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The Response of Osteoblasts and Bone to Sinusoidal Electromagnetic Fields: Insights from the Literature

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Abstract

Electromagnetic fields (EMFs) have been proposed as a tool to ameliorate bone formation and healing. Despite their promising results, however, they have failed to enter routine clinical protocols to treat bone conditions where higher bone mass has to be achieved. This is no doubt also due to a fundamental lack of knowledge and understanding on their effects and the optimal settings for attaining the desired therapeutic effects. This review analysed the available in vitro and in vivo studies that assessed the effects of sinusoidal EMFs (SEMFs) on bone and bone cells, comparing the results and investigating possible mechanisms of action by which SEMFs interact with tissues and cells. The effects of SEMFs on bone have not been as thoroughly investigated as pulsed EMFs; however, abundant evidence shows that SEMFs affect the proliferation and differentiation of osteoblastic cells, acting on multiple cellular mechanisms. SEMFs have also proven to increase bone mass in rodents under normal conditions and in osteoporotic animals.

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References

  1. Henkel J, Woodruff MA, Epari DR et al (2013) Bone regeneration based on tissue engineering conceptions—a 21st century perspective. Bone Res 1:216–248. https://doi.org/10.4248/BR201303002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Minisola S, Cipriani C, Occhiuto M, Pepe J (2017) New anabolic therapies for osteoporosis. Intern Emerg Med 12:915–921. https://doi.org/10.1007/s11739-017-1719-4

    Article  PubMed  Google Scholar 

  3. Jilka RL (2007) Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40:1434–1446. https://doi.org/10.1016/j.bone.2007.03.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bilezikian JP, Hattersley G, Fitzpatrick LA et al (2018) Abaloparatide-SC improves trabecular microarchitecture as assessed by trabecular bone score (TBS): a 24-week randomized clinical trial. Osteoporos Int 29:323–328. https://doi.org/10.1007/s00198-017-4304-9

    Article  CAS  PubMed  Google Scholar 

  5. Cosman F, Crittenden DB, Adachi JD et al (2016) Romosozumab treatment in postmenopausal women with osteoporosis. N Engl J Med 375:1532–1543. https://doi.org/10.1056/NEJMoa1607948

    Article  CAS  PubMed  Google Scholar 

  6. Delgado-Calle J, Sato AY, Bellido T (2017) Role and mechanism of action of sclerostin in bone. Bone 96:29–37. https://doi.org/10.1016/j.bone.2016.10.007

    Article  CAS  PubMed  Google Scholar 

  7. Mansour A, Mezour MA, Badran Z, Tamimi F (2017) *Extracellular Matrices for bone regeneration: a literature review. Tissue Eng Part A 23:1436–1451. https://doi.org/10.1089/ten.TEA.2017.0026

    Article  PubMed  Google Scholar 

  8. Juignet L, Charbonnier B, Dumas V et al (2017) Macrotopographic closure promotes tissue growth and osteogenesis in vitro. Acta Biomater 53:536–548. https://doi.org/10.1016/j.actbio.2017.02.037

    Article  CAS  PubMed  Google Scholar 

  9. Kumar A, Placone JK, Engler AJ (2017) Understanding the extracellular forces that determine cell fate and maintenance. Development 144:4261–4270. https://doi.org/10.1242/dev.158469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Draenert FG, Nonnenmacher A-L, Kämmerer PW et al (2013) BMP-2 and bFGF release and in vitro effect on human osteoblasts after adsorption to bone grafts and biomaterials. Clin Oral Implants Res 24:750–757. https://doi.org/10.1111/j.1600-0501.2012.02481.x

    Article  PubMed  Google Scholar 

  11. Iskander MF (2013) Electromagnetic fields and waves. Waveland Press, Long Grove

    Google Scholar 

  12. Olson P, Amit H (2006) Changes in earth’s dipole. Naturwissenschaften 93:519–542. https://doi.org/10.1007/s00114-006-0138-6

    Article  CAS  PubMed  Google Scholar 

  13. Roberts PH, Glatzmaier GA (2000) Geodynamo theory and simulations. Rev Mod Phys 72:1081–1123. https://doi.org/10.1103/RevModPhys.72.1081

    Article  Google Scholar 

  14. Birks LE, Struchen B, Eeftens M et al (2018) Spatial and temporal variability of personal environmental exposure to radio frequency electromagnetic fields in children in Europe. Environ Int 117:204–214. https://doi.org/10.1016/J.ENVINT.2018.04.026

    Article  PubMed  Google Scholar 

  15. Squillaro T, Galano G, De Rosa R et al (2018) Concise review: the effect of low-dose ionizing radiation on stem cell biology: a contribution to radiation risk. Stem Cells 36:1146–1153. https://doi.org/10.1002/stem.2836

    Article  PubMed  Google Scholar 

  16. Boice Jr J, Meinhold C, Alexakhin R (2005) Annals of the ICRP Published on behalf of the International Commission on Radiological Protection International Commission on Radiological Protection Members of the Main Commission of the ICRP

  17. Funk RHW, Monsees T, Özkucur N (2009) Electromagnetic effects—from cell biology to medicine. Prog Histochem Cytochem 43:177–264. https://doi.org/10.1016/J.PROGHI.2008.07.001

    Article  PubMed  Google Scholar 

  18. Wertheimer N, Leeper E (1979) Electrical wiring configurations and childhood cancer. Am J Epidemiol 109:273–284

    Article  CAS  PubMed  Google Scholar 

  19. Robinette CD, Silverman C, Jablon S (1980) Effects upon health of occupational exposure to microwave radiation (radar). Am J Epidemiol 112:39–53

    Article  CAS  PubMed  Google Scholar 

  20. Pall ML (2018) Wi-Fi is an important threat to human health. Environ Res 164:405–416. https://doi.org/10.1016/j.envres.2018.01.035

