Skip to main content
Log in

Mechanic stress generated by a time-varying electromagnetic field on bone surface

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

Bone cells sense mechanical load, which is essential for bone growth and remodeling. In a fracture, this mechanism is compromised. Electromagnetic stimulation has been widely used to assist in bone healing, but the underlying mechanisms are largely unknown. A recent hypothesis suggests that electromagnetic stimulation could influence tissue biomechanics; however, a detailed quantitative understanding of EM-induced biomechanical changes in the bone is unavailable. This paper used a muscle/bone model to study the biomechanics of the bone under EM exposure. Due to the dielectric properties of the muscle/bone interface, a time-varying magnetic field can generate both compressing and shear stresses on the bone surface, where many mechanical sensing cells are available for cellular mechanotransduction. I calculated these stresses and found that the shear stress is significantly greater than the compressing stress. Detailed parametric analysis suggests that both the compressing and shear stresses are dependent on the geometrical and electrical properties of the muscle and the bone. These stresses are also functions of the orientation of the coil and the frequency of the magnetic field. It is speculated that the EM field could apply biomechanical influence to fractured bone, through the fine-tuning of the controllable field parameters.

Mechanic stress on bone surface in a time-varying magnetic field.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

B o :

Intensity of the time-varying magnetic field (Tesla)

ω :

Angular frequency of the time-varying magnetic field radians.

E A :

Intensity of the electric field induced by the time-varying magnetic field in the air (V/m)

E M :

Intensity of the electric field induced by the time-varying magnetic field in the muscle (V/m)

E B :

Intensity of the electric field induced by the time-varying magnetic field in the bone (V/m)

ρ AM :

Surface charge density on the air/muscle interface (C/m2)

ρ MB :

Surface charge density on the muscle/bone interface (C/m2)

P rAM :

Normal stress on the air/muscle interface (N/m2)

P rMB :

Normal stress on the muscle/bone interface (N/m2)

P θAM :

Sheer stress on the air/muscle interface (N/m2)

P θMB :

Sheer stress on the muscle/bone interface (N/m2)

R M :

Radius of the arm (m)

R B :

Radius of the bone (m)

References

  1. Yasuda I (1953) Fundamental aspects of fracture treatment. J Kyoto Med Soc 4:395–406

  2. Aaron RK, Ciombor DM, Simon BJ (2004) Treatment of nonunions with electric and electromagnetic fields. Clin Orthop Relat Res 419:21–29

    Article  Google Scholar 

  3. Akhouayri O, Lafage-Proust MH, Rattner A, Laroche N, Caillot-Augusseau A, Alexandre C, Vico L (1999) Effects of static or dynamic mechanical stresses on osteoblast phenotype expression in three-dimensional contractile collagen gels. J Cell Biochem 76(2):217–230

    Article  CAS  Google Scholar 

  4. Aslamazov LG, Varlamov AA (2001) The Wonder of Physics. World Scientific, Singapore

  5. Bae C, Butler PJ (2008) Finite element analysis of microelectrotension of cell membranes. Biomech Model Mechanobiol 7(5):379–386. https://doi.org/10.1007/s10237-007-0093-y

    Article  PubMed  Google Scholar 

  6. Bashir S, Perez JM, Horvath JC, Pascual-Leone A (2013) Differentiation of motor cortical representation of hand muscles by navigated mapping of optimal TMS current directions in healthy subjects. J Clin Neurophysiol 30(4):390–395. https://doi.org/10.1097/WNP.0b013e31829dda6b

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bryant G, Wolfe J (1987) Electromechanical stresses produced in the plasma membranes of suspended cells by applied electric fields. J Membr Biol 96(2):129–139

    Article  CAS  Google Scholar 

  8. Chakkalakal DA, Johnson MW, Harper RA, Katz JL (1980) Dielectric properties of fluid-saturated bone. IEEE Trans Biomed Eng 27(2):95–100

    Article  CAS  Google Scholar 

  9. Ciombor DM, Aaron RK (2005) The role of electrical stimulation in bone repair. Foot Ankle Clin 10(4):579–593, vii. https://doi.org/10.1016/j.fcl.2005.06.006

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Cowin SC (2002) Mechanosensation and fluid transport in living bone. J Musculoskelet Neuronal Interact 2(3):256–260

    CAS  PubMed  Google Scholar 

  12. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC (2004) The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115(2):255–266

