On bone adaptation due to venous stasis

Journal of Biomechanics

Volumn 36, Issue 10, 2003, Pages 1439-1451

  Wang, Liyun ^a   Fritton, Susannah P ^b   Weinbaum, Sheldon ^c   Cowin, Stephen C ^c,d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b City University of New York   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d NONE   (United States)

Author keywords

Interstitial fluid flow; Intramedullary pressure; Mechanical loading; Periosteum; Shear stress

Indexed keywords

BLOOD; BONE; CELLS; PHYSIOLOGY; PULSATILE FLOW; SHEAR STRESS;

BIOLOGICAL STRESSES; BLOOD CIRCULATION;

BIOMECHANICS;

ADAPTATION; ARTICLE; BONE CELL; BONE STRESS; CIRCULATION; EXTRAVASCULAR SPACE; FLUID FLOW; HEART CONTRACTION; INTERSTITIAL FLUID; MECHANICAL STRESS; MODEL; MUSCLE CONTRACTION; OSTEOCYTE; PERIOSTEUM; PRIORITY JOURNAL; SHEAR STRESS; VENOUS STASIS; WEIGHT BEARING;

EID: 0141788745     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0021-9290(03)00241-0     Document Type: Article

References (70)

1. Ajubi N.E., Klein-Nulend J., Nijweide P.J., Vrijheid-Lammers T., Alblas M.J., Burger E.H. Pulsating fluid flow increases prostaglandin production by cultured chicken osteocytes - a cytoskeleton-dependent process. Biochemical and Biophysical Research Communications. 225:1996;62-68.
2. Allen F.D., Hung C.T., Pollack S.R., Brighton C.T. Serum modulates the intracellular calcium response of primary cultured bone cells to shear flow. Journal of Biomechanics. 33:2000;1585-1591.
3. Anderson W. Studies of the lymphatic pathways of bone and bone marrow. Journal of Bone and Joint Surgery. 42A:1960;716.
4. Arnoldi C.C., Lemperg R., Linderholm H. Immediate effect of osteotomy on the intramedullary pressure in the femoral head and neck in patients with degenerative osteoarthritis. Acta Orthopaedica Scandinavica. 42:1971;454-455.
5. Arnoldi C.C., Linderholm H., Mussbichler H. Venous engorgement and intraosseous hypertension in osteoarthritis of the hip. Journal of Bone and Joint Surgery, British Volume. 54:1972;409-421.
6. Azuma H. Intraosseous pressure as a measure of hemodynamic changes in bone marrow. Angiology. 15:1964;396-406.
7. Bakker A.D., Soejima K., Klein-Nulend J., Burger E.H. The production of nitric oxide and prostaglandin E(2) by primary bone cells is shear stress dependent. Journal of Biomechanics. 34:2001;671-677.
8. Bazantova I. The blood and lymph bed in Haversian bone. Folia Morphol. 37:1989;213-215.
9. Bergula A.P., Huang W., Frangos J.A. Femoral vein ligation increases bone mass in the hindlimb suspended rat. Bone. 24:1999;171-177.
10. Bronk J.T., Meadows T.H., Kelly P.J. The relationship of increased capillary filtration and bone formation. Clinical Orthopaedics. 293:1993;338-345.
11. Brookes M., Revell W.J. Blood Supply to Bone. 1998;Springer, London.
12. Cheng B., Zhao S., Luo J., Sprague E., Bonewald L.F., Jiang J.X. Expression of functional gap junctions and regulation by fluid flow in osteocyte-like MLO-Y4 cells. Journal of Bone and Mineral Research. 16:2001;249-259.
13. Cooper R.R., Milgram J.W., Robinson R.A. Morphology of the osteon. An electron microscopic study. Journal of Bone and Joint Surgery, American Volume. 48:1966;1239-1271.
14. Cowin S.C. Bone poroelasticity. Journal of Biomechanics. 32:1999;217-238.
15. Cowin S.C., Weinbaum S., Zeng Y. A case for bone canaliculi as the anatomical site of strain generated potentials. Journal of Biomechanics. 28:1995;1281-1297.
16. Curtis T.A., Ashrafi S.H., Weber D. Canalicular communication in the cortices of human long bones. Anatomical Record. 212:1985;336-344.
17. Dillaman R.M., Roer R.D., Gay D.M. Fluid movement in bone. theoretical and empirical Journal of Biomechanics. 24:1991;163-177.
18. Donahue S.W., Jacobs C.R., Donahue H.J. Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. American Journal of Physiology - Cell Physiology. 281(5):2001;C1635-C1641.
19. Ficat P.R., Arlet J. Ischemia and Necroses of Bone. 1980;Williams & Wilkins, Baltimore.
20. Fritton, S.P., Rubin, C.T., 2001. In vivo measurement of bone deformations using strain gauges. In: Cowin, S.C. (Ed.), Bone Mechanics Handbook. CRC Press, Boca Raton, FL. pp. 8-1 to 8-41.
21. Fritton S.P., McLeod K.J., 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.
22. Green N.E., Griffin P.P. Intra-osseous venous pressure in Legg-Perthes disease. Journal of Bone and Joint Surgery, American Volume. 64:1982;666-671.
