Advertisement

The Application of Pulsed Electromagnetic Fields (PEMFs) for Bone Fracture Repair: Past and Perspective Findings

Abstract

Bone fractures are one of the most commonly occurring injuries of the musculoskeletal system. A highly complex physiological process, fracture healing has been studied extensively. Data from in vivo, in vitro and clinical studies, have shown pulsed electromagnetic fields (PEMFs) to be highly influential in the fracture repair process. Whilst the underlying mechanisms acting to either inhibit or advance the physiological processes are yet to be defined conclusively, several non-invasive point of use devices have been developed for the clinical treatment of fractures. With the complexity of the repair process, involving many components acting at different time steps, it has been a challenge to determine which PEMF exposure parameters (i.e., frequency of field, intensity of field and dose) will produce the most optimal repair. In addition, the development of an evidence-backed device comes with challenges of its own, with many elements (including process of exposure, construct materials and tissue densities) being highly influential to the field exposed. The objective of this review is to provide a broad recount of the applications of PEMFs in bone fracture repair and to then demonstrate what is further required for enhanced therapeutic outcomes.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

References

  1. 1.

    Adie, S., I. Harris, J. Naylor, H. Rae, A. Dao, S. Yong, and V. Ying 2011. Pulsed electromagnetic field stimulation for acute tibial shaft fractures: a multicenter, double-blind, randomized trial. J. Bone Joint Surg. 93(17):1569–1576.

  2. 2.

    Ament, C. and E. Hofer 2000. A fuzzy logic model of fracture healing. J. Biomech. 33(8):961–968.

  3. 3.

    Andreykiv, A., F. Van Keulen, and P. Prendergast 2008. Simulation of fracture healing incorporating mechanoregulation of tissue differentiation and dispersal/proliferation of cells. Biomech. Model. Mechanobiol. 7(6):443–461.

  4. 4.

    Androjna, C., B. Fort, M. Zborowski, and R. J. Midura 2014. Pulsed electromagnetic field treatment enhances healing callus biomechanical properties in an animal model of osteoporotic fracture. Bioelectromagnetics, 35(6):396–405.

  5. 5.

    Assiotis, A., N. P. Sachinis, and B. E. Chalidis 2012. Pulsed electromagnetic fields for the treatment of tibial delayed unions and nonunions. A prospective clinical study and review of the literature. J. Orthop. Surg. Res. 7(1):1.

  6. 6.

    Atalay, Y., N. Gunes, M. D. Guner, V. Akpolat, M. S. Celik, and R. Guner 2015. Pentoxifylline and electromagnetic field improved bone fracture healing in rats. Drug Des. Dev. Ther. 9:5195–5201.

  7. 7.

    Bailón-Plaza, A. and M. C. van der Meulen 2003. Beneficial effects of moderate, early loading and adverse effects of delayed or excessive loading on bone healing. J.Biomech. 36(8):1069–1077.

  8. 8.

    Bailón-Plaza, A. and M. C. Vander Meulen 2001. A mathematical framework to study the effects of growth factor influences on fracture healing. J.Theor. Biol. 212(2):191–209.

  9. 9.

    Barker, A., R. Dixon, W. Sharrard, and M. Sutcliffe 1984. Pulsed magnetic field therapy for tibial non-union: interim results of a double-blind trial. The Lancet, 323(8384):994–996.

  10. 10.

    Barnaba, S., R. Papalia, L. Ruzzini, A. Sgambato, N. Maffulli, and V. Denaro 2013. Effect of pulsed electromagnetic fields on human osteoblast cultures. Physiother. Res. Int. 18(2):109–114.

  11. 11.

    Bassett, C. A. L. 1967. Biologic significance of piezoelectricity. Calcif. Tissue Res. 1(1):252–272.

  12. 12.

    Bassett, C. A. L. 1982. Pulsing electromagnetic fields: a new method to modify cell behavior in calcified and noncalcified tissues. Calcif. Tissue Int. 34(1):1–8.

  13. 13.

    Bassett, C. A. L. 1993. Beneficial effects of electromagnetic fields. J. Cell. Biochem. 51(4):387–393.

  14. 14.

    Bassett, C., S. Mitchell, and S. Gaston 1981. Treatment of ununited tibial diaphyseal fractures with pulsing electromagnetic fields. J. Bone Joint Surg. Am. 63(4):511–523.