    Article  Google Scholar 

  13. Di Palma F, Chamson A, Lafage-Proust MH, Jouffray P, Sabido O, Peyroche S, Vico L, Rattner A (2004) Physiological strains remodel extracellular matrix and cell-cell adhesion in osteoblastic cells cultured on alumina-coated titanium alloy. Biomaterials 25(13):2565–2575

    Article  Google Scholar 

  14. Engelhardt H, Sackmann E (1988) On the measurement of shear elastic moduli and viscosities of erythrocyte plasma membranes by transient deformation in high frequency electric fields. Biophys J 54(3):495–508. https://doi.org/10.1016/S0006-3495(88)82982-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gehl J (2003) Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand 177(4):437–447

    Article  CAS  Google Scholar 

  16. Goldenberg NM, Steinberg BE (2010) Surface charge: a key determinant of protein localization and function. Cancer Res 70(4):1277–1280. https://doi.org/10.1158/0008-5472.CAN-09-2905

    Article  CAS  PubMed  Google Scholar 

  17. Griffiths DJ (1999) Introduction to electrodynamics, 3rd edn. Prentice Hall, New Jersey

  18. Grumet AE, Wyatt JL Jr, Rizzo JF 3rd (2000) Multi-electrode stimulation and recording in the isolated retina. J Neurosci Methods 101(1):31–42

    Article  CAS  Google Scholar 

  19. Hannouche D, Petite H, Sedel L (2001) Current trends in the enhancement of fracture healing. J Bone Joint Surg 83(2):157–164

    Article  CAS  Google Scholar 

  20. Hu WF, Lai MC, Seol Y, Young YN (2016) Vesicle electrohydrodynamic simulations by coupling immersed boundary and immersed interface method. J Comput Phys 317:66–81

    Article  Google Scholar 

  21. Hyuga H, Kinosita K, Wakabayashi N (1991) Deformation of vesicles under the influence of strong electric-fields. Jpn J Appl Phys 1 30(5):1141–1148

    Article  Google Scholar 

  22. Hyuga H, Kinosita K, Wakabayashi N (1991) Deformation of vesicles under the influence of strong rlectric-fields .2. Jpn J Appl Phys 1 30(6):1333–1335

  23. Ingber D (1991) Integrins as mechanochemical transducers. Curr Opin Cell Biol 3(5):841–848

    Article  CAS  Google Scholar 

  24. Janssen AM, Oostendorp TF, Stegeman DF (2015) The coil orientation dependency of the electric field induced by TMS for M1 and other brain areas. J Neuroeng Rehabil 12:47. https://doi.org/10.1186/s12984-015-0036-2

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kaspar D, Seidl W, Neidlinger-Wilke C, Ignatius A, Claes L (2000) Dynamic cell stretching increases human osteoblast proliferation and CICP synthesis but decreases osteocalcin synthesis and alkaline phosphatase activity. J Biomech 33(1):45–51

    Article  CAS  Google Scholar 

  26. Kawata A, Mikuni-Takagaki Y (1998) Mechanotransduction in stretched osteocytes--temporal expression of immediate early and other genes. Biochem Biophys Res Commun 246(2):404–408. https://doi.org/10.1006/bbrc.1998.8632

    Article  CAS  PubMed  Google Scholar 

  27. Kotnik T, Miklavcic D (2000) Analytical description of transmembrane voltage induced by electric fields on spheroidal cells. Biophys J 79(2):670–679. https://doi.org/10.1016/S0006-3495(00)76325-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kotnik T, Miklavcic D (2000) Second-order model of membrane electric field induced by alternating external electric fields. IEEE Trans Biomed Eng 47(8):1074–1081. https://doi.org/10.1109/10.855935

    Article  CAS  PubMed  Google Scholar 

  29. Kotnik T, Bobanovic F, Miklavcic D (1997) Sensitivity of Transmembrane voltage induced by applied electric fields—a theoretical analysis. Bioelectrochem Bioenerg 43(2):285–291

    Article  CAS  Google Scholar 

  30. Kotnik T, Miklavcic D, Slivnik T (1998) Time course of transmembrane voltage induced by time-varying electric field - a method for theoretical analysis and its application. Bioelectrochem Bioenerg 45:3–16

