Coupling between Osseointegration and Mechanotransduction to Maintain Foreign Body Equilibrium in the Long-Term: A Comprehensive Overview
Abstract
1. Introduction
2. Bone Tissue and Immune System
3. Foreign Body Reaction and Osseointegration
4. Current Immunomodulation Strategies in Osseointegrated Implants
5. Coupling between Osseointegration and Mechanotransduction to Maintain FBE Long-Term
6. Concluding Remarks
Author Contributions
Conflicts of Interest
References
- Trindade, R.; Albrektsson, T.; Wennerberg, A. Current concepts for the biological basis of dental implants: Foreign body equilibrium and osseointegration dynamics. Oral Maxillofac. Surg. Clin. N. Am. 2015, 27, 175–183. [Google Scholar] [CrossRef] [PubMed]
- Hamlet, S.; Ivanovski, S. Inflammatory Cytokine Response to Titanium Surface Chemistry and Topography. In The Immune Response to Implanted Materials and Devices; Corradetti, B., Ed.; Springer: Cham, Switzerland, 2017; pp. 151–167. ISBN 978-3-319-45433-7. [Google Scholar]
- Wennerberg, A.; Albrektsson, T. Current challenges in successful rehabilitation with oral implants. J. Oral Rehabil. 2011, 38, 286–294. [Google Scholar] [CrossRef] [PubMed]
- Trindade, R.; Albrektsson, T.; Galli, S.; Prgomet, Z.; Tengvall, P.; Wennerberg, A. Osseointegration and foreign body reaction: Titanium implants activate the immune system and suppress bone resorption during the first 4 weeks after implantation. Clin. Implant Dent. Relat. Res. 2018, 20, 82–91. [Google Scholar] [CrossRef]
- Albrektsson, T.; Dahlin, C.; Jemt, T.; Sennerby, L.; Turri, A.; Wennerberg, A. Is marginal bone loss around oral implants the result of a provoked foreign body reaction? Clin. Implant Dent. Relat. Res. 2014, 16, 155–165. [Google Scholar] [CrossRef] [PubMed]
- Chrcanovic, B.R.; Kisch, J.; Albrektsson, T.; Wennerberg, A. A retrospective study on clinical and radiological outcomes of oral implants in patients followed up for a minimum of 20 years. Clin. Implant Dent. Relat. Res. 2018, 20, 199–207. [Google Scholar] [CrossRef] [PubMed]
- Trindade, R.; Albrektsson, T.; Tengvall, P.; Wennerberg, A. Foreign Body Reaction to Biomaterials: On Mechanisms for Buildup and Breakdown of Osseointegration. Clin. Implant Dent. Relat. Res. 2016, 18, 192–203. [Google Scholar] [CrossRef] [PubMed]
- Albrektsson, T.; Canullo, L.; Cochran, D.; De Bruyn, H. “Peri-Implantitis”: A Complication of a Foreign Body or a Man-Made “Disease”. Facts and Fiction. Clin. Implant Dent Relat. Res. 2016, 18, 840–849. [Google Scholar] [CrossRef] [PubMed]
- Scarritt, M.E.; Londono, R.; Badylak, S.F. Host Response to Implanted Materials and Devices: An Overview. In The Immune Response to Implanted Materials and Devices; Corradetti, B., Ed.; Springer: Cham, Switzerland, 2017; pp. 1–14. ISBN 978-3-319-45433-7. [Google Scholar]
- Hotchkiss, K.M.; Ayad, N.B.; Hyzy, S.L.; Boyan, B.D.; Olivares-Navarrete, R. Dental implant surface chemistry and energy alter macrophage activation in vitro. Clin. Oral Implants Res. 2017, 28, 414–423. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Mao, X.; Tan, L.; Friis, T.; Wu, C.; Crawford, R.; Xiao, Y. Osteoimmunomodulatory properties of magnesium scaffolds coated with β-tricalcium phosphate. Biomaterials 2014, 35, 8553–8565. [Google Scholar] [CrossRef]