    Article  CAS  PubMed  Google Scholar 

  21. Hug K, Röösli M (2012) Therapeutic effects of whole-body devices applying pulsed electromagnetic fields (PEMF): a systematic literature review. Bioelectromagnetics 33:95–105. https://doi.org/10.1002/bem.20703

    Article  PubMed  Google Scholar 

  22. Markov MS (2007) Magnetic Field Therapy: a Review. Electromagn Biol Med 26:1–23. https://doi.org/10.1080/15368370600925342

    Article  PubMed  Google Scholar 

  23. Markov M (2015) XXIst century magnetotherapy. Electromagn Biol Med 34:190–196. https://doi.org/10.3109/15368378.2015.1077338

    Article  CAS  PubMed  Google Scholar 

  24. Pilla A (2015) Pulsed electromagnetic fields: from signaling to healing. Electromagnetic Fields in biology and medicine. CRC Press, Boca Raton, pp 29–48

    Chapter  Google Scholar 

  25. Wertheimer N, Leeper E (1982) Adult cancer related to electrical wires near the home. Int J Epidemiol 11:345–355

    Article  CAS  PubMed  Google Scholar 

  26. Bastuji-Garin S, Richardson S, Zittoun R (1990) Acute leukaemia in workers exposed to electromagnetic fields. Eur J Cancer Clin Oncol 26:1119–1120. https://doi.org/10.1016/0277-5379(90)90266-V

    Article  CAS  Google Scholar 

  27. Sermage-Faure C, Demoury C, Rudant J et al (2013) Childhood leukaemia close to high-voltage power lines—the Geocap study, 2002–2007. Br J Cancer 108:1899–1906. https://doi.org/10.1038/bjc.2013.128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kheifets L, Ahlbom A, Crespi CM et al (2010) Pooled analysis of recent studies on magnetic fields and childhood leukaemia. Br J Cancer 103:1128–1135. https://doi.org/10.1038/sj.bjc.6605838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Matanoski G, Breysse P, Elliott E (1991) Electromagnetic field exposure and male breast cancer. Lancet 337:737. https://doi.org/10.1016/0140-6736(91)90325-J

    Article  CAS  PubMed  Google Scholar 

  30. Cancer IA for R on (2002) Nonionizing radiation, Part 1: static and extremely low-frequency (ELF) electric and magnetic fields. IARC Monogr Eval Carcinog Risks Humans 80:391–395

    Google Scholar 

  31. Bua L, Tibaldi E, Falcioni L et al (2018) Results of lifespan exposure to continuous and intermittent extremely low frequency electromagnetic fields (ELFEMF) administered alone to Sprague Dawley rats. Environ Res 164:271–279. https://doi.org/10.1016/J.ENVRES.2018.02.036

    Article  CAS  PubMed  Google Scholar 

  32. Qi G, Zuo X, Zhou L et al (2015) Effects of extremely low-frequency electromagnetic fields (ELF-EMF) exposure on B6C3F1 mice. Environ Health Prev Med 20:287–293. https://doi.org/10.1007/s12199-015-0463-5

    Article  PubMed  PubMed Central  Google Scholar 

  33. Mccormick DL, Boorman GA, Findlay JC et al (1999) Chronic toxicity/oncogenicity evaluation of 60 Hz (power frequency) magnetic fields in B6C3F1 mice. Toxicol Pathol 27:279–285. https://doi.org/10.1177/019262339902700302

    Article  CAS  PubMed  Google Scholar 

  34. Mihai CT, Rotinberg P, Brinza F, Vochita G (2014) Extremely low-frequency electromagnetic fields cause DNA strand breaks in normal cells. J Environ Heal Sci Eng 12:15. https://doi.org/10.1186/2052-336X-12-15

    Article  CAS  Google Scholar 

  35. Ivancsits S, Diem E, Jahn O, Ruediger HW (2003) Intermittent extremely low frequency electromagnetic fields cause DNA damage in a dose-dependent way. Int Arch Occup Environ Health 76:431–436. https://doi.org/10.1007/s00420-003-0446-5

    Article  CAS  PubMed  Google Scholar 

  36. Pilla AA (2013) Nonthermal electromagnetic fields: from first messenger to therapeutic applications. Electromagn Biol Med 32:123–136. https://doi.org/10.3109/15368378.2013.776335

    Article  CAS  PubMed  Google Scholar 

  37. Galli C, Pedrazzi G, Mattioli-Belmonte M, Guizzardi S (2018) The use of pulsed electromagnetic fields to promote bone responses to biomaterials in vitro and in vivo. Int J Biomater 2018:1–15. https://doi.org/10.1155/2018/8935750

    Article  Google Scholar 

  38. Zhou J, Wang J-Q, Ge B-F et al (2014) Different electromagnetic field waveforms have different effects on proliferation, differentiation and mineralization of osteoblasts in vitro. Bioelectromagnetics 35:30–38. https://doi.org/10.1002/bem.21794

    Article  CAS  PubMed  Google Scholar 

  39. Simonet WS, Lacey DL, Dunstan CR et al (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89:309–319

    Article  CAS  PubMed  Google Scholar 

  40. Tsuda E, Goto M, Mochizuki S et al (1997) Isolation of a novel cytokine from human fibroblasts that specifically inhibits osteoclastogenesis. Biochem Biophys Res Commun 234:137–142. https://doi.org/10.1006/BBRC.1997.6603

    Article  CAS  PubMed  Google Scholar 

  41. Yasuda H, Shima N, Nakagawa N et al (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin͞ osteoclastogenesis-inhibitory factor and is identical to TRANCE͞RANKL. Cell Biol 95:3597–3602

    CAS  Google Scholar 

  42. Martin TJ, Sims NA (2015) RANKL/OPG; Critical role in bone physiology. Rev Endocr Metab Disord 16:131–139. https://doi.org/10.1007/s11154-014-9308-6

    Article  CAS  PubMed  Google Scholar 

  43. Raucci A, Bellosta P, Grassi R et al (2008) Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways. J Cell Physiol 215:442–451. https://doi.org/10.1002/jcp.21323

