Physical stimulations and their osteogenesis-inducing mechanisms

VIEWS - 226 (Abstract) 21 (PDF)
Cijun Shuai, Wenjing Yang, Shuping Peng, Chengde Gao, Wang Guo, Yuxiao Lai, Pei Feng

Abstract


Physical stimulations such as magnetic, electric and mechanical stimulation could enhance cell activity and promote bone formation in bone repair process via activating signal pathways, modulating ion channels, regulating bone-related gene expressions, etc. In this paper, bioeffects of physical stimulations on cell activity, tissue growth and bone healing were systematically summarized, which especially focused on their osteogenesis-inducing mechanisms. Detailedly, magnetic stimulation could produce Hall effect which improved the permeability of cell membrane and promoted the migration of ions, especially accelerating the extracellular calcium ions to pass through cell membrane. Electric stimulation could induce inverse piezoelectric effect which generated electric signals, accordingly up-regulating intracellular calcium levels and growth factor synthesis. And mechanical stimulation could produce mechanical signals which were converted into corresponding biochemical signals, thus activating various signaling pathways on cell membrane and inducing a series of gene expressions. Besides, the equipments of physical stimulation system were discussed. The opportunities and challenges of physical stimulations were also presented from the perspective of bone repair.

Keywords


physical stimulations; cell activity; osteogenesis-inducing mechanisms; bone repair

Full Text:

PDF

References


Dhand C, Ong S T, Dwivedi N, et al., 2016, Bio-inspired in situ crosslinking and mineralization of electrospun collagen scaffolds for bone tissue engineering. Biomaterials, 104: 323–338. https://doi.org/10.1016/j.biomaterials.2016.07.007

Naveena N, 2012, Biomimetic composites and stem cells interaction for bone and cartilage tissue regeneration. J Mater Chem, 22(12): 5239–5253. https://doi.org/10.1039/C1JM14401D

Praemer A, Furner S, Rice D P, 1992, Musculoskeletal conditions in the United States. Amer Academy of Orthopaedic.

Caterini R, Potenza V, Ippolito E, et al., 2016, Treatment of recalcitrant atrophic non-union of the humeral shaft with BMP-7, autologous bone graft and hydroxyapatite pellets. Injury, 47: S71–S77. https://doi.org/10.1016/j.injury.2016.07.044

Schwartz A M, Schenker M L, Ahn J, et al., 2017, Building better bone: The weaving of biologic and engineering strategies for managing bone loss. J Orthop Res, 35(9): 1855–1864. https://doi.org/10.1002/jor.23592

Shuai C, Feng P, Wu P, et al., 2016, A combined nanostructure constructed by graphene and boron nitride nanotubes reinforces ceramic scaffolds. Chemical Engineering Journal, 313: 487–497. https://doi.org/10.1016/j.cej.2016.11.095

Feng P, Wu P, Gao C, et al., 2018, A multi-material scaffold with tunable properties: Towards bone tissue repair. Advanced Science, 1700817: 1–15.

Hu K, Olsen B R, 2016, The roles of vascular endothelial growth factor in bone repair and regeneration. Bone, 91: 30–38. https://doi.org/10.1016/j.bone.2016.06.013

Yang F, Wang J, Hou J, et al., 2013, Bone regeneration using cell-mediated responsive degradable PEG-based scaffolds incorporating with rhBMP-2. Biomaterials, 34(5): 1514–1528. https://doi.org/10.1016/j.biomaterials.2012.10.058

Rumpler M, Woesz A, Manjubala I, et al., 2010, Three-dimensional growth behavior of osteoblasts on biomimetic hydroxylapatite scaffolds. J Biomed Mater Res A, 81(1): 40–50. https://doi.org/10.1002/jbm.a.30940

Zhang H, Ahmad M, Gronowicz G, 2003, Effects of transforming growth factor-beta 1 (TGF-1) on in vitro mineralization of human osteoblasts on implant materials. Biomaterials, 24(12): 2013–2020. https://doi.org/10.1016/S0142-9612(02)00616-6

Zhu Y, Yang Q, Yang M, et al., 2017, Protein corona of magnetic hydroxyapatite scaffold improves cell proliferation via activation of mitogen-activated protein kinase signaling pathway. Acs Nano, 11(4): 3690–3704. https://doi.org/10.1021/acsnano.6b08193

Puricelli E, Dutra N B, Ponzoni D, 2009, Histological evaluation of the influence of magnetic field application in autogenous bone grafts in rats. Head Face Med, 5: 1. https://doi.org/10.1186/1746-160X-5-1

Kim I S, Song J K, Zhang Y L, et al., 2006, Biphasic electric current stimulates proliferation and induces VEGF production in osteoblasts. Biochim Biophys Acta, 1763(9): 907–916. https://doi.org/10.1016/j.bbamcr.2006.06.007

Muttini A, 2014, Effect of electric current stimulation in combination with external fixator on bone healing in a sheep fracture model. V Vet Ital, 50(4): 249–257. https://doi.org/10.12834/VetIt.271.963.2

Panseri S, Russo A, Sartori M, et al., 2013, Modifying bone scaffold architecture in vivo with permanent magnets to facilitate fixation of magnetic scaffolds. Bone, 56(2): 432–439. https://doi.org/10.1016/j.bone.2013.07.015

