Effects of low-intensity pulsed ultrasound therapy on fracture healing: A systematic review and meta-analysis

American Journal of Physical Medicine and Rehabilitation

Volumn 91, Issue 4, 2012, Pages 349-367

  Bashardoust Tajali, Siamak ^a,b   Houghton, Pamela ^a,b   MacDermid, Joy C ^a,b   Grewal, Ruby ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b ST JOSEPH S HEALTH CENTRE   (Canada)

Author keywords

Bone Healing; Fracture; Low Intensity Pulsed Ultrasound; Ultrasound

Indexed keywords

BONE REGENERATION; CASE CONTROL STUDY; FEMALE; FOLLOW UP; FRACTURE; FRACTURE HEALING; HUMAN; MALE; META ANALYSIS; METHODOLOGY; PHYSIOLOGY; RADIOGRAPHY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TIME; TREATMENT OUTCOME; ULTRASOUND THERAPY;

BONE REGENERATION; CASE-CONTROL STUDIES; FEMALE; FOLLOW-UP STUDIES; FRACTURE HEALING; FRACTURES, BONE; HUMANS; MALE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TIME FACTORS; TREATMENT OUTCOME; ULTRASONIC THERAPY;

EID: 84859109423     PISSN: 08949115     EISSN: None     Source Type: Journal    
DOI: 10.1097/PHM.0b013e31822419ba     Document Type: Review

References (106)