  15. 15.

    Bassett, C., R. Pawluk, and A. Pilla 1974. Acceleration of fracture repair by electromagnetic fields. A surgically noninvasive method. Ann. N Y Acad. Sci. 238:242–262.

  16. 16.

    Beck, B. R., G. O. Matheson, G. Bergman, T. Norling, M. Fredericson, A. R. Hoffman, and R. Marcus 2008. Do capacitively coupled electric fields accelerate tibial stress fracture healing? A randomized controlled trial. Am. J. Sports Med. 36(3):545–553.

  17. 17.

    Behrens, S. B., M. E. Deren, and K. O. Monchik 2013. A review of bone growth stimulation for fracture treatment. Curr. Orthop. Pract. 24(1):84–91.

  18. 18.

    Bernhardt, J. 1979. The direct influence of electromagnetic fields on nerve-and muscle cells of man within the frequency range of 1 hz to 30 mhz. Radiat. Environ. Biophys. 16(4):309–323.

  19. 19.

    Betti, E., S. Marchetti , R. Cadossi , C. Faldini, and A. Faldini. Effect of stimulation by low-frequency pulsed electromagnetic fields in subjects with fracture of the femoral neck. In: 1999. In: Electricity and Magnetism in Biology and Medicine, edited by F. Bersani. Springer: New York, 1999, pp. 853–855

  20. 20.

    Biomet ®. Biomet ®orthopak ® non-invasive bone growth stimulator system.

  21. 21.

    Brighton, C. T., W. Wang, R. Seldes, G. Zhang, and S. R. Pollack 2001. Signal transduction in electrically stimulated bone cells. J. Bone Joint Surg. Am. 83(10):1514–1523.

  22. 22.

    Byrne, D. P., D. Lacroix, and P. J. Prendergast 2011. Simulation of fracture healing in the tibia: Mechanoregulation of cell activity using a lattice modeling approach. J. Orthop. Res. 29(10):1496–1503.

  23. 23.

    Carlier, A., L. Geris, J. Lammens, and H. Van Oosterwyck 2015. Bringing computational models of bone regeneration to the clinic. Wiley Interdiscip. Rev. Syst. Biol. Med. 7(4):183–194.

  24. 24.

    Carter, D. R., G. S. Beaupre, N. J. J. Giori, J. A. J. A. Helms, and G. S. Beaupré 1998. Mechanobiology of skeletal regeneration. Clin. Orthop. Relat. Res. 355(355):S41–55.

  25. 25.

    Ceccarelli, G., N. Bloise, M. Mantelli, G. Gastaldi, L. Fassina, M. G. Cusella De Angelis, D. Ferrari, M. Imbriani, and L. Visai 2013. AA comparative analysis of the in vitro effects of pulsed electromagnetic field treatment on osteogenic differentiation of two different mesenchymal cell lineages. BioRes. Open Access 2(4):283–294.

  26. 26.

    Chao, E. Y. S., N. Inoue, U. Ripamonti, and S. Fenwick 2003. Biophysical stimulation of bone fracture repair, regeneration and remodelling. Eur. Cells Mater. 6(1979):72–85.

  27. 27.

    Checa, S. and P. J. Prendergast 2009. A mechanobiological model for tissue differentiation that includes angiogenesis: a lattice-based modeling approach. Ann. Biomed. Eng. 37(1):129–145.

  28. 28.

    Chen, C.-H., Y.-S. Lin, Y.-C. Fu, C.-K. Wang, S.-C. Wu, G.-J. Wang, R. Eswaramoorthy, Y.-H. Wang, C.-Z. Wang, Y.-H. Wang, and Others 2013. Electromagnetic fields enhance chondrogenesis of human adipose-derived stem cells in a chondrogenic microenvironment in vitro. J. Appl. Physiol. 114(5):647–655.

  29. 29.

    Chen, G., F. Niemeyer, T. Wehner, U. Simon, M. A. Schuetz, M. J. Pearcy, and L. E. Claes 2009. Simulation of the nutrient supply in fracture healing. J. Biomech. 42(15):2575–2583.

  30. 30.

