Tissue adaptation as a dynamical process far from equilibrium

Bone

Volumn 19, Issue 2, 1996, Pages 143-149

  Weinans, H ^a,b   Prendergast, Patrick J ^c  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Bone adaptation; Feedback control; Instability; Irreversibility; Tissue adaptation

Indexed keywords

ARTICLE; BIOMECHANICS; BONE REMODELING; COMPUTER SIMULATION; DYNAMICS; IMPLANT; JOINT FUNCTION; MORPHOGENESIS; OSTEOPOROSIS; POSITIVE FEEDBACK; SENSOR; TISSUE GROWTH;

EID: 0030220712     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/8756-3282(96)00143-3     Document Type: Article

References (78)

1. 1. Aarden, E. M., Burger, E. H., and Nijweide, P. J. Function of osteocytes in bone. J Cell Biochem 55:287-299; 1994.
2. 2. Beaupré, G. S., Orr, T. E., and Carter, D. R. An approach for time-dependant modeling and remodeling - Theoretical development & Application: A preliminary remodeling simulation. J Orthop Res 8:651-670; 1990.
3. 3. Blenman, P. R., Carter, D. R., and Beaupré, G. S. Role of mechanical loading in the progressive ossification of a fracture callus. J Orthop Res 7:398-407; 1989.
4. 4. Brand, R. A. Autonomous informational stability in connective tissues. Med Hypoth 37:107-114; 1992.
5. 5. Burr, D. B., Schaffler, M. B., Yang, K. H., Lukoschek, M., Sivaneri, N., Blaha, J. D., and Radin, E. L. Skeletal change in response to altered strain environments: Is woven bone a response to elevated strain. Bone 10:223-233; 1989.
6. 6. Burr, D. B., Schaffler, M. B., Yang, K. H., Wu, D. D., Lukoschek, M., Kandzari, D., Sivaneri, N., Blaha, J. D., and Radin, E. L. The effects of altered strain environments on bone tissue kenetics. Bone 10:215-221; 1989.
7. 7. Carter, D. R. Mechanical loading history and skeletal biology. J. Biomech 20:1095-1109; 1987.
8. 8. Carter, D. R., Blenman, P. R., and Beaupré, G. S. Correlations between mechanical stress history and tissue differentiation in initial fracture healing. J Orthop Res 6:736-748; 1988.
9. 9. Carter, D. R. and Giori, N. J. Effect of mechanical stress on tissue differentiation in the bony implant bed. In: Davis, J. E., Ed. The Bone-Biomaterial Interface. Toronto: University of Toronto Press; 1991; 367-376.
10. 10. Carter, D. R., Fyhrie, D. P., and Whalen, R. T. Trabecular bone density and loading history: Regulation of connective tissue biology by mechanical energy. J Biomech 20:785-794; 1987.
11. 11. Carter, D. R., Orr, T. E., and Fyhrie, D. P. Relationships between loading history and femoral cancellous bone architecture. J Biomech 22:231-244; 1989.
12. 12. Carter, D. R., Orr, T. E., Fyhrie, D. P., and Schurman, D. J. Influences of mechanical stress on prenatal and postnatal skeletal development. Clin Orthop Rel Res 219:237-250; 1987.
13. 13. Carter, D. R., van der Meulen, M. C. H., and Beaupré, G. S. Mechanical factors in bone growth and development. Bone 18:5S-10S; 1996.
14. 14. Cooke, J. and Zeeman, E. C. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theoret Biol 58:455-476; 1976.
15. 15. Cowin, S. C. The mechanical properties of bone. In: Selvadurai, A. P. S., Ed. Studies in applied mechanics 5A: Mechanics of structured media; 1981; 151-184.
16. 16. Cowin, S. C. Mechanical modelling of the strain adaptation process in bone. Calcif Tissue Int 36:S98-S103; 1984.
17. 17. Cowin, S. C. Wollf's law of trabecular architecture at remodeling equilibrium. J Biomech Eng.
18. 18. Cowin, S. C., Hart, R. T., Balser, J. R., and Kohn, D. H. Functional adaptation in long bones: Establishing in vivo values for surface remodeling rate coefficients. J Biomech 18:665-684; 1985.
