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Critical Reviews™ in Biomedical Engineering

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Bone Bioelectricity and Bone-Cell Response to Electrical Stimulation: A Review

Volumen 49, Edición 1, 2021, pp. 1-19
DOI: 10.1615/CritRevBiomedEng.2021035327
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Taylor deVet
McMaster School of Biomedical Engineering, McMaster University, Hamilton, Ontario, Canada
Akiv Jhirad
McMaster School of Biomedical Engineering, McMaster University, Hamilton, Ontario, Canada
Laura Pravato
McMaster School of Biomedical Engineering, McMaster University, Hamilton, Ontario, Canada
Gregory R. Wohl
McMaster School of Biomedical Engineering, McMaster University, Hamilton, Ontario, Canada; Department of Mechanical Engineering, McMaster University, Hamilton, Ontario, Canada

SINOPSIS

It is hypothesized that bone cells can sense mechanical force in the extracellular network via an electrical signal. This has led to the use of electrical stimulation (ES) to improve fracture repair and mitigate bone loss. Although overlap exists in bone maintenance and fracture healing mechanics, the processes involved in both are very different, resulting in dissimilar behaviors from the cells. Osteocytes are the most abundant cell type in bone tissue, and their basic structure and lineage are fairly well understood, but much debate is present regarding their behavior, with even less known about their behavior in electrical environments. A wide range of research exists on cell behavior under different types of ES, but it is difficult to draw conclusions due to the large variance in stimulation parameters, cell types, and origins (locations and species). By exploring behavior of multiple bone-cell types under different forms of ES, as well as mechanical stimulation through fluid flow, we can determine more about cell reactions to stimuli. In turn, a better understanding of cell response has the potential to improve and broaden therapeutic applications of ES for bone healing and bone loss mitigation, and enhance outcomes for osseointegration into implantable medical devices. These require greater understanding of the bone cellular environment from an electrical perspective as well as cellular responses to ES.

PALABRAS CLAVE: electrical stimulation, bone, fracture repair, pulsed electromagnetic field, capacitive coupling, in vitro, in vivo
REFERENCIAS

  1. Fukada E, Yasuda I. On the piezoelectric effect of bone. J Phys Soc Jpn. 1957 Oct 15;12(10):1158-62. .

  2. Bassett CAL. Electrical effects in bone. Sci Am. 1965;213(4):18-25. .

  3. Bassett CAL, Becker RO. Generation of electric potentials by bone in response to mechanical stress. Science. 1962 Sep 28;137(3535):1063-4. .

  4. Marino AA, Becker RO. Piezoelectric effect and growth control in bone. Nature. 1970 Oct;228(5270):473-4. .

  5. Brighton CT, Hozack WJ, Brager MD, Windsor RE, Pollack SR, Vreslovic EJ, Kotwick JE. Fracture healing in the rabbit fibula when subjected to various capacitively coupled electrical fields. J Orthop Res. 1985;3(3):331-40. .

  6. Kane WJ. Direct current electrical bone growth stimulation for spinal fusion. Spine (Phila, PA 1976). 1988;13(3):363-5. .

  7. Akhter S, Qureshi AR, Aleem I, El-Khechen HA, Khan S, Sikder O, Khan M, Bhandari M, Aleem I. Efficacy of electrical stimulation for spinal fusion: A systematic review and meta-analysis of randomized controlled trials. Sci Rep. 2020;10(1):1-12. .

  8. Fredericks DC, Nepola JV, Baker JT, Abbott J, Simon B. Effects of pulsed electromagnetic fields on bone healing in a rabbit tibial osteotomy model. J Orthop Trauma. 2000;14(2):93-100. .

  9. Saltzman C, Lightfoot A, Amendola A. PEMF as treatment for delayed healing of foot and ankle arthrodesis. Foot Ankle Int. 2004;25(11):771-3. .

  10. Chao PHG, Roy R, Mauck RL, Liu W, Valhmu WB, Hung CT. Chondrocyte translocation response to direct current electric fields. J Biomech Eng. 2000 Jun 1;122(3):261-7. .

  11. Huang CP, Chen XM, Chen ZQ. Osteocyte: The impresario in the electrical stimulation for bone fracture healing. Med Hypoth. 2008 Jan;70(2):287-90. .

  12. Isaacson BM, Bloebaum RD. Bone bioelectricity: What have we learned in the past 160 years? J Biomed Mater Res A. 2010;95:1270-9. .