- Sato, T.; Pajarinen, J.; Behn, A.; Jiang, X.; Lin, T.H.; Loi, F.; Yao, Z.; Egashira, K.; Yang, F.; Goodman, S.B. The effect of local IL-4 delivery or CCL2 blockade on implant fixation and bone structural properties in a mouse model of wear particle induced osteolysis. J. Biomed. Mater. Res. A 2016, 104, 2255–2262. [Google Scholar] [CrossRef]
- Nojehdehi, S.; Soudi, S.; Hesampour, A.; Rasouli, S.; Soleimani, M.; Hashemi, S.M. Immunomodulatory effects of mesenchymal stem cell-derived exosomes on experimental type-1 autoimmune diabetes. J. Cell Biochem. 2018, 119, 9433–9443. [Google Scholar] [CrossRef] [PubMed]
- Amengual-Peñafiel, L.; Jara-Sepúlveda, M.C.; Parada-Pozas, L.; Marchesani-Carrasco, F.; Cartes-Velásquez, R.; Galdames-Gutiérrez, B. Immunomodulation of Osseointegration Through Extracorporeal Shock Wave Therapy. Dent. Hypotheses 2018, 9, 45–50. [Google Scholar] [CrossRef]
- Van der Meulen, M.C.; Huiskes, R. Why mechanobiology? A survey article. J. Biomech. 2002, 35, 401–404. [Google Scholar] [CrossRef]
- Yusko, E.C.; Asbury, C.L. Force is a signal that cells cannot ignore. Mol. Biol. Cell 2014, 25, 3717–3725. [Google Scholar] [CrossRef] [PubMed]
- Zhao, L.; Wu, Z.; Zhang, Y. Low-magnitude mechanical vibration may be applied clinically to promote dental implant osseointegration. Med. Hypotheses 2009, 72, 451–452. [Google Scholar] [CrossRef] [PubMed]
- Mennens, S.F.B.; van den Dries, K.; Cambi, A. Role for Mechanotransduction in Macrophage and Dendritic Cell Immunobiology. Results Probl. Cell Differ. 2017, 62, 209–242. [Google Scholar] [CrossRef] [PubMed]
- Zetao, C.; Travis, K.; Rachael, M.; Ross, C.; Jiang, C.; Chengtie, W.; Yin, X. Osteoimmunomodulation for the development of advanced bone biomaterials. Mater. Today 2016, 19, 304–321. [Google Scholar] [CrossRef]
- Albrektsson, T.; Chrcanovic, B.; Östman, P.O.; Sennerby, L. Initial and long-term crestal bone responses to modern dental implants. Periodontol. 2000 2017, 73, 41–50. [Google Scholar] [CrossRef]
- Zhao, E.; Xu, H.; Wang, L.; Kryczek, I.; Wu, K.; Hu, Y.; Wang, G.; Zou, W. Bone marrow and the control of immunity. Cell Mol. Immunol. 2012, 9, 11–19. [Google Scholar] [CrossRef]
- Calvi, L.M.; Adams, G.B.; Weibrecht, K.W.; Weber, J.M.; Olson, D.P.; Knight, M.C.; Martin, R.P.; Schipani, E.; Divieti, P.; Bringhurst, F.R.; et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425, 841–846. [Google Scholar] [CrossRef] [PubMed]
- Kikuta, J.; Ishii, M. Osteoclast migration, differentiation and function: Novel therapeutic targets for rheumatic diseases. Rheumatology 2013, 52, 226–234. [Google Scholar] [CrossRef] [PubMed]
- Mazo, I.B.; Honczarenko, M.; Leung, H.; Cavanagh, L.L.; Bonasio, R.; Weninger, W. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity 2005, 22, 259–270. [Google Scholar] [CrossRef] [PubMed]
- Arboleya, L.; Castañeda, S. Osteoimmunology. Reumatol. Clin. 2013, 9, 303–315. [Google Scholar] [CrossRef] [PubMed]
- Monroe, D.G.; McGee-Lawrence, M.E.; Oursler, M.J.; Westendorf, J.J. Update on Wnt signaling in bone cell biology and bone disease. Gene 2012, 492, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Theill, L.E.; Boyle, W.J.; Penninger, J.M. RANK-L and RANK: T cell, bone loss and mammalian evolution. Annu. Rev. Immunol. 2002, 20, 795–823. [Google Scholar] [CrossRef] [PubMed]
