77
Views
0
CrossRef citations to date
0
Altmetric
Research Article

The prevention effect of pulsed electromagnetic fields treatment on senile osteoporosis in vivo via improving the inflammatory bone microenvironment

, , , , , , , & ORCID Icon show all
Pages 46-60 | Received 13 Sep 2022, Accepted 26 Oct 2023, Published online: 08 Feb 2024

References

  • Androjna, C., C. S. Yee, C. R. White, E. I. Waldorff, J. T. Ryaby, M. Zborowski, T. Alliston, and R. J. Midura. 2021. A comparison of alendronate to varying magnitude PEMF in mitigating bone loss and altering bone remodeling in skeletally mature osteoporotic rats. Bone 143:115–761. doi:10.1016/j.bone.2020.115761.
  • Ansalone, C., J. Cole, S. Chilaka, F. Sunzini, S. Sood, J. Robertson, S. Siebert, I. B. McInnes, and C. S. Goodyear. 2021. TNF is a homoeostatic regulator of distinct epigenetically primed human osteoclast precursors. Ann. Rheum. Dis. 80 :748–57. doi:10.1136/annrheumdis-2020-219262.
  • An, Y., H. Zhang, C. Wang, F. Jiao, H. Xu, X. Wang, W. Luan, F. Ma, L. Ni, X. Tang, et al. 2019. Activation of ROS/MAPKs/NF-κB/NLRP3 and inhibition of efferocytosis in osteoclast-mediated diabetic osteoporosis. Faseb J. 33 :12515–27. doi:10.1007/978-981-13-3681-2_16.
  • Aspray, T. J., and T. R. Hill. 2019. Osteoporosis and the ageing skeleton. Subcell. Biochem. 91:453–76. doi:10.1007/978-981-13-3681-2_16.
  • Bassett, C. A., R. J. Pawluk, A. A. Pilla, and A. A. Pilla. 1974. Augmentation of bone repair by inductively coupled electromagnetic fields. Science 184 :575–77. doi:10.1126/science.184.4136.575.
  • Cai, J., X. Shao, Z. Yan, X. Liu, Y. Yang, E. Luo, and D. Jing. 2020. Differential skeletal response in adult and aged rats to independent and combinatorial stimulation with pulsed electromagnetic fields and mechanical vibration. Faseb J. 34 :3037–50. doi:10.1096/fj.201902779R.
  • Cao, J. J., T. J. Wronski, U. Iwaniec, L. Phleger, P. Kurimoto, B. Boudignon, and B. P. Halloran. 2005. Aging increases stromal/osteoblastic cell-induced osteoclastogenesis and alters the osteoclast precursor pool in the mouse. J. Bone Miner. Res. 20 :1659–68. doi:10.1359/JBMR.050503.
  • Chan, A. K., X. Tang, N. V. Mummaneni, D. Coughlin, E. Liebenberg, A. Ouyang, S. Dudli, M. Lauricella, N. Zhang, E. I. Waldorff, et al. 2019. Pulsed electromagnetic fields reduce acute inflammation in the injured rat-tail intervertebral disc. JOR. Spine 2 :e1069. doi:10.1002/jsp2.1069.
  • Charatcharoenwitthaya, N., S. Khosla, E. J. Atkinson, L. K. McCready, and B. L. Riggs. 2007. Effect of blockade of TNF-α and interleukin-1 action on bone resorption in early postmenopausal women. J. Bone Miner. Res. 22 :724–29. doi:10.1359/jbmr.070207.
  • Chen, W., P. Tang, S. Fan, X. Jiang, and M. Fortina. 2022. A novel inhibitor INF 39 promotes osteogenesis via blocking the NLRP3/IL-1β axis. Biomed. Res. Int. 2022:1–12. doi:10.1155/2022/7250578.
  • Crandall, C. J., S. Vasan, A. LaCroix, M. S. LeBoff, J. A. Cauley, J. A. Robbins, R. D. Jackson, and D. C. Bauer. 2018. Bone turnover markers are not associated with hip fracture risk: A case-control study in the Women’s health initiative. J. Bone. Mineral Res 33:1199–1208. doi:10.1002/jbmr.3471. 7
  • Fahimfar, N., S. Noorali, S. Yousefi, S. Gharibzadeh, G. Shafiee, N. Panahi, M. Sanjari, R. Heshmat, F. Sharifi, N. Mehrdad, et al. 2021. Prevalence of osteoporosis among the elderly population of Iran. Arch. Osteoporos 16 :16. doi:10.1007/s11657-020-00872-8.
  • Ferrucci, L., and E. Fabbri. 2018. Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty. Nat. Rev. Cardiol 15 :505–22. doi:10.1038/s41569-018-0064-2.