  13. Duncan RL, Turner CH. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int. 1995 Nov;57(5):344-58. .

  14. Mycielska ME, Djamgoz MBA. Cellular mechanisms of direct-current electric field effects: Galvanotaxis and metastatic disease. J Cell Sci. 2004;117:1631-9. .

  15. Nabil Y, Abdalfattah S, Lotfy M. A clinical study on the effect of electric stimulation on segment transfer distraction osteogenesis for mandibular reconstruction. Egypt J Oral Maxillofac Surg. 2014;5(1):10-5. .

  16. Otter MW, McLeod KJ, Rubin CT. Effects of electromagnetic fields in experimental fracture repair. Clin Orthop Relat Res. 1998;355:S90-104. .

  17. Inoue N, Ohnishi I, Chen D, Deitz LW, Schwardt JD, Chao EYS. Effect of pulsed electromagnetic fields (PEMF) on late-phase osteotomy gap healing in a canine tibial model. J Orthop Res. 2002;20(5):1106-14. .

  18. Hassler CR, Rybicki EF, Diegle RB, Clark LC. Studies of enhanced bone healing via electrical stimuli. Comparative effectiveness of various parameters. Clin Orthop Relat Res. 1977;124:9-19. .

  19. Lirani-Galvao APR, Bergamaschi CT, Silva OL, Lazaretti-Castro M. Electrical field stimulation improves bone mineral density in ovariectomized rats. Brazilian J Med Biol Res. 2006 Nov;39(11):1501-5. .

  20. Sert C, Deniz M, Duz MZ, Aksen F, Kaya A. The preventive effect on bone loss of 50-Hz, 1-mT electromagnetic field in ovariectomized rats. J Bone Miner Metab. 2002;20(6):345-9. .

  21. Eser P, De Bruin ED, Telley I, Lechner HE, Knecht H, Stussi E. Effect of electrical stimulation-induced cycling on bone mineral density in spinal cordinjured patients. Eur J Clin Invest. 2003;33(5):412-9. .

  22. Eyres KS, Saleh M, Kanis JA. Effect of pulsed electro-magnetic fields on bone formation and bone loss during limb lengthening. Bone. 1996;18(6):505-9. .

  23. Chang K, Chang WHS. Pulsed electromagnetic fields prevent osteoporosis in an ovariectomized female rat model: A prostoglandin E2-associated process. Bioelectromagnetics. 2003;24(3):189-98. .

  24. Brighton CT, Katz MJ, Goll SR, Nichols CE, Pollack SR. Prevention and treatment of sciatic denervation disuse osteoporosis in the rat tibia with capacitively coupled electrical stimulation. Bone. 1985;6(2):87-97. .

  25. McLeod KJ, Rubin CT. The effect of low-frequency electrical fields on osteogenesis. J Bone Joint Surg Ser A. 1992;74(6):920-9. .

  26. Rubin CT, McLeod KJ, Lanyon LE. Prevention of oste-oporosis by pulsed electromagnetic fields. J Bone Joint Surg Ser A. 1989;71(3):411-7. .

  27. Boskey AL. Bone composition: Relationship to bone fragility and antiosteoporotic drug effects. Bonekey Rep. 2013;2:447. .

  28. Anderson JC, Eriksson C. Piezoelectric properties of dry and wet bone. Nature. 1970 Aug;227(5257):491-2. .

  29. Anderson JC, Eriksson C. Electrical properties of wet collagen. Nature. 1968;218:166-8. .

  30. Reinish GB, Nowick AS. Piezoelectric properties of bone as functions of moisture content. Nature. 1975 Feb;253(5493):626-7. .

  31. Konikoff JJ. Origin of the osseous bioelectric potentials: A review. Ann Clin Lab Sci. 1975;5:330-8. .

  32. Ahn AC, Grodzinsky AJ. Relevance of collagen piezo-electricity to "Wolff's Law": A critical review. Med Eng Phys. 2009;31(7):733-41. .

  33. Rubinacci A, Tessari L. A correlation analysis between bone formation rate and bioelectric potentials in rabbit tibia. Calcif Tissue Int. 1983 Dec;35(1):728-31. .

  34. Hung CT, Allen FD, Pollack SR, Brighton CT. What is the role of the convective current density in the real-time calcium response of cultured bone cells to fluid flow? J Biomech. 1996 Nov 1;29(11):1403-9. .

