Assessment of the effect of pulsed electromagnetic field application on the healing of bone defects in rats with heparin-induced osteoporosis

References

• Akkaş, P. D. N., Y. Yeni, B. E. D. Turan, and U. Günel. 1997. Effect of medication on biomechanical properties of rabbit bones: Heparin induced osteoporosis. Clin. Rheumatol. 16:585–95. doi:10.1007/BF02247799.
   PubMed Web of Science ®Google Scholar
• Ariyoshi, W., T. Takahashi, T. Kanno, H. Ichimiya, K. Shinmyouzu, H. Takano, T. Koseki, and T. Nishihara. 2008. Heparin inhibits osteoclastic differentiation and function. J. Cell. Biochem. 103:1707–17. doi:10.1002/jcb.21559.
   PubMed Web of Science ®Google Scholar
• Barak, S., M. Neuman, G. Iezzi, A. Piattelli, V. Perrotti, and Y. Gabet. 2016. A new device for improving dental implants anchorage: A histological and micro-computed tomography study in the rabbit. Clin. Oral Implants Res. 27 (8):935–42. doi: 10.1111/clr.12661.
   PubMed Web of Science ®Google Scholar
• Basset, C. A. L. 1982. Pulsing electromagnetic fields: A new method to modify cell behavior in calcified and non calcified tissues. Calcif. Tissue Int. 34:1–8. doi:10.1007/BF02411199.
   PubMed Web of Science ®Google Scholar
• Beikler, T., and T. F. Flemmig. 2003. Implants in the medically compromised patient. Crit. Rev. Oral Biol. Med. 14:305–16. doi:10.1177/154411130301400407.
   PubMedGoogle Scholar
• Canè, V., P. Botti, and S. Soana. 1993. Pulsed magnetic fields improve osteoblast activity during the repair of an experimental osseous defect. J. Orthop. Res. 11:664–70. doi:10.1002/jor.1100110508.
   PubMed Web of Science ®Google Scholar
• Chang, K., and W. Chang. 2003. Pulsed electromagnetic fields prevent osteoporosis in an ovariectomized female rat model: A prostaglandin E2‐associated process. Bioelectromagnetics 24:189–98. doi:10.1002/bem.10078.
   PubMed Web of Science ®Google Scholar
• Chang, W. H., K. Jimmy, and J. Sun. 2005. Bone defect healing enhanced by pulsed electromagnetic fields stimulation: In vitro bone organ culture model. J. Med. Biological Eng. 25:27–32.
   Google Scholar
• Demir, H. 2012. Osteoporoz Tanı ve Tedavisinde Biyokimyasal Markerler Turkiye Klinikleri. J. PM&R-Special Topics 5:29–33.
   Google Scholar
• Diniz, P., K. Shomura, K. Soejima, and G. Ito. 2002. Effects of pulsed electromagnetic field (PEMF) stimulation on bone tissue like formation are dependent on the maturation stages of the osteoblasts. Bioelectromagnetics 23:398–405. doi:10.1002/bem.10032.
   PubMed Web of Science ®Google Scholar
• Eraslan, G., A. Bilgili, D. Eşsiz, and H. Saltaş. 2002. The effects of an electromagnetic Field (90 Hz and 5 mT) on Some Blood Electrolyte (Ca++, P+++, Na+, K+, Cl-)Levels in Male Mice. Turk. J. Vet. Anim. Sci. 26:1233–36.
   Web of Science ®Google Scholar
• Fredericks, D. C., J. V. Nepola, J. T. Baker, J. Abbott, and B. Simon. 2000. Effects of pulsed electromagnetic fields on bone healing in a rabbit tibial osteotomy model. J. Orthop. Trauma 14:93–100. doi:10.1097/00005131-200002000-00004.
   PubMed Web of Science ®Google Scholar
• Griffith, G. C., and R. P. Boggs. 1964. The clinical usage of heparin. Am. J. Cardiol. 14:39–46. doi:10.1016/0002-9149(64)90103-1.
   PubMed Web of Science ®Google Scholar
• Gürer, N., R. Başak, C. Bahadır, H. Koç, H. Nur, and Y. Polat. 2005. Kemik mineral yoğunluğu ile kemik döngüsünün biyokimyasal göstergelerinin ilişkisi. Türk Fiz Tip Rehab Derg 51:54–57.
   Google Scholar
• Hanafy, E., S. Elhafez, F. Aly, and M. Elazhary. 2008. Loss of bone calcium in exposure to 50 Hz magnetic fields. Electromagn. Biol. Med. 27:402–08. doi:10.1080/15368370802473505.
