Positive effects of pulsed electromagnetic fields on behavior, immune function, and oxidative and inflammatory state in old mice

References

• Alvarado, C., P. Álvarez, L. Jiménez, and M. De la Fuente. 2006. Oxidative stress in leukocytes from young prematurely aging mice is reversed by supplementation with biscuits rich in antioxidants. Dev. Comp. Immunol. 30 :1168‐1180. doi:10.1016/j.dci.2006.03.004.
   PubMed Web of Science ®Google Scholar
• Arranz, L., J. H. Camaño, J. M. Lord, and M. De la Fuente. 2010. Preserved immune functions and controlled leukocyte oxidative stress in naturally long-lived mice: Possible role of nuclear factor kappa B. J. Gerontol. A Biol. Sci. Med. Sci. 65 :941–50. doi:10.1093/gerona/glq101.
   PubMed Web of Science ®Google Scholar
• Baeza, I., N. M. De Castro, L. Giménez-Llort, and M. De la Fuente. 2010. Ovariectomy, a model of menopause in rodents, causes premature aging of the nervous and immune systems. J. Neuroimmunol. 219 :90–99. doi:10.1016/j.jneuroim.2009.12.008.
   PubMed Web of Science ®Google Scholar
• Brenes, G. A., B. W. Penninx, P. H. Judd, E. Rockwell, D. D. Sewell, and J. L. Wetherell. 2008. Anxiety, depression and disability across the lifespan. Aging Ment. Health 12 :158–63. doi:10.1080/13607860601124115.
   PubMed Web of Science ®Google Scholar
• Chang, C. W., and I. N. Lien. 1994. Tardy effect of neurogenic muscular atrophy by magnetic stimulation. Am. J. Phys. Med. Rehabil. 73 :275–79. doi:10.1097/00002060-199407000-00009.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Chappell, M., and S. Payne. 2020. Cellular homeostasis and membrane potential. in: Physiology for engineers. Biosys. Biorobot 24 :22–34. Springer, Cham.
   Google Scholar
• Choleris, E., A. W. Thomas, M. Kavaliers, and F. S. Prato. 2001. A detailed ethological analysis of the mouse open field test: Effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci. Biobehav. R. 25 :235–60. doi:10.1016/S0149-7634(01)00011-2.
   PubMed Web of Science ®Google Scholar
• Cossarizza, A., S. Angioni, F. Petraglia, A. R. Genazzani, D. Monti, M. Capri, F. Bersani, R. Cadossi, and C. Franceschi. 1993. Exposure to low frequency pulsed electromagnetic fields increases interleukin-1 and interleukin-6 production by human peripheral blood mononuclear cells. Exp. Cell Res. 204 :385–87. doi:10.1006/excr.1993.1048.
   PubMed Web of Science ®Google Scholar
• De la Fuente, M. 2018a. Bio-psycho-social bridge: The psychoneuroimmune system in successful aging. In The Cambridge handbook of successful aging (Cambridge handbooks in psychology, ed. R. Fernández-Ballesteros, A. Benetos, and J. Robine, 265–80. Cambridge: Cambridge University Press. doi:10.1017/9781316677018.017.
   Google Scholar
• De la Fuente, M. 2018b. Oxidation and inflammation in the immune and nervous systems, a link between aging and anxiety. In Handbook of Immunosenescence 1–31. Springer International Publishing. doi:10.1007/978-3-319-64597-1_115-1.
   Google Scholar
• De la Fuente, M., M. Miñano, V. Manuel Victor, M. Del Rio, M. D. Ferrández, A. Díez, and J. Miquel. 1998. Relation between exploratory activity and immune function in aged mice: A preliminary study. Mech. Ageing Dev. 102 :263–77. doi:10.1016/S0047-6374(98)00015-3.
   PubMed Web of Science ®Google Scholar
• De la Fuente, M., and J. Miquel. 2009. An update of the oxidation-inflammation theory of aging: The involvement of the immune system in oxi‐inflamm‐aging. Curr. Pharm. Des. 15 :3003–26. doi:10.2174/138161209789058110.
