Low-magnitude high-frequency mechanical signals accelerate and augment endochondral bone repair: Preliminary evidence of efficacy

Journal of Orthopaedic Research

Volumn 27, Issue 7, 2009, Pages 922-930

  Goodship, Allen E ^a,b   Lawes, Timothy J ^a,b   Rubin, Clinton T ^c  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c St Francis Hospital The Heart Center   (United States)

Author keywords

Callus; Endochondral bone repair; Fracture healing; Loading; Mechanical

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BONE MINERAL; BONE REMODELING; BONE TISSUE; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; FEMALE; FRACTURE; FRACTURE EXTERNAL FIXATION; FRACTURE HEALING; MECHANOTRANSDUCTION; MOBILIZATION; NONHUMAN; OSTEOTOMY; PERIOSTEUM; PRIORITY JOURNAL; RADIOGRAPHY; TORSION;

ABSORPTIOMETRY, PHOTON; ALLOYS; ANIMALS; BONE DENSITY; DISEASE MODELS, ANIMAL; EXTERNAL FIXATORS; FEMALE; FRACTURE HEALING; LOCOMOTION; OSTEOTOMY; SHEEP; STRESS, MECHANICAL; TIBIA; TIBIAL FRACTURES; TORSION, MECHANICAL; WEIGHT-BEARING;

EID: 67649600832     PISSN: 07360266     EISSN: None     Source Type: Journal    
DOI: 10.1002/jor.20824     Document Type: Article

References (54)