    Claes, L., P. Augat, G. Suger, and H. J. Wilke 1997. Influence of size and stability of the osteotomy gap on the success of fracture healing. J. Orthop. Res. 15(4):577–584.

  31. 31.

    Claes, L. E. and C. A. Heigele 1999. Magnitudes of local stress and strain along bony surfaces predict the course and type of fracture healing. J. Biomech. 32(3):255–266.

  32. 32.

    Claes, L., S. Recknagel, and A. Ignatius 2012. Fracture healing under healthy and inflammatory conditions. Nat. Rev. Rheumatol. 8(3):133–143.

  33. 33.

    Clement, N., A. Duckworth, L. Biant, M. McQueen, et al. 2017. The changing epidemiology of fall-related fractures in adults. Injury, 48(4):819–824.

  34. 34.

    De Haas, W. G., A. Beupr, H. Cameron, and E. English 1986. The canadian experience with pulsed magnetic fields in the treatment of ununited tibial fractures. Clinical Rrthopaedics and Related Research, 208:55–58.

  35. 35.

    De Haas, W. G., M. A. Lazarovici, and D. M. Morrison 1979. The effect of low frequency magnetic fields on the healing of the osteotomized rabbit radius. Clin. Orthop. Relat. Res. (145):245–251.

  36. 36.

    Dimitriou, R., E. Tsiridis, and P. V. Giannoudis 2005. Current concepts of molecular aspects of bone healing. Injury, 36(12):1392–1404.

  37. 37.

    Einhorn, T. A. 2005. The science of fracture healing. J. Orthop.Trauma 19(10 Suppl):S4–S6.

  38. 38.

    Faldini, C., M. Cadossi, D. Luciani, E. Betti, E. Chiarello, and S. Giannini 2010. Electromagnetic bone growth stimulation in patients with femoral neck fractures treated with screws: prospective randomized double-blind study. Curr. Orthop. Pract. 21(3):282–287.

  39. 39.

    Fu, Y.-C., C.-C. Lin, J.-K. Chang, C.-H. Chen, I.-C. Tai, G.-J. Wang, and M.-L. Ho 2014. A novel single pulsed electromagnetic field stimulates osteogenesis of bone marrow mesenchymal stem cells and bone repair. PloS ONE, 9(3):e91581.

  40. 40.

    Funk, R. H. W., T. Monsees, and N. Özkucur 2009. Electromagnetic effects - From cell biology to medicine. Progress in Histochemistry and Cytochemistry, 43(4):177–264.

  41. 41.

    Geris, L. 2014. Regenerative orthopaedics: In vitro, in vivo ... in silico. Int. Orthop. 38(9):1771–1778.

  42. 42.

    Geris, L., A. Gerisch, J. V. Sloten, R. Weiner, and H. V. Oosterwyck 2008. Angiogenesis in bone fracture healing: a bioregulatory model. J. Theor. Biol. 251(1):137–158.

  43. 43.

    Geris, L., Y. Guyot, J. Schrooten, and I. Papantoniou 2016. In silico regenerative medicine: how computational tools allow regulatory and financial challenges to be addressed in a volatile market. Interface Focus, 6(2):20150105.

  44. 44.

    Geris, L., J. Vander Sloten, and H. Van Oosterwyck 2009. In silico biology of bone modelling and remodelling: regeneration. Philos. Trans. R. Soc. A 367(1895):2031–2053.

  45. 45.

    Giannoudis, P., S. Psarakis, and G. Kontakis 2007. Can we accelerate fracture healing?: a critical analysis of the literature. Injury, 38(1):S81–S89.

  46. 46.

    Grace, K. L., W. J. Revell, and M. Brookes 1998. The effects of pulsed electromagnetism on fresh fracture healing: osteochondral repair in the rat femoral groove. Orthopaedics 21(3): 297–302.

  47. 47.

    Grodzinsky, A. 2011. Field, Forces and Flows in Biological Systems. London: Garland Science.

  48. 48.

    Gupta, A. K., K. P. Srivastava, S. Avasthi, et al. 2009. Pulsed electromagnetic stimulation in nonunion of tibial diaphyseal fractures. Indian J. Orthop. 43(2):156.

  49. 49.