    Article  CAS  Google Scholar 

  31. Krasteva VT, Papazov SP, Daskalov IK (2003) Peripheral nerve magnetic stimulation: influence of tissue non-homogeneity. Biomed Eng Online 2:19. https://doi.org/10.1186/1475-925X-2-19

    Article  PubMed  PubMed Central  Google Scholar 

  32. Laakso I, Hirata A, Ugawa Y (2014) Effects of coil orientation on the electric field induced by TMS over the hand motor area. Phys Med Biol 59(1):203–218. https://doi.org/10.1088/0031-9155/59/1/203

    Article  PubMed  Google Scholar 

  33. Lacroix D, Prendergast PJ (2002) A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J Biomech 35(9):1163–1171

    Article  CAS  Google Scholar 

  34. Lakes RS, JLK R (1977) Dielectric relaxation in cortical bone. J Appl Phys 48(2):808–811

    Article  Google Scholar 

  35. Larsson S, Kim W, Caja VL, Egger EL, Inoue N, Chao EY (2001) Effect of early axial dynamization on tibial bone healing: a study in dogs. Clin Orthop Relat Res 388:240–251

    Article  Google Scholar 

  36. Leblanc AD, Schneider VS, Evans HJ, Engelbretson DA, Krebs JM (1990) Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res Off J Am Soc Bone Miner Res 5(8):843–850. https://doi.org/10.1002/jbmr.5650050807

    Article  CAS  Google Scholar 

  37. LeBlanc A, Shackelford L, Schneider V (1998) Future human bone research in space. Bone 22(5 Suppl):113S–116S

    Article  CAS  Google Scholar 

  38. Lee DC, Grill WM (2005) Polarization of a spherical cell in a nonuniform extracellular electric field. Ann Biomed Eng 33(5):603–615

    Article  Google Scholar 

  39. Liedert A, Kaspar D, Augat P, Ignatius A, Claes L (2005) Mechanobiology of bone tissue and bone cells. In: Kamkin A, Kiseleva I (eds) Mechanosensitivity in cells and tissues. Academia, Moscow

  40. Lipman KM, Dodelson R, Hays RM (1966) The surface charge of isolated toad bladder epithelial cells. Mobility, effect of pH and divalent ions. J Gen Physiol 49(3):501–516

    Article  CAS  Google Scholar 

  41. Mansfield P, Harvey PR (1993) Limits to neural stimulation in echo-planar imaging. Magn Reson Med 29(6):746–758

    Article  CAS  Google Scholar 

  42. McConnell LC, Vlahovska PM, Miksis MJ (2015) Vesicle dynamics in uniform electric fields: squaring and breathing. Soft Matter 11(24):4840–4846. https://doi.org/10.1039/c5sm00585j

    Article  CAS  PubMed  Google Scholar 

  43. Mills KR, Boniface SJ, Schubert M (1992) Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol 85(1):17–21

    Article  CAS  Google Scholar 

  44. Neidlinger-Wilke C, Wilke HJ, Claes L (1994) Cyclic stretching of human osteoblasts affects proliferation and metabolism: a new experimental method and its application. J Orthop Res 12(1):70–78. https://doi.org/10.1002/jor.1100120109

    Article  CAS  PubMed  Google Scholar 

  45. Nelson S (2015) Dielectric properties of Agricultural materials and their applications. Elsevier, London

    Google Scholar 

  46. Pawar SD, Murugavel P, Lal DM (2009) Effect of relative humidity and sea level pressure on electrical conductivity of air over Indian Ocean. J Geophys Res 114(D02205):1–8

  47. Pilla AA (2002) Low-intensity electromagnetic and mechanical modulation of bone growth and repair: are they equivalent? J Orthop Sci 7(3):420–428. https://doi.org/10.1007/s007760200073

    Article  PubMed  Google Scholar 

  48. Polk C, Song JH (1990) Electric fields induced by low frequency magnetic fields in inhomogeneous biological structures that are surrounded by an electric insulator. Bioelectromagnetics 11(3):235–249

    Article  CAS  Google Scholar 

  49. Riske KA, Dimova R (2006) Electric pulses induce cylindrical deformations on giant vesicles in salt solutions. Biophys J 91(5):1778–1786. https://doi.org/10.1529/biophysj.106.081620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kamm R, Lammerding J, Mofrad M (2010) Cellular Nanomechanics. In: Bhushan B (ed) Springer handbook of nanotechnology. Springer, Verlag Berlin