1. Claes LE, Wilke HJ, Augat P, et al. 1995. Effect of dynamization on gap healing of diaphyseal fractures under external fixation. Clin Biomech (Bristol, Avon) 10:227-234.
2. Gardner TN, Mishra S. 2003. The biomechanical environment of a bone fracture and its influence upon the morphology of healing. Med Eng Phys 25:455-464. (Pubitemid 36645163)
3. Augat P, Simon U, Liedert A, et al. 2005. Mechanics and mechano-biology of fracture healing in normal and osteoporotic bone. Osteoporos Int 16(Suppl 2):S36-S43. (Pubitemid 46232119)
4. Chao EY, Aro HT, Lewallen DG, et al. 1989. The effect of rigidity on fracture healing in external fixation. Clin Orthop 241:24-35. (Pubitemid 19101240)
5. Augat P, Merk J, Ignatius A, et al. 1996. Early, full weightbearing with flexible fixation delays fracture healing. Clin Orthop Relat Res 328:194-202. (Pubitemid 26231143)
6. Goodship AE, Watkins PE, Rigby HS, et al. 1993. The role of fixator frame stiffness in the control of fracture healing. An experimental study. J Biomech 26:1027-1035. (Pubitemid 23235560)
7. Wolff J. 1986. The law of bone remodeling. Berlin: Springer.
8. Marsh DR, Li G. 1999. The biology of fracture healing: optimising outcome. Br Med Bull 55:856-869.
9. Goodship AE, Kenwright J. 1985. The influence of induced micromovement upon the healing of experimental tibial fractures. J Bone Joint Surg [Br] 67:650-655. (Pubitemid 16228160)
10. Kenwright J, Richardson JB, Cunningham JL, et al. 1991. Axial movement and tibial fractures. A. controlled randomised trial of treatment. J Bone Joint Surg [Br] 73:654-659.
11. Carter DR, Blenman PR, Beaupre GS. 1998. Correlations between mechanical stress history and tissue differentiation in initial fracture healing. J Orthop Res 6:736-748.
12. Carter DR, Orr TE, Fyhrie DP, et al. 1987. Influences of mechanical stress on prenatal and postnatal skeletal development. Clin Orthop 219:237-250. (Pubitemid 17085876)
13. Huiskes R, Chao EY, Crippen TE. 1985. Parametric analyses of pin-bone stresses in external fracture fixation devices. J Orthop Res 3:341-349. (Pubitemid 16247035)
14. Carter DR, Vasu R, Spengler DM, et al. 1981. Stress fields in the unplated and plated canine femur calculated from in vivo strain measurements. J Biomech 14:63-70. (Pubitemid 11215082)
15. Goodship AE, Cunningham JL, Kenwright J. 1998. Strain rate and timing of stimulation in mechanical modulation of fracture healing. Clin Orthop Relat Res 322(Suppl.):S105-S115. (Pubitemid 128699931)
16. Kenwright J, Goodship AE. 1989. Controlled mechanical stimulation in the treatment of tibial fractures. Clin Orthop Relat Res 241:36-47. (Pubitemid 19101241)
17. Richardson JB, Cunningham JL, Goodship AE, et al. 1994. Measuring stiffness can define healing of tibial fractures. J Bone Joint Surg [Br] 76:389-394. (Pubitemid 24148337)
18. Aaron R, Bolander M. 2005. Physical regulation of skeletal repair. Rosemont, IL: American Academy of Orthopaedic Surgeons.
19. Rubin CT, Lanyon LE. 1985. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 37:411-417. (Pubitemid 15015324)
20. Rubin CT, Lanyon LE. 1984. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg [Am] 66:397-402. (Pubitemid 14169460)
21. O'Connor JA, Lanyon LE, MacFie H. 1982. The influence of strain rate on adaptive bone remodelling. J Biomech 15:767-781. (Pubitemid 13178607)
22. Goodship AE, Lanyon LE, McFie H. 1979. Functional adaptation of bone to increased stress. An experimental study. J Bone Joint Surg [Am] 61:539-546. (Pubitemid 10161983)
23. Rubin C, Turner AS, Bain S. 2001. Anabolism: low mechanical signals strengthen long bones. Nature 412:603-604. (Pubitemid 32772264)
24. Fritton SP, McLeod KJ, Rubin CT. 2000. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech 33:317-325. (Pubitemid 30004029)
25. Carter DR, Caler WE. 1985. A cumulative damage model for bone fracture. J Orthop Res 3:84-90. (Pubitemid 15148024)
26. Phillips SJ, Thorton K, Barker L, et al. 1991. Using magnostrictive metal as a pump for biomedical application. ASAIO Trans 37:M509-M510.
27. Carter DR, Caler WE, Spengler DM, et al. 1981. Fatigue behavior of adult cortical bone: the influence of mean strain and strain range. Acta Orthop Scand 52:481-490. (Pubitemid 12237998)
28. Lawes TJ, Scott JC, Goodship AE. 2004. Increased insertion torque delays pin-bone interface loosening in external fixation with tapered bone screws. J Orthop Trauma 18:617-622.
29. Zar JH. 1996. Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall.
30. Hadjiargyrou M, Lombardo F, Zhao S, et al. 2002. Transcriptional profiling of bone regeneration: insight into the molecular complexity of wound repair. J Biol Chem. 277:30177-30182.
31. Wozney JM, Rosen V. 1998. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin Orthop 346:26-37. (Pubitemid 28046864)
32. Heckman JD, Ryaby JP, McCabe J, et al. 1994. Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J Bone Joint Surg [Am] 76:26-34. (Pubitemid 24081801)
33. Rubin C, Turner AS, Muller R, et al. 2002. Quantity and quality of trabecular bone in the femur are enhanced by a strongly anabolic, noninvasive mechanical intervention. J Bone Miner Res 17:349-357. (Pubitemid 34087668)
34. Rubin CT, Sommerfeldt DW, Judex S, et al. 2001. Inhibition of osteopenia by low magnitude, high-frequency mechanical stimuli. Drug Discov Today 6:848-858. (Pubitemid 32734513)
35. Adams DJ, Spirt AA, Brown TD, et al. 1997. Testing the daily stress stimulus theory of bone adaptation with natural and experimentally controlled strain histories. J Biomech 30:671-678. (Pubitemid 27309816)
36. Huang RP, Rubin CT, McLeod KJ. 1999. Changes in postural muscle dynamics as a function of age. J Gerontol A Biol Sci Med Sci 54:B352-B357. (Pubitemid 29441771)
37. Clamann HP. 1969. Statistical analysis of motor unit firing patterns in a human skeletal muscle. Biophys J 9:1233-1251.
38. Person RS, Kudina LP. 1972. Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. Electroencephalogr Clin Neurophysiol 32:471-483.
39. Carter DR, Vasu R. 1981. Plate and bone stresses for single- and double-plated femoral fractures. J Biomech 14:55-62. (Pubitemid 11215081)
40. Rubin CT, Lanyon LE. 1982. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol 101:187-211.
41. Brunelli MP, Einhorn TA. 1998. Medical management of osteoporosis. Fracture prevention. Clin Orthop 348:15-21.
42. Augat P, Margevicius K, Simon J, et al. 1998. Local tissue properties in bone healing: influence of size and stability of the osteotomy gap. J Orthop Res 16:475-481. (Pubitemid 28427699)
43. Augat P, Reeb H, Claes LE. 1996. Prediction of fracture load at different skeletal sites by geometric properties of the cortical shell. J Bone Miner Res 11:1356-1363. (Pubitemid 26282537)
44. Kelly PJ, An KN, Chao EYS, et al. 1985. Fracture healing: biomechanical, fluid dynamic and electrical considerations. In: Peck WA, editor. Bone mineral research. New York: Elsevier. p 295-319.
45. Claes L, Eckert-Hubner K, Augat P. 2003. The fracture gap size influences the local vascularization and tissue differentiation in callus healing. Langenbecks Arch Surg 388:316-322. (Pubitemid 37376817)
46. Rubin J, Rubin C, Jacobs CR. 2006. Molecular pathways mediating mechanical signaling in bone. Gene 367:1-16. (Pubitemid 43286736)
47. Burger EH, Klein-Nulen J. 1999. Responses of bone cells to biomechanical forces in vitro. Adv Dent Res 13:93-98.
48. Rubin J, Fan X, Biskobing DM, et al. 1999. Osteoclastogenesis is repressed by mechanical strain in an in vitro model. J Orthop Res 17:639-645.
49. Noble BS, Peet N, Stevens HY, et al. 2003. Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol 284:C934-C943. (Pubitemid 36336949)
50. Einhorn TA. 1996. Enhancement of fracture healing. Instr Course Lect 45:401-416.
51. Rubin CT, Capilla E, Luu YK, et al. 2007. Adipogenesis is inhibited by brief, daily exposure to high-frequency, extremely low-magnitude mechanical signals. Proc Natl Acad Sci USA 104:17879-17884. (Pubitemid 350210928)
52. Rubin CT, Gross TS, McLeod KJ, et al. 1995. Morphologic stages in lamellar bone formation stimulated by a potent mechanical stimulus. J Bone Miner Res 10:488-495.
53. Judex S, Boyd SK, Qin YX, et al. 2003. Adaptations of trabecular bone to low magnitude vibrations result in more uniform stress and strain under load. Ann Biomed Eng 31:12-20.
54. Rubin J, Rubin CT, McLeod KJ. 1995. Biophysical modulation of cell and tissue structure and function. Crit Rev Eukaryot Gene Expr 5:177-191.