1. Paterson D: Treatment of nonunion with a constant direct current: A totally implantable system. Orthop Clin North Am 1984;15:47-59 (Pubitemid 14185834)
2. Childs SG: Stimulators of bone healing. Biologic and biomechanical. Orthop Nurs 2003;22:421-8
3. Trock DH: Electromagnetic fields and magnets: Investigational treatment for musculoskeletal disorders. Rheum Dis Clin North Am 2000;26:51-62 (Pubitemid 30091721)
4. Hannouche D, Petite H, Sedel L: Current trends in the enhancement of fracture healing. J Bone Joint Surg 2001;83:157-64 (Pubitemid 32242006)
5. Buckwalter JA, Einhorn TA, Marsh JL: Bone and joint healing. In: Bucholz RW, Heckman JD, Court- Brown C, et al. Rockwood and Green's Fractures in Adults. ed 6. Philadelphia, PA: Lippincott Williams & Wilkins; 2006:297-311.
6. Moholkar KD, Ziran BH: Bone and joint healing. In: Bucholz RW, Heckman JD, Court-Brown C, et al. Rockwood and Green's Fractures in Adults. ed 6. Philadelphia, PA: Lippincott Williams & Wilkins; 2006:564-611
7. March D: Concepts of fracture union, delayed union and nonunion. Clin Orthop Relat Res 1998;(355 suppl): S22-30
8. Aronson J: The Ilizarov technique for bone regeneration and repair. In: Lieberman JR, Friedlaender GE, Bone Regeneration and Repair, Biology and Clinical Application. New Jersey: Humana Press; 2005:195-223
9. Heckman JD, Ryaby JP, McCabe J, et al: Acceleration of tibial fracture healing by non-invasive, low intensity pulsed ultrasound. J Bone Joint Surg 1994; 76:26-34 (Pubitemid 24081801)
10. Kristiansen TK, Ryaby JP, McCabe J, et al: Accelerated healing of distal radial fractures with the use of specific, low intensity ultrasound. J Bone Joint Surg 1997;79:961-73
11. Malizos KN, Hantes ME, Protopappas V, et al: Low intensity pulsed ultrasound for bone healing: An overview. Injury 2006;37S:(suppl 1)S56-62 (Pubitemid 44316772)
12. Goodship AE, Kennwright J: The influence of induced micro movement upon the healing of experimental tibial fractures. J Bone Joint Surg 1985; 67B:650-5 (Pubitemid 16228160)
13. Barden RM, Sinkora GL: Bone stimulators for fusions and fractures. Nurs Clin North Am 1991;26:89-103
14. Benazzo F, Mosconi M, Beccarisi G: Use of capacitive coupled electric fields in stress fractures in athletes. Clin Orthop Relat Res 1995;310:145-9
15. Cundy PJ, Paterson DC: A ten year review of treatment of delayed union and nonunion with an implanted bone growth stimulation. Clin Orthop Relat Res 1990;259:216-22 (Pubitemid 20336123)
16. Gersh MR: Microcurrent electrical stimulation: Putting it in perspective. Clin Manage 1987;9:51-4
17. Gordjestani M, Dermaut L, Thierens H: Infrared laser and bone metabolism: A pilot study. Int J Oral Maxillofac Surg 1994;23:54-6 (Pubitemid 124012629)
18. Bashardoust Tajali S, Ebrahimi E, Kazemi S, et al: Effects of He-Ne laser irradiation on osteosynthesis. Osteosynth Trauma Care 2003;11:S17-20 (Pubitemid 37118028)
19. Schortinghuis J, Stegenga B, Raghoebar GM, et al: Ultrasound stimulation of Maxillofacial bone healing. Crit Rev Oral Biol Med 2003;14:63-74
20. Rubin C, Bolander M, Ryaby JP, et al: The use of low intensity ultrasound to accelerate the healing of fractures. J Bone Joint Surg Am 2001;83:259-70 (Pubitemid 32163721)
21. Watson T, Young SR: Therapeutic ultrasound. In: Watson T. Electrotherapy Evidence-Based Practice. Edinburgh, UK: Churchill Livingstone; 2008:179-200.
22. Dalecki D: Mechanical bio effects of ultrasound. Ann Rev Biomed Eng 2004;6:229-48
23. Dyson M: Role of ultrasound in wound healing. In: Kloth LC, McCulloch JM, Feedar JA. Wound Healing: Alternatives in Management. Philadelphia, PA: FA Davis; 1990:259-85