Jiang P, Zhang Y, Zhu C, et al., 2016, Fe3O4/BSA particles induce osteogenic differentiation of mesenchymal stem cells under static magnetic field. Acta Biomaterialia, 46: 141–150. https://doi.org/10.1016/j.actbio.2016.09.020

Wang J, An Y, Li F, et al., 2014, The effects of pulsed electromagnetic field on the functions of osteoblasts on implant surfaces with different topographies. Acta Biomater, 10(2): 975–985. https://doi.org/10.1016/j.actbio.2013.10.008

Hu W W, Hsu Y T, Cheng Y C, et al., 2014, Electrical stimulation to promote osteogenesis using conductive polypyrrole films. Mater Sci Eng C Mater Biol Appl, 37(4): 28–36. https://doi.org/10.1016/j.msec.2013.12.019

Clark C C, Wang W, Brighton C T, 2014, Up-regulation of expression of selected genes in human bone cells with specific capacitively coupled electric fields. J Orthop Res, 32(7): 894–903. https://doi.org/10.1002/jor.22595

Li J K, Chang W H, Lin J C, et al., 2003, Cytokine release from osteoblasts in response to ultrasound stimulation. Biomaterials, 24(13): 2379–2385. https://doi.org/10.1016/S0142-9612(03)00033-4

Liu C, Abedian R, Meister R, et al., 2012, Influence of perfusion and compression on the proliferation and differentiation of bone mesenchymal stromal cells seeded on polyurethane scaffolds. Biomaterials, 33(4): 1052–1064. https://doi.org/10.1016/j.biomaterials.2011.10.041

Chang W H, Chen L J, Lin F H, 2010, Effect of pulse-burst electromagnetic field stimulation on osteoblast cell activities. Bioelectromagnetics, 25(6): 457–465. https://doi.org/10.1002/bem.20016

Rosenberg J N, Turchetta J, 1993, Magnetic coil stimulation of the brachial plexus. Arch Phys Med Rehabil, 74(9): 928–932.

Balint R, Cassidy N J, Cartmell S H, 2013, Electrical stimulation: A novel tool for tissue engineering. Tissue Eng Part B Rev, 19(1): 48–57. https://doi.org/10.1089/ten.TEB.2012.0183

Kim I S, Song J K, Yu L Z, et al., 2006, Biphasic electric current stimulates proliferation and induces VEGF pro­duction in osteoblasts. Biochim Biophys Acta, 1763(9): 907–916. https://doi.org/10.1016/j.bbamcr.2006.06.007

Supronowicz P R, Ajayan P M, Ullmann K R, et al., 2002, Novel current-conducting composite substrates for exposing osteoblasts to alternating current stimulation. J Biomed Mater Res, 59(3): 499–506.

Zhao Z, Watt C, Karystinou A, et al., 2011, Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur Cell Mater, 22: 344–358.

Mogil R J, Kaste S C, Jr F R, et al., 2016, Effect of low-magnitude, high-frequency mechanical stimulation on BMD among young childhood cancer survivors: A randomized clinical trial. JAMA Oncol, 2(7): 908–914. https://doi.org/10.1001/jamaoncol.2015.6557

Baskett P J, 1992, Advances in cardiopulmonary resuscitation. Br J Anaesth, 69(2): 182–193.

Bars D L, Gozariu M, Cadden S W, 2001, Animal models of nociception. Pharmacol Rev, 53(4): 597–652.

Athanasiou K A, Zhu C, Lanctot D R, et al., 2000, Fundamentals of biomechanics in tissue engineering of bone. Tissue Eng, 6(4): 361–381. https://doi.org/10.1089/107632700418083

Zhang J, Ding C, Ren L, et al., 2014, The effects of static magnetic fields on bone. Prog Biophys Mol Biol, 114(3): 146–152. https://doi.org/10.1016/j.pbiomolbio.2014.02.001

Wieland D C, Krywka C, Mick E, et al., 2015, Investigation of the inverse piezoelectric effect of trabecular bone on a micrometer length scale using synchrotron radiation. Acta Biomater, 25: 339–346. https://doi.org/10.1016/j.actbio.2015.07.021

Papachroni K K, Karatzas D N, Papavassiliou K A, et al., 2009, Mechanotransduction in osteoblast regulation and bone disease. Trends Mol Med, 15(5): 208–216. https://doi.org/10.1016/j.molmed.2009.03.001

Kotani H, Kawaguchi H, Shimoaka T, et al., 2002, Strong static magnetic field stimulates bone formation to a definite orientation in vitro and in vivo. J Bone Miner Res, 17(10): 1814–1821. https://doi.org/10.1359/jbmr.2002.17.10.1814

Markov M S, Hazlewood C F, 2009, Electromagnetic field dosimetry for clinical application. Environmentalist, 29(2): 161–168. https://doi.org/10.1007/s10669-009-9219-3

Luben R A, Cain C D, Chen C Y, et al., 1982, Effects of electromagnetic stimuli on bone and bone cells in vitro: Inhibition of responses to parathyroid hormone by low-energy low-frequency fields. Proc Natl Acad Sci U S A, 79(13): 4180–4184. https://doi.org/10.1073/pnas.79.13.4180

Adams C S, Mansfield K, Perlot R L, et al., 2001, Matrix regulation of skeletal cell apoptosis. Role of calcium and phosphate ions. J Biol Chem, 276(23): 20316–20322. https://doi.org/10.1074/jbc.M006492200