  • Franceschi, C., M. Bonafè, S. Valensin, F. Olivieri, M. De Luca, E. Ottaviani, and G. D. Benedictis. 2000. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 908 :244–54. doi:10.1111/j.1749-6632.2000.tb06651.x.
  • He, B., X. Yin, D. Hao, X. Zhang, Z. Zhang, K. Zhang, and X. B. Yang. 2020. Blockade of IL-6 alleviates bone loss induced by modeled microgravity in mice. Can. J. Physiol. Pharmacol. 98 :678–83. doi:10.1139/cjpp-2019-0632.
  • Hong, J. E., C. G. Lee, S. Hwang, J. Kim, M. Jo, D. H. Kang, S. H. Yoo, W. S. Kim, Y. Lee, and K. J. Rhee. 2023. Pulsed electromagnetic field (PEMF) treatment ameliorates murine model of collagen-induced arthritis. Int. J. Mol. Sci 24 :1137. doi:10.3390/ijms24021137.
  • Jiang, N., J. An, K. Yang, J. Liu, C. Guan, C. Ma, and X. Tang. 2021. NLRP3 inflammasome: A new target for prevention and control of osteoporosis? Front. Endocrinol. (Lausanne) 12:752–546. doi:10.3389/fendo.2021.752546.
  • Kanis, J. A., C. Cooper, R. Rizzoli, and J. Y. Reginster. 2019. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos. Int 30 :3–44. doi:10.1007/s00198-018-4704-5.
  • Kato, K., H. Tokuda, R. Matsushima-Nishiwaki, H. Natsume, A. Kondo, Y. Ito, O. Kozawa, and T. Otsuka. 2012. AMPK limits IL-1-stimulated IL-6 synthesis in osteoblasts: Involvement of IκB/NF-κB pathway. Cell. Signal. 24 :1706–12. doi:10.1016/j.cellsig.2012.04.012.
  • Kim, J. M., C. Lin, Z. Stavre, M. B. Greenblatt, and J. H. Shim. 2020. Osteoblast-osteoclast communication and bone homeostasis. Cells 9 :2073. doi:10.3390/cells9092073.
  • König, D., S. Oesser, S. Scharla, D. Zdzieblik, and A. Gollhofer. 2018. Specific collagen peptides improve bone mineral density and bone markers in postmenopausal women—A randomized controlled study. Nutrients 10 :97. doi:10.3390/nu10010097.
  • Kwan Tat, S., M. Padrines, S. Théoleyre, D. Heymann, and Y. Fortun. 2004. IL-6, RANKL, TNF-alpha/IL-1: Interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev. 15 :49–60. doi:10.1016/j.cytogfr.2003.10.005.
  • Lacativa, P. G., and M. L. Farias. 2010. Osteoporosis and inflammation. Arq. Bras. Endocrinol. Metabol. 54 :123–32. doi:10.1590/s0004-27302010000200007.
  • Lee, W. S., E. G. Lee, M. S. Sung, Y. J. Choi, and W. H. Yoo. 2018. Atorvastatin inhibits osteoclast differentiation by suppressing NF-κB and MAPK signaling during IL-1β-induced osteoclastogenesis. Korean J. Intern. Med. 33 :397–406. doi:10.3904/kjim.2015.244.
  • Liu, S., J. Du, D. Li, P. Yang, Y. Kou, C. Li, Q. Zhou, Y. Lu, T. Hasegawa, and M. Li. 2020. Oxidative stress induced pyroptosis leads to osteogenic dysfunction of MG63 cells. J. Mol. Histol. 51 :221–32. doi:10.1007/s10735-020-09874-9.
  • Liu, J., X. Huang, J. Zhou, L. Li, H. Xiao, M. Qu, and Z. Sun. 2022. Pulsed electromagnetic field alleviates synovitis and inhibits the NLRP3/Caspase-1/GSDMD signaling pathway in osteoarthritis rats. Electromagn. Biol. Med 41:101–07. doi:10.1080/15368378.2021.2021933.
  • Miyamoto, H., Y. Sawaji, T. Iwaki, T. Masaoka, E. Fukada, M. Date, and K. Yamamoto. 2019. Intermittent pulsed electromagnetic field stimulation activates the mTOR pathway and stimulates the proliferation of osteoblast-like cells. Bioelectromagnetics 40 :412–21. doi:10.1002/bem.22207.
  • Pena-Philippides, J. C., Y. Yang, O. Bragina, S. Hagberg, E. Nemoto, and T. Roitbak. 2014. Effect of pulsed electromagnetic field (PEMF) on infarct size and inflammation after cerebral ischemia in mice. Transl. Stroke. Res 5 :491–500. doi:10.1007/s12975-014-0334-1.