    Article  CAS  PubMed  Google Scholar 

  44. Yang Y, Tao C, Zhao D et al (2009) EMF acts on rat bone marrow mesenchymal stem cells to promote differentiation to osteoblasts and to inhibit differentiation to adipocytes. Bioelectromagnetics 31:277–285. https://doi.org/10.1002/bem.20560

    Article  CAS  Google Scholar 

  45. Song M-Y, Yu J-Z, Zhao D-M et al (2014) The time-dependent manner of sinusoidal electromagnetic fields on rat bone marrow mesenchymal stem cells proliferation, differentiation, and mineralization. Cell Biochem Biophys 69:47–54. https://doi.org/10.1007/s12013-013-9764-8

    Article  CAS  PubMed  Google Scholar 

  46. Song M, Zhao D, Wei S et al (2014) The effect of electromagnetic fields on the proliferation and the osteogenic or adipogenic differentiation of mesenchymal stem cells modulated by dexamethasone. Bioelectromagnetics 35:479–490. https://doi.org/10.1002/bem.21867

    Article  CAS  PubMed  Google Scholar 

  47. Yong Y, Ming ZD, Feng L et al (2016) Electromagnetic fields promote osteogenesis of rat mesenchymal stem cells through the PKA and ERK1/2 pathways. J Tissue Eng Regen Med 10:E537–E545. https://doi.org/10.1002/term.1864

    Article  CAS  PubMed  Google Scholar 

  48. Zhu BY, Yang ZD, Chen XR et al (2018) Exposure duration is a determinant of the effect of sinusoidal electromagnetic fields on peak bone mass of young rats. Calcif Tissue Int 103:1–12. https://doi.org/10.1007/s00223-018-0396-2

    Article  CAS  Google Scholar 

  49. Galli C, Pedrazzi G, Guizzardi S (2019) The cellular effects of Pulsed Electromagnetic Fields on osteoblasts: A review. Bioelectromagnetics. https://doi.org/10.1002/bem.22187

  50. Liu C, Yu J, Yang Y et al (2013) Effect of 1 mT sinusoidal electromagnetic fields on proliferation and osteogenic differentiation of rat bone marrow mesenchymal stromal cells. Bioelectromagnetics 34:453–464. https://doi.org/10.1002/bem.21791

    Article  CAS  PubMed  Google Scholar 

  51. Sul AR, Park S-N, Suh H (2006) Effects of sinusoidal electromagnetic field on structure and function of different kinds of cell lines. Yonsei Med J 47:852–861. https://doi.org/10.3349/ymj.2006.47.6.852

    Article  PubMed  PubMed Central  Google Scholar 

  52. Zhou J, Wang J, Ge B et al (2012) Effect of 3.6-mT sinusoidal electromagnetic fields on proliferation and differentiation of osteoblasts in vitro. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 34:353–358. https://doi.org/10.3881/j.issn.1000-503X.2012.04.008

    Article  CAS  PubMed  Google Scholar 

  53. Yu J, Wu H, Yang Y, et al (2014) Osteogenic differentiation of bone mesenchymal stem cells regulated by osteoblasts under EMF exposure in a co-culture system. J Huazhong Univ Sci Technol [Medical Sci 34:247–253 . https://doi.org/10.1007/s11596-014-1266-4

  54. Söhl G, Willecke K An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 10:173–80

  55. Sáez JC, Berthoud VM, Brañes MC et al (2003) Plasma Membrane Channels Formed by Connexins: their Regulation and Functions. Physiol Rev 83:1359–1400. https://doi.org/10.1152/physrev.00007.2003

    Article  PubMed  Google Scholar 

  56. Yamaguchi DT, Huang J, Ma D, Wang PKC (2002) Inhibition of gap junction intercellular communication by extremely low-frequency electromagnetic fields in osteoblast-like models is dependent on cell differentiation. J Cell Physiol 190:180–188. https://doi.org/10.1002/jcp.10047

    Article  CAS  PubMed  Google Scholar 

  57. Lohmann CH, Schwartz Z, Liu Y et al (2003) 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 21:326–334. https://doi.org/10.1016/S0736-0266(02)00137-7

    Article  CAS  PubMed  Google Scholar 

  58. Ledda M, D’Emilia E, Giuliani L et al (2015) Nonpulsed sinusoidal electromagnetic fields as a noninvasive strategy in bone repair: the effect on human mesenchymal stem cell osteogenic differentiation. Tissue Eng Part C Methods 21:207–217. https://doi.org/10.1089/ten.TEC.2014.0216

    Article  CAS  PubMed  Google Scholar 

  59. Zhong C, Zhang X, Xu Z, He R (2018) Effects of Low-Intensity Electromagnetic Fields on the Proliferation and Differentiation of Cultured Mouse Bone Marrow Stromal Cells. 92:1208–1219

    Google Scholar 

  60. Zhou J, Ming LG, Ge BF et al (2011) Effects of 50 Hz sinusoidal electromagnetic fields of different intensities on proliferation, differentiation and mineralization potentials of rat osteoblasts. Bone 49:753–761. https://doi.org/10.1016/j.bone.2011.06.026

    Article  CAS  PubMed  Google Scholar 

  61. Yan JL, Zhou J, Ma HP et al (2015) Pulsed electromagnetic fields promote osteoblast mineralization and maturation needing the existence of primary cilia. Mol Cell Endocrinol 404:132–140. https://doi.org/10.1016/j.mce.2015.01.031

    Article  CAS  PubMed  Google Scholar 

  62. Zhang X, Liu X, Pan L, Lee I (2010) Magnetic fields at extremely low-frequency (50 Hz, 0.8 mT) can induce the uptake of intracellular calcium levels in osteoblasts. Biochem Biophys Res Commun 396:662–666. https://doi.org/10.1016/j.bbrc.2010.04.154