  35. Salzstein RA, Pollack SR, Mak AFT, Petrov N. Electro-mechanical potentials in cortical bone-I. A continuum ap-proach. J Biomech. 1987 Jan;20(3):261-70. .

  36. Singh S, Saha S. Electrical properties of bone. A review. Clin Orthop Relat Res. 1984;166:249-71. .

  37. Albrektsson T. Osteoinduction, osteoconduction and osseointegration. Eur Spine J. 2001;10(2):96. .

  38. Becker RO. The bioelectric factors in amphibianlimb regeneration. J Bone Joint Surg Am. 1961;43A(5): 643-56. .

  39. Rubinacci A, Villa I, Dondi Benelli F, Borgo E, Ferretti M, Palumbo C, Marotti G. Osteocyte-bone lining cell system at the origin of steady ionic current in damaged amphibian bone. Calcif Tissue Int. 1998 Oct 1;63(4):331-9. .

  40. Bassett CAL, Pawluk RJ, Pilla AA. Augmentation of bone repair by inductively coupled electromagnetic fields. Science. 1974;184(4136):575-7. .

  41. Anisimov AI. Action of direct current on bone tissue. Bull Exp Biol Med. 1974 Sep;78(3):1069-71. .

  42. Brighton CT, Hunt RM. Ultrastructure of electrically induced osteogenesis in the rabbit medullary canal. J Orthop Res. 1986;4(1):27-36. .

  43. Shandler HS, Weinstein S, Nathan LE. Facilitated healing of osseous lesions in the canine mandible after electrical stimulation. J Oral Surg. 1979 Nov;37(11):787-92. .

  44. Friedenberg ZB, Andrews ET, Smolenski BI, Pearl BW, Brighton CT. Bone reaction to varying amounts of direct current. Surg Gynecol Obstet. 1970 Nov;131(5):894-9. .

  45. Norton LA, Moore RR. Bone growth in organ culture modified by an electric field. J Dent Res. 1972 Sep 9;51(5):1492-9. .

  46. Brighton CT, Friedenberg ZB, Black J, Esterhai JL, Mitchell JEJ, Montique F. Electrically induced osteogenesis. Relationship between charge, current density, and the amount of bone formed: Introduction of a new cathode concept. Clin Orthop Relat Res. 1981;161:122-32. .

  47. Treharne RW, Brighton CT, Korostoff E, Pollack SR. An in vitro study of electrical osteogenesis using direct and pulsating currents. Clin Orthop Relat Res. 1979;145:300-6. .

  48. Noda M, Sato A. Appearance of osteoclasts and osteoblasts in electrically stimulated bones cultured on chorio-allantoic membranes. Clin Orthop Relat Res. 1985 Mar 1;193:288-98. .

  49. Cochran GVB. Experimental methods for stimulation of bone healing by means of electrical energy. Bull NY Acad Med J Urban Heal. 1972 Aug;48(7):899-911. .

  50. Bassett CAL, Pawluk RJ, Becker RO. Effects of electric currents on bone in vivo. Nature. 1964 Nov 1;204(4959):652-4. .

  51. Ferrier J, Ross SM, Kanehisa J, Aubin JE. Osteoclasts and osteoblasts migrate in opposite directions in response to a constant electrical field. J Cell Physiol. 1986;129(3):283-8. .

  52. Marino AA. Direct current and bone growth. In: Marino AA, editor. Modern bioelectricity. 1st ed. New York, NY: Marcel Dekker, Inc.; 1988. p. 657-709. .

  53. Jee WS, Yao W. Overview: Animal models of osteopenia and osteoporosis. J Musculoskel Neuron Interact. 2001;1(3):193-207. .

  54. Lirani-Galvao APR, Chavassieux P, Portero-Muzy N, Bergamaschi CT, Silva OL, Carvalho AB, Lazaretti-Castro M, Delmas PD. Low-intensity electrical stimulation counteracts the effects of ovariectomy on bone tissue of rats: Effects on bone microarchitecture, viability of osteocytes, and nitric oxide expression. Calcif Tissue Int. 2009 Jun 21;84(6):502-9. .

  55. Korenstein R, Somjen D, Fischler H, Binderman I. Capacitative pulsed electric stimulation of bone cells. Induction of cyclic-AMP changes and DNA synthesis. Mol Cell Res. 1984 Apr;803(4):302-7. .