Wã³Jcik-Piotrowicz K, Kaszuba-Zwoiå„Ska J, Rokita E, et al., 2016, Cell viability modulation through changes of Ca(2+)-dependent signalling pathways. Prog Biophys Mol Biol, 121(1): 45–53. https://doi.org/10.1016/j.pbiomolbio.2016.01.004

Zhang X, Liu X, Pan L, et al., 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(3): 662–666. https://doi.org/10.1016/j.bbrc.2010.04.154

Pounder N M, Harrison A J, 2008, Low intensity pulsed ultrasound for fracture healing: A review of the clinical evidence and the associated biological mechanism of action. Ultrasonics, 48(4): 330–338. https://doi.org/10.1016/j.ultras.2008.02.005

Otter M W, Mcleod K J, Rubin C T, 1998, Effects of electromagnetic fields in experimental fracture repair. Clin Orthop Relat Res, 355S(355 Suppl): 90–104.

Supronowicz P R, Ajayan P M, Ullmann K R, et al., 2002, Novel current-conducting composite substrates for exposing osteoblasts to alternating current stimulation. J Biomed Mater Res, 59(3): 499–506.

Brighton C T, Wang W, Seldes R, et al., 2001, Signal transduction in electrically stimulated bone cells. J Bone Joint Surg Am, 83-A(10): 1514–1523.

Kim I S, Song J K, Song Y M, et al., 2009, Novel effect of biphasic electric current on in vitro osteogenesis and cytokine production in human mesenchymal stromal cells. Tissue Eng Part A, 15(9): 2411–2422. https://doi.org/10.1089/ten.tea.2008.0554

Xu J, Wang W, Clark C C, et al., 2009, Signal transduction in electrically stimulated articular chondrocytes involves translocation of extracellular calcium through voltage-gated channels 1. Osteoarthritis Cartilage, 17(3): 397–405. https://doi.org/10.1016/j.joca.2008.07.001

Zhuang H, Wang W, Seldes R M, et al., 1997, Electrical stimulation induces the level of TGF-β1 mRNA in osteoblastic cells by a mechanism involving calcium/calmodulin pathway. Biochem Biophys Res Commun, 237(2): 225–229. https://doi.org/10.1006/bbrc.1997.7118

Hroniktupaj M, Rice W L, Croningolomb M, et al., 2011, Osteoblastic differentiation and stress response of human mesenchymal stem cells exposed to alternating current electric fields. Biomed Eng Online, 10(1): 9. https://doi.org/10.1186/1475-925X-10-9

Baylink D J, Finkelman R D, Mohan S, 1993, Growth factors to stimulate bone formation. J Bone Miner Res, 8(S2): S565–S572. https://doi.org/10.1002/jbmr.5650081326

Pelissier P, Masquelet A C, Bareille R, et al., 2010, Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration. J Orthop Res, 22(1): 73–79. https://doi.org/10.1016/S0736-0266(03)00165-7

Fitzsimmons R J, Strong D D, Mohan S, et al., 1992, Low-amplitude, low-frequency electric field-stimulated bone cell proliferation may in part be mediated by increased IGF-II release. J Cell Physiol, 150(1): 84–89. https://doi.org/10.1002/jcp.1041500112

Ijiri K, Matsunaga S, Fukuda T, et al., 1995, Indomethacin inhibition of ossification induced by direct current stimulation. J Orthop Res, 13(1): 123–131. https://doi.org/10.1002/jor.1100130118

Ignatius A, Blessing H, Liedert A, et al., 2005, Tissue engineering of bone: effects of mechanical strain on osteoblastic cells in type I collagen matrices. Biomaterials, 26(3): 311–318. https://doi.org/10.1016/j.biomaterials.2004.02.045

Knippenberg M, Helder M N, Doulabi B Z, et al., 2005, Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng, 11(12): 1780–1788. https://doi.org/10.1089/ten.2005.11.1780

Morita Y, Watanabe S, Ju Y, et al., 2013, Determination of optimal cyclic uniaxial stretches for stem cell-to-tenocyte differentiation under a wide range of mechanical stretch conditions by evaluating gene expression and protein synthesis levels. Acta Bioeng Biomech, 15(3): 71–79.

Tsuzuki T, Okabe K, Kajiya H, et al., 2000, Osmotic membrane stretch increases cytosolic Ca(2+) and inhibits bone resorption activity in rat osteoclasts. Jpn J Physiol, 50(1): 67–76.

Naruse K, Miyauchi A, Itoman M, et al., 2003, Distinct Anabolic Response of Osteoblast to Low–Intensity Pulsed Ultrasound. J Bone Miner Res, 18(2): 360–369. https://doi.org/10.1359/jbmr.2003.18.2.360

Lianyun X U, 2011, Investigation of pressure loading rates on streaming potentials in bone. Chinese Science: Technical Science, 54(6): 1376–1381.