24. Maintz G: Tierexperimentelle untersuchungen uber dle wirkung der ultraschallwellen auf die knochenregeneration. Strahlentherapie 1950;82:631-8
25. Corradi C, Cozzolino A: Ultrasound and bone callus formation during function [in Italian]. Arch Ortop 1953;66:77-98
26. Duarte LR: The stimulation of bone growth by ultrasound. Arch Orthop Trauma Surg 1983;101:153-9 (Pubitemid 13092928)
27. Pilla AA, Mont MA, Nasser PR, et al: Non-invasive low intensity pulsed ultrasound accelerates bone healing in the rabbit. J Orthop Trauma 1990;4:246-53
28. Yang KH, Parvizi J, Wang SJ, et al: Exposure to low intensity ultrasound increases aggrecan gene expression in a rat femur fracture model. J Orthop Res 1996;14:802-9 (Pubitemid 26376526)
29. El-Bialy TH, Royston TJ, Magin RL, et al: The effect of pulsed ultrasound on mandibular distraction. Ann Biomed Eng 2002;30:1251-6
30. El-Bialy TH, El-Shamy I, Graber TM. The use of low intensity ultrasound to accelerate the healing of fractures. Angle Orthod 2003;73:631-9
31. Erdogen O, Esen E, Ustun Y, et al: Effects of low intensity pulsed ultrasound on healing of mandibular fractures: An experimental study in rabbits. J Oral Maxillofac Surg 2006;64:180-8 (Pubitemid 43087777)
32. Ikai H, Tamura T, Watanabe T, et al: Low intensity pulsed ultrasound accelerates periodontal wound healing after flap surgery. J Periodontal Res 2008; 43:212-6
33. Claes L, Willie B: The enhancement of bone regeneration by ultrasound. Prog Biophys Mol Biol 2007; 93:384-98 (Pubitemid 44809399)
34. Xavier CAM, Duarte LR: Estimulaca ultra-sonica de calo osseo: Applicaca clinica. Rev Brasileira Ortop 1983;18:73-80
35. El-Mowafi H, Mohsen M: The effect of low intensity pulsed ultrasound on callus maturation in tibial distraction osteogenesis. Int Orthop 2005;29:121-4 (Pubitemid 40558562)
36. Rutten S, Nolte PA, Guit GL, et al: Use of low intensity pulsed ultrasound for posttraumatic nonunions of the tibia: A review of patients treated in the Netherlands. J Trauma 2007;62:902-8 (Pubitemid 46624208)
37. Tsumaki N, Kakiuchi M, Sasaki J, et al: Low intensity pulsed ultrasound accelerates maturation of callus in patients treated with opening-wedge high tibial osteotomy by hemicallotasis. J Bone Joint Surg 2004;86:2399-405 (Pubitemid 39473078)
38. Lerner A, Stein H, Soudry M: Compound highenergy limb fractures with delayed union: Our experience with adjuvant ultrasound stimulation (Exogen). Ultrasonics 2004;42:915-7
39. Gold SM, Wasserman R: Preliminary results of tibial bone transports with pulsed low intensity ultrasound (Exogen). J Orthop Trauma 2005;19:10-6 (Pubitemid 40309432)
40. Jingushi S, Mizuno K, Matsushita T, et al: Low intensity pulsed ultrasound treatment for postoperative delayed union or nonunion of long bone fractures. J Orthop Sci 2007;12:35-41 (Pubitemid 46169937)
41. Nolte PA, Van der Krans A, Patka P, et al: Low intensity pulsed ultrasound in the treatment of nonunions. J Trauma 2001;51:693-703
42. Rutten S, Nolte PA, Korstjens CM, et al: Low intensity pulsed ultrasound increases bone volume, osteoid thickness and mineral apposition rate in the area of fracture healing in patients with a delayed union of the osteotomized fibula. Bone 2008;43: 348-54
43. Leung KS, Lee WS, Tsui HF, et al: Complex tibial fracture outcomes following treatment with low intensity pulsed ultrasound. Ultrasound Med Biol 2004;30:389-95
44. Cook SD, Ryaby JP, McCabe J, et al: Acceleration of tibia and distal radius fracture healing in patients who smoke. Clin Orthop Relat Res 1997;337:198-207 (Pubitemid 27172065)