  • Peng, L., C. Fu, L. Wang, Q. Zhang, Z. Liang, C. He, and Q. Wei. 2021. The effect of pulsed electromagnetic fields on angiogenesis. Bioelectromagnetics 42 :250–58. doi:10.1002/bem.22330.
  • Pietschmann, P., D. Mechtcheriakova, A. Meshcheryakova, U. Föger-Samwald, and I. Ellinger. 2016. Immunology of osteoporosis: A mini-review. Gerontology 62 :128–37. doi:10.1159/000431091.
  • Qu, X., J. Mei, Z. Yu, Z. Zhai, H. Qiao, and K. Dai. 2018. Lenalidomide regulates osteocytes fate and related osteoclastogenesis via IL-1β/NF-κB/RANKL signaling. Biochem. Biophys. Res. Commun. 501 :547–55. doi:10.1016/j.bbrc.2018.05.035.
  • Ross, C. L., D. C. Ang, and G. Almeida-Porada. 2019. Targeting mesenchymal stromal cells/pericytes (MSCs) with pulsed electromagnetic field (PEMF) has the potential to treat rheumatoid arthritis. Front. Immunol 10:266. doi:10.3389/fimmu.2019.00266.
  • Ruscitti, P., P. Cipriani, F. Carubbi, V. Liakouli, F. Zazzeroni, P. Di Benedetto, O. Berardicurti, E. Alesse, and R. Giacomelli. 2015. The role of IL-1β in the bone loss during rheumatic diseases. Mediators Inflamm. 2015:1–10. doi:10.1155/2015/782382.
  • Salari, N., H. Ghasemi, L. Mohammadi, M. H. Behzadi, E. Rabieenia, S. Shohaimi, and M. Mohammadi. 2021. The global prevalence of osteoporosis in the world: A comprehensive systematic review and meta-analysis. J. Orthop. Surg. Res 16 :609. doi:10.1186/s13018-021-02772-0.
  • Samelson, E. J., K. E. Broe, H. Xu, L. Yang, S. Boyd, E. Biver, P. Szulc, J. Adachi, S. Amin, E. Atkinson, et al. 2019. Cortical and trabecular bone microarchitecture as an independent predictor of incident fracture risk in older women and men in the bone microarchitecture international consortium (BoMIC): A prospective study. Lancet. Diabetes. Endocrinol 7 :34–43. doi:10.1016/s2213-8587(18)30308-5.
  • Selvamurugan, N., S. Kwok, A. Vasilov, S. C. Jefcoat, and N. C. Partridge. 2007. Effects of BMP-2 and pulsed electromagnetic field (PEMF) on rat primary osteoblastic cell proliferation and gene expression. J. Orthop. Res. 25:1213–20. doi:10.1002/jor.20409.
  • Shao, X., Y. Yang, Z. Tan, Y. Ding, E. Luo, D. Jing, and J. Cai. 2021. Amelioration of bone fragility by pulsed electromagnetic fields in type 2 diabetic KK-Ay mice involving Wnt/β-catenin signaling. Am. J. Physiol. Endocrinol. Metab. 320:E951–e966. doi:10.1152/ajpendo.00655.2020.
  • Snouwaert, J. N., M. Nguyen, P. W. Repenning, R. Dye, E. W. Livingston, M. Kovarova, S. S. Moy, B. E. Brigman, T. A. Bateman, J. P. Ting, et al. 2016. An NLRP3 mutation causes arthropathy and osteoporosis in humanized mice. Cell. Rep 17 :3077–88. doi:10.1016/j.celrep.2016.11.052.
  • Srivastava, M., and C. Deal. 2002. Osteoporosis in elderly: Prevention and treatment. Clin. Geriatr. Med. 18:529–55. doi:10.1016/s0749-0690(02)00022-8.
  • Vincenzi, F., A. Ravani, S. Pasquini, S. Merighi, S. Gessi, S. Setti, R. Cadossi, P. A. Borea, and K. Varani. 2017. Pulsed electromagnetic field exposure reduces hypoxia and inflammation damage in neuron-like and microglial cells. J. Cell. Physiol. 232:1200–08. doi:10.1002/jcp.25606.
  • Vinhas, A., M. T. Rodrigues, A. I. Gonçalves, R. L. Reis, and M. E. Gomes. 2020. Pulsed electromagnetic field modulates tendon cells response in IL-1β-conditioned environment. J. Orthop. Res. 38:160–72. doi:10.1002/jor.24538.