    Article  CAS  PubMed  Google Scholar 

  63. Tong J, Sun L, Zhu B et al (2017) Pulsed electromagnetic fields promote the proliferation and differentiation of osteoblasts by reinforcing intracellular calcium transients. Bioelectromagnetics 38:541–549. https://doi.org/10.1002/bem.22076

    Article  CAS  PubMed  Google Scholar 

  64. Petecchia L, Sbrana F, Utzeri R et al (2015) Electro-magnetic field promotes osteogenic differentiation of BM-hMSCs through a selective action on Ca(2+)-related mechanisms. Sci Rep 5:13856. https://doi.org/10.1038/srep13856

    Article  PubMed  PubMed Central  Google Scholar 

  65. McLaughlin KA, Levin M (2018) Bioelectric signaling in regeneration: mechanisms of ionic controls of growth and form. Dev Biol 433:177–189. https://doi.org/10.1016/J.YDBIO.2017.08.032

    Article  CAS  PubMed  Google Scholar 

  66. Ross CL, Siriwardane M, Almeida-Porada G et al (2015) The effect of low-frequency electromagnetic field on human bone marrow stem/progenitor cell differentiation. Stem Cell Res 15:96–108. https://doi.org/10.1016/J.SCR.2015.04.009

    Article  PubMed  PubMed Central  Google Scholar 

  67. Panagopoulos DJ, Karabarbounis A, Margaritis LH (2002) Mechanism for action of electromagnetic fields on cells. Biochem Biophys Res Commun 298:95–102. https://doi.org/10.1016/S0006-291X(02)02393-8

    Article  CAS  PubMed  Google Scholar 

  68. Blackman CF, Benane SG, House DE, Joines WT (1985) Effects of ELF (1–120 Hz) and modulated (50 Hz) RF fields on the efflux of calcium ions from brain tissue in vitro. Bioelectromagnetics 6:1–11. https://doi.org/10.1002/bem.2250060102

    Article  CAS  PubMed  Google Scholar 

  69. McLeod BR, Liboff AR (1987) Cyclotron resonance in cell membranes: the theory of the mechanism. mechanistic approaches to interactions of electric and electromagnetic fields with living systems. Springer, US, pp 97–108

    Chapter  Google Scholar 

  70. Blackman CF, Blanchard JP, Benane SG, House DE (1994) Empirical test of an ion parametric resonance model for magnetic field interactions with PC-12 cells. Bioelectromagnetics 15:239–260

    Article  CAS  PubMed  Google Scholar 

  71. Lerchl A, Reiter RJ, Howes KA et al (1991) Evidence that extremely low frequency Ca(2+)-cyclotron resonance depresses pineal melatonin synthesis in vitro. Neurosci Lett 124:213–215

    Article  CAS  PubMed  Google Scholar 

  72. Bauréus Koch CLM, Sommarin M, Persson BRR et al (2003) Interaction between weak low frequency magnetic fields and cell membranes. Bioelectromagnetics 24:395–402. https://doi.org/10.1002/bem.10136

    Article  PubMed  Google Scholar 

  73. Blanchard JP, Blackman CF (1994) Clarification and application of an ion parametric resonance model for magnetic field interactions with biological systems. Bioelectromagnetics 15:217–238. https://doi.org/10.1002/bem.2250150306

    Article  CAS  PubMed  Google Scholar 

  74. Zorov DB, Juhaszova M, Sollott SJ (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 94:909–950. https://doi.org/10.1152/physrev.00026.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Genestra M (2007) Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Cell Signal 19:1807–1819. https://doi.org/10.1016/J.CELLSIG.2007.04.009

    Article  CAS  PubMed  Google Scholar 

  76. Cadenas S (2018) Mitochondrial uncoupling, ROS generation and cardioprotection. Biochim Biophys Acta - Bioenerg 1859:940–950. https://doi.org/10.1016/J.BBABIO.2018.05.019

    Article  CAS  PubMed  Google Scholar 

  77. Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462. https://doi.org/10.1016/j.cub.2014.03.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Cheng G, Zhai Y, Chen K et al (2011) Sinusoidal electromagnetic field stimulates rat osteoblast differentiation and maturation via activation of NO–cGMP–PKG pathway. Nitric Oxide 25:316–325. https://doi.org/10.1016/J.NIOX.2011.05.009

    Article  CAS  PubMed  Google Scholar 

  79. Patruno A, Amerio P, Pesce M et al (2010) Extremely low frequency electromagnetic fields modulate expression of inducible nitric oxide synthase, endothelial nitric oxide synthase and cyclooxygenase-2 in the human keratinocyte cell line HaCat: potential therapeutic effects in wound healing. Br J Dermatol 162:258–266. https://doi.org/10.1111/j.1365-2133.2009.09527.x

    Article  CAS  PubMed  Google Scholar 

  80. Schnoke M, Midura RJ (2007) Pulsed electromagnetic fields rapidly modulate intracellular signaling events in osteoblastic cells: comparison to parathyroid hormone and insulin. J Orthop Res 25:933–940. https://doi.org/10.1002/jor.20373

    Article  CAS  PubMed  Google Scholar 

  81. Lin HY, Lin YJ (2011) In vitro effects of low frequency electromagnetic fields on osteoblast proliferation and maturation in an inflammatory environment. Bioelectromagnetics 32:552–560. https://doi.org/10.1002/bem.20668

    Article  CAS  PubMed  Google Scholar 

  82. De Mattei M, Gagliano N, Moscheni C et al (2005) Changes in polyamines, c-myc and c-fos gene expression in osteoblast-like cells exposed to pulsed electromagnetic fields. Bioelectromagnetics 26:207–214. https://doi.org/10.1002/bem.20068