Hsu S H, Chang J C, 2010, The static magnetic field accelerates the osteogenic differentiation and mineralization of dental pulp cells. Cytotechnology, 62(2): 143–155. https://doi.org/10.1007/s10616-010-9271-3

Yamamoto Y, Ohsaki Y, Goto T, et al., 2003, Effects of static magnetic fields on bone formation in rat osteoblast cultures. J Dent Res, 82(12): 962–966. https://doi.org/10.1177/154405910308201205

Aliabouzar M, Zhang L G, Sarkar K, 2016, Lipid coated microbubbles and low intensity pulsed ultrasound enhance chondrogenesis of human mesenchymal stem cells in 3D printed scaffolds. Sci Rep, 6: 37728. https://doi.org/10.1038/srep37728

Jian Z, Chong D, Peng S, 2014, Alterations of mineral elements in osteoblast during differentiation under hypo, moderate and high static magnetic fields. Biol Trace Elem Res, 162(1–3): 153–157. https://doi.org/10.1007/s12011-014-0157-7

Di S, Tian Z, Qian A, et al., 2012, Large gradient high magnetic field affects FLG29.1 cells differentiation to form osteoclast-like cells. Int J Radiat Biol, 88(11): 806–813. https://doi.org/10.3109/09553002.2012.698365

Huang J, Liu W, Liang Y, et al., 2018, Preparation and biocompatibility of diphasic magnetic nanocomposite scaffold. Mater Sci Eng C Mater Biol Appl, 87: 70–77. https://doi.org/10.1016/j.msec.2018.02.003

Yun H M, Ahn S J, Park K R, et al., 2016, Magnetic nanocomposite scaffolds combined with static magnetic field in the stimulation of osteoblastic differentiation and bone formation. Biomaterials, 85: 88–98. https://doi.org/10.1016/j.biomaterials.2016.01.035

Feng S W, Lo Y J, Chang W J, et al., 2010, Static magnetic field exposure promotes differentiation of osteoblastic cells grown on the surface of a poly-L-lactide substrate. Med Biol Eng Comput, 48(8): 793–798. https://doi.org/10.1007/s11517-010-0639-5

Yan J L, Zhou J, Ma H P, 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

Zhou J, Xue-Yan L I, Chen K M, et al., 2010, Effect of sinusoidal electricity magnetic field at different intensity on the differentiation and collagen-I,BMP-2 mRNA expression of osteoblasts in vitro. Chin J Med Phys, 5: 2173–2177.

Kamolmatyakul S, Jinorose U, Prinyaroj P, et al., 2008, Responses of human normal osteoblast cells and osteoblast-like cell line, MG-63 cells, to pulse electromagnetic field (PEMF). Songklanakarin J Sci Technol, 30(1): 25–29.

Diniz P, Shomura K, Soejima K, et al., 2002, Effects of pulsed electromagnetic field (PEMF) stimulation on bone tissue like formation are dependent on the maturation stages of the osteoblasts. Bioelectromagnetics, 23(5): 398–405. https://doi.org/10.1002/bem.10032

Wang P, Liu J, Yang Y, et al., 2017, Differential intensity-dependent effects of pulsed electromagnetic fields on RANKL-induced osteoclast formation, apoptosis, and bone resorbing ability in RAW264.7 cells. Bioelectromagnetics, 38(8): 602–612. https://doi.org/10.1002/bem.22070

Chang K, Hongshong C W, Yu Y H, et al., 2004, Pulsed electromagnetic field stimulation of bone marrow cells derived from ovariectomized rats affects osteoclast formation and local factor production. Bioelectromagnetics, 25(2): 134–141. https://doi.org/10.1002/bem.10168

Zhao Z, Watt C, Karystinou A, et al., 2011, Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur Cell Mater, 22: 344–358.

Banks T A, Luckman P S, Frith J E, et al., 2015, Effects of electric fields on human mesenchymal stem cell behaviour and morphology using a novel multichannel device. Integr Biol (Camb), 7(6): 693–712. https://doi.org/10.1039/c4ib00297k

Creecy C M, O'Neill C F, Arulanandam B P, et al., 2013, Mesenchymal stem cell osteodifferentiation in response to alternating electric current. Tissue Eng Part A, 19(3–4): 467–474. https://doi.org/10.1089/ten.TEA.2012.0091

Wang X, Gao Y, Shi H, et al., 2016, Influence of the intensity and loading time of direct current electric field on the directional migration of rat bone marrow mesenchymal stem cells. Front Med, 10(3): 286–296. https://doi.org/10.1007/s11684-016-0456-9

Grunert P C, Jonitz-Heincke A, Su Y, et al., 2014, Establish­ment of a novel in vitro test setup for electric and magnetic stimulation of human osteoblasts. Cell Biochem Biophys, 70(2): 805–817. https://doi.org/10.1007/s12013-014-9984-6

Jin G H, Kim G H, 2013, The effect of sinusoidal AC electric stimulation of 3D PCL/CNT and PCL/β-TCP based bio-composites on cellular activities for bone tissue regeneration. J Mater Chem B, 1(10): 1439–1452.

Rubin C, Bolander M, Ryaby J P, et al., 2001, The use of low-intensity ultrasound to accelerate the healing of fractures. J Bone Joint Surg Am, 83-A(2): 259–270.