45. Gebauer D, Correll J: Pulsed low intensity ultrasound. A new salvage procedure for delayed unions and nonunions after leg lengthening in children. J Pediatr Orthop 2005;25:750-4 (Pubitemid 41546410)
46. Ricardo M. The effect of ultrasound on the healing of muscle pediculated bone graft in scaphoid nonunion. Int Orthop 2006;30:123-7
47. Lubbert PHW, Van der Rijt RHH, Hoorntje LE, et al: Low intensity pulsed ultrasound (LIPUS) I fresh clavicle fractures: A multi-centre double blind randomised controlled trial. Injury 2008;39:1444-52
48. Mayr E, Frankel V, Ruter A: UltrasoundVan alternative healing method for nonunions? Arch Orthop Trauma Surg 2000;120:1-8 (Pubitemid 30009177)
49. Handolin L, Kiljunen V, Arnala I, et al: No long term effects of ultrasound therapy on bioabsorbable screw fixed lateral malleolar fracture. Scand J Surg 2005; 94:239-42 (Pubitemid 41444927)
50. Schortinghuis J, Bronckers ALJJ, Stegenga B, et al: Ultrasound to stimulate early bone formation in a distraction gap: A double blind randomised clinical pilot trial in the edentulous mandible. Arch Oral Biol 2005;50:411-20 (Pubitemid 40307183)
51. Handolin L, Kiljunen V, Arnala I, et al: Effect of ultrasound therapy on bone healing of lateral malleolar fractures of the ankle joint fixed with bioabsorbable screws. J Orthop Sci 2005;10:391-5 (Pubitemid 41264826)
52. Handolin L, Kiljunen V, Arnala I, et al: The effect of low intensity ultrasound and bioabsorbable selfreinforced poly-L-lactide screw fixation on bone in lateral malleolar fractures. Arch Orthop Trauma Surg 2005;125:317-21 (Pubitemid 40895352)
53. Rue JPH, Armstrong DW, Frassica FJ, et al: The effect of pulsed ultrasound in the treatment of tibial stress fractures. Orthopedics 2004;27:1192-5 (Pubitemid 39549595)
54. Emami A, Larsson A, Petren-Mallmin M, et al: Serum bone markers after intramedullary fixed tibial fractures. Clin Orthop Relat Res 1999;368:220-9 (Pubitemid 29533998)
55. Emami A, Petren-Mallmin M, Larsson S: No effect of low intensity ultrasound on healing time of intramedullary fixed tibial fractures. J Orthop Trauma 1999;13:252-7
56. Cohen MM Jr.: The new bone biology: Pathologic, molecular, and clinical correlates. Am J Med Genet A 2006;140:2646-706 (Pubitemid 44865095)
57. Reher P, Doan N, Bradnock B, et al: Effect of ultrasound on the production of IL-8, basic FGF and VEGF. Cytokines 1999;11:416-23 (Pubitemid 29259636)
58. Wu CC, Lewallen DG, Bolander ME, et al: Exposure to low intensity ultrasound stimulates proteoglycan synthesis in rat chondrocytes by increasing aggrecan gene expression. Trans Orthop Res Soc 1996;21:622
59. Parvizi J, Wu CC, Lewallen DG, et al: Low intensity ultrasound stimulates proteoglycan synthesis in rat chondrocytes by increasing aggrecan gene expression. J Orthop Res 1999;17:488-94 (Pubitemid 29383607)
60. Ito M, Azuma Y, Ohta T, et al: Effects of ultrasound and 1, 25-dihydroxyvitamin D3 on growth factor secretion in co-cultures of osteoblasts and endothelial cells. Ultrasound Med Biol 2000;26:161-6 (Pubitemid 30045534)
61. Reher P, Harris M, Whiteman M, et al: Ultrasound stimulates nitric oxide and prostaglandin E2 production by human osteoblasts. Bone 2002;31:236-41 (Pubitemid 34754453)
62. Busse JW, Bhandari M, Kulkarni AV, et al: The effect of low intensity pulsed ultrasound therapy on time to fracture healing: A meta analysis. CMAJ 2002; 166:437-41 (Pubitemid 34164092)
63. Walker NA, Denegar CR, Preische J: Low intensity pulsed ultrasound and pulsed electromagnetic field in the treatment of tibial fractures: A systematic review. J Athl Train 2007;42:530-5 (Pubitemid 351377902)