23. Grimm M., Williams J. Measurement of permeability in human calcaneal trabecular bone. Journal of Biomechanics. 30:1997;743-745.
24. Hillsley M.V., Frangos J.A. Bone tissue engineering. the role of interstitial fluid flow Biotechnology and Bioengineering. 43:1994;573-581.
25. Hung C.T., Pollack S.R., Reilly T.M., Brighton C.T. Real-time calcium response of cultured bone cells to fluid flow. Clinical Orthopaedics. 313:1995;256-269.
26. Jacobs C.R., Yellowley C.E., Davis B.R., Zhou Z., Cimbala J.M., Donahue H.J. Differential effect of steady versus oscillating flow on bone cells. Journal of Biomechanics. 31:1998;969-976.
27. Jiang G.L., White C.R., Stevens H.Y., Frangos J.A. Temporal gradients in shear stimulate osteoblastic proliferation via ERK1/2 and retinoblastoma protein. American Journal of Physiology - Endocrinology and Metabolism. 283:2002;E383-E389.
28. Johnson D.L., McAllister T.N., Frangos J.A. Fluid flow stimulates rapid and continuous release of nitric oxide in osteoblasts. American Journal of Physiology. 271:1996;E205-E208.
29. Kasperk, C., Bundschuh, B., Sommer, U., Schweizer, B., Lieder, A., van den Heuvel, L., Soexeri-Ludwig, S., Holl, M., Nawroth, P., Boercsoek, I., Liegibel, U.M., 2002. Fluid shear of very low magnitude stimulates growth and improves anchorage of human osteoblastic cells in vitro. ASBMR 24th Annual Meeting, San Antonio, TX. September 20-24, 2002.
30. Keanini R.G., Roer R.D., Dillaman R.M. A theoretical model of circulatory interstitial fluid flow and species transport within porous cortical bone. Journal of Biomechanics. 28:1995;901-914.
31. Kelly P.J., Bronk J.T. Venous pressure and bone formation. Microvascular Research. 39:1990;364-375.
32. Kelly P.J., Montgomery R.J., Bronk J.T. Reaction of the circulatory system to injury and regeneration. Clinical Orthopaedics. 254:1990;275-288.
33. Kiaer T. Bone perfusion and oxygenation. Animal experiments and clinical observations. Acta Orthopaedica Scandinavica, Supplemenum. 257:1994;1-41.
34. Klein-Nulend J., Semeins C.M., Ajubi N.E., Nijweide P.J., Burger E.H. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts - correlation with prostaglandin upregulation. Biochemical and Biophysical Research Communications. 217:1995;640-648.
35. Lawson P.T. Assistant Laboratory Animal Technician Training Manual. 2000;American Association for Laboratory Animal Science, Memphis.
36. Li G.P., Bronk J.T., An K.N., Kelly P.J. Permeability of cortical bone of canine tibiae. Microvascular Research. 34:1987;302-310.
37. Lilly A.D., Kelly P.J. Effects of venous ligation on bone remodeling in the canine tibia. Journal of Bone and Joint Surgery, American Volume. 52:1970;515-520.
38. Liu S.L., Ho T.C. The role of venous hypertension in the pathogenesis of Legg-Perthes disease. A clinical and experimental study. Journal of Bone and Joint Surgery, American Volume. 73:1991;194-200.
39. McAllister T.N., Frangos J.A. Steady and transient fluid shear stress simulate NO release in osteoblasts through distinct biochemical pathways. Journal of Bone and Mineral Research. 14:1999;930-936.
40. Mukherjee N., Saris D.B., Schultz F.M., Berglund L.J., An K.N., O'Driscoll S. The enhancement of periosteal chondrogenesis in organ culture by dynamic fluid pressure. Journal of Orthopaedic Research. 19:2001;524-530.
41. Owan I., Burr D.B., Turner C.H., Qiu J., Tu Y., Onyia J.E., Duncan R.L. Mechanotransduction in bone. osteoblasts are more responsive to fluid forces than mechanical strain American Journal of Physiology. 273:1997;C810-C815.
42. Pavalko F.M., Chen N.X., Turner C.H., Burr D.B., Atkinson S., Hsieh Y.F., Qiu J., Duncan R.L. Fluid shear-induced mechanical signaling in MC3T3-E1 osteoblasts requires cytoskeleton-integrin interactions. American Journal of Physiology. 275:1998;C1591-C1601.
43. Qin, Y-X, Kaplan, T., Saldanha, A., Rubin, C., 2003. Fluid pressure gradients, arising from oscillations in intramedullary pressure, are correlated with the formation of bone and inhibition of intracortical porosity. Journal of Biomechanics this issue, doi:10.1016/S0021-9290(03)00127-1 .
44. Raab-Cullen D.M., Thiede M.A., Petersen D.N., Kimmel D.B., Recker R.R. Mechanical loading stimulates rapid changes in periosteal gene expression. Calcified Tissue International. 55:1994;473-478.