    Article  CAS  PubMed  Google Scholar 

  83. Ehnert S, Fentz A-K, Schreiner A et al (2017) Extremely low frequency pulsed electromagnetic fields cause antioxidative defense mechanisms in human osteoblasts via induction of ·O2− and H2O2. Sci Rep 7:14544. https://doi.org/10.1038/s41598-017-14983-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ehnert S, Falldorf K, Fentz AK et al (2015) Primary human osteoblasts with reduced alkaline phosphatase and matrix mineralization baseline capacity are responsive to extremely low frequency pulsed electromagnetic field exposure—clinical implication possible. Bone Reports 3:48–56. https://doi.org/10.1016/j.bonr.2015.08.002

    Article  PubMed  PubMed Central  Google Scholar 

  85. Diniz P, Soejima K, Ito G (2002) Nitric oxide mediates the effects of pulsed electromagnetic field stimulation on the osteoblast proliferation and differentiation. Nitric Oxide 7:18–23. https://doi.org/10.1016/S1089-8603(02)00004-6

    Article  CAS  PubMed  Google Scholar 

  86. Reale M, De Lutiis MA, Patruno A et al (2006) Modulation of MCP-1 and iNOS by 50-Hz sinusoidal electromagnetic field. Nitric Oxide 15:50–57. https://doi.org/10.1016/J.NIOX.2005.11.010

    Article  CAS  PubMed  Google Scholar 

  87. Chen G, Deng C, Li Y-P (2012) TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 8:272–288. https://doi.org/10.7150/ijbs.2929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Fathi E, Farahzadi R (2017) Enhancement of osteogenic differentiation of rat adipose tissue-derived mesenchymal stem cells by zinc sulphate under electromagnetic field via the PKA, ERK1/2 and Wnt/β-catenin signaling pathways. PLoS ONE 12:e0173877. https://doi.org/10.1371/journal.pone.0173877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Bodamyali T, Bhatt B, Hughes FJ et al (1998) 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 250:458–461. https://doi.org/10.1006/bbrc.1998.9243

    Article  CAS  PubMed  Google Scholar 

  90. Patterson TE, Sakai Y, Grabiner MD et al (2006) Exposure of murine cells to pulsed electromagnetic fields rapidly activates the mTOR signaling pathway. Bioelectromagnetics 27:535–544. https://doi.org/10.1002/bem.20244

    Article  CAS  PubMed  Google Scholar 

  91. Selvamurugan N, Kwok S, Vasilov A et al (2007) Effects of BMP-2 and pulsed electromagnetic field (PEMF) on rat primary osteoblastic cell proliferation and gene expression. J Orthop Res 25:1213–1220. https://doi.org/10.1002/jor.20409

    Article  CAS  PubMed  Google Scholar 

  92. Varani K, Vincenzi F, Ravani A et al (2017) Adenosine receptors as a biological pathway for the anti-inflammatory and beneficial effects of low frequency low energy pulsed electromagnetic fields. Mediators Inflamm 2017:2740963. https://doi.org/10.1155/2017/2740963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Vincenzi F, Targa M, Corciulo C et al (2013) Pulsed electromagnetic fields increased the anti-inflammatory effect of A2A and A3 adenosine receptors in human T/C-28a2 chondrocytes and hFOB 1.19 osteoblasts. PLoS ONE 8:1–10. https://doi.org/10.1371/journal.pone.0065561

    Article  CAS  Google Scholar 

  94. Xie YF, Shi WG, Zhou J et al (2016) Pulsed electromagnetic fields stimulate osteogenic differentiation and maturation of osteoblasts by upregulating the expression of BMPRII localized at the base of primary cilium. Bone 93:22–32. https://doi.org/10.1016/j.bone.2016.09.008

    Article  CAS  PubMed  Google Scholar 

  95. Benmerah A (2013) The ciliary pocket. Curr Opin Cell Biol 25:78–84. https://doi.org/10.1016/J.CEB.2012.10.011

    Article  CAS  PubMed  Google Scholar 

  96. Kaksonen M, Roux A (2018) Mechanisms of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 19:313–326. https://doi.org/10.1038/nrm.2017.132

    Article  CAS  PubMed  Google Scholar 

  97. Zhou J, Gao Y, Zhu B et al (2019) Sinusoidal electromagnetic fields increase peak bone mass in rats by activating Wnt10b/β=catenin in primary cilia of osteoblasts. J Bone Miner Res 1:1–10. https://doi.org/10.1002/jbmr.3704

    Article  CAS  Google Scholar 

  98. Satir P, Pedersen LB, Christensen ST (2010) The primary cilium at a glance. J Cell Sci 123:499–503. https://doi.org/10.1242/jcs.050377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Pedersen LB, Schrøder JM, Satir P, Christensen ST (2012) The ciliary cytoskeleton. Compr Physiol 2:779–803. https://doi.org/10.1002/cphy.c110043

    Article  PubMed  Google Scholar 

  100. Rattner JB, Sciore P, Ou Y et al (2010) Primary cilia in fibroblast-like type B synoviocytes lie within a cilium pit: a site of endocytosis. Histol Histopathol 25:865–875

    PubMed  Google Scholar 

  101. Molla-Herman A, Ghossoub R, Blisnick T et al (2010) The ciliary pocket: an endocytic membrane domain at the base of primary and motile cilia. J Cell Sci 123:1785–1795. https://doi.org/10.1242/jcs.059519

    Article  CAS  PubMed  Google Scholar 

  102. Schneider L, Clement CA, Teilmann SC et al (2005) PDGFRαα signaling is regulated through the primary cilium in fibroblasts. Curr Biol 15:1861–1866. https://doi.org/10.1016/j.cub.2005.09.012

    Article  CAS  PubMed  Google Scholar 

  103. Clement CA, Ajbro KD, Koefoed K et al (2013) TGF-β signaling is associated with endocytosis at the pocket region of the primary cilium. Cell Rep 3:1806–1814. https://doi.org/10.1016/j.celrep.2013.05.020