    Chapter  Google Scholar 

  51. Ruohonen J, Panizza M, Nilsson J, Ravazzani P, Grandori F, Tognola G (1996) Transverse-field activation mechanism in magnetic stimulation of peripheral nerves. Electroencephalogr Clin Neurophysiol 101(2):167–174

    Article  CAS  Google Scholar 

  52. Salvador R, Silva S, Basser PJ, Miranda PC (2011) Determining which mechanisms lead to activation in the motor cortex: a modeling study of transcranial magnetic stimulation using realistic stimulus waveforms and sulcal geometry. Clin Neurophysiol 122(4):748–758. https://doi.org/10.1016/j.clinph.2010.09.022

    Article  CAS  PubMed  Google Scholar 

  53. Schultz LGHHL (1936) The dielectric constant of air at radiofrequencies. Physics 7:133–136. https://doi.org/10.1063/1.1745374

    Article  Google Scholar 

  54. Semrov D, Miklavcic D (1998) Calculation of the electrical parameters in electrochemotherapy of solid tumours in mice. Comput Biol Med 28(4):439–448

    Article  CAS  Google Scholar 

  55. Sniadecki NJ (2010) A tiny touch: activation of cell signaling pathways with magnetic nanoparticles. Endocrinology 151(2):451–457. https://doi.org/10.1210/en.2009-0932

    Article  CAS  PubMed  Google Scholar 

  56. Stratton J (1941) Electromagnetic theory. McGraw-Hill, New York

    Google Scholar 

  57. Toma CD, Ashkar S, Gray ML, Schaffer JL, Gerstenfeld LC (1997) Signal transduction of mechanical stimuli is dependent on microfilament integrity: identification of osteopontin as a mechanically induced gene in osteoblasts. J Bone Miner Res 12(10):1626–1636. https://doi.org/10.1359/jbmr.1997.12.10.1626

    Article  CAS  PubMed  Google Scholar 

  58. Veerapaneni S (2016) Integral equation methods for vesicle electrohydrodynamics in three dimensions. J Comput Phys 317:66–81

    Article  Google Scholar 

  59. Ye H, Curcuru A (2015) Vesicle biomechanics in a time-varying magnetic field. BMC Biophys 8(1):2. https://doi.org/10.1186/s13628-014-0016-0

    Article  PubMed  PubMed Central  Google Scholar 

  60. Ye H, Curcuru A (2016) Biomechanics of cell membrane under low-frequency time-varying magnetic field: a shell model. Med Biol Eng Comput 54(12):1871–1881. https://doi.org/10.1007/s11517-016-1478-9

    Article  PubMed  Google Scholar 

  61. Ye H, Steiger A (2015) Neuron matters: electric activation of neuronal tissue is dependent on the interaction between the neuron and the electric field. J Neuroeng Rehabil 12:65. https://doi.org/10.1186/s12984-015-0061-1

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ye H, Cotic M, Carlen PL (2007) Transmembrane potential induced in a spherical cell model under low-frequency magnetic stimulation. J Neural Eng 4(3):283–293. https://doi.org/10.1088/1741-2560/4/3/014

    Article  PubMed  Google Scholar 

  63. Ye H, Cotic M, Fehlings MG, Carlen PL (2011) Transmembrane potential generated by a magnetically induced transverse electric field in a cylindrical axonal model. Med Biol Eng Comput 49(1):107–119. https://doi.org/10.1007/s11517-010-0704-0

    Article  PubMed  Google Scholar 

  64. Yonemori K, Matsunaga S, Ishidou Y, Maeda S, Yoshida H (1996) Early effects of electrical stimulation on osteogenesis. Bone 19(2):173–180

    Article  CAS  Google Scholar 

  65. You L, Cowin SC, Schaffler MB, Weinbaum S (2001) A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34(11):1375–1386

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Austin Curcuru helped with the validation of the equations and Stephanie Kaszuba assisted with editing of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hui Ye.