19. 19. Cowin, S. C., Moss-Salentijn, L., and Moss, M. L. Candidates for the mechanosensory system in bone. J Biomech Eng 113:191-197; 1991.
20. 20. Cowin, S. C. and van Buskirk, W. C. Internal bone remodeling induced by a medullary pin. J Biomech 11:269-275; 1978.
21. 21. Cowin, S. C. and van Buskirk, W. C. Surface bone remodeling induced by a medullary pin. J Biomech 12:269-276; 1979.
22. 22. Duncan, R. L. and Turner. C. H. Mechanotransduction and the functional response of bone to mechanical strain. Calcified Tissue Int 57:344-358; 1995.
23. 23. Eriksen, E. F. and Langdhal, B. Bone remodeling and its consequences for bone structure. In: Odgaard, A. and Weinans, H., Eds. Bone structure and remodeling. Singapore: World Scientific; 1995; 25-36.
24. 24. Firoozbakhsh, K. and Aleyaasin, M. The effect of stress concentration on bone remodeling: Theoretical predictions. J Biomech Eng 111:355-360; 1989.
25. 25. Frost, H. M. In: Intermediary organisation of the skeleton. Vols I & II. Boca Raton, FL: CRC; 1986.
26. 26. Frost, H. M. Perspectives: Bone's mechanical usage windows. Bone Miner 19:257-271; 1992.
27. 27. Fyhrie, D. P. and Carter, D. R. A unifying principle relating stress to trabecular bone morphoiogy. J Orthop Res 4:304-317; 1986.
28. 28. Fyhrie, D. P. and Schaffler, M. B. The adaptation of bone apparent density to applied load. J Biomech 28:135-146; 1995.
29. 29. Giori, N. J., Beaupré, G. S., and Carter, D. R. Cellular shape and pressure may mediate mechanical control of tissue composition in tendons. J Orthop Res 11:581-591; 1993.
30. 30. Hart, R. T., Davy, D. T., and Heiple, K. G. A computational method for stress analysis of adaptive elastic materials with a view towards applications in strain induced bone remodeling. J Biomech Eng 106:342-350; 1984.
31. 31. Hart, R. T. and Fritton, S. P. Introduction to finite element based simulation of functional adaptation of cancellous bone. Forma, 1996.
32. 32. Harrigan, T. P. and Hamilton, J. J. Bone strain sensation via transmembrane potential changes in surface osteoblasts: loading rate and microstructural implications. J Biomech 26:183-200; 1993.
33. 33. Huiskes, R. and Hollister, S. J. From structure to process, from organ to cell. Recent developments in FE-analysis in orthopaedic biomechanics. J Biomech Eng 115:520-527; 1993.
34. 34. Huiskes, R. and van Rietbergen, B. Preclinical testing of total hip stems. The effect of coating placement. Clin Orthop Rel Res 319:64-76; 1995.
35. 35. Huiskes, R., Weinans, H., Grootenboer, H. J., Dalstra, M., Fudala, B., and Slooff, T. J. Adaptive bone remodeling theory applied to prosthetic design analysis. J Biomech 20:1135-1150; 1987.
36. 36. Jacobs, C. R., Levenston, M. E., Beaupré, G. S., Simo, J. C., and Carter, D. R. Numerical instabilities in bone remodeling simulations. The advantages of a node based finite element approach. J Biomech 28:449-459; 1995.
37. 37. Kauffman, S. A. In: The Origins of Order. Self-organization and Selection in Evolution. Oxford; Oxford: University Press; 1993.
38. 38. Keaveny, T. M. and Ulla, I. M. The effects of variations in the amount and distribution of bone ingrowth on bone stresses around a fully porous-coated hip prosthesis. In: Advances in Bioengineering. Hull, M. L., Ed. BED-Vol. 31; 1995; 279-280.
39. 39. Lanyon, L. E. Osteocytes, strain detection, bone modeling and remodeling. Calcif Tissue Int 53 (Suppl. 1):S102-S107; 1993.