    Gómez-Benito, M. J., J. M. García-Aznar, J. H. Kuiper, and M. Doblaré 2005. Influence of fracture gap size on the pattern of long bone healing: a computational study. J. Theor. Biol. 235(1):105–119.

  50. 50.

    De Haas, W., J. Watson, and D. Morrison 1980. Non-invasive treatment of ununited fractures of the tibia using electrical stimulation. Bone Joint J. 62(4):465–470.

  51. 51.

    Haddad, J. B., A. G. Obolensky, and P. Shinnick 2007. The biologic effects and the therapeutic mechanism of action of electric and electromagnetic field stimulation on bone and cartilage: new findings and a review of earlier work. J. Altern. Complement. Med. 13(5):485–490.

  52. 52.

    Hak, D. J., D. Fitzpatrick, J. A. Bishop, J. L. Marsh, S. Tilp, R. Schnettler, H. Simpson, and V. Alt 2014. Delayed union and nonunions: epidemiology, clinical issues, and financial aspects. Injury, 45:S3–S7.

  53. 53.

    Heermeier, K., M. Spanner, J. Träger, R. Gradinger, P. G. Strauss, W. Kraus, and J. Schmidt 1998. Effects of extremely low frequency electromagnetic field (EMF) on collagen type I mRNA expression and extracellular matrix synthesis of human osteoblastic cells. Bioelectromagnetics, 19(4):222–231.

  54. 54.

    Hinsenkamp, M., F. Burny, M. Donkerwolcke, and E. Coussaert 1984. Electromagnetic stimulation of fresh fractures treated with hoffmann® external fixation. Orthopedics, 7(3):411–416.

  55. 55.

    Ibiwoye, M. O., K. A. Powell, M. D. Grabiner, T. E. Patterson, Y. Sakai, M. Zborowski, A. Wolfman, and R. J. Midura 2004. Bone mass is preserved in a critical-sized osteotomy by low energy pulsed electromagnetic fields as quantitated by in vivo micro-computed tomography. J. Orthop. Res. 22(5):1086–1093.

  56. 56.

    Inoue, N., I. Ohnishi, D. Chen, L. W. Deitz, J. D. Schwardt, and E. Chao 2002. Effect of pulsed electromagnetic fields (PEMF) on late-phase osteotomy gap healing in a canine tibial model. J. Orthop. Res. 20(5):1106–1114.

  57. 57.

    Isaksson, H. 2012. Recent advances in mechanobiological modeling of bone regeneration. Mech. Res. Commun. 42:22–31.

  58. 58.

    Isaksson, H., C. C. van Donkelaar, R. Huiskes, J. Yao, and K. Ito 2008. Determining the most important cellular characteristics for fracture healing using design of experiments methods. J. Theor. Biol. 255(1):26–39.

  59. 59.

    Isaksson, H., W. Wilson, C. C. van Donkelaar, R. Huiskes, and K. Ito 2006. Comparison of biophysical stimuli for mechano-regulation of tissue differentiation during fracture healing. J. Biomech. 39(8):1507–1516.

  60. 60.

    Jansen, J. H. W., O. P. van der Jagt, B. J. Punt, J. A. N. Verhaar, J. P. T. M. van Leeuwen, H. Weinans, and H. Jahr 2010. Stimulation of osteogenic differentiation in human osteoprogenitor cells by pulsed electromagnetic fields: an in vitro study. BMC Musculoskelet. Disord. 11(1):1.

  61. 61.

    Kaivosoja, E., V. Sariola, Y. Chen, and Y. T. Konttinen 2015. The effect of pulsed electromagnetic fields and dehydroepiandrosterone on viability and osteo-induction of human mesenchymal stem cells. J. Tissue Eng. Regen. Med. 9(1):31–40.

  62. 62.

    Kalfas, I. H. 2001. Principles of bone healing. Neurosurg. Focus 10(4):E1.

  63. 63.

    Kirkpatrick, C., V. Krump-Konvalinkova, R. Unger, F. Bittinger, M. Otto, and K. Peters 2002. Tissue response and biomaterial integration: the efficacy of in vitro methods. Biomol. Eng. 19(2):211–217.

  64. 64.

    Lacroix, D., P. J. Prendergast, G. Li, and D. Marsh 2002. Biomechanical model to simulate tissue differentiation and bone regeneration: application to fracture healing. Med. Biol. Eng. Comput. 40(1):14–21.