    Article  CAS  PubMed  Google Scholar 

  104. Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609–622. https://doi.org/10.1038/nrm2748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Travis AJ, Merdiushev T, Vargas LA et al (2001) Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and guinea pig spermatozoa. Dev Biol 240:599–610. https://doi.org/10.1006/DBIO.2001.0475

    Article  CAS  PubMed  Google Scholar 

  106. Treviño CL, Serrano CJ, Beltrán C et al (2001) Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm. FEBS Lett 509:119–125. https://doi.org/10.1016/S0014-5793(01)03134-9

    Article  PubMed  Google Scholar 

  107. Schrøder JM, Larsen J, Komarova Y et al (2011) EB1 and EB3 promote cilia biogenesis by several centrosome-related mechanisms. J Cell Sci 124:2539–2551. https://doi.org/10.1242/jcs.085852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Pedersen LB, Mogensen JB, Christensen ST (2016) Endocytic control of cellular signaling at the primary cilium. Trends Biochem Sci 41:784–797. https://doi.org/10.1016/j.tibs.2016.06.002

    Article  CAS  PubMed  Google Scholar 

  109. Wang P, Tang C, Wu J et al (2018) Pulsed electromagnetic fields regulate osteocyte apoptosis, RANKL/OPG expression, and its control of osteoclastogenesis depending on the presence of primary cilia. J Cell Physiol Early view. https://doi.org/10.1002/jcp.27734

    Article  Google Scholar 

  110. Taulman PD, Haycraft CJ, Balkovetz DF, Yoder BK (2001) Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell 12:589–599. https://doi.org/10.1091/mbc.12.3.589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Clevers H (2006) Wnt/β-catenin signaling in development and disease. Cell 127:469–480. https://doi.org/10.1016/J.CELL.2006.10.018

    Article  CAS  PubMed  Google Scholar 

  112. Komiya Y, Habas R (2008) Wnt signal transduction pathways. Organogenesis 4:68–75

    Article  PubMed  PubMed Central  Google Scholar 

  113. Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133:3231–3244. https://doi.org/10.1242/dev.02480

    Article  CAS  PubMed  Google Scholar 

  114. Glass DA, Bialek P, Ahn JD et al (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8:751–764. https://doi.org/10.1016/J.DEVCEL.2005.02.017

    Article  CAS  PubMed  Google Scholar 

  115. Mao J, Wang J, Liu B et al (2001) Low-density lipoprotein receptor-related protein-5 binds to axin and regulates the canonical wnt signaling pathway. Mol Cell 7:801–809. https://doi.org/10.1016/S1097-2765(01)00224-6

    Article  CAS  PubMed  Google Scholar 

  116. MacDonald BT, He X (2012) Frizzled and LRP5/6 receptors for Wnt/β-catenin signaling. Cold Spring Harb Perspect Biol 4:1–10. https://doi.org/10.1101/cshperspect.a007880

    Article  CAS  Google Scholar 

  117. Gao C, Chen Y-G (2010) Dishevelled: the hub of Wnt signaling. Cell Signal 22:717–727. https://doi.org/10.1016/j.cellsig.2009.11.021

    Article  CAS  PubMed  Google Scholar 

  118. MacDonald BT, Tamai K, He X (2009) Wnt/β-Catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9–26. https://doi.org/10.1016/J.DEVCEL.2009.06.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Lin CC, Lin RW, Chang CW et al (2015) Single-pulsed electromagnetic field therapy increases osteogenic differentiation through Wnt signaling pathway and sclerostin downregulation. Bioelectromagnetics 36:494–505. https://doi.org/10.1002/bem.21933

    Article  CAS  PubMed  Google Scholar 

  120. Zhai M, Jing D, Tong S et al (2016) Pulsed electromagnetic fields promote in vitro osteoblastogenesis through a Wnt/β-catenin signaling-associated mechanism. Bioelectromagnetics 37:152–162. https://doi.org/10.1002/bem.21961

    Article  CAS  PubMed  Google Scholar 

  121. Zhou Y, Wang P, Chen H et al (2015) Effect of pulsed electromagnetic fields on osteogenic differentiation and Wnt/β-catenin signaling pathway in rat bone marrow mesenchymal stem cells. Sichuan Da Xue Xue Bao Yi Xue Ban 46:347–353

    CAS  PubMed  Google Scholar 

  122. Tucker RW, Pardee A (1979) Centriole Ciliation Is Related to Quiescence and DNA Synthesis in 3T3 Cells. Cell 17:527–535

    Article  CAS  PubMed  Google Scholar 

  123. Kim S, Tsiokas L (2011) Cilia and cell cycle re-entry: more than a coincidence. Cell Cycle 10:2683–2690. https://doi.org/10.4161/cc.10.16.17009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Kim S, Lee K, Choi J-H et al (2015) Nek2 activation of Kif24 ensures cilium disassembly during the cell cycle. Nat Commun 6:8087. https://doi.org/10.1038/ncomms9087

    Article  CAS  PubMed  Google Scholar 

  125. Pala R, Alomari N, Nauli S (2017) Primary cilium-dependent signaling mechanisms. Int J Mol Sci 18:2272. https://doi.org/10.3390/ijms18112272

    Article  CAS  PubMed Central  Google Scholar 

  126. Delling M, Indzhykulian AA, Liu X et al (2016) Primary cilia are not calcium-responsive mechanosensors. Nature 531:656–660. https://doi.org/10.1038/nature17426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Simons M, Gloy J, Ganner A et al (2005) Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37:537–543. https://doi.org/10.1038/ng1552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Aaron RK, Ciombor DM, Keeping H et al (1999) Power frequency fields promote cell differentiation coincident with an increase in transforming growth factor-?1 expression. Bioelectromagnetics 20:453–458. https://doi.org/10.1002/(SICI)1521-186X(199910)20:7%3c453:AID-BEM7%3e3.0.CO;2-H