  56. Lewis KJ, Frikha-Benayed D, Louie J, Stephen S, Spray DC, Thi MM, Seref-Ferlengez Z, Majeska RJ, Weinbaum S, Schaffler MB. Osteocyte calcium signals encode strain magnitude and loading frequency in vivo. Proc Natl Acad Sci. 2017 Oct 31;114(44):11775-80. .

  57. Hung CT, Allen FD, Pollack SR, Brighton CT. What is the role of the convective current density in the real-time calcium response of cultured bone cells to fluid flow? J Biomech. 1996;29(11):1403-9. .

  58. Aaron RK, Boyan BD, Ciombor DM, Schwartz Z, Simon BJ. Stimulation of growth factor synthesis by electric and electromagnetic fields. Clin Orthop Relat Res. 2004;419:30-7. .

  59. Lohmann CH, Schwartz Z, Liu Y, Guerkov H, Dean DD, Simon B, Boyan BD. Pulsed electromagnetic field stimulation of MG63 osteoblast-like cells affects differentiation and local factor production. J Orthop Res. 2000 Jul;18(4):637-46. .

  60. Stein GS, Lian JB. Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr Rev. 1993;14(4):424-42. .

  61. Meng S, Rouabhia M, Zhang Z. Electrical stimulation modulates osteoblast proliferation and bone protein production through heparin-bioactivated conductive scaffolds. Bioelectromagnetics. 2013 Apr 1;34(3):189-99. .

  62. Hopper RA, Verhalen JP, Tepper OT, Mehrara BJ, Detch R, Chang EI, Baharestani S, Simon BJ, Gurtner GC. Osteoblasts stimulated with pulsed electromagnetic fields increase HUVEC proliferation via a VEGF-A independent mechanism. Bioelectromagnetics. 2009 Apr;30(3):189-97. .

  63. Griffin M, Sebastian A, Colthurst J, Bayat A. Enhancement of differentiation and mineralisation of osteo blast-like cells by degenerate electrical waveform in an in vitro electrical stimulation model compared to capacitive coupling. PLoS One. 2013 Sep 11;8(9):e72978. .

  64. Hartig M, Joos U, Wiesmann HP. Capacitively coupled electric fields accelerate proliferation of osteoblast-like primary cells and increase bone extracellular matrix formation in vitro. Eur Biophys J. 2000;29(7):499-506. .

  65. Bodamyali T, Bhatt B, Hughes FJ, Winrow VR, Kanczler JM, Simon B, Abbott J, Blake DR, Stevens CR. Pulsed electromagnetic fields simultaneously induce osteogenesis and upregulate transcription of bone morphogenetic proteins 2 and 4 in rat osteoblasts in vitro. Biochem Biophys Res Commun. 1998;250(2):458-61. .

  66. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A. Bone morphogenetic proteins: A critical review. Cell Signal. 2011;23(4):609-20. .

  67. Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z, Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999;5(6):623-8. .

  68. Peng H, Wright V, Usas A, Gearhart B, Shen H-C, Cummins J, Huard J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 2002;110(6):751-9. .

  69. Yakar S, Rosen CJ, Beamer WG, Ackert-Bicknell CL, Wu Y, Liu J-L, Ooi GT, Setser J, Frystyk J, Boisclair YR, Le-Roith D. Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest. 2002;110(6):771-81. .

  70. Chang WHS, Chen LT, Sun JS, Lin FH. Effect of pulse-burst electromagnetic field stimulation on osteoblast cell activities. Bioelectromagnetics. 2004;25(6):457-65. .

  71. He Z, Selvamurugan N, Warshaw J, Partridge NC. Pulsed electromagnetic fields inhibit human osteoclast formation and gene expression via osteoblasts. Bone. 2018 Jan 1;106:194-203. .

  72. Jing D, Zhai M, Tong S, Xu F, Cai J, Shen G, Wu Y, Li X, Xie K, Liu J, Xu Q, Luo E. Pulsed electromagnetic fields promote osteogenesis and osseointegration of porous titanium implants in bone defect repair through a Wnt/p-catenin signaling-associated mechanism. Sci Rep. 2016 Aug 24;6(1):1-13. .

  73. Min Y, Liu Y, Poojari Y, Wu JC, Hildreth BE, Rosol TJ, Epstein AJ. Self-doped polyaniline-based interdigitated electrodes for electrical stimulation of osteoblast cell lines. Synth Met. 2014 Dec 1;198:308-13. .