64. Griffin XL, Costello I, Costa ML: The role of low intensity pulsed ultrasound therapy in the management of acute fractures: A systematic review. J Trauma 2008;65:1446-52
65. Busse JW, Kaur J, Mollon B, et al: Low intensity pulsed ultrasounography for fractures: Systematic review of randomised controlled trials. BMJ 2009; 338:b351, 1-9
66. Maher CG, Sherrington C, Herbert RD, et al: Reliability of PEDro scale for rating quality of randomized control trials. Phys Ther 2003;83:713-21 (Pubitemid 37238882)
67. Day SM, Ostrum RF, Chao EYS, et al: Bone injury, regeneration, and repair. In: Buckwalter JA, Einhorn TA, Simon SR. Orthopaedic Basic Science: Biology and Biomechanics of the Musculoskeletal System. ed 2. Rosemont, IL: American Academy of Orthopaedic Surgeons; 2000:371-99.
68. Cochrane Collaboration. Cochrane Reviewers' Handbook 4.2.6, Updated September 2006. Oxford, UK: Cochrane Collaboration; 2006.
69. Legome E, Pancu D: Future applications for emergency ultrasound. Emerg Med Clin North Am 2004; 22:817-27 (Pubitemid 39037706)
70. Warden SJ, Bennell KL, McMeeken JM, et al: Can conventional therapeutic ultrasound units be used to accelerate fracture repair? Phys Ther Rev 1999;4: 117-26
71. Hadjiargyrou M, Mcleod K, Ryaby JP, et al: Enhancement of fracture healing by low intensity ultrasound. Clin Orthop Relat Res 1998;355S; S216-29
72. Khan Y, Laurencin CT: Fracture repair with ultrasound: Clinical and cell-based evaluation. J Bone Joint Surg Am 2008;90:138-44 (Pubitemid 351329133)
73. Fini M, Giavaresi G, Setti S, et al: Current trends in the enhancement of biomaterial osteointegration: Biophysical stimulation. Int J Artif Organs 2004; 27:681-90 (Pubitemid 39369012)
74. Nelson FR, Brighton CT, Ryaby J, et al: Use of physical forces in bone healing. J Am Acad Orthop Surg 2003;11:344-54
75. Warden SJ, Bennell KL, McMeeken JM, et al: Acceleration of fresh fracture repair using the sonic accelerated fracture healing system (SAFHS): A review. Calcif Tissue Int 2000;66:157-63 (Pubitemid 30056712)
76. Einhorn TA: Current concepts review. Enhancement of fracture healing. J Bone Joint Surg Am 1995; 77:940-56
77. Victoria G, Petrisor B, Drew B, et al: Bone stimulation for fracture healing: What's all the fuss? Indian J Orthop 2009;43:117-20
78. Van der Windt DAWM, Van der Heijden GJMG, Van den Berg SGM, et al: Ultrasound therapy for musculoskeletal disorders: A systematic review. Pain 1999;81:257-71 (Pubitemid 29257896)
79. Erdogan O, Esen E: Biological aspects and clinical importance of ultrasound therapy in bone healing. J Ultrasound Med 2009;28:765-76
80. Harle J, Mayia F, Olsen I, et al: Effects of ultrasound on transforming growth factor-B genes in bone cells. Eur Cell Mater 2005;10:70-7
81. Korstjens CM, Nolte PA, Burger EH, et al: Stimulation of bone cell differentiation by low intensity ultrasound. A histomorphometric in Vitro study. J Orthop Res 2004;22:495-500 (Pubitemid 38489724)
82. Nolte PA, Klein-Nulend J, Albers GHR, et al: Low intensity ultrasound stimulates endochondral ossification in Vitro. J Orthop Res 2001;19:301-7 (Pubitemid 32331707)
83. Borsje MA, Ren Y, Haan-Visser HW, et al: Comparison of low intensity pulsed ultrasound and pulsed electromagnetic field treatments on OPG and RANKL expression in human osteoblast Y like cells. Angle Orthod 2010;80:498-503
84. Wiltink A, Nijweide PJ, Oosterbaan WA, et al: Effect of therapeutic ultrasound on endochondral ossification. Ultrasound Med Biol 1995;21:121-7
85. Dyson M, Brookes M: Stimulation of bone repair by ultrasound. Ultrasound Med Biol 1983;Suppl 2:61-6