  • Wang, L., K. Chen, X. Wan, F. Wang, Z. Guo, and Z. Mo. 2017. NLRP3 inflammasome activation in mesenchymal stem cells inhibits osteogenic differentiation and enhances adipogenic differentiation. Biochem. Biophys. Res. Commun. 484 :871–77. doi:10.1016/j.bbrc.2017.02.007.
  • Wu, Q., X. Zhou, D. Huang, Y. Ji, and F. Kang. 2017. IL-6 enhances osteocyte-mediated osteoclastogenesis by promoting JAK2 and RANKL activity in vitro. Cell. Physiol. Biochem. 41 :1360–69. doi:10.1159/000465455.
  • Xu, L., L. Zhang, Z. Wang, C. Li, S. Li, L. Li, Q. Fan, and L. Zheng. 2018. Melatonin suppresses estrogen deficiency-induced osteoporosis and promotes osteoblastogenesis by inactivating the NLRP3 inflammasome. Calcif. Tissue Int. 103 :400–10. doi:10.1007/s00223-018-0428-y.
  • Yang, X., H. Guo, W. Ye, L. Yang, and C. He. (2021). Pulsed Electromagnetic Field Attenuates Osteoarthritis Progression in a Murine Destabilization-Induced Model through Inhibition of TNF-α and IL-6 Signaling. CARTILAGE 13 (2_suppl):1665S–1675S. dio:10.1177/19476035211049561.
  • Yang, F., Y. Jia, Q. Sun, C. Zheng, C. Liu, W. Wang, L. Du, S. Kang, X. Niu, and J. Li. 2020. Raloxifene improves TNF‑α‑induced osteogenic differentiation inhibition of bone marrow mesenchymal stem cells and alleviates osteoporosis. Exp. Ther. Med 20 :309–14. doi:10.3892/etm.2020.8689.
  • Yang, X., C. Qu, J. Jia, and Y. Zhan. 2019. NLRP3 inflammasome inhibitor glyburide expedites diabetic-induced impaired fracture healing. Immunobiology 224 :786–91. doi:10.1016/j.imbio.2019.08.008.
  • Yao, Z., S. J. Getting, and I. C. Locke. 2021. Regulation of TNF-Induced osteoclast differentiation. Cells 11 :132. doi:10.3390/cells11010132.
  • Yuan, J., F. Xin, and W. Jiang. 2018. Underlying signaling pathways and therapeutic applications of pulsed electromagnetic fields in bone repair. Cell. Physiol. Biochem. 46 :1581–94. doi:10.1159/000489206.
  • Zang, Y., J. H. Song, S. H. Oh, J. W. Kim, M. N. Lee, X. Piao, J. W. Wang, O. S. Kim, T. S. Kim, S. H. Kim, et al. 2020. Targeting NLRP3 inflammasome reduces age-related experimental alveolar bone loss. J. Dent. Res. 99 :1287–95. doi:10.1177/0022034520933533.
  • Zhang, J., H. Xu, Z. Han, P. Chen, Q. Yu, Y. Lei, Z. Li, M. Zhao, and J. Tian. 2017. Pulsed electromagnetic field inhibits RANKL-dependent osteoclastic differentiation in RAW264.7 cells through the Ca(2+)-calcineurin-NFATc1 signaling pathway. Biochem. Biophys. Res. Commun. 482 :289–95. doi:10.1016/j.bbrc.2016.11.056.
  • Zhong, W., Z. Rao, J. Rao, G. Han, P. Wang, T. Jiang, X. Pan, S. Zhou, H. Zhou, and X. Wang. 2020. Aging aggravated liver ischemia and reperfusion injury by promoting STING-mediated NLRP3 activation in macrophages. Aging. Cell 19 :e13186. doi:10.1111/acel.13186.
  • Zhou, J., S. Chen, H. Guo, L. Xia, H. Liu, Y. Qin, and C. He. 2013. Pulsed electromagnetic field stimulates osteoprotegerin and reduces RANKL expression in ovariectomized rats. Rheumatol. Int. 33 :1135–41. doi:10.1007/s00296-012-2499-9.
  • Zhou, J., Y. Liao, H. Xie, Y. Liao, Y. Zeng, N. Li, G. Sun, Q. Wu, and G. Zhou. 2017. Effects of combined treatment with ibandronate and pulsed electromagnetic field on ovariectomy-induced osteoporosis in rats. Bioelectromagnetics 38 :31–40. doi:10.1002/bem.22012.
  • Zhou, J., J. Wang, M. Qu, X. Huang, L. Yin, Y. Liao, F. Huang, P. Ning, P. Zhong, and Y. Zeng. 2022. Effect of the pulsed electromagnetic field treatment in a rat model of senile osteoporosis in vivo. Bioelectromagnetics 43 :438–47. doi:10.1002/bem.22423.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.