  74. Esmail MY, Sun L, Yu L, Xu H, Shi L, Zhang J. Effects of PEMF and glucocorticoids on proliferation and differentiation of osteoblasts. Electromagn Biol Med. 2012 Dec 1;31(4):375-81. .

  75. Tian J, Shi R, Liu Z, Ouyang H, Yu M, Zhao C, Zou Y, Jiang D, Zhang J, Li Z. Self-powered implantable electrical stimulator for osteoblasts' proliferation and differentiation. Nano Energy. 2019 May 1;59:705-14. .

  76. Barnaba S, Papalia R, Ruzzini L, Sgambato A, Maffulli N, Denaro V. Effect of pulsed electromagnetic fields on human osteoblast cultures. Physiother Res Int. 2013 Jun 1;18(2):109-14. .

  77. Hiemer B, Krogull M, Bender T, Ziebart J, Krueger S, Bader R, Jonitz-Heincke A. Effect of electric stimulation on human chondrocytes and mesenchymal stem cells under normoxia and hypoxia. Mol Med Rep. 2018 Aug 1;18(2):2133-41. .

  78. Wang J, An Y, Li F, Li D, Jing D, Guo T, Luo E, Ma C. The effects of pulsed electromagnetic field on the functions of osteoblasts on implant surfaces with different topographies. Acta Biomater. 2014 Feb 1;10(2):975-85. .

  79. Matsunaga S. Histological and histochemical investigations of constant direct current stimulated intramedullary callus. J Japan Orthop Assoc. 1986 Dec;60(12):1293-303. .

  80. Brighton CT, Wang W, Seldes R, Zhang G, Pollack SR. Signal transduction in electrically stimulated bone cells. J Bone Joint Surg Ser A. 2001;83(10):1514-23. .

  81. Aarden EM, Nijweide PJ, Van Der Plas A, Alblas MJ, Mackie EJ, Horton MA, Helfrich MH. Adhesive properties of isolated chick osteocytes in vitro. Bone. 1996 Apr;18(4):305-13. .

  82. Palumbo C. A three-dimensional ultrastructural study of osteoid-osteocytes in the tibia of chick embryos. Cell Tissue Res. 1986 Oct;246(1):125-31. .

  83. Burger EH, Klein-Nulend J. Mechanotransduction in bone-Role of the lacunocanalicular network. FASEB J. 1999 May 1;13(9001):S101-12. .

  84. Knothe Tate ML, Adamson JR, Tami AE, Bauer TW. The osteocyte. Int J Biochem Cell Biol. 2004 Jan;36(1):1-8. .

  85. Lohmann CH, Schwartz Z, Liu Y, Li Z, Simon B, Sylvia VL, Dean DD, Bonewald LF, Donahue HJ, Boyan BD. Pulsed electromagnetic fields affect phenotype and connexin 43 protein expression in MLO-Y4 osteocyte-like cells and ROS 17/2.8 osteoblast-like cells. J Orthop Res. 2003 Mar;21(2):326-34. .

  86. Wang P, Tang C, Wu J, Yang Y, Yan Z, Liu X, Shao X, Zhai M, Gao J, Liang S, Luo E, Jing D. Pulsed electro-magnetic fields regulate osteocyte apoptosis, RANKL/OPG expression, and its control of osteoclastogenesis depending on the presence of primary cilia. J Cell Physiol. 2019;234(7):10588-601. .

  87. Tanaka K, Matsuo T, Ohta M, Sato T, Tezuka K, Nijweide PJ, Katoh Y, Hakeda Y, Kumegawa M. Time-lapse micro-cinematography of osteocytes. Miner Electrolyte Metab. 1995;21(1-3):189-92. .

  88. Kramer I, Halleux C, Keller H, Pegurri M, Gooi JH, Weber PB, Feng JQ, Bonewald LF, Kneissel M. Osteocyte Wnt/p-catenin signaling is required for normal bone homeostasis. Mol Cell Biol. 2010;30(12):3071-85. .

  89. Bronckers ALJJ, Goei W, Luo G, Karsenty G, D'Souza RN, Lyaruu DM, Burger EH. DNA fragmentation during bone formation in neonatal rodents assessed by transferase-mediated end labeling. J Bone Miner Res. 1996 Dec 3;11(9):1281-91. .

  90. Chang K, Chang WHS, Huang S, Huang S, Shih C. Pulsed electromagnetic fields stimulation affects osteoclast formation by modulation of osteoprotegerin, RANK ligand and macrophage colony-stimulating factor. J Orthop Res. 2005 Nov;23(6):1308-14. .