   PubMed Web of Science ®Google Scholar
• Del-Cerro, E., M. Lambea, J. Félix, N. Salazar, M. Gueimonde, and M. De la Fuente. 2021. Daily ingestion of Akkermansia mucciniphila for one month promotes healthy aging and increases lifespan in old female mice. Biogerontology 23 :35–52. doi:10.1007/s10522-021-09943-w.
   PubMed Web of Science ®Google Scholar
• Della Bella, E., M. Tschon, C. Stagni, D. Dallari, and M. Fini. 2015. Biophysical stimulation for nonunions. J. Biol. Regul. Homeost. Agents 29 :25–38.
   PubMedGoogle Scholar
• Díaz-Del Cerro, E., N. Ceprián, J. Félix, and M. De la Fuente. 2022. A short social interaction between adult and old mice improves the homeostatic systems and increases healthy longevity. Exp. Gerontol. 158:111653. doi:10.1016/j.exger.2021.111653.
   PubMed Web of Science ®Google Scholar
• Elabd, C., W. Cousin, P. Upadhyayula, R. Y. Chen, M. S. Chooljian, J. Li, S. Kung, K. P. Jiang, and I. M. Conboy. 2014. Oxytocin is an age-specific circulating hormone that is necessary for muscle maintenance and regeneration. Nat. Commun. 5 :4082. doi:10.1038/ncomms5082.
   PubMed Web of Science ®Google Scholar
• Franceschi, C., M. Bonafè, S. Valensin, F. Olivieri, M. De Luca, E. Ottaviani, and G. De 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.
   PubMed Web of Science ®Google Scholar
• Franco, R., C. D. Bortner, and J. A. Cidlowski. 2006. Potential roles of electrogenic ion transport and plasma membrane depolarization in apoptosis. J. Membr. Biol. 209 :43–58. doi:10.1007/s00232-005-0837-5.
   PubMed Web of Science ®Google Scholar
• Garrido, A., J. Cruces, N. Ceprián, C. Hernández-Sánchez, and M. De la Fuente. 2018. Premature aging in behavior and immune functions in tyrosine hydroxylase haploinsufficient female mice. A longitudinal study. Brain Behav. Immun. 69:440–55. doi:10.1016/j.bbi.2018.01.003.
   PubMed Web of Science ®Google Scholar
• Gems, D., and L. Partridge. 2008. Stress-response hormesis and aging: “that which does not kill us makes us stronger”. Cell Metab. 7 :200–03. doi:10.1016/j.cmet.2008.01.001.
   PubMed Web of Science ®Google Scholar
• Gessi, S., S. Merighi, D. Fazzi, A. Stefanelli, K. Varani, and P. A. Borea. 2011. Adenosine receptor targeting in health and disease. Expert. Opin. Investing. Drugs 20 :1591–609. doi:10.1517/13543784.2011.627853.
   PubMed Web of Science ®Google Scholar
• Giusti, A., M. Giovale, M. Ponte, F. Fratoni, U. Tortorolo, A. De Vincentiis, and G. Bianchi. 2013. Short-term effect of low-intensity, pulsed, electromagnetic fields on gait characteristics in older adults with low bone mineral density: A pilot randomized-controlled trial. Geriatr. Gerontol. Int. 13 :393–97. doi:10.1111/j.1447-0594.2012.00915.x.
   PubMed Web of Science ®Google Scholar
• Gómez-Ochoa, I., P. Gómez-Ochoa, F. Gómez-Casal, E. Cativiela, and L. Larrad-Mur. 2011. Pulsed electromagnetic fields decrease proinflammatory cytokine secretion (IL-1β and TNF- α) on human fibroblast-like cell culture. Rheumatol. Int. 31 :1283–89. doi:10.1007/s00296-010-1488-0.