Appendix - Determining unknown coefficients C n, D n in Eq. (3) using boundary conditions (A)-(D)

Appendix - Determining unknown coefficients C n, D n in Eq. (3) using boundary conditions (A)-(D)

Since V is bounded at r = 0 and r → ∞, from Eq. (3),

$$ {D}_A=0\kern0.5em {A}_B=0 $$

Therefore, expressions for the potential distribution in the extracellular media, the membrane, and in the cytoplasm are:

$$ {V}_A=\frac{A_A}{r}\sin \theta $$
(A-1)
$$ {V}_M=\left(\frac{A_M}{r}+{D}_Mr\right)\sin \theta $$
(A-2)
$$ {V}_B={D}_Br\sin \theta $$
(A-3)

Substitution of A0r (Eq. 9) and the \( \overset{\rightharpoonup }{r} \) components of ∇V in the three regions into (1) yielded the expressions of the normal components of the electric fields in the three regions:

$$ {E}_{Ar}=-\frac{j\omega {B}_0C}{2}\sin \theta +\frac{A_A}{r^2}\sin \theta $$
(A-4)
$$ {E}_{Mr}=-\frac{j\omega {B}_0C}{2}\sin \theta +\left(\frac{A_M}{r^2}-{D}_M\right)\sin \theta $$
(A-5)
$$ {E}_{Br}=-\frac{j\omega {B}_0C}{2}\sin \theta -{D}_B\sin \theta $$
(A-6)

Following boundary condition (A), V is continuous at the air/limb interface (r = RM) and muscle/bone interface (r = RB),

$$ \frac{A_A}{R_M}=\frac{A_M}{R_M}+{D}_M{R}_M $$
(A-7)
$$ \frac{A_M}{R_B}+{D}_M{R}_B={D}_B{R}_B $$
(A-8)

From the boundary condition (B), that the normal components of the current densities are continuous between two different media (Eqs. 1 and 2), we can obtain the following equations:

$$ {S}_A\left(-\frac{j\omega {B}_0C}{2}+\frac{A_A}{R_M^2}\right)={S}_M\left(-\frac{j\omega {B}_0C}{2}+\frac{A_M}{R_M^2}-{D}_M\right) $$
(A-9)
$$ {S}_M\left(-\frac{j\omega {B}_0C}{2}+\frac{A_M}{R_B^2}-{D}_M\right)={S}_B\left(-\frac{j\omega {B}_0C}{2}-{D}_B\right) $$
(A-10)

Equations (A-7) through (A-10) yielded the last four unknown coefficients:

$$ {\displaystyle \begin{array}{l}{A}_A=\frac{j\omega {B}_0C}{2}\frac{R_M^2\left[\left({S}_A+{S}_M\right)\left({S}_M-{S}_D\right){R}_B^2+\left({S}_A-{S}_M\right)\left({S}_M+{S}_B\right){R}_M^2\right]}{\left({S}_A-{S}_M\right)\left({S}_M-{S}_B\right){R}_B^2+\left({S}_A+{S}_M\right)\left({S}_M+{S}_B\right){R}_M^2}\\ {}{A}_M=\frac{j\omega {B}_0C}{2}\frac{2{R}_B^2{R}_M^2{S}_A\left({S}_M-{S}_B\right)}{\left({S}_A-{S}_M\right)\left({S}_M-{S}_B\right){R}_B^2+\left({S}_A+{S}_M\right)\left({S}_M+{S}_B\right){R}_M^2}\\ {}{D}_M=-\frac{j\omega {B}_0C}{2}\frac{\left({S}_A-{S}_M\right)\left[\left({S}_M-{S}_B\right){R}_B^2-\left({S}_M+{S}_B\right){R}_M^2\right]}{\left({S}_A-{S}_M\right)\left({S}_M-{S}_B\right){R}_B^2+\left({S}_A+{S}_M\right)\left({S}_M+{S}_B\right){R}_M^2}\\ {}{D}_B=-\frac{j\omega {B}_0C}{2}\frac{\left({S}_A-{S}_M\right)\left({S}_M-{S}_B\right){R}_B^2+\left[{S}_A\left({S}_B-3{S}_M\right)+{S}_M\left({S}_M+{S}_B\right)\right]{R}_M^2}{\left({S}_A-{S}_M\right)\left({S}_M-{S}_B\right){R}_B^2+\left({S}_A+{S}_M\right)\left({S}_M+{S}_B\right){R}_M^2}\end{array}} $$

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, H. Mechanic stress generated by a time-varying electromagnetic field on bone surface. Med Biol Eng Comput 56, 1793–1805 (2018). https://doi.org/10.1007/s11517-018-1814-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-018-1814-3

Keywords

Navigation