  91. Chang K, Chang WHS, Tsai MT, Shih C. Pulsed electro-magnetic fields accelerate apoptotic rate in osteoclasts. Conn Tissue Res. 2006 Jul;47(4):222-8. .

  92. Rubin J, McLeod KJ, Titus L, Nanes MS, Catherwood BD, Rubin CT. Formation of osteoclast-like cells is suppressed by low frequency, low intensity electric fields. J Orthop Res. 1996 Jan 1;14(1):7-15. .

  93. Dauben TJ, Ziebart J, Bender T, Zaatreh S, Kreikemeyer B, Bader R. A novel in vitro system for comparative analyses of bone cells and bacteria under electrical stimulation. Biomed Res Int. 2016;2016:5178640. .

  94. Brummer SB, Turner MJ. Electrical stimulation of the nervous system: The principle of safe charge injection with noble metal electrodes. Bioelectrochem Bioenerg. 1975;2(1):13-25. .

  95. Brummer SB, Robblee LS, Hambrecht FT. Criteria for selecting electrodes for electrical stimulation: Theortical and practical considerations. Ann NY Acad Sci. 1983 Jun 1;405(1):159-71. .

  96. Sandvik EL, McLeod BR, Parker AE, Stewart PS. Direct electric current treatment under physiologic saline conditions kills Staphylococcus epidermidis biofilms via electrolytic generation of hypochlorous acid. PLoS One. 2013 Feb 4;8(2):e55118. .

  97. Brighton CT, Adler S, Black J, Itada N, Friedenberg ZB. Cathodic oxygen consumption and electrically induced osteogenesis. Clin Orthop Relat Res. 1975;107:277-82. .

  98. Wang Q, Zhong S, Ouyang J, Jiang L, Zhang Z, Xie Y, Luo S. Osteogenesis of electrically stimulated bone cells mediated in part by calcium ions. Clin Orthop Relat Res. 1998;(348):259-68. .

  99. Merrill DR, Bikson M, Jefferys JGR. Electrical stimulation of excitable tissue: Design of efficacious and safe protocols. J Neurosci Meth. 2005;41:171-98. .

  100. Bodamyali T, Kanczler JM, Simon B, Blake DR, Stevens CR. Effect of faradic products on direct current-stimulated calvarial organ culture calcium levels. Biochem Biophys Res Commun. 1999 Nov 2;264(3):657-61. .

  101. Srirussamee K, Mobini S, Cassidy NJ, Cartmell SH. Direct electrical stimulation enhances osteogenesis by inducing BMP2 and SPP1 expressions from macrophages and preosteoblasts. Biotechnol Bioeng. 2019;116(12):3421-32. .

  102. Cho M, Hunt TK, Hussain MZ. Hydrogen peroxide stimulates macrophage vascular endothelial growth factor release. Am J Physiol Heart Circ Physiol. 2001 May;280(5):H2357-63. .

  103. Ehrensberger MT, Tobias ME, Nodzo SR, Hansen LA, Luke-Marshall NR, Cole RF, Wild LM, Campagnari AA. Cathodic voltage-controlled electrical stimulation of titanium implants as treatment for methicillin-resistant Staph- ylococcus aureus periprosthetic infections. Biomaterials. 2014 Feb 1;41:97-105. .

  104. Asadi MR, Torkaman G. Bacterial inhibition by electrical stimulation. Adv Wound Care. 2014 Feb;3(2):91-7. .

  105. Kaysinger KK, Ramp WK. Extracellular pH modulates the activity of cultured human osteoblasts. J Cell Bio-chem. 1998;68(1):83-9. .

  106. Bushinsky DA. Metabolic alkalosis decreases bone calcium efflux by suppressing osteoclasts and stimulating osteoblasts. Am J Physiol. 1996 Jul;271(1 Pt 2):F216-22. .

  107. Srirussamee K. Direct electrical stimulation approaches for bone repair and regeneration [dissertation]. Manchester, UK: University of Manchester; 2019. .

  108. Kumar A, Nune KC, Misra RDK. Electric field-mediated growth of osteoblasts: The significant impact of dynamic flow of medium. Biomater Sci. 2016 Jan 1;4(1):136-44. .

  109. Kumar A, Nune KC, Misra RDK. Understanding the response of pulsed electric field on osteoblast functions in three-dimensional mesh structures. J Biomater Appl. 2016 Oct 1;31(4):594-605. .