  65. 65.

    Little, D. G., M. Ramachandran, and A. Schindeler 2007. The anabolic and catabolic responses in bone repair. Bone Joint J. 89(4):425–433.

  66. 66.

    Luo, F., T. Hou, Z. Zhang, Z. Xie, X. Wu, and J. Xu 2012. Effects of pulsed electromagnetic field frequencies on the osteogenic differentiation of human mesenchymal stem cells. Orthopedics, 35(4):e526–e531.

  67. 67.

    Markov, M. S. 2007. Pulsed electromagnetic field therapy history, state of the art and future. The Environmentalist, 27(4):465–475.

  68. 68.

    Mayer-Wagner, S., A. Passberger, B. Sievers, J. Aigner, B. Summer, T. S. Schiergens, V. Jansson, and P. E. Müller 2011. Effects of low frequency electromagnetic fields on the chondrogenic differentiation of human mesenchymal stem cells. Bioelectromagnetics, 32(4):283–290.

  69. 69.

    Maziarz, A., B. Kocan, M. Bester, S. Budzik, M. Cholewa, T. Ochiya, and A. Banas 2016. How electromagnetic fields can influence adult stem cells: positive and negative impacts. Stem Cell Res. Ther. 7(1):1.

  70. 70.

    Midura, R. J., M. O. Ibiwoye, K. A. Powell, Y. Sakai, T. Doehring, M. D. Grabiner, T. E. Patterson, M. Zborowski, and A. Wolfman 2005. Pulsed electromagnetic field treatments enhance the healing of fibular osteotomies. J. Orthop. Res. 23(5):1035–1046.

  71. 71.

    Milde, F., M. Bergdorf, and P. Koumoutsakos 2008. A hybrid model for three-dimensional simulations of sprouting angiogenesis. Biophys. J. 95(7):3146–60.

  72. 72.

    Moore, A. and D. Burris 2014. An analytical model to predict interstitial lubrication of cartilage in migrating contact areas. J. Biomech. 47(1):148–153.

  73. 73.

    Nandra, R., L. Grover, and K. Porter 2016. Fracture non-union epidemiology and treatment. Trauma, 18(1):3–11.

  74. 74.

    Nasr, S., S. Hunt, N. A. Duncan, et al. 2013. Effect of screw position on bone tissue differentiation within a fixed femoral fracture. J. Biomed. Sci. Eng. 6(12):71.

  75. 75.

    Nunamaker, D. M. 1998. Experimental models of fracture repair. Clin. Orthop. Relat. Res. 355:S56–S65.

  76. 76.

    Ongaro, A., A. Pellati, L. Bagheri, C. Fortini, S. Setti, and M. De Mattei 2014. Pulsed electromagnetic fields stimulate osteogenic differentiation in human bone marrow and adipose tissue derived mesenchymal stem cells. Bioelectromagnetics, 35(6):426–436.

  77. 77.

    Orthofix ®. Magnetic properties of materials.

  78. 78.

    Orthofix ®. Products & tissue forms.

  79. 79.

    Ossatec ®. Bone growth stimulator.

  80. 80.

    Panagopoulos, D. J., A. Karabarbounis, and L. H. Margaritis 2002. Mechanism for action of electromagnetic fields on cells. Biochem. Biophys. Res. Commun. 298(1):95–102.

  81. 81.

    Pasco, J. A., S. E. Lane, S. L. Brennan-Olsen, K. L. Holloway, E. N. Timney, G. Bucki-Smith, A. G. Morse, A. G. Dobbins, L. J. Williams, N. K. Hyde, et al. 2015. The epidemiology of incident fracture from cradle to senescence. Calcif. Tissue Int. 97(6):568–576.

  82. 82.

    Peiffer, V., A. Gerisch, D. Vandepitte, H. Van Oosterwyck, and L. Geris 2011. A hybrid bioregulatory model of angiogenesis during bone fracture healing. Biomech. Model. Mechanobiol. 10(3):383–395.

  83. 83.

    Petecchia, L., F. Sbrana, R. Utzeri, M. Vercellino, C. Usai, L. Visai, M. Vassalli, and P. Gavazzo 2015. Electro-magnetic field promotes osteogenic differentiation of BM-hMSCs through a selective action on Ca2+-related mechanisms. Sci. Rep. doi: https://doi.org/10.1038/srep13856

  84. 84.