- Srivastava, R.K.; Dar, H.Y.; Mishra, P.K. Immunoporosis: Immunology of Osteoporosis-Role of T Cells. Front. Immunol. 2018, 9, 657. [Google Scholar] [CrossRef] [PubMed]
- Alnaeeli, M.; Park, J.; Mahamed, D.; Penninger, J.M.; Teng, Y.T. Dendritic cells at the osteo-immune interface: Implications for inflammation-induced bone loss. J. Bone Miner. Res. 2007, 22, 775–780. [Google Scholar] [CrossRef] [PubMed]
- Caetano-Lopes, J.; Canhão, H.; Fonseca, J.E. Osteoimmunology-the hidden immune regulation of bone. Autoimmun. Rev. 2009, 8, 250–255. [Google Scholar] [CrossRef]
- Kaur, S.; Raggatt, L.J.; Batoon, L.; Hume, D.A.; Levesque, J.P.; Pettit, A.R. Role of bone marrow macrophages in controlling homeostasis and repair in bone and bone marrow niches. Semin. Cell Dev. Biol. 2017, 61, 12–21. [Google Scholar] [CrossRef]
- Batoon, L.; Millard, S.M.; Raggatt, L.J.; Pettit, A.R. Osteomacs and Bone Regeneration. Curr. Osteoporos. Rep. 2017, 15, 385–395. [Google Scholar] [CrossRef]
- Chang, M.K.; Raggatt, L.J.; Alexander, K.A.; Kuliwaba, J.S.; Fazzalari, N.L.; Schroder, K.; Maylin, E.R.; Ripoll, V.M.; Hume, D.A.; Pettit, A.R. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J. Immunol. 2008, 181, 1232–1244. [Google Scholar] [CrossRef] [PubMed]
- Raggatt, L.J.; Wullschleger, M.E.; Alexander, K.A.; Wu, A.C.; Millard, S.M.; Kaur, S.; Maugham, M.L.; Gregory, L.S.; Steck, R.; Pettit, A.R. Fracture healing via periosteal callus formation requires macrophages for both initiation and progression of early endochondral ossification. Am. J. Pathol. 2014, 184, 3192–3204. [Google Scholar] [CrossRef] [PubMed]
- Andrew, J.G.; Andrew, S.M.; Freemont, A.J.; Marsh, D.R. Inflammatory cells in normal human fracture healing. Acta Orthop. Scand. 1994, 65, 462–466. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.M.; Cramer, S. Perspectives on the inflammatory, healing, and foreign body responses to biomaterials and medical devices. In Host Response to Biomaterials. The Impact of Host Response on Biomaterial Selection; Badylak, S., Ed.; Elsevier: New York, NY, USA, 2015; pp. 13–36. ISBN 9780128001967. [Google Scholar]
- Hosgood, G. Wound healing. The role of platelet-derived growth factor and transforming growth factor beta. Vet. Surg. 1993, 22, 490–495. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.M.; Jiang, S. Implications of the Acute and Chronic Inflammatory Response and the Foreign Body Reaction to the Immune Response of Implanted Biomaterials. In The Immune Response to Implanted Materials and Devices; Corradetti, B., Ed.; Springer: Cham, Switzerland, 2017; pp. 15–36. ISBN 978-3-319-45433-7. [Google Scholar]
- Hu, W.J.; Eaton, J.W.; Ugarova, T.P.; Tang, L. Molecular basis of biomaterial-mediated foreign body reaction. Blood 2001, 98, 1231–1238. [Google Scholar] [CrossRef] [PubMed]
- Christo, S.N.; Diener, K.R.; Bachhuka, A.; Vasilev, K.; Hayball, J.D. Innate Immunity and Biomaterials at the Nexus: Friends or Foes. BioMed Res. Int. 2015. [Google Scholar] [CrossRef]
- Arvidsson, S.; Askendal, A.; Tengvall, P. Blood plasma contact activation on silicon, titanium, and aluminum. Biomaterials 2007, 28, 1346–1354. [Google Scholar] [CrossRef]