  110. Kodama HA, Amagai Y, Sude H, Kasai S, Yamamoto S. Establishment of a clonal osteogenic cell line from newborn mouse calvaria. Jpn J Oral Biol. 1981;23:899-901. .

  111. Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF. Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res. 1997;12:2014-23. .

  112. Kato Y, Boskey AL, Spevak L, Dallas M, Hori M, Bonewald LF. Establishment of an osteoid preosteocyte-like cell MLO-A5 that spontaneously mineralizes in culture. J Bone Miner Res. 2001;16(9):1622-33. .

  113. Rodan SB, Imai Y, Thiede MA, Wesolowski G, Thompson D, Bar-Shavit Z, Shull S, Mann K, Rodan GA. Characterization of a human osteosarcoma cell line (Saos-2) with osteoblastic properties. Cancer Res. 1987;47:4961-6. .

  114. Kalajzic I. A new osteocytic cell line, raising new questions and opportunities. J Bone Miner Res. 2019;34:977-8. .

  115. Divieti Pajevic P. New and old osteocytic cell lines and 3D models. Curr Osteop Rep. 2020;18:551-8. .

  116. Qadan MA, Piuzzi NS, Boehm C, Bova W, Moos M, Midura RJ, Hascall VC, Malcuit C, Muschler GF. Variation in primary and culture-expanded cells derived from connective tissue progenitors in human bone marrow space, bone trabecular surface and adipose tissue. Cyto-therapy. 2018 Mar 1;20(3):343-60. .

  117. Borsje MA, Ren Y, De Haan-Visser HW, Kuijerd R. Comparison of low-intensity pulsed ultrasound and pulsed electromagnetic field treatments on OPG and RANKL expression in human osteoblast-like cells. Angle Orthod. 2010 May 1;80(3):498-503. .

  118. He J, Zhang Y, Chen J, Zheng S, Huang H, Dong X. Effects of pulsed electromagnetic fields on the expression of NFATc1 and CAII in mouse osteoclast-like cells. Aging Clin Exp Res. 2015 Feb 1;27(1):13-9. .

  119. Bins-Ely LM, Cordero EB, Souza JCM, Teughels W, Benfatti CAM, Magini RS. In vivo electrical application on titanium implants stimulating bone formation. J Periodont Res. 2017 Jun 1;52(3):479-84. .

  120. Portan DV, Deligianni DD, Papanicolaou GC, Kostopoulos V, Psarras GC, Tyllianakis M. Combined optimized effect of a highly self-organized nanosubstrate and an electric field on osteoblast bone cells activity. Biomed Res Int. 2019;2019:7574635. .

  121. Ribeiro C, Moreira S, Correia V, Sencadas V, Rocha JG, Gama FM, Gomez Ribelles JL, Lanceros-Mendez S. Enhanced proliferation of pre-osteoblastic cells by dynamic piezoelectric stimulation. RSC Adv. 2012 Nov 28;2(30):11504-9. .

  122. Masureik C, Eriksson C. Preliminary clinical evaluation of the effect of small electrical currents on the healing ofjaw fractures. Clin Orthop Relat Res. 1977 May 1;4:84-91. .

  123. Brighton CT, Black J, Friedenberg ZB, Esterhai JL, Day LJ, Connolly JF. A multicenter study of the treatment of non-union with constant direct current. J Bone Joint Surg Ser A. 1981;63(1):2-13. .

  124. Mendonja JS, Neves LMG, Esquisatto MAM, Mendonja FAS, Santos GMT. Comparative study of the application of microcurrent and AsGa 904 nm laser radiation in the process of repair after calvaria bone excision in rats. Laser Phys. 2013;23(3):035605. .

  125. France JC, Norman TL, Santrock RD, McGrath B, Simon BJ. The efficacy of direct current stimulation for lumbar intertransverse process fusions in an animal model. Spine (Phila, PA 1976). 2001;26(9):1002-7. .

  126. Fredericks DC, Smucker J, Petersen EB, Bobst JA, Gan JC, Simon BJ, Glazer P. Effects of direct current electrical stimulation on gene expression of osteopromotive factors in a posterolateral spinal fusion model. Spine (Phila, PA 1976). 2007 Jan;32(2):174-81. .

  127. Friedenberg ZB, Zemsky LM, Pollis RP, Brighton CT. The response of non-traumatized bone to direct current. J Bone Joint Surg Ser A. 1974;56(5):1023-30. .