    Phillips, A. M. 2005. Overview of the fracture healing cascade. Injury, 36 (3):S5–7.

  85. 85.

    Pivonka, P. and C. R. Dunstan 2012. Role of mathematical modeling in bone fracture healing. BoneKEY Rep. doi: https://doi.org/10.1038/bonekey.2012.221

  86. 86.

    Pivonka, P. and S. V. Komarova 2010. Mathematical modeling in bone biology: from intracellular signaling to tissue mechanics. Bone, 47(2):181–189.

  87. 87.

    Pérez, M. A. and P. J. Prendergast 2007. Random-walk models of cell dispersal included in mechanobiological simulations of tissue differentiation. J. Biomech. 40(10):2244–2253.

  88. 88.

    Ross, C. L., M. Siriwardane, G. Almeida-Porada, C. D. Porada, P. Brink, G. J. Christ, and B. S. Harrison 2015. The effect of low-frequency electromagnetic field on human bone marrow stem/progenitor cell differentiation. Stem Cell Res. 15(1):96–108.

  89. 89.

    Ryaby, J. T. 1998. Clinical effects of electromagnetic and electric fields on fracture healing. Clin. Orthop. Relat. Res. 355:S205–S215.

  90. 90.

    Schwartz, Z., B. Simon, M. Duran, G. Barabino, R. Chaudhri, and B. Boyan 2008. Pulsed electromagnetic fields enhance bmp-2 dependent osteoblastic differentiation of human mesenchymal stem cells. J. Orthop. Res. 26(9):1250–1255.

  91. 91.

    Scott, G. and J. King 1994. A prospective, double-blind trial of electrical capacitive coupling in the treatment of non-union of long bones. J. Bone Joint Surg. Am. 76(6):820–826.

  92. 92.

    Sharrard, W., M. Sutcliffe, M. Robson, and A. Maceachern 1982. The treatment of fibrous non-union of fractures by pulsing electromagnetic stimulation. Bone Joint J. 64(2):189–193.

  93. 93.

    Shefelbine, S. J., P. Augat, L. Claes, and U. Simon 2005. Trabecular bone fracture healing simulation with finite element analysis and fuzzy logic. J. Biomech. 38(12):2440–2450.

  94. 94.

    Shi, H.-F., J. Xiong, Y.-X. Chen, J.-F. Wang, X.-S. Qiu, Y.-H. Wang, and Y. Qiu 2013. Early application of pulsed electromagnetic field in the treatment of postoperative delayed union of long-bone fractures: a prospective randomized controlled study. BMC Musculoskelet. Disord. 14(1):1.

  95. 95.

    Simon, U., P. Augat, M. Utz, and L. Claes 2003. Simulation of tissue development and vascularisation in the callus healing process. Trans. Annu. Meet. Orthop. Res. Soc. 28:O299.

  96. 96.

    Simon, U., P. Augat, M. Utz, and L. Claes 2011. A numerical model of the fracture healing process that describes tissue development and revascularisation. Comput. Methods Biomech. Biomed. Eng. 14(1):79–93.

  97. 97.

    Simonis, R., E. Parnell, P. Ray, and J. Peacock 2003. Electrical treatment of tibial non-union: a prospective, randomised, double-blind trial. Injury, 34(5):357–362.

  98. 98.

    Steinberg, F. U. 1980. The effects of immobilization on bone. In The Immobilized Patient, pp.  33–63. Springer.

  99. 99.

    Sun, L.-Y., D.-K. Hsieh, P.-C. Lin, H.-T. Chiu, and T.-W. Chiou 2010. Pulsed electromagnetic fields accelerate proliferation and osteogenic gene expression in human bone marrow mesenchymal stem cells during osteogenic differentiation. Bioelectromagnetics, 31(3):209–219.

  100. 100.

    Sun, L.-Y., D.-K. Hsieh, T.-C. Yu, H.-T. Chiu, S.-F. Lu, G.-H. Luo, T. K. Kuo, O. K. Lee, and T.-W. Chiou 2009. Effect of pulsed electromagnetic field on the proliferation and differentiation potential of human bone marrow mesenchymal stem cells. Bioelectromagnetics, 30(4):251–260.