- Mills, C.D.; Kincaid, K.; Alt, J.M.; Heilman, M.J.; Hill, A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 2000, 164, 6166–6173. [Google Scholar] [CrossRef]
- Mosser, D.M.; Edwards, J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8, 958–969. [Google Scholar] [CrossRef]
- Lucas, T.; Waisman, A.; Ranjan, R.; Roes, J.; Krieg, T.; Müller, W.; Roers, A.; Eming, S.A. Differential roles of macrophages in diverse phases of skin repair. J. Immunol. 2010, 184, 3964–3977. [Google Scholar] [CrossRef]
- Trindade, R.; Albrektsson, T.; Tengvall, P.; Wennerberg, A. Bone immune response to Titanium, PEEK and Copper- Osseointegration and the Immune-inflammatory balance. Clin. Oral Implants Res. 2018, 29, 138. [Google Scholar] [CrossRef][Green Version]
- Anderson, J.M.; Rodriguez, D.T.; Chang, A. Foreign body reaction to biomaterials. Semin. Immunol. 2008, 20, 86–100. [Google Scholar] [CrossRef] [PubMed]
- Barbeck, M.; Booms, P.; Unger, R.; Hoffmann, V.; Sader, R.; Kirkpatrick, C.J.; Ghanaati, S. Multinucleated giant cells in the implant bed of bone substitutes are foreign body giant cells-New insights into the material-mediated healing process. J. Biomed. Mater. Res. A 2017, 105, 1105–1111. [Google Scholar] [CrossRef] [PubMed]
- Scatena, M.; Eaton, K.V.; Jackson, M.F.; Lund, S.A.; Giachelli, C.M. Macrophages: The Bad, the Ugly, and the Good in the Inflammatory Response to Biomaterials. In The Immune Response to Implanted Materials and Devices; Corradetti, B., Ed.; Springer: Cham, Switzerland, 2017; pp. 37–62. ISBN 978-3-319-45433-7. [Google Scholar]
- Donath, K.; Laass, M.; Günzl, H.J. The histopathology of different foreign body reactions in oral soft tissue and bone tissue. Virchows Arch. A Pathol. Anat. Histopathol. 1992, 420, 131–137. [Google Scholar] [CrossRef] [PubMed]
- Vigneri, A. Macrophage fusion: Molecular mechanisms. Methods Mol. Biol. 2008, 475, 149–161. [Google Scholar] [CrossRef]
- Romagnani, S. T-cell subsets [Th1 versus Th2]. Ann. Allergy Asthma Immunol. 2000, 85, 9–18. [Google Scholar] [CrossRef]
- Lin, T.; Jämsen, E.; Lu, L.; Nathan, K.; Pajarinen, J.; Goodman, S. Modulating Innate Inflammatory Reactions in the Application of Orthopedic Biomaterials. In Progress in Biology, Manufacturing, and Industry Perspectives; Li, B., Webster, T., Eds.; Springer: Cham, Switzerland, 2018; pp. 199–218. ISBN 978-3-319-89542-0. [Google Scholar]
- Biguetti, C.C.; Cavalla, F.; Silveira, E.M.; Fonseca, A.C.; Vieira, A.E.; Tabanez, A.P.; Rodrigues, D.C.; Trombone, A.P.F.; Garlet, G.P. Oral implant osseointegration model in C57Bl/6 mice: Microtomographic, histological, histomorphometric and molecular characterization. J. Appl. Oral Sci. 2018, 26, e20170601. [Google Scholar] [CrossRef]
- Dohan Ehrenfest, D.M.; Del Corso, M.; Kang, B.; Leclercq, P.; Mazor, Z.; Horowitz, R.A.; Russe, P.; Oh, H.; Zou, D.; Shibli, J.A.; et al. Identification card and codification of the chemical and morphological characteristics of 62 dental implant surfaces. Part 3: Sand-blasted/acid-etched [SLA type] and related surfaces [Group 2A, main subtractive process]. POSEIDO 2014, 2, 37–55. [Google Scholar]
- Clean Implant. Available online: http://www.cleanimplant.com/ (accessed on 25 November 2018).