   PubMed Web of Science ®Google Scholar
• Gordon, G. A. 2007. Designed electromagnetic pulsed therapy: Clinical applications. J. Cell. Physiol. 212 :579–82. doi:10.1002/jcp.21025.
   PubMed Web of Science ®Google Scholar
• Gözen, H., C. Demirel, M. Akan, and M. Tarakçioğlu. 2017. Pulsed electromagnetic field effects on antioxidant levels of diabetic rats. Eur. J. Ther 23 :152–58. doi:10.5152/EurJTher.2017.139.
   Google Scholar
• Guayerbas, N., M. Puerto, V. M. Víctor, J. Miquel, and M. De la Fuente. 2002. Leukocyte function and life span in a murine model of premature immunosenescence. Exp. Gerontol. 37 :249–56. doi:10.1016/S0531-5565(01)00190-5.
   PubMed Web of Science ®Google Scholar
• Hattapoğlu, E., İ. Batmaz, B. Dilek, M. Karakoç, S. Em, and R. Çevik. 2019. Efficiency of pulsed electromagnetic fields on pain, disability, anxiety, depression, and quality of life in patients with cervical disc herniation: A randomized controlled study. Turk. J. Med. Sci. 49 :1095–101. doi:10.3906/sag-1901-65.
   PubMed Web of Science ®Google Scholar
• Hissin, P. J., and R. Hilf. 1976. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74 :214–26. doi:10.1016/0003-2697(76)90326-2.
   PubMed Web of Science ®Google Scholar
• Hunsche, C., I. Martínez de Toda, O. Hernandez, B. Jiménez, L. E. Díaz, A. Marcos, and M. De la Fuente. 2020. The supplementations with 2-hydroxyoleic acid and n-3 polyunsaturated fatty acids revert oxidative stress in various organs of diet-induced obese mice. Free Radic. Res. 54 :455–66. doi:10.1080/10715762.2020.1800004.
   PubMed Web of Science ®Google Scholar
• Hyun-Soo, B., J. In-Ho, and L. Sang-Deok. 2014. Effects of pulsed electromagnetic field on blood components, antioxidant enzymes and free radicals in hyperlipidemia rats. Digit. Converg. Res 12 :349–56. doi:10.14400/JDC.2014.12.7.349.
   Google Scholar
• Iannitti, T., G. Fistetto, A. Esposito, V. Rottigni, and B. Palmieri. 2013. Pulsed electromagnetic field therapy for management of osteoarthritis-related pain, stiffness and physical function: Clinical experience in the elderly. Clin. Interv. Aging 8:1289–93. doi:10.2147/CIA.S35926.
   PubMed Web of Science ®Google Scholar
• Kassed, C. A., and M. Herkenham. 2004. NF-kappaB p50-deficient mice show reduced anxiety-like behaviors in tests of exploratory drive and anxiety. Behav. Brain Res. 154 :577–84. doi:10.1016/j.bbr.2004.03.026.
   PubMed Web of Science ®Google Scholar
• Klöting, I., C. Nitschke, and J. van den Brandt. 2003. Impact of genetic profiles on experimental studies: Outbred versus wild rats. Toxicol. App. l Pharmacol. 189 :68–71. doi:10.1016/S0041-008X(03)00099-1.
   PubMed Web of Science ®Google Scholar
• Lawrence, R. A., and R. F. Burk. 1976. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 71 :952–58. doi:10.1016/0006-291X(76)90747-6.
   PubMed Web of Science ®Google Scholar
• Li, Z., F. Yao, L. Cheng, W. Cheng, L. Qi, S. Yu, L. Zhang, X. Zha, and J. Jing. 2019. Low frequency pulsed electromagnetic field promotes the recovery of neurological function after spinal cord injury in rats. J. Orthop. Res. 37 :449–56. doi:10.1002/jor.24172.