    Article  CAS  PubMed  Google Scholar 

  129. Zhou J, Ma X-N, Gao Y et al (2016) Sinusoidal electromagnetic fields promote bone formation and inhibit bone resorption in rat femoral tissues in vitro. Electromagn Biol Med 35:75–83. https://doi.org/10.3109/15368378.2014.971958

    Article  PubMed  Google Scholar 

  130. Zhou J, Wang J, Ma X et al (2013) Effect of sinusoidal electromagnetic fields on rats femur tissue cultivation in vitro. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 30:562–566

    PubMed  Google Scholar 

  131. Zhou Y, Li X, Li W, Qin R (2017) Effects of 1.8 mT sinusoidal electromagnetic fields of different frequencies on bone mineral density and bone histomorphometry of young rats. Sheng Wu Gong Cheng Xue Bao 33:1158–1167. https://doi.org/10.13345/j.cjb.170013

    Article  PubMed  Google Scholar 

  132. Gao Y-H, Zhen P, Zhou J et al (2014) Effect of sinusoidal electromagnetic field on bone mineral density and histomorphometry of rats at different time points. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 36:660–667. https://doi.org/10.3881/j.issn.1000-503X.2014.06.019

    Article  PubMed  Google Scholar 

  133. Gao Y, Cheng K, Ge B et al (2015) Effects of 50 Hz sinusoidal electromagnetic field with different intensities on rat peak bone mass. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 32(116–9):136

    Google Scholar 

  134. Gao Y, Li S, Zhou Y et al (2016) Screening the optimal time of sinusoidal alternating electromagnetic field for the bone biomechanical properties of rat. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 33:520–525

    PubMed  Google Scholar 

  135. Gao Y, Cheng K, Ge B-F et al (2014) Effect of different-intensity SEMFs on bone mineral density and histomorphometry in SD rats. Zhongguo Gu Shang 27:933–937

    PubMed  Google Scholar 

  136. Gao Y-H, Zhou Y-F, Li S-F et al (2017) Effect of 50 Hz 1.8 mT sinusoidal electromagnetic fields on bone mineral density in growing rats. Zhongguo Gu Shang 30:1113–1117. https://doi.org/10.3969/j.issn.1003-0034.2017.12.008

    Article  PubMed  Google Scholar 

  137. Zhou Y, Gao Y, Zhen P, Chen K (2016) Effects of 1.8 mT sinusoidal alternating electromagnetic fields of different frequencies on bone biomechanics of young rats. Zhejiang Da Xue Xue Bao Yi Xue Ban 45:561–567

    PubMed  Google Scholar 

  138. Khanduja KL, Syal N (2003) Sinusoidal electromagnetic field of SO Hz helps in retaining calcium in tibias of aged rats. Indian J Exp Biol 41:201–204

    CAS  PubMed  Google Scholar 

  139. Jing D, Cai J, Wu Y et al (2014) Pulsed electromagnetic fields partially preserve bone mass, microarchitecture, and strength by promoting bone formation in hindlimb-suspended rats. J Bone Miner Res 29:2250–2261. https://doi.org/10.1002/jbmr.2260

    Article  CAS  PubMed  Google Scholar 

  140. Li B, Bi J, Li W et al (2017) Effects of pulsed electromagnetic fields on histomorphometry and osteocalcin in disuse osteoporosis rats. Technol Heal Care 25:13–20. https://doi.org/10.3233/THC-171301

    Article  Google Scholar 

  141. Shen W-W, Zhao J-H (2009) Pulsed electromagnetic fields stimulation affects BMD and local factor production of rats with disuse osteoporosis. Bioelectromagnetics 31:113–119. https://doi.org/10.1002/bem.20535

    Article  CAS  Google Scholar 

  142. Jing D, Shen G, Huang J et al (2010) Circadian rhythm affects the preventive role of pulsed electromagnetic fields on ovariectomy-induced osteoporosis in rats. Bone 46:487–495. https://doi.org/10.1016/j.bone.2009.09.021

    Article  PubMed  Google Scholar 

  143. Jiang Y, Gou H, Wang S et al (2016) Effect of pulsed electromagnetic field on bone formation and lipid metabolism of glucocorticoid-induced osteoporosis rats through canonical Wnt signaling pathway. Evid Based Complement Altern Med 2016:4927035. https://doi.org/10.1155/2016/4927035

    Article  Google Scholar 

  144. Zhou J, He H, Yang L et al (2012) Effects of pulsed electromagnetic fields on bone mass and Wnt/β-catenin signaling pathway in ovariectomized rats. Arch Med Res 43:274–282. https://doi.org/10.1016/j.arcmed.2012.06.002

    Article  CAS  PubMed  Google Scholar 

  145. Zhou J, Chen S, Guo H et al (2013) Pulsed electromagnetic field stimulates osteoprotegerin and reduces RANKL expression in ovariectomized rats. Rheumatol Int 33:1135–1141. https://doi.org/10.1007/s00296-012-2499-9

    Article  CAS  PubMed  Google Scholar 

  146. Jing D, Li F, Jiang M et al (2013) Pulsed electromagnetic fields improve bone microstructure and strength in ovariectomized rats through a Wnt/Lrp5/β-catenin signaling-associated mechanism. PLoS ONE 8:e79377. https://doi.org/10.1371/journal.pone.0079377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Lei T, Liang Z, Li F et al (2018) Pulsed electromagnetic fields (PEMF) attenuate changes in vertebral bone mass, architecture and strength in ovariectomized mice. Bone 108:10–19. https://doi.org/10.1016/j.bone.2017.12.008

    Article  CAS  PubMed  Google Scholar 

  148. Chang K, Chang WH-S (2003) Pulsed electromagnetic fields prevent osteoporosis in an ovariectomized female rat model: a prostaglandin E2-associated process. Bioelectromagnetics 24:189–198. https://doi.org/10.1002/bem.10078

    Article  CAS  PubMed  Google Scholar 

  149. Bilotta TW, Zati A, Gnudi S et al (1994) Electromagnetic fields in the treatment of postmenopausal osteoporosis: an experimental study conducted by densitometric, dry ash weight and metabolic analysis of bone tissue. Chir Organi Mov 79:309–313