   PubMed Web of Science ®Google Scholar
• Huang, L., W. Wang, D. Xiao, L. Yang, Z. Lei, and C. He. 2008b. [Effect of pulsed electromagnetic fields of different treatment time on bone mineral density of femur in ovariectomized rats]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 22:548–50.
   PubMedGoogle Scholar
• Huang, L. Q., H. C. He, C. Q. He, J. Chen, and L. Yang. 2008a. Clinical update of pulsed electromagnetic fields on osteoporosis. Chin. Med. J. 121:2095–99. doi:10.1097/00029330-200810020-00028.
   PubMed Web of Science ®Google Scholar
• Hwang, K. G., J. H. Lee, M. J. Kim, K. S. Shim, and J. W. Kim. 2002. A study of effect of pulsed electromagnetic fields on osteogenesis in rabbit cranial bone defect. J. Korean Assoc. Oral Maxillofac Surg. 28:264–73.
   Google Scholar
• Jing, D., G. Shen, J. Huang, K. Xie, J. Cai, Q. Xu, X. Wu, and E. Luo. 2010. Circadian rhythm affects the preventive role of pulsed electromagnetic fields on ovariectomy-induced osteoporosis in rats. Bone February 46 (2):487–95. doi:10.1016/j.bone.2009.09.021.
   PubMed Web of Science ®Google Scholar
• Jing, D., J. Cai, Y. Wu, G. Shen, F. Li, Q. Xu, K. Xie, C. Tang, J. Liu, and W. Guo. 2014a. Pulsed electromagnetic fields partially preserve bone mass, microarchitecture, and strength by promoting bone formation in hindlimb‐suspended rats. J. Bone Miner. Res. 29:2250–61. doi:10.1002/jbmr.2260.
   PubMed Web of Science ®Google Scholar
• Jing, D., J. Cai, Y. Wu, G. Shen, M. Zhai, S. Tong, Q. Xu, K. Xie, X. Wu, and C. Tang. 2014b. Moderate-intensity rotating magnetic fields do not affect bone quality and bone remodeling in hindlimb suspended rats. PLoS ONE 9:e102956. doi:10.1371/journal.pone.0102956.
   PubMed Web of Science ®Google Scholar
• Kanat, E., H. Çelen, M. Yıldırım, N. Dıraz, A. Alp, and M. Yurtkuran. 2008. Primer osteoporoz hastalarında demografik veriler, biyokimyasal ölçümler, dxa değerleri ve kırık arasındaki ilişki. Uludag Üniv Tip Fak Derg 34:27–30.
   Google Scholar
• Kang, K. S., J. M. Hong, J. A. Kang, J. W. Rhie, Y. H. Jeong, and D. W. Cho. 2013. Regulation of osteogenic differentiation of human adipose-derived stem cells by controlling electromagnetic field conditions. Exp. Mol. Med. 45:e6. doi:10.1038/emm.2013.11.
   Web of Science ®Google Scholar
• Kanis, J. A., and C. C. Glüer. 2000. An update on the diagnosis and assessment of osteoporosis with densitometry. Osteoporos Int 11:192–202. doi:10.1007/s001980050281.
   PubMed Web of Science ®Google Scholar
• Kapi, E., M. Bozkurt, C. T. Selcuk, M. S. Celik, V. Akpolat, F. B. Isik, B. H. Bozarslan, and Y. Celik. 2015. Comparison of effects of pulsed electromagnetic field stimulation on platelet-rich plasma and bone marrow stromal stem cell using rat zygomatic bone defect model. Ann. Plast. Surg. 75:565–71. doi:10.1097/SAP.0000000000000160.
   PubMed Web of Science ®Google Scholar
• Leidig-Bruckner, G., F. Raue, and K. Frank-Raue. 2012. Secondary osteoporosis-relevant clinical characteristics in diagnosis and therapy. Dtsch. Med. Wochenschr. 137:326–32. doi:10.1055/s-0031-1298867.
   PubMed Web of Science ®Google Scholar
• Leisner, S., R. Shahar, I. Aizenberg, D. Lichovsky, and T. Levin-Harrus. 2002. The effect of short‐duration, high‐intensity electromagnetic pulses on fresh ulnar fractures in rats. J. Vet. Med. A 49:33–37. doi:10.1046/j.1439-0442.2002.00386.x.