- Konttinen, Y.T.; Pajarinen, J.; Takakubo, Y.; Gallo, J.; Nich, C.; Takagi, M.; Goodman, S.B. Macrophage polarization and activation in response to implant debris: Influence by “particle disease” and “ion disease”. J. Long Term Eff. Med. Implants 2014, 24, 267–281. [Google Scholar] [CrossRef]
- Albrektsson, T.; Chrcanovic, B.; Mölne, J.; Wennerberg, A. Foreign body reactions, marginal bone loss and allergies to titanium implants. Eur. J. Oral Implantol. 2018, 11, S37–S46. [Google Scholar]
- Høl, P.J.; Kristoffersen, E.K.; Gjerdet, N.R.; Pellowe, A.S. Novel Nanoparticulate and Ionic Titanium Antigens for Hypersensitivity Testing. Int. J. Mol. Sci. 2018, 19, 1101. [Google Scholar] [CrossRef]
- Goodman, S.B.; Gibon, E.; Pajarinen, J.; Lin, T.H.; Keeney, M.; Ren, P.G.; Nich, C.; Yao, Z.; Egashira, K.; Yang, F.; et al. Novel biological strategies for treatment of wear particle-induced periprosthetic osteolysis of orthopaedic implants for joint replacement. J. R. Soc. Interface 2014, 11, 20130962. [Google Scholar] [CrossRef]
- Xu, L.C.; Siedlecki, C.A. Effects of surface wettability and contact time on protein adhesion to biomaterial surfaces. Biomaterials 2007, 28, 3273–3283. [Google Scholar] [CrossRef]
- Luu, T.U.; Gott, S.C.; Woo, B.W.; Rao, M.P.; Liu, W.F. Micro- and Nanopatterned Topographical Cues for Regulating Macrophage Cell Shape and Phenotype. ACS Appl. Mater. Interfaces 2015, 7, 28665–28672. [Google Scholar] [CrossRef] [PubMed]
- Thompson, W.R.; Rubin, C.T.; Rubin, J. Mechanical regulation of signaling pathways in bone. Gene 2012, 503, 179–193. [Google Scholar] [CrossRef] [PubMed]
- Vasconcelos, D.M.; Santos, S.G.; Lamghari, M.; Barbosa, M.A. The two faces of metal ions: From implants rejection to tissue repair/regeneration. Biomaterials 2016, 84, 262–275. [Google Scholar] [CrossRef] [PubMed]
- Martinez, F.O.; Sica, A.; Mantovani, A.; Locati, M. Macrophage activation and polarization. Front. Biosci. 2008, 13, 453–461. [Google Scholar] [CrossRef]
- Gilbert, L.; He, X.; Farmer, P.; Boden, S.; Kozlowski, M.; Rubin, J.; Nanes, M.S. Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 2000, 141, 3956–3964. [Google Scholar] [CrossRef] [PubMed]
- Lin, T.H.; Pajarinen, J.; Sato, T.; Loi, F.; Fan, C.; Cordova, L.A.; Nabeshima, A.; Gibon, E.; Zhang, R.; Yao, Z.; et al. NF-kappaB decoy oligodeoxynucleotide mitigates wear particle-associated bone loss in the murine continuous infusion model. Acta Biomater. 2016, 41, 273–281. [Google Scholar] [CrossRef]
- Kumar, V.A.; Taylor, N.L.; Shi, S.; Wickremasinghe, N.C.; D’Souza, R.N.; Hartgerink, J.D. Selfassembling multidomain peptides tailor biological responses through biphasic release. Biomaterials 2015, 52, 71–78. [Google Scholar] [CrossRef]
- Viganò, M.; Sansone, V.; d’Agostino, M.C.; Romeo, P.; Perucca Orfei, C.; de Girolamo, L. Mesenchymal stem cells as therapeutic target of biophysical stimulation for the treatment of musculoskeletal disorders. J. Orthop. Surg. Res. 2016, 11, 163. [Google Scholar] [CrossRef] [PubMed]