   PubMed Web of Science ®Google Scholar
• Ma, F., W. Li, X. Li, B. H. Tran, R. Suguro, R. Guan, C. Hou, H. Wang, A. Zhang, Y. Zhu, et al. 2016. Novel protective effects of pulsed electromagnetic field ischemia/reperfusion injury rats. Biosci. Rep. 36 :e00420. doi:10.1042/BSR20160082.
   PubMed Web of Science ®Google Scholar
• Markov, M. S., and A. P. Colbert. 2001. Magnetic and electromagnetic field therapy. J. Back Musculoskelet. Rehabil. 15 :17–29. doi:10.3233/BMR-2000-15103.
   Web of Science ®Google Scholar
• Martínez de Toda, I., N. Ceprián, E. Díaz-Del Cerro, and M. De la Fuente. 2021. The role of immune cells in Oxi-inflamm-aging. Cells 10 :2974. doi:10.3390/cells10112974.
   PubMed Web of Science ®Google Scholar
• Martínez de Toda, I., I. Maté, C. Vida, J. Cruces, and M. De la Fuente. 2016. Immune function parameters as markers of biological age and predictors of longevity. Aging (Albany NY) 8 :3110–19. doi:10.18632/aging.101116.
   PubMedGoogle Scholar
• Martínez de Toda, I., C. Vida, A. Garrido, and M. De la Fuente. 2020. Redox parameters as markers of the rate of aging and predictors of life span. J. Gerontol. A Biol. Sci. Med. Sci. 75 :613–20. doi:10.1093/gerona/glz033.
   PubMed Web of Science ®Google Scholar
• Massey, V., and C. H. Williams. 1965. On the reaction mechanism of yeast glutathione reductase. J. Biol. Chem. 240 :4470–80. doi:10.1016/S0021-9258(18)97085-7.
   PubMed Web of Science ®Google Scholar
• Ouyang, J., B. Zhang, L. Kuang, P. Yang, X. Du, H. Qi, N. Su, M. Jin, J. Yang, Y. Xie, et al. 2020. Pulsed electromagnetic field inhibits synovitis via enhancing the efferocytosis of macrophages. Biomed. Res. Int. 2020:4307385. doi:10.1155/2020/4307385.
   PubMed Web of Science ®Google Scholar
• Rao, V., S. Kaja, and S. Gentile (2016). Ion channels in aging and aging-related diseases, molecular mechanisms of the aging process and rejuvenation. Available at: https://www.intechopen.com/books/molecular-mechanismsof-the-aging-process-and-rejuvenation/ion-channels-in-aging-and-agingrelated-diseases
   Google Scholar
• Rosado, M. M., M. Simkó, M. O. Mattsson, and C. Pioli. 2018. Immune-modulating perspectives for low frequency electromagnetic fields in innate immunity. Front. Public Health 6:85. doi:10.3389/fpubh.2018.00085.
   PubMed Web of Science ®Google Scholar
• Salchner, P., G. Lubec, and N. Singewald. 2004. Decreased social interaction in aged rats may not reflect changes in anxiety-related behaviour. Behav. Brain Res. 151 :1–8. doi:10.1016/j.bbr.2003.07.002.
   PubMed Web of Science ®Google Scholar
• Santini, M. T., G. Rainaldi, and P. L. Indovina. 2009. Cellular effects of extremely low frequency (ELF) electromagnetic fields. Int. J. Radiat. Biol. 85 :294–313. doi:10.1080/09553000902781097.
   PubMed Web of Science ®Google Scholar
• Streit, A., B. C. Watson, J. D. Granata, T. M. Philbin, H. N. Lin, J. P. O’Connor, and S. Lin. 2016. Effect on clinical outcome and growth factor synthesis with adjunctive use of pulsed electromagnetic fields for fifth metatarsal nonunion fracture: A double-blind randomized study. Foot Ankle Int. 37 :919–23. doi:10.1177/1071100716652621.