Naruse K, Miyauchi A, Itoman M, et al., 2003, Distinct anabolic response of osteoblast to low-intensity pulsed ultrasound. J Bone Miner Res, 18(2): 360–369. https://doi.org/10.1359/jbmr.2003.18.2.360

Sant'Anna E F, Leven R M, Virdi A S, et al., 2005, Effect of low intensity pulsed ultrasound and BMP-2 on rat bone marrow stromal cell gene expression. J Orthop Res, 23(3): 646–652. https://doi.org/10.1016/j.orthres.2004.09.007

Yang R S, Lin W L, Chen Y Z, et al., 2005, Regulation by ultrasound treatment on the integrin expression and differentiation of osteoblasts. Bone, 36(2): 276–283. https://doi.org/10.1016/j.bone.2004.10.009

Sun J S, Hong R C, Chang W H, et al., 2001, In vitro effects of low-intensity ultrasound stimulation on the bone cells. J Biomed Mater Res, 57(3): 449–456.

Korstjens C M, Nolte P A, Burger E H, et al., 2004, Stimulation of bone cell differentiation by low-intensity ultrasound––a histomorphometric in vitro study. J Orthop Res, 22(3): 495–500. https://doi.org/10.1016/j.orthres.2003.09.011

Xuan Z, Castro N J, Wei Z, et al., 2016, Improved human bone marrow mesenchymal stem cell osteogenesis in 3D bioprinted tissue scaffolds with low intensity pulsed ultrasound stimulation. Sci Rep, 6: 32876. https://doi.org/10.1038/srep32876

Aliabouzar M, Lee S J, Zhou X, et al., 2018, Effects of scaffold microstructure and low intensity pulsed ultrasound on chondrogenic differentiation of human mesenchymal stem cells. Biotechnol Bioeng, 115(2): 495–506. https://doi.org/10.1002/bit.26480

Tang L L, Wang Y L, Pan J, et al., 2004, The effect of step-wise increased stretching on rat calvarial osteoblast collagen production. J Biomech, 37(1): 157–161. https://doi.org/10.1016/S0021-9290(03)00237-9

Jagodzinski M, Drescher M, Zeichen J, et al., 2004, Effects of cyclic longitudinal mechanical strain and dexamethasone on osteogenic differentiation of human bone marrow stromal cells. Eur Cell Mater, 7: 35–41. https://doi.org/10.22203/eCM

Kearney E M, Farrell E, Prendergast P J, et al., 2010, Tensile strain as a regulator of mesenchymal stem cell osteogenesis. Ann Biomed Eng, 38(5): 1767–1779. https://doi.org/10.1007/s10439-010-9979-4

Sanchez C, Pesesse L, Gabay O, et al., 2012, Regulation of subchondral bone osteoblast metabolism by cyclic compression. Arthritis Rheum, 64(4): 1193–1203. https://doi.org/10.1002/art.33445

Li J, Rose E, Frances D, et al., 2012, Effect of oscillating fluid flow stimulation on osteocyte mRNA expression. J Biomech, 45(2): 247–251. https://doi.org/10.1016/j.jbiomech.2011.10.037

Liu X, Zhang X, Lee I, 2010, A quantitative study on morphological responses of osteoblastic cells to fluid shear stress. Acta Biochim Biophys Sin (Shanghai), 42(3): 195–201. https://doi.org/10.1093/abbs/ gmq004

Li P, Ma Y C, Shen H L, et al., 2012, Cytoskeletal reorganization mediates fluid shear stress-induced ERK5 activation in osteoblastic cells. Cell Biol Int, 36(3): 229–236. https://doi.org/10.1042/CBI20110113

Stiehler M, Bünger C, Baatrup A, et al., 2009, Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cell. J Biomed Mater Res A, 89(1): 96–107. https://doi.org/10.1002/jbm.a.31967

Chen G, Rui X, Chang Z, et al., 2017, Responses of MSCs to 3D scaffold matrix mechanical properties under oscillatory perfusion culture. ACS Appl Mater Interfaces, 9(2): 1207–1218. https://doi.org/10.1021/acsami.6b10745

Shah F A, Snis A, Matic A, et al., 2016, 3D printed Ti6Al4V implant surface promotes bone maturation and retains a higher density of less aged osteocytes at the bone-implant interface. Acta Biomater, 30: 357–367. https://doi.org/10.1016/j.actbio.2015.11.013

Lee J W, Kang K S, Lee S H, et al., 2011, Bone regeneration using a microstereolithography-produced customized poly(propylene fumarate)/diethyl fumarate photopolymer 3D scaffold incorporating BMP-2 loaded PLGA microspheres. Biomaterials, 32(3): 744–752. https://doi.org/10.1016/j.biomaterials.2010.09.035

Peng F, Yu X, Wei M, 2011, In vitro cell performance on hydroxyapatite particles/poly(-lactic acid) nanofibrous scaffolds with an excellent particle along nanofiber orientation. Acta Biomater, 7(6): 2585–2592. https://doi.org/10.1016/j.actbio.2011.02.021

Perez R A, El-Fiqi A, Park J H, et al., 2014, Therapeutic bioactive microcarriers: Co-delivery of growth factors and stem cells for bone tissue engineering. Acta Biomater, 10(1): 520–530. https://doi.org/10.1016/j.actbio.2013.09.042

Seyednejad H, Gawlitta D, Kuiper R V, et al., 2012, In vivo biocompatibility and biodegradation of 3D-printed porous scaffolds based on a hydroxyl-functionalized poly(ε-caprolactone). Biomaterials, 33(17): 4309–4318. https://doi.org/10.1016/j.biomaterials.2012.03.002