   Google Scholar
• Li, J., W. H. S. Chang, H. W. Jan, R. C. Ruaan, H. C. Liu, and J. S. Sun. 2003. Optimum parameters of specific 7.5 Hz single pulsed electromagnetic field stimulation on osteoblast growth. Electromagn. Biol. Med. 22:87–101. doi:10.1081/JBC-120024619.
   Web of Science ®Google Scholar
• Li, K., S. Ma, Y. Li, G. Ding, Z. Teng, J. Liu, D. Ren, Y. Guo, L. Ma, and G. Guo. 2014. Effects of PEMF exposure at different pulses on osteogenesis of MC3T3-E1 cells. Arch. Oral Biol. 59:921–27. doi:10.1016/j.archoralbio.2014.05.015.
   PubMed Web of Science ®Google Scholar
• Libouban, H., M. F. Moreau, E. Legrand, M. F. Baslé, M. Audran, and D. Chappard. 2001. Comparison insight dual X-ray absorptiometry (DXA), histomorphometry, ash weight, and morphometric indices for bone evaluation in an animal model (the orchidectomized rat) of male osteoporosis. Calcif. Tissue Int. 68:31–37. doi:10.1007/BF02685000.
   PubMed Web of Science ®Google Scholar
• Matsunaga, S., T. Sakou, and K. Ijiri. 1996. Osteogenesis by pulsing electromagnetic fields (PEMFs): Optimum stimulation setting. In Vivo 10:351.
   PubMed Web of Science ®Google Scholar
• Mätzsch, T., D. Bergqvist, U. Hedner, B. Nilsson, and P. Ostergaard. 1986. Heparin-induced osteoporosis in rats. Thromb. Haemost. 56:293–94. doi:10.1055/s-0038-1661669.
   PubMed Web of Science ®Google Scholar
• Meller, Y., R. Kestenbaum, M. Mozes, G. Mozes, R. Yagil, and S. Shany. 1984a. Mineral and endocrine metabolism during fracture healing in dogs. Clin. Orthop. 187:294–95.
   Google Scholar
• Meller, Y., R. Shainkin-Kestenbaum, S. Shany, I. Zuilli, N. Yankowitz, J. Giat, A. Konforti, and G. Torok. 1984b. parathyroid hormone, calcitonin, and vitamin d metabolites during normal fracture healing in humans. Clin. Orthop. 183:238–45.
   Google Scholar
• Monreal, M., L. Vinas, L. Monreal, S. Lavin, E. Lafoz, and A. M. Angles. 1990. Heparin-related osteoporosis in rats. Pathophysiol. Haemost. Thromb. 20:204–07. doi:10.1159/000216128.
   Google Scholar
• Muir, J. M., J. Hirsh, J. I. Weitz, M. Andrew, E. Young, and S. G. Shaughnessy. 1997. A histomorphometric comparison of the effects of heparin and low-molecular-weight heparin on cancellous bone in rats. Blood 89:3236–42. doi:10.1182/blood.V89.9.3236.
   PubMed Web of Science ®Google Scholar
• Muir, J. M., M. Andrew, J. Hirsh, J. Weitz, E. Young, P. Deschamps, and S. Shaughnessy. 1996. Histomorphometric analysis of the effects of standard heparin on trabecular bone in vivo. Blood 88:1314–20. doi:10.1182/blood.V88.4.1314.bloodjournal8841314.
   PubMed Web of Science ®Google Scholar
• Mutoh, S., N. Takeshita, T. Yoshino, and I. Yamaguchi. 1993. Characterization of heparin-induced osteopenia in rats. Endocrinology 133:2743. doi:10.1210/endo.133.6.8243298.
   PubMed Web of Science ®Google Scholar
• Öncel, S. 2012. Sekonder Osteoporoz. Turkiye Klinikleri J PM&R-Special Topics 5:49–55.
   Google Scholar
• Otter, M. W., K. J. McLeod, and C. T. Rubin. 1998. Effects of electromagnetic fields in experimental fracture repair. Clin. Orthop. 355:S90–S104. doi:10.1097/00003086-199810001-00011.
   PubMedGoogle Scholar
• P S, B., A. C. Muniz Rennó, D. A. Ribeiro, R. Fangel, O. Peitl, E. D. Zanotto, and N. A. Parizotto. 2011. Biosilicate® and low‐level laser therapy improve bone repair in osteoporotic rats. J. Tissue Eng. Regen. Med. 5:229–37. doi:10.1002/term.309.