45. Reich K.M., Gay C.V., Frangos J.A. Fluid shear stress as a mediator of osteoblast cyclic adenosine monophosphate production. Journal of Cellular Physiology. 143:1990;100-104.
46. Rouhana, S., Johnson, M., Chakkalakal, D., Harper, R., 1981. Permeability of compact bone. In: Joint ASME-ASCE Conference, Boulder, CO Vol. AMD 43, pp. 169-172.
47. Rubin C., Turner A.S., Bain S., Mallinckrodt C., McLeod K. Anabolism. Low mechanical signals strengthen long bones. Nature. 412:2001;603-604.
48. Sakai K., Mohtai M., Iwamoto Y. Fluid shear stress increases transforming growth factor beta 1 expression in human osteoblast-like cells. modulation by cation channel blockades Calcified Tissue International. 63:1998;515-520.
49. Saris D.B., Sanyal A., An K.N., Fitzsimmons J.S., O'Driscoll S.W. Periosteum responds to dynamic fluid pressure by proliferating in vitro. Journal of Orthopaedic Research. 17:1999;668-677.
50. Shim S.S., Hawk H.E., Yu W.Y. The relationship between blood flow and marrow cavity pressure of bone. Surgery, Gynecology and Obstetrics. 135:1972;353-360.
51. Smalt R., Mitchell F.T., Howard R.L., Chambers T.J. Induction of NO and prostaglandin E2 in osteoblasts by wall-shear stress but not mechanical strain. American Journal of Physiology. 273:1997;E751-E758.
52. Stein A.H.J., Morgan H.C., Reynolds F.C. Variations in normal bone-marrow pressures. Journal of Bone and Joint Surgery. 39-A:1957;1129-1134.
53. Tondevold E. Haemodynamics of long bones. An experimental study on dogs. Acta Orthopaedica Scandinavica Supplementum. 205:1983;9-48.
54. Torrance A.G., Mosley J.R., Suswillo R.F., Lanyon L.E. Noninvasive loading of the rat ulna in vivo induces a strain-related modeling response uncomplicated by trauma or periostal pressure. Calcified Tissue International. 54:1994;241-247.
55. Torzilli P.A., Takebe K., Burstein A.H., Zika J.M., Heiple K.G. The material properties of immature bone. Journal of Biomechanical Engineering. 104:1982;12-20.
56. Trueta J. The role of the vessels in osteogenesis. Journal of Bone and Joint Surgery. 45B:1963;402-418.
57. Wadhwa S., Godwin S.L., Peterson D.R., Epstein M.A., Raisz L.G., Pilbeam C.C. Fluid flow induction of cyclo-oxygenase 2 gene expression in osteoblasts is dependent on an extracellular signal-regulated kinase signaling pathway. Journal of Bone and Mineral Research. 17:2002;266-274.
58. Wang L., Fritton S.P., Cowin S.C., Weinbaum S. Fluid pressure relaxation depends upon osteonal microstructure. modeling an oscillatory bending experiment Journal of Biomechanics. 32:1999;663-672.
59. Wang L., Cowin S.C., Weinbaum S., Fritton S.P. Modeling tracer transport in an osteon under cyclic loading. Annals of Biomedical Engineering. 28:2000;1200-1209.
60. Weinbaum S., Cowin S.C., Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. Journal of Biomechanics. 27:1994;339-360.
61. Welch R.D., Johnston C.E. 2nd, Waldron M.J., Poteet B. Bone changes associated with intraosseous hypertension in the caprine tibia. Journal of Bone and Joint Surgery, American Volume. 75:1993;53-60.
62. Wilkes C.H., Visscher M.B. Some physiological aspects of bone marrow pressure. Journal of Bone and Joint Surgery, American Volume. 57:1975;49-57.
63. Williams J.L., Iannotti J.P., Ham A., Bleuit J., Chen J.H. Effects of fluid shear stress on bone cells. Biorheology. 31:1994;163-170.
64. You, L., 2002. A new view of mechanotransduction in bone cells. Ph.D. Thesis. City University of New York, New York.
65. You L., Cowin S.C., Schaffler M.B., 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.
66. You J., Reilly G.C., Zhen X., Yellowley C.E., Chen Q., Donahue H.J., Jacobs C.R. Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. Journal of Biological Chemistry. 276:2001;13365-13371.
67. Zachos T.A., Aiken S.W., DiResta G.R., Healey J.H. Interstitial fluid pressure and blood flow in canine osteosarcoma and other tumors. Clinical Orthopaedics. 385:2001;230-236.
68. Zaman G., Dallas S.L., Lanyon L.E. Cultured embryonic bone shafts show osteogenic responses to mechanical loading. Calcified Tissue International. 51:1992;132-136.
69. Zeng Y., Cowin S.C., Weinbaum S. A fiber matrix model for fluid flow and streaming potentials in the canaliculi of an osteon. Annals of Biomedical Engineering. 22:1994;280-292.
70. Zhang D., Weinbaum S., Cowin S.C. Estimates of the peak pressures in bone pore water. Journal of Biomechanical Engineering. 120:1998;697-703.