Yang W F, Long L, Wang R, et al., 2018, Surface-modified hydroxyapatite nanoparticle-reinforced polylactides for three-dimensional printed bone tissue engineering scaffolds. J Biomed Nanotechnol, 14(2): 294–303. https://doi.org/10.1166/jbn.2018.2495

Wang H, Zhao S, Zhou J, et al., 2015, Biocompatibility and osteogenic capacity of borosilicate bioactive glass scaffolds loaded with Fe3O4 magnetic nanoparticles. J Mater Chem B, 3(21): 4377–4387. https://doi.org/10.1039/C5TB00062A

He L, Zhao P, Han Q, et al., 2013, Surface modification of poly- l -lactic acid fibrous scaffolds by a molecular-designed multi-walled carbon nanotube multilayer for enhancing cell interactions. Carbon, 56(56): 224–234. http://dx.doi.org/10.1016/j.carbon.2013.01.025

Wu C, Xia L, Han P, et al., 2015, Graphene-oxide-modified β-tricalcium phosphate bioceramics stimulate in vitro and in vivo osteogenesis. Carbon, 93: 116–129. https://doi.org/10.1016/j.carbon.2015.04.048

Shuai C, Guo W, Wu P, et al., 2018, A graphene oxide-Ag co-dispersing nanosystem: Dual synergistic effects on antibacterial activities and mechanical properties of poly­mer scaffolds. Chem Eng J, 347:322–333. https://doi.org/10.1016/j.cej.2018.04.092

Zhang J, Zhao S, Zhu M, et al., 2014, 3D-printed magnetic Fe3O4/MBG/PCL composite scaffolds with multifunctionality of bone regeneration, local anticancer drug delivery and hyperthermia. J Mater Chem B, 2(43): 7583–7595. https://doi.org/10.1039/C4TB01063A

Arjmand M, Ardeshirylajimi A, Maghsoudi H, et al., 2017, Osteogenic differentiation potential of mesenchymal stem cells cultured on nanofibrous scaffold improved in the presence of pulsed electromagnetic field. J Cell Physiol, 233(2): 1061–1070. https://doi.org/10.1002/jcp.25962

Gao C, Peng S, Feng P, et al., 2017, Bone biomaterials and interactions with stem cells. Bone Res, 5: 17059. https://doi.org/10.1038/boneres.2017.59

Gao C, Feng P, Peng S, et al., 2017, Carbon nanotubes, graphene and boron nitride nanotubes reinforced bioactive ceramics for bone repair. Acta Biomater, 61: 1–20. https://doi.org/10.1016/j.actbio.2017.05.020

Sun S, Titushkin I, Cho M, 2006, Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry, 69(2): 133–141. https://doi.org/10.1016/j.bioelechem.2005.11.007

Midura R J, Ibiwoye M O, Powell K A, et al., 2005, Pulsed electromagnetic field treatments enhance the healing of fibular osteotomies. J Orthop Res, 23(5): 1035–1046. https://doi.org/10.1016/j.orthres.2005.03.015

Friedenberg Z B, Harlow M C, Brighton C T, 1971, Healing of nonunion of the medial malleolus by means of direct current: A case report. J Trauma, 11(10): 883–885.

Paterson D C, Lewis G N, Cass C A, 1980, Treatment of delayed union and nonunion with an implanted direct current stimulator. Clin Orthop Relat Res, 148: 117–128.

Nolte P A, Van d K A, Patka P, et al., 2001, Low-intensity pulsed ultrasound in the treatment of nonunions. J Trauma, 51(4): 693–702.

Yan Q C, Tomita N, Ikada Y, 1998, Effects of static magnetic field on bone formation of rat femurs. Med Eng Phys, 20(6): 397–402. https://doi.org/10.1016/S1350-4533(98)00051-4

Xu S, Tomita N, Ohata R, et al., 2001, Static magnetic field effects on bone formation of rats with an ischemic bone model. Biomed Mater Eng, 11(3): 257–263.

Xu S, Okano H, Tomita N, et al., 2011, Recovery effects of a 180 mT static magnetic field on bone mineral density of osteoporotic lumbar vertebrae in ovariectomized rats. Evid Based Complement Alternat Med, 2011(4136): 1–8. https://doi.org/10.1155/2011/620984

Shen W W, Zhao J H, 2010, Pulsed electromagnetic fields stimulation affects BMD and local factor production of rats with disuse osteoporosis. Bioelectromagnetics, 31(2): 113–119. https://doi.org/10.1002/bem.20535

Taniguchi N, Kanai S, Kawamoto M, et al., 2004, Study on application of static magnetic field for adjuvant arthritis rats. Evid Based Complement Alternat Med, 1(2): 187–191. https://doi.org/10.1093/ecam/neh024

Taniguchi N, Kanai S, 2007, Efficacy of static magnetic field for locomotor activity of experimental osteopenia. Evid Based Complement Alternat Med, 4(1): 99–105. https://doi.org/10.1093/ecam/nel067

Puricelli E, Ulbrich L M, Ponzoni D, et al., 2006, Histo­logical analysis of the effects of a static magnetic field on bone healing process in rat femurs. Head Face Med, 2: 43. https://doi.org/10.1186/1746-160X-2-43

Puricelli E, Dutra N B, Ponzoni D, 2009, Histological evaluation of the influence of magnetic field application in autogenous bone grafts in rats. Head Face Med, 5: 1. https://doi.org/10.1186/1746-160X-5-1

Leesungbok R, Ahn S J, Lee S W, et al., 2013, The effects of a static magnetic field on bone formation around a sandblasted, large-grit, acid-etched-treated titanium implant. J Oral Implantol, 39(S1): 248–255.