   PubMed Web of Science ®Google Scholar
• Rajgopal, R., M. Butcher, J. I. Weitz, and S. G. Shaughnessy. 2006. Heparin synergistically enhances interleukin-11 signaling through up-regulation of the MAPK pathway. J. Biol. Chem. 281:20780–87. doi:10.1074/jbc.M600169200.
   PubMed Web of Science ®Google Scholar
• Rao, T. M., G. Lakshmipathi, T. Sastry, and O. Ramakrishna. 2001. Biochemical changes following ulnar segmental defect repair with fibrillar collagen-hydroxyapatite, and porous hydroxyapatite implants in canines. Indian J. Anim. Res. 35:112–15.
   Google Scholar
• Schober, A., M. Yanik, and G. Fischer. 1982. Electrolytic changes in the white mouse under the influence of weak magnetic fields. Zentralbl Bakteriol Mikrobiol Hyg B 176:305–15.
   PubMedGoogle Scholar
• Sert, C., D. Mustafa, M. Z. Düz, F. Akşen, and A. Kaya. 2002. The preventive effect on bone loss of 50-Hz, 1-mT electromagnetic field in ovariectomized rats. J. Bone Miner. Metab. 20:345–49. doi:10.1007/s007740200050.
   PubMed Web of Science ®Google Scholar
• Seyhan, N., and A. Canseven. 2006. In vivo effects of ELF MFs on collagen synthesis, free radical processes, natural antioxidant system, respiratory burst system, immune system activities, and electrolytes in the skin, plasma, spleen, lung, kidney, and brain tissues. Electromagn. Biol. Med. 25:291. doi:10.1080/15368370601054787.
   PubMed Web of Science ®Google Scholar
• Shakya, G., M. Zama, H. Aithal, R. John, and M. Baghel. 2014. Biochemical changes following electro-acupuncture and static magnetic field therapy in rabbits for bone defect healing. Vet World 7:83–86. doi:10.14202/vetworld.2014.83-86.
   Google Scholar
• Shaughnessy, S. G., J. Hirsh, M. Bhandari, J. M. Muir, E. Young, and J. I. Weitz. 1999. A histomorphometric evaluation of heparin-induced bone loss after discontinuation of heparin treatment in rats. Blood 93:1231–36. doi:10.1182/blood.V93.4.1231.
   PubMed Web of Science ®Google Scholar
• Simon, R. R., and S. G. Shaughnessy. 2004. Effects of anticoagulants on bone. Clin. Rev. Bone Miner. Metab. 2:151–58. doi:10.1385/BMM:2:2:151.
   Google Scholar
• Suryawanshi, S., S. Maiti, and G. Singh. 2001. A comparative study of two different fixation techniques in the management of tibial metaphyseal fracture in dogs. J. Appl. Anim. Res. 20:89–98. doi:10.1080/09712119.2001.9706741.
   Web of Science ®Google Scholar
• Swaminathan, R. 2001. Biochemical markers of bone turnover. Clin. Chim. Acta 313:95–105. doi:10.1016/S0009-8981(01)00656-8.
   PubMed Web of Science ®Google Scholar
• Takano-Yamamoto, T., M. Kawakami, and M. Sakuda. 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. 71:1920–25. doi:10.1177/00220345920710121301.
   PubMed Web of Science ®Google Scholar
• Taylor, K. F., N. Inoue, B. Rafiee, J. E. Tis, K. A. McHale, and E. Chao. 2006. Effect of pulsed electromagnetic fields on maturation of regenerate bone in a rabbit limb lengthening model. J. Orthop. Res. 24:2–10. doi:10.1002/jor.20014.
   PubMed Web of Science ®Google Scholar
• van der Jagt, O. P., J. C. van der Linden, J. H. Waarsing, J. A. Verhaar, and H. Weinans. 2012. Systemic treatment with pulsed electromagnetic fields do not affect bone microarchitecture in osteoporotic rats. Int. Orthop. 36:1501–06. doi:10.1007/s00264-011-1471-8.
   PubMed Web of Science ®Google Scholar
• Yang, H. J., R. Y. Kim, and S. J. Hwang. 2015. Pulsed electromagnetic fields enhance bone morphogenetic protein-2 dependent-bone regeneration. Tissue Eng. 21:2629–37. doi:10.1089/ten.tea.2015.0032.
   Google Scholar
• Zhong, C., X. Zhang, Z. Xu, and R. He. 2012. Effects of low-intensity electromagnetic fields on the proliferation and differentiation of cultured mouse bone marrow stromal cells. Phys. Ther. 92:1208–19. doi:10.2522/ptj.20110224.
   PubMed Web of Science ®Google Scholar