40. 40. Levenston, M. E., Beaupré, G. S., Schurman, D. J., and Carter, D. R. Computer simulations of stress related bone remodeling around noncemented acetabular components. J Arthroplasty 8:595-605; 1993.
41. 41. Lewis, J., Slack, J. M. W., and Wolpert, L. Thresholds in development. J Theor Biol 65:579-590; 1977.
42. 42. Martin, R. B. Potential instabilities in bone remodeling. Proceedings of the American Society of Biomechanics 1995; 29-30.
43. 43. Martin, R. B. and Burr, D. B. In: Structure, Function and Adaptation in Compact Bone. New York: Raven; 1989.
44. 44. Meinhardt, H. In: Models of Biological Pattern Formation. London: Academic; 1982; 108-120.
45. 45. Mikié, B. and Carter, D. R. Bone strain gage data and theoretical models of functional adaptation. J Biomech 28:465-469; 1995.
46. 46. Mow, V. C., Ratcliffe, A., and Poole, A. R. Cartilage and diarthrodial joints as paradigms for hierarchial materials and structures. Biomaterials 13:67-97; 1992.
47. 47. Mullender, M. G., Huiskes, R., and Weinans, H. A physiological approach to the simulation of bone remodeling as a self-organizational control process. J Biomech 27:1389-1394; 1994.
48. 48. Mullender, M. G. and Huiskes, R. A proposal for the regulatory mechanism of Wolff s law. J Orthop Res 13:503-512; 1995.
49. 49. Murray, J. D. In: Mathematical Biology. Berlin: Springer; 1989.
50. 50. Nicolis, G. and Prigogine, I. In: Self-organization in nonequilibrium systems. From dissipative structures to order through fluctuations. New York: Wiley; 1977.
51. 51. Orr, T. E., Beaupré, G. S., Carter. D. R., and Schurman, D. J. Computer predictions of bone remodeling around porous-coated implants. J Arthroplasty 5:191-200; 1990.
52. 52. Oster, G. F., Shubin, N., Murray, J. D., and Alberch, P. Evolution and morphogenetic rules: The shape of the vertebrate limb in ontogeny and phylogeny. Evolution 42:862-864; 1988.
53. 53. Parfitt, A. M. The quantum concept of bone remodeling and turnover: Implications for the pathogenesis of osteoporosis. Calcif Tissue Int 28:1-5; 1979.
54. 54. Parfitt, A. M. Osteonal and hemiosteonal remodeling: The spatial and temporal framework for signal traffic in adult human bone. J Cell Biochem 55:273-286; 1994.
55. 55. Pauwels, F. Grundriss einer Biomechanik der Frakturheilung. In: Verhandlungen der Deutschen Orthopädischen Gesellschaft. Stuttgart: Ferdinand Enke Verlag; 62-108; 1941. Translated by Manquet, P. and Furlong, R. Biomechanics of fracture healing. In: Biomechanics of the Locomotor Apparatus. Berlin: Springer; 1980; 106-137.
56. 55. Pauwels, F. Grundriss einer Biomechanik der Frakturheilung. In: Verhandlungen der Deutschen Orthopädischen Gesellschaft. Stuttgart: Ferdinand Enke Verlag; 62-108; 1941. Translated by Manquet, P. and Furlong, R. Biomechanics of fracture healing. In: Biomechanics of the Locomotor Apparatus. Berlin: Springer; 1980; 106-137.
57. 56. Perren, S. M. Physical and biological aspects of fracture healing with special reference to internal fixation. Clin Orthop Rel Res 138:175-196; 1979.
58. 57. Prendergast, P. J., Huiskes, R., and Søballe, K. Biomechanical influences on tissue differentiation at implant interfaces. Trans Orthop Res Soc 51:527; 1996.
59. 58. Prendergast, P. J. and Taylor, D. Design of intramedullary prostheses to prevent bone loss: predictions based on damage stimulated remodeling. J Biomed Eng 14:499-506; 1992.
60. 59. Prendergast, P. J. and Taylor, D. Prediction of bone adaptation using damage accumulation. J Biomech 27:1067-1076; 1994.