86. Tsai CL, Chang WH, Liu TK, et al: Ultrasound can affect bone healing both locally and systemically. Chin J Physiol 1991;34:213-22
87. Tsai CL Chang WH, Liu TK: Preliminary studies of duration and intensity of ultrasonic treatments on fracture repair. Chin J Physiol 1992;35:21-6
88. Tsai CL, Chang WH, Liu TK, et al: Ultrasonic effect on fracture repair and prostaglandin E2 production. Chin J Physiol 1992;35:168
89. Chan CW, Qin L, Lee KM, et al: Dose-dependent effect of low intensity pulsed ultrasound on callus formation during rapid distraction osteogenesngis. J Orthop Res 2006;24:2072-9 (Pubitemid 44717969)
90. Li J, Waugh LJ, Hui SL, et al: Low intensity pulsed ultrasound and nonsteroidal anti-inflammatory drugs have opposing effects during stress fracture repair. J Orthop Res 2007;25:1559-67 (Pubitemid 350293803)
91. Lin FH, Lin CC, Lu CM, et al: The effects of ultrasound stimulation on DP-bioglass bone substitute. Med Eng Phys 1995;17:20-6
92. Claes L, Ruter A, Mayr E: Low intensity ultrasound enhances maturation of callus after segmental transport. Clin Orthop Relat Res 2005;430:189-94 (Pubitemid 40096151)
93. Mayr E, Laule A, Suger G, et al: Radiographic results of callus distraction aided by pulsed low intensity ultrasound. J Orthop Trauma 2001;15:407-14 (Pubitemid 33130619)
94. Sato W, Matsushita T, Nakamura K: Acceleration of increase in bone mineral content by low intensity ultrasound energy in leg lengthening. J Ultrasound Med 1999;18:699-702
95. Giannini S, Giombini A, Rita Moneta M, et al: Low intensity pulsed ultrasound in the treatment of traumatic hand fracture in an elite athlete. Am J Phys Med Rehabil 2004;83:921-5 (Pubitemid 39557474)
96. Fujioka H, Tsunoda M, Noda M, et al: Treatment of ununited fracture of the hook of Hamate by low intensity pulsed ultrasound: A case report. J Hand Surg 2000;25A:77-9 (Pubitemid 30078126)
97. Behari J, Singh S: Ultrasound propagation in Fin vivo bone. Ultrasonics 1981;19:87-90
98. Kristiansen TK: The effect of low power specifically programmed ultrasound on the healing time of fresh fractures using a Colles' model. J Orthop Trauma 1990;4:227-8
99. Busse JW, Bhandari M: Therapeutic ultrasound and fracture healing: A survey of beliefs and practices. Arch Phys Med Rehabil 2004;85:1653-6 (Pubitemid 39349410)
100. Gilsanz V, Al Wren T, Sanchez M, et al: Low level, high frequency mechanical signals enhance musculoskeletal development of young women with low BMD. J Bone Miner Res 2006;21:1464-74 (Pubitemid 44300053)
101. Thurmuller P, Troulis M, O'Neill MJ, et al: Use of ultrasound to assess healing of a mandibular distraction wound. J Oral Maxillofac Surg 2002;60:1038-44 (Pubitemid 34971249)
102. Chapman I, MacNally NA, Tucker S: Ultrasound induced changes in rates of influx and efflux of potassium ions in rat thymocytes in vitro. Ultrasound Med Biol 1980;6:47-58 (Pubitemid 10128817)
103. Ryaby JT, Matthew J, Duarte-Alves P: Low intensity pulsed ultrasound increases calcium incorporation in both differentiating cartilage and bone cell cultures. Trans Orthop Res Soc 1989;14:15
104. Ryaby JT, Matthew J, Duarte-Alves P: Low intensity pulsed ultrasound affects Adenylate cyclase and TGFbeta synthesis in osteoblastic cells. Trans Orthop Res Soc 1992;17:590
105. Kokubu T, Matsui N, Fujioka H, et al: Low intensity pulsed ultrasound exposure increases prostaglandin E2 production via the induction of cyclooxygenase-2 mRNA in mouse osteoblasts. Biochem Biophys Res Commun 1999;256:284-7 (Pubitemid 29298875)
106. Romano CL, Romano D, Logoluso N: Low intensity pulsed ultrasound for the treatment of bone delayed union or nonunion: A review. Ultrasound Med Biol 2009;35:529-36