  101. 101.

    Tsiridis, E., N. Upadhyay, and P. Giannoudis 2007. Molecular aspects of fracture healing: Which are the important molecules? Injury, 38(SUPPL. 1): S11–S25.

  102. 102.

    Vavva, M. G., K. N. Grivas, A. Carlier, D. Polyzos, L. Geris, H. Van Oosterwyck, and D. I. Fotiadis. A mechano-regulatory model for bone healing predictions under the influence of ultrasound. In Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. p. 921, 2015b

  103. 103.

    Vavva, M. G., K. Grivas, D. Polyzos, D. I. Fotiadis, A. Carlier, L. Geris, and H. Van Oosterwyck. A mathematical model for bone healing predictions under the ultrasound effect. In Ultrasonic Characterization of Bone (ESUCB), 2015 6th European Symposium on IEEE, 2015a, pp. 1–4.

  104. 104.

    Vecchia, P., R. Matthes, G. Ziegelberger, J. Lin, R. Saunders, and A. Swerdlow. Exposure to high frequency electromagnetic fields, biological effects and health consequences (100 khz-300 ghz). International Commission on Non-Ionizing Radiation Protection. 2009

  105. 105.

    Vetter, A., F. Witt, O. Sander, G. Duda, and R. Weinkamer 2012. The spatio-temporal arrangement of different tissues during bone healing as a result of simple mechanobiological rules. Biomech. Model. Mechanobiol. 11(1–2):147–160.

  106. 106.

    Walther, M., F. Mayer, W. Kafka, and N. Schütze 2007. Effects of weak, low-frequency pulsed electromagnetic fields (bemer type) on gene expression of human mesenchymal stem cells and chondrocytes: an in vitro study. Electromagn. Biol. Med. 26(3):179–190.

  107. 107.

    Watts, J. J., J. Abimanyi-Ochom, and K. M. Sanders 2013. Osteoporosis costing all australians: a new burden of disease analysis-2012 to 2022. Melbourne: Osteoporosis Australia

  108. 108.

    Wehner, T., L. Claes, F. Niemeyer, D. Nolte, and U. Simon 2010. Influence of the fixation stability on the healing time a numerical study of a patient-specific fracture healing process. Clin. Biomech. 25(6):606–612.

  109. 109.

    Wilson, C. J., M. A. Schütz, and D. R. Epari 2016. Computational simulation of bone fracture healing under inverse dynamisation. Biomech. Model. Mechanobiol. 16(1): 1–10.

  110. 110.

    Wraighte, P. J. and B. E. Scammell 2006. Principles of fracture healing. Surgery (Oxford), 24(6):198–207.

  111. 111.

    Zamanian, A. and C. Hardiman 2005. Electromagnetic radiation and human health: a review of sources and effects. High Freq. Electron. 4(3):16–26.

  112. 112.

    Zhang, Y., D. Khan, J. Delling, and E. Tobiasch 2012. Mechanisms underlying the osteo- and adipo-differentiation of human mesenchymal stem cells. Sci. World J. 2012:793823.

  113. 113.

    Zhou, J., L. G. Ming, B. F. Ge, J. Q. Wang, R. Q. Zhu, Z. Wei, H. P. Ma, C. J. Xian, and K. M. Chen 2011. Effects of 50Hz sinusoidal electromagnetic fields of different intensities on proliferation, differentiation and mineralization potentials of rat osteoblasts. Bone, 49(4):753–761.

Download references

Acknowledgments

This research is supported by RMIT University, through the SECE Top Up Scholarship and the RMIT Enabling Capability Platform Capability Development Fund.

Author information

Correspondence to C. Daish.

Additional information

Associate editor Michael R. Torry oversaw the review of this article.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Daish, C., Blanchard, R., Fox, K. et al. The Application of Pulsed Electromagnetic Fields (PEMFs) for Bone Fracture Repair: Past and Perspective Findings. Ann Biomed Eng 46, 525–542 (2018) doi:10.1007/s10439-018-1982-1

Download citation

Keywords

  • Tissue scale
  • Bone repair
  • Cell scale
  • Review
  • Computational modeling
  • Clinical devices