.J., and Jacobs C.R. Osteoblastic cells have refractory periods for fluid-flow-induced intracellular calcium oscillations for short bouts of flow and display multiple low-magnitude oscillations during long-term flow. Journal of Biomechanics 36 (2003) 35-43
8. Fritton S.P., McLeod K.J., and Rubin C.T. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. Journal of Biomechanics 33 (2000) 317-325
9. Frost H.M. Bone "mass" and the "mechanostat": a proposal. Anatomical Record 219 (1987) 1-9
10. Goodship A.E., Lanyon L.E., and McFie H. Functional adaptation of bone to increased stress. An experimental study. Journal of Bone and Joint Surgery American 61 (1979) 539-546
11. Guilak F., Ratcliffe A., and Mow V.C. Chondrocyte deformation and local tissue strain in articular cartilage: a confocal microscopy study. Journal of Orthopaedic Research 13 (1995) 410-421
12. Han Y., Cowin S.C., Schaffler M.B., and Weinbaum S. Mechanotransduction and strain amplification in osteocyte cell processes. Proceedings of the National Academy of Science 101 (2004) 16689-16694
13. Jacobs C.R., Yellowley C.E., Davis B.R., Zhou Z., Cimbala J.M., and Donahue H.J. Differential effect of steady versus oscillating flow on bone cells. Journal of Biomechanics 31 (1998) 969-976
14. Klein-Nulend J., van der Plas A., Semeins C.M., Ajubi N.E., Frangos J.A., Nijweide P.J., and Burger E.H. Sensitivity of osteocytes to biomechanical stress in vitro. Federation of American Societies for Experimental Biology 9 (1995) 441-445
15. Knapp H.F., Reilly G.C., Stemmer A., Niederer P., and Knothe Tate M.L. Development of preparation methods for and insights obtained from atomic force microscopy of fluid spaces in cortical bone. Scanning 24 (2002) 25-33
16. Knothe Tate M.L. Mixing mechanisms and net solute transport in bone. Annals of Biomedical Engineering 29 (2001) 810-811
17. Knothe Tate M.L. Interstitial fluid flow. In: Cowin S.C. (Ed). Bone Biomechanics Handbook. second ed (2001), CRC Press, New York, NY, USA 1-29
18. Knothe Tate M.L. "Whither flows the fluid in bone?" An osteocyte's perspective. Journal of Biomechanics 36 (2003) 1409-1424
19. Knothe Tate M.L., Knothe U., and Niederer P. Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and functional adaptation. American Journal of Medical Sciences 316 (1998) 189-195
20. Knothe Tate M.L., Niederer P., and Knothe U. In vivo tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone 22 (1998) 107-117
21. Knothe Tate M.L., Niederer P., 1998. A theoretical FE-based model developed to predict the relative contribution of convective and diffusive transport mechanisms for the maintenance of local equilibria within cortical bone. Advances in Heat and Mass Transfer in Biotechnology, (Ed. S. Clegg) The American Society of Mechanical Engineers, HTD - Vol. 362/BED - Vol. 40, 133-142.
22. McGarry J.G., Klein-Nulend J., Mullender M.G., and Prendergast P.J. A comparision of strain and fluid shear stress in stimulating bone cell responses-a computational and experimental study. Federations of American Societies for Experimental Biology 19 (2005) 482-484
23. Nicolella D.P., Moravits D.E., Gale A.M., Bonewald L.F., and Lankford J. Osteocyte lacunae tissue strain in cortical bone. Journal of Biomechanics 39 (2006) 1735-1743
24. Owan I., Burr D.B., Turner C.H., Qiu J., Tu Y., Onyia J.E., and Duncan R.L. Mechanotransduction in bone: osteoblasts are more responsive to fluid forces than mechanical strain. American Journal of Physiology 273 (1997) C810-C815
25. Pienkowski D., and Pollack S.R. The origin of stress-generated potentials in fluid-saturated bone. Journal of Orthopaedic Research 1 (1983) 30-41
26. Reich K.M., and Frangos J.A. Effect of flow on prostaglandin E2 and inositol trisphosphate levels in osteoblasts. American Journal of Physiology 261 (1991) C428-C432
27. Reilly G.C., Knapp H.F., Stemmer A., Neiderer P., and Knothe Tate M.L. Investigation of the morphology of the lacunocanalicular system of cortical bone using atomic force microscopy. Annals of Biomedical Engineering 29 (2001) 1074-1081
28. Rubin C.T., and Lanyon L.E. Regulation of bone formation by applied dynamic loads. Journal of Bone and Joint Surgery American 66 (1984) 397-402
29. Scherft J.P. The lamina limitans of the organic matrix of calcified cartilage and bone. Journal of Ultrastructural Research 38 (1972) 318-331
30. Smalt R., Mitchell F.T., Howard R.L., and Chambers T.J. Induction of NO and prostaglandin E2 in osteoblasts by wall-shear stress but no mechanical strain. American Journal of Physiology 273 (1997) E751-E758
31. Steck R., and Knothe Tate M.L. In silico stochastic network models that emulate the molecular sieving characteristics of bone. Annals of Biomedical Engineering 33 (2005) 87-94
32. Tami A.E., Nasser P., Verborgt O., Schaffler M.B., and Knothe Tate M.L. The role of interstitial fluid flow in the remodeling response to fatigue loading. Journal of Bone and Mineral Research 7 (2002) 2030-2037
33. Verborgt O., Gibson G.J., and Schaffler M.B. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. Journal of Bone and Mineral Research 15 (2000) 60-67
34. Weinbaum S., Cowin S.C., and Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. Journal of Biomechanics 27 (1994) 339-360
35. You J., Yellowley C.E., Donahue H.J., Zhang Y., Chen Q., and Jacobs C.R. Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. Journal of Biomechanical Engineering 122 (2000) 387-393
36. You L., Cowin S.C., Schaffler M.B., and Weinbaum S. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. Journal of Biomechanics 34 (2001) 1375-1386
37. You L.D., Weinbaum S., Cowin S.C., and Schaffler M.B. Ultrastructure of the osteocyte process and its pericellular matrix. Anatomical Record 278 (2004) 505-513