61. 60. Roux, W. Der Zuchtende Kampf der Teile, oder die "Teilauslese" im Organismus. Leipzig: Wilhem Englemann; 1891. See also: Roux, W. Anpassungslehre, Histomechanik und Histochemie. Mit Bemerkunngen uber die Entwicklung und Formgestaltung der Gelenke (Adaptation, histomechanics and histochemistry, with a notation about the development and formation of bones). Virchows Archiv 207:168-209; 1912.
62. 60. Roux, W. Der Zuchtende Kampf der Teile, oder die "Teilauslese" im Organismus. Leipzig: Wilhem Englemann; 1891. See also: Roux, W. Anpassungslehre, Histomechanik und Histochemie. Mit Bemerkunngen uber die Entwicklung und Formgestaltung der Gelenke (Adaptation, histomechanics and histochemistry, with a notation about the development and formation of bones). Virchows Archiv 207:168-209; 1912.
63. 61. Schrödinger, E. In: What is life? The physical aspect of the living cell. Cambridge: Cambridge University Press; 1945.
64. 62. Taber, L. A. Biomechanics of growth, remodeling, and morphogenesis. Appl Mech Rev 48:487-545; 1995.
65. 63. Thorn, R. Stabilité structurelle et morphogénèse. Essai d'une théorie générale des modèles. Reading, MA: Benjamin; 1972, Translated by Fowler, D.H. Structural stability and morphogenesis: an outline of a general theory of models. 5th Reprint: Reading, MA: Addison-Wesley; 1989.
66. 63. Thorn, R. Stabilité structurelle et morphogénèse. Essai d'une théorie générale des modèles. Reading, MA: Benjamin; 1972, Translated by Fowler, D.H. Structural stability and morphogenesis: an outline of a general theory of models. 5th Reprint: Reading, MA: Addison-Wesley; 1989.
67. 64. Turing, A. M. The chemical basis of morphogenesis. Proc Royal Soc (London) 237:37-72; 1952.
68. 65. Turner, C. H. Homeostatic control of bone structure: An application of feedback theory. Bone 12:203-217; 1991.
69. 66. Turner, C. H., Anne, V., and Pidaparti, R. M. Convergence and uniqueness of bone adaptation models. Trans Orthop Res Soc 18:527; 1993.
70. 67. Turner, C. H., Forwood, M. R., Rho, J-Y., and Yoshikawa, T. Mechanical loading thresholds for lamellar and woven bone formation. J Bone Miner Res 9:87-97; 1994.
71. 68. van der Meulen, M. C. H., Beaupré, G. S., and Carter, D. R. Mechanobiologic influences in long bone cross-sectional growth. Bone 14:635-642; 1993.
72. 69. van der Meulen, M. C. H., Morey-Holton, E. R., and Carter, D. R. Himdlimb suspension diminishes femoral cross-sectional growth in the rat. J Orthop Res 13:700-707; 1995.
73. 70. van Rietbergen, B., Huiskes, R., Weinans, H., Sumner, D. R., Turner, T. M., and Galante, J. O. The mechanism of bone remodeling and resorption around press-fitted THA stems. J Biomech 26:369-382; 1993.
74. 71. Weinans, H., Huiskes, R., and Grootenboer, H. J. The behavior of adaptive bone remodeling simulation models. J Biomech 25:1425-1441; 1992.
75. 72. Weinans, H., Huiskes, R., and Grootenboer, H. J. Effects of fit and bonding characteristics of femoral stems on adaptive bone remodeling. J Biomech Eng 116:393-400; 1994.
76. 73. Weinans, H. and Parfitt, A. M. Trabecular bone degeneration measured from radiographs. Trans 42nd Orthop Res Soc 21:643; 1996.
77. 74. Wong, M. and Carter, D. R. A theoretical model of endochondral ossification and bone architectural construction in long bone ontogeny. Anat Embryol 181:523-532; 1990.
78. 75. Zioupos, P., Cunrey, J. D., Mirza, M. S., and Barton, D. C. Experimentally determined microcracking around a circular hole in a flat plate of bone: Comparison with predicted stresses. Proc Trans R Soc London B 347:383-396; 1995.