Inoue N, Ohnishi I, Chen D, et al., 2002, Effect of pulsed electromagnetic fields (PEMF) on late-phase osteotomy gap healing in a canine tibial model. J Orthop Res, 20(5): 1106–1114. https://doi.org/10.1016/S0736-0266(02)00031-1

Zaki M G, Gadallah N A, Mansour M, et al., 1999, Enhanced fracture healing with pulsed electromagnetic field. Egypt Rheumatol Rehab, 26(4): 845–854.

El-Hakim I E, Azim A M, El-Hassan M F, et al., 2004, Preliminary investigation into the effects of electrical stimulation on mandibular distraction osteogenesis in goats. Int J Oral Maxillofac Surg, 33(1): 42–47. https://doi.org/10.1054/ijom.2003.0445

Fredericks D C, Smucker J, Petersen E B, et al., 2007, Effects of direct current electrical stimulation on gene expression of osteopromotive factors in a posterolateral spinal fusion model. Spine (Phila Pa 1976), 32(2): 174–181. https://doi.org/10.1097/01.brs.0000251363.77027.49

Park S H, Silva M, 2004, Neuromuscular electrical stimulation enhances fracture healing: Results of an animal model. J Orthop Res, 22(2): 382–387. https://doi.org/10.1016/j.orthres.2003.08.007

Chen S C, Lai C H, Chan W P, et al., 2005, Increases in bone mineral density after functional electrical sti­mulation cycling exercises in spinal cord injured pa­tients. Disabil Rehabil, 27(22): 1337–1341. https://doi.org/10.1080/09638280500164032

Azuma Y, Ito M, Harada Y, et al., 2001, Low-intensity pulsed ultrasound accelerates rat femoral fracture healing by acting on the various cellular reactions in the fracture callus. J Bone Miner Res, 16(4): 671–680. https://doi.org/10.1359/jbmr.2001.16.4.671

Takikawa S, Matsui N, Kokubu T, et al., 2001, Low-intensity pulsed ultrasound initiates bone healing in rat nonunion fracture model. J Ultrasound Med, 20(3): 197–205. https://doi.org/10.7863/jum.2001.20.3.197

Fritton J C, Myers E R, Wright T M, et al., 2005, Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia. Bone, 36(6): 1030–1038. https://doi.org/10.1016/j.bone.2005.02.013

Lambers F M, Schulte F A, Kuhn G, et al., 2011, Mouse tail vertebrae adapt to cyclic mechanical loading by increasing bone formation rate and decreasing bone resorption rate as shown by time-lapsed in vivo imaging of dynamic bone morphometry. Bone, 49(6): 1340–1350. https://doi.org/10.1016/j.bone.2011.08.035

Peptan A I, Lopez A, Kopher R A, et al., 2008, Responses of intramembranous bone and sutures upon in vivo cyclic tensile and compressive loading. Bone, 42(2): 432–438. https://doi.org/10.1016/j.bone.2007.05.014

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(2): 487–495. https://doi.org/10.1016/j.bone.2009.09.021

Sanchez C, Gabay O, Salvat C, et al., 2009, Mechanical loading highly increases IL-6 production and decreases OPG expression by osteoblasts. Osteoarthritis Cartilage, 17(4): 473–481. https://doi.org/10.1016/j.joca.2008.09.007

Zhou J, Liao Y, Zeng Y, et al., 2017, Effect of inter­vention initiation timing of pulsed electromagnetic field on ovariectomy-induced osteoporosis in rats. Bioelectromagnetics, 38(6): 456-465. https://doi.org/10.1002/bem.22059

Aydin N, Bezer M, 2011, The effect of an intramedullary implant with a static magnetic field on the healing of the osteotomised rabbit femur. Int Orthop, 35(1): 135–141. https://doi.org/10.1007/s00264-009-0932-9

Saifzadeh S, Hobbenaghi R, Jalali F S S, et al., 2007, Effect of a static magnetic field on bone healing in the dog: Radiographic and histopathological studies. Iran J Vet Res, 8(1): 8–15.

Zhang H, Gan L, Zhu X, et al., 2018, Moderate-intensity 4mT static magnetic fields prevent bone architectural deterioration and strength reduction by stimulating bone formation in streptozotocin-treated diabetic rats. Bone, 107: 36–44. https://doi.org/10.1016/j.bone.2017.10.024

Zhang J, Meng X, Ding C, et al., 2016, Regulation of osteoclast differentiation by static magnetic fields. Electromagn Biol Med, 36(1): 8–19. https://doi.org/10.3109/15368378.2016.1141362

Cai Q, Shi Y, Shan D, et al., 2015, Osteogenic differentiation of MC3T3-E1 cells on poly(L-lactide)/Fe3O4 nanofibers with static magnetic field exposure. Mater Sci Eng C Mater Biol Appl, 55: 166–173. https://doi.org/10.1016/j.msec.2015.05.002

Boda S K, Thrivikraman G, Basu B, 2015, Magnetic field assisted stem cell differentiation – Role of substrate magnetization in osteogenesis. J Mater Chem B, 3(16): 3150–3168.