   PubMed Web of Science ®Google Scholar
• Tappa, B., H. Amao, A. Ogasa, and K. W. Takahashi. 1989. Changes in the estrous cycle and number of ovulated and fertilized ova in aging female IVCS mice. Jikken. Dobutsu. 38 :115–19. doi:10.1538/expanim1978.38.2_115.
   PubMed Web of Science ®Google Scholar
• Téglás, T., G. Dörnyei, K. Bretz, and C. Nyakas. 2018. Whole-body pulsed EMF stimulation improves cognitive and psychomotor activity in senescent rats. Behav. Brain Res. 349:163–68. doi:10.1016/j.bbr.2018.04.036.
   PubMed Web of Science ®Google Scholar
• Vadalà, M., J. C. Morales-Medina, A. Vallelunga, B. Palmieri, C. Laurino, and T. Iannitti. 2016. Mechanisms and therapeutic effectiveness of pulsed electromagnetic field therapy in oncology. Cancer Med. 5 :3128–39. doi:10.1002/cam4.861.
   PubMed Web of Science ®Google Scholar
• Veronesi, F., M. Cadossi, G. Giavaresi, L. Martini, S. Setti, R. Buda, S. Giannini, and M. Fini. 2015. Pulsed electromagnetic fields combined with a collagenous scaffold and bone marrow concentrate enhance osteochondral regeneration: An in vivo study. BMC Musculoskelet. Disord. 16 :233. doi:10.1186/s12891-015-0683-2.
   PubMed Web of Science ®Google Scholar
• Vincenzi, F., S. Pasquini, S. Setti, S. Salati, R. Cadossi, P. A. Borea, and K. Varani. 2020. Pulsed electromagnetic fields stimulate HIF-1α-Independent VEGF release in 1321N1 human astrocytes protecting neuron-like SH-SY5Y cells from oxygen-glucose deprivation. Int. J. Mol. Sci. 21 :8053. doi:10.3390/ijms21218053.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Vincenzi, F., M. Targa, C. Corciulo, S. Gessi, S. Merighi, S. Setti, R. Cadossi, M. B. Goldring, P. A. Borea, and K. Varani. 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 :e65561. doi:10.1371/journal.pone.0065561.
   PubMed Web of Science ®Google Scholar
• Wade, B. 2013. A review of pulsed electromagnetic field (PEMF) Mechanisms at a cellular level: A rationale for clinical use. Am. J. Health Res. 1 :51–55. doi:10.11648/j.ajhr.20130103.13.
   Google Scholar
• Wang, C., Y. Liu, Y. Wang, Z. Wei, D. Suo, G. Ning, Q. Wu, S. Feng, and C. Wan. 2019. Low-frequency pulsed electromagnetic field promotes functional recovery, reduces inflammation and oxidative stress, and enhances HSP70 expression following spinal cord injury. Mol. Med. Rep. 19 :1687–93. doi:10.3892/mmr.2019.9820.
   PubMed Web of Science ®Google Scholar
• Yang, J., L. Sun, X. Fan, B. Yin, Y. Kang, S. An, and L. Tang. 2018. Pulsed electromagnetic fields alleviate streptozotocin-induced diabetic muscle atrophy. Mol. Med. Rep. 18 :1127–33. doi:10.3892/mmr.2018.9067.
   PubMed Web of Science ®Google Scholar
• Zheng, Y., L. Mei, S. Li, Ma T, Xia B, Hao Y, Gao X, Wei B, Wei Y, Jing D. 2022. Pulsed electromagnetic field alleviates intervertebral disc degeneration by activating sirt1-autophagy signaling network. Front Bioeng. Biotechnol 10:853872. doi:10.3389/fbioe.2022.853872.
   PubMed Web of Science ®Google Scholar
• Zou, J., Y. Chen, J. Qian, and H. Yang. 2017. Effect of a low frequency pulsed electromagnetic field on expression and secretion of IL-1β and TNF-α in nucleus pulposus cells. J. Int. Med. Res. 5 :462–70. doi:10.1177/0300060516683077.
   Google Scholar