  128. Fonseca JH, Bagne L, Meneghetti DH, dos Santos GMT, Esquisatto MAM, de Andrade TAM, do Amaral MEC, Felonato M, Caetano GF, Santamaria M, Mendonja FAS. Electrical stimulation: Complementary therapy to improve the performance of grafts in bone defects? J Biomed Mater Res B Appl Biomater. 2019 May 28;107(4):924-32. .

  129. Zhang J, Li M, Kang ET, Neoh KG. Electrical stimulation of adipose-derived mesenchymal stem cells in conductive scaffolds and the roles of voltage-gated ion channels. Acta Biomater. 2016 Mar 1;32:46-56. .

  130. Eischen-Loges M, Oliveira KMC, Bhavsar MB, Barker JH, Leppik L. Pretreating mesenchymal stem cells with electrical stimulation causes sustained longlasting pro-osteogenic effects. Peer J. 2018 Jun 11;6:e4959. .

  131. Zhao Z, Watt C, Karystinou A, Roelofs AJ, McCaig CD, Gibson IR, De Bari C. Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur Cells Mater. 2011;22(0):344-58. .

  132. Wang Z, Clark CC, Brighton CT. Up-regulation of bone morphogenetic proteins in cultured murine bone cells with use of specific electric fields. J Bone Joint Surg Ser A. 2006;88(5):1053-65. .

  133. Qi Z, Xia P, Pan S, Zheng S, Fu C, Chang Y, Ma Y, Wang J, Yang X. Combined treatment with electrical stimulation and insulin-like growth factor-1 promotes bone regeneration in vitro. PLoS One. 2018 May 10;13(5):e0197006. .

  134. Zhang J, Neoh KG, Hu X, Kang ET, Wang W. Combined effects of direct current stimulation and immobilized BMP-2 for enhancement of osteogenesis. Biotechnol Bioeng. 2013 May 1;110(5):1466-75. .

  135. Tong J, Sun L, Zhu B, Fan Y, Ma X, Yu L, Zhang J. Pulsed electromagnetic fields promote the proliferation and differentiation of osteoblasts by reinforcing intracellular calcium transients. Bioelectromagnetics. 2017 Oct 1;38(7):541-9. .

  136. Gittens RA, Olivares-Navarrete R, Rettew R, Butera RJ, Alamgir FM, Boyan BD, Schwartz Z. Electrical polarization of titanium surfaces for the enhancement of osteoblast differentiation. Bioelectromagnetics. 2013 Dec 1;34(8):599-612. .

  137. Konstantinou E, Zagoriti Z, Pyriochou A, Poulas K. Microcurrent stimulation triggers MAPK signaling and TGF-pi release in fibroblast and osteoblast-like cell lines. Cells. 2020 Aug 19;9(9):1924. .

  138. Ercan B, Webster TJ. The effect of biphasic electrical stimulation on osteoblast function at anodized nano-tubular titanium surfaces. Biomaterials. 2010 May 1;31(13):3684-93. .

CITADO POR

  1. Zimmermann Ulf, Ebner Cathérine, Su Yukun, Bender Thomas, Bansod Yogesh Deepak, Mittelmeier Wolfram, Bader Rainer, van Rienen Ursula, Numerical Simulation of Electric Field Distribution around an Instrumented Total Hip Stem, Applied Sciences, 11, 15, 2021. Crossref

  2. Dong Shaojie, Zhang Yuwei, Mei Yukun, Zhang Yifei, Hao Yaqi, Liang Beilei, Dong Weijiang, Zou Rui, Niu Lin, Researching progress on bio-reactive electrogenic materials with electrophysiological activity for enhanced bone regeneration, Frontiers in Bioengineering and Biotechnology, 10, 2022. Crossref

  3. Sahm Franziska, Freiin Grote Vivica, Zimmermann Julius, Haack Fiete, Uhrmacher Adelinde M., van Rienen Ursula, Bader Rainer, Detsch Rainer, Jonitz-Heincke Anika, Long-term stimulation with alternating electric fields modulates the differentiation and mineralization of human pre-osteoblasts, Frontiers in Physiology, 13, 2022. Crossref

  4. Sahm Franziska, Jakovljevic Ana, Bader Rainer, Detsch Rainer, Jonitz-Heincke Anika, Is There an Influence of Electrically Stimulated Osteoblasts on the Induction of Osteoclastogenesis?, Applied Sciences, 12, 22, 2022. Crossref

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