Singh R K, Patel K D, Lee J H, et al., 2014, Potential of magnetic nanofiber scaffolds with mechanical and biological properties applicable for bone regeneration. PLoS One, 9(4): e91584. https://doi.org/10.1371/journal.pone.0091584

Zhang Y, Zhai D, Xu M, et al., 2016, 3D-printed bioceramic scaffolds with Fe3O4/graphene oxide nanocomposite interface for hyperthermia therapy of bone tumor cells. J Mater Chem B, 4(17): 2874–2886.

Lei T, Liang Z, Li F, et al., 2017, 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

Adams E (inventor & assignee), Apparatus and method for invasive electrical stimulation of bone fractures. US patent. US4602638A, 1986 October 3.

Yonemori K, Matsunaga S, Ishidou Y, et al., 1996, Early effects of electrical stimulation on osteogenesis. Bone, 19(2): 173–180. https://doi.org/10.1016/8756-3282(96)00169-X

Szewczenko J, 2007, Influence of bone union electro­stimulation on corrosion of bone stabilizer in rabbits. Arch Mater Sci Eng, 28(5): 277–280.

Jr B T, Black J, Brighton C T, et al., 1983, Electrical osteo­genesis by low direct current. J Orthop Res, 1(2): 120–128. https://doi.org/10.1002/jor.1100010202

Brighton C T, Hozack W J, Brager M D, et al., 1985, Fracture healing in the rabbit fibula when subjected to various capacitively coupled electrical fields. J Orthop Res, 3(3): 331–340. https://doi.org/10.1002/jor.1100030310

Brighton C T, Pollack S R, 1985, Treatment of recalcitrant non-union with a capacitively coupled electrical field. A preliminary report. J Bone Joint Surg Am, 67(4): 577–585.

Fitzsimmons R J, Strong D D, Mohan S, et al., 1992, Low-amplitude, low-frequency electric field-stimulated bone cell proliferation may in part be mediated by increased IGF-II release. J Cell Physiol, 150(1): 84–89. https://doi.org/10.1002/jcp.1041500112

Romano C L, Romano D, Logoluso N, 2009, Low-intensity pulsed ultrasound for the treatment of bone delayed union or nonunion: A review. Ultrasound Med Biol, 35(4): 529–536. https://doi.org/10.1016/j.ultrasmedbio.2008.09.029

Naruse K, Mikuni-Takagaki Y, Azuma Y, et al., 2000, Anabolic response of mouse bone-marrow-derived stromal cell clone ST2 cells to low-intensity pulsed ultrasound. Biochem Biophys Res Commun, 268(1): 216–220. https://doi.org/10.1006/bbrc.2000.2094

Iwashina T, Mochida J, Miyazaki T, et al., 2006, Low-intensity pulsed ultrasound stimulates cell proliferation and proteoglycan production in rabbit intervertebral disc cells cultured in alginate. Biomaterials, 27(3): 354–361. https://doi.org/10.1016/j.biomaterials.2005.06.031

Fermor B, Weinberg J B, Pisetsky D S, et al., 2001, The effects of static and intermittent compression on nitric oxide production in articular cartilage explants. J Orthop Res, 19(4): 729–737. https://doi.org/10.1016/S0736-0266(00)00049-8

Zhong Z, Zeng X L, Ni J H, et al., 2013, Comparison of the biological response of osteoblasts after tension and compression. Eur J Orthod, 35(1): 59–65. https://doi.org/10.1093/ejo/cjr016

Jiang J, Zhao L G, Teng Y J, et al., 2015, ERK5 signalling pathway is essential for fluid shear stress-induced COX-2 gene expression in MC3T3-E1 osteoblast. Mol Cell Biochem, 406(1–2): 237–243. https://doi.org/10.1007/s11010-015-2441-z

Tan S D, Vries T J D, Kuijpers-Jagtman A M, et al., 2007, Osteocytes subjected to fluid flow inhibit osteoclast formation and bone resorption. Bone, 41(5): 745–751. https://doi.org/10.1016/j.bone.2007.07.019

You L, Temiyasathit S, Lee P, et al., 2008, Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone, 42(1): 172–179. https://doi.org/10.1016/j.bone.2007.09.047

Kim C H, You L, Yellowley C E, et al., 2006, Oscillatory fluid flow-induced shear stress decreases osteoclastogenesis through RANKL and OPG signaling. Bone, 39(5): 1043–1047. https://doi.org/10.1016/j.bone.2006.05.017

Cheung W Y, Liu C, Tonelli-Zasarsky R M, et al., 2015, Osteocyte apoptosis is mechanically regulated and induces angiogenesis in vitro. J Orthop Res, 29(4): 523–530. https://doi.org/10.1002/jor.21283.




DOI: http://dx.doi.org/10.18063/ijb.v4i2.138

Refbacks

  • There are currently no refbacks.


Copyright (c) 2018 Cijun Shuai, Wenjing Yang, Shuping Peng, Chengde Gao, Wang Guo, Yuxiao Lai, Pei Feng

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Recent Articles | About Journal | For Author | Fees | About Whioce

Copyright © Whioce Publishing Pte Ltd. All Rights Reserved.