    CAS  PubMed  Google Scholar 

  150. Zati A, Gnudi S, Mongiorgi R et al (1993) Effects of pulsed magnetic fields in the therapy of osteoporosis induced by ovariectomy in the rat. Boll Soc Ital Biol Sper 69:469–475

    CAS  PubMed  Google Scholar 

  151. Androjna C, Fort B, Zborowski M, Midura RJ (2014) Pulsed electromagnetic field treatment enhances healing callus biomechanical properties in an animal model of osteoporotic fracture. Bioelectromagnetics 35:396–405. https://doi.org/10.1002/bem.21855

    Article  PubMed  Google Scholar 

  152. Yang X, He H, Zhou Y et al (2017) Pulsed electromagnetic field at different stages of knee osteoarthritis in rats induced by low-dose monosodium iodoacetate: effect on subchondral trabecular bone microarchitecture and cartilage degradation. Bioelectromagnetics 38:227–238. https://doi.org/10.1002/bem.22028

    Article  CAS  PubMed  Google Scholar 

  153. Li J, Zeng Z, Zhao Y et al (2017) Effects of low-intensity pulsed electromagnetic fields on bone microarchitecture, mechanical strength and bone turnover in type 2 diabetic db/db mice. Sci Rep 7:10834. https://doi.org/10.1038/s41598-017-11090-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Huegel J, Choi DS, Nuss CA et al (2018) Effects of pulsed electromagnetic field therapy at different frequencies and durations on rotator cuff tendon-to-bone healing in a rat model. J shoulder Elb Surg 27:553–560. https://doi.org/10.1016/j.jse.2017.09.024

    Article  Google Scholar 

  155. Taylor KF, Inoue N, Rafiee B et al (2006) Effect of pulsed electromagnetic fields on maturation of regenerate bone in a rabbit limb lengthening model. J Orthop Res 24:2–10. https://doi.org/10.1002/jor.20014

    Article  PubMed  Google Scholar 

  156. Midura RJ, Ibiwoye MO, Powell KA et al (2005) Pulsed electromagnetic field treatments enhance the healing of fibular osteotomies. J Orthop Res 23:1035–1046. https://doi.org/10.1016/j.orthres.2005.03.015

    Article  PubMed  Google Scholar 

  157. Landry PS, Sadasivan KK, Marino AA, Albright JA (1997) Electromagnetic fields can affect osteogenesis by increasing the rate of differentiation. Clin Orthop Relat Res 338:262–270

    Article  Google Scholar 

  158. Takano-Yamamoto T, Kawakami M, Sakuda M (1992) Effect of a pulsing electromagnetic field on demineralized bone-matrix-induced bone formation in a bony defect in the premaxilla of rats. J Dent Res 71:1920–1925. https://doi.org/10.1177/00220345920710121301

    Article  CAS  PubMed  Google Scholar 

  159. van der Jagt OP, van der Linden JC, Waarsing JH et al (2012) Systemic treatment with pulsed electromagnetic fields do not affect bone microarchitecture in osteoporotic rats. Int Orthop 36:1501–1506. https://doi.org/10.1007/s00264-011-1471-8

    Article  PubMed  PubMed Central  Google Scholar 

  160. Van Der Jagt OP, Van Der Linden JC, Waarsing JH et al (2014) Electromagnetic fields do not affect bone micro-architecture in osteoporotic rats. Bone Jt Res 33:230–235. https://doi.org/10.1302/2046-3758.37.2000221

    Article  Google Scholar 

  161. Sert C, Mustafa D, Zahir Düz M et al (2002) The preventive effect on bone loss of 50-Hz, 1-mT electromagnetic field in ovariectomized rats. J Bone Min Metab 20:345–349

    Article  CAS  Google Scholar 

  162. Akpolat V, Celik MS, Celik Y et al (2009) Treatment of osteoporosis by long-term magnetic field with extremely low frequency in rats. Gynecol Endocrinol 25:524–529. https://doi.org/10.1080/09513590902972075

    Article  CAS  PubMed  Google Scholar 

  163. Lei T, Li F, Liang Z et al (2017) Effects of four kinds of electromagnetic fields (EMF) with different frequency spectrum bands on ovariectomized osteoporosis in mice. Sci Rep 7:553. https://doi.org/10.1038/s41598-017-00668-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Liu C, Zhang Y, Fu T et al (2017) Effects of electromagnetic fields on bone loss in hyperthyroidism rat model. Bioelectromagnetics 38:137–150. https://doi.org/10.1002/bem.22022

    Article  CAS  PubMed  Google Scholar 

  165. Canè V, Botti P, Soana S (1993) Pulsed magnetic fields improve osteoblast activity during the repair of an experimental osseous defect. J Orthop Res 11:664–670. https://doi.org/10.1002/jor.1100110508

    Article  PubMed  Google Scholar 

  166. Canè V, Botti P, Farneti D, Soana S (1991) Electromagnetic stimulation of bone repair: a histomorphometric study. J Orthop Res 9:908–917. https://doi.org/10.1002/jor.1100090618

    Article  PubMed  Google Scholar 

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  1. Department of Medicine and Surgery, University of Parma, Parma, Italy

    C. Galli

  2. Department of Medicine and Surgery, Histology and Embryology Lab, University of Parma, Parma, Italy

    M. Colangelo & S. Guizzardi

  3. Department of Medicine and Surgery, Neuroscience Unit, University of Parma, Via Volturno 39, 43126, Parma, Italy

    G. Pedrazzi

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Galli, C., Colangelo, M., Pedrazzi, G. et al. The Response of Osteoblasts and Bone to Sinusoidal Electromagnetic Fields: Insights from the Literature. Calcif Tissue Int 105, 127–147 (2019). https://doi.org/10.1007/s00223-019-00554-9

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