- Gao, F.; Chiu, S.M.; Motan, D.A.; Zhang, Z.; Chen, L.; Ji, H.L.; Tse, H.F.; Fu, Q.-L.; Lian, Q. Mesenchymal Stem Cell and Immunomodulation: Current Status and Future Prospects. Cell Death Dis. 2016, 7, e2062. [Google Scholar] [CrossRef] [PubMed]
- Guilak, F.; Cohen, D.M.; Estes, B.T.; Gimble, J.M.; Liedtke, W.; Chen, C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5, 17–26. [Google Scholar] [CrossRef] [PubMed]
- Carver, W.; Esch, A.M.; Fowlkes, V.; Goldsmith, E.C. The Biomechanical Environment and Impact on Tissue Fibrosis. In The Immune Response to Implanted Materials and Devices; Corradetti, B., Ed.; Springer: Cham, Switzerland, 2017; pp. 169–188. ISBN 978-3-319-45433-7. [Google Scholar]
- Leung, D.Y.; Glagov, S.; Mathews, M.B. Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science 1976, 191, 475–477. [Google Scholar] [CrossRef] [PubMed]
- Dunn, S.L.; Olmedo, M.L. Mechanotransduction: Relevance to physical therapist practice—Understanding our ability to affect genetic expression through mechanical forces. Phys. Ther. 2016, 96, 712–721. [Google Scholar] [CrossRef] [PubMed]
- Ingber, D.E. Tensegrity: The architectural basis of cellular mechanotransduction. Annu. Rev. Physiol. 1997, 59, 575–599. [Google Scholar] [CrossRef] [PubMed]
- MacKenna, D.A.; Dolfi, F.; Vuori, K.; Ruoslahti, E. Extracellular signal-regulated kinase and c-Jun NH2-terminal kinase activation by mechanical stretch is integrin-dependent and matrix specific in rat cardiac fibroblasts. J. Clin. Investig. 1998, 101, 301–310. [Google Scholar] [CrossRef] [PubMed]
- Ghoveizi, R.; Alikhasi, M.; Siadat, M.R.; Siadat, H.; Sorouri, M. A radiographic comparison of progressive and conventional loading on crestal bone loss and density in single dental implants: A randomized controlled trial study. J. Dent. 2013, 10, 155–163. [Google Scholar]
- Piattelli, A.; Corigliano, M.; Scarano, A.; Costigliola, G.; Paolantonio, M. Immediate loading of titanium plasma-sprayed implants: An histologic analysis in monkeys. J. Periodontol. 1998, 69, 321–327. [Google Scholar] [CrossRef]
- Huang, H.; Wismeijer, D.; Shao, X.; Wu, G. Mathematical evaluation of the influence of multiple factors on implant stability quotient values in clinical practice: A retrospective study. Ther. Clin. Risk Manag. 2016, 12, 1525–1532. [Google Scholar] [CrossRef]
- Sennerby, L.; Ericson, L.E.; Thomsen, P.; Lekholm, U.; Astrand, P. Structure of the bone-titanium interface in retrieved clinical oral implants. Clin. Oral Implants Res. 1991, 2, 103–111. [Google Scholar] [CrossRef] [PubMed]
- Duyck, J.; Cooman, M.D.; Puers, R.; van Oosterwyck, H.; Sloten, J.V.; Naert, I. A repeated sampling bone chamber methodology for the evaluation of tissue differentiation and bone adaptation around titanium implants under controlled mechanical conditions. J. Biomech. 2004, 37, 1819–1822. [Google Scholar] [CrossRef] [PubMed]
- Ogden, J.A.; Tóth-Kischkat, A.; Schultheiss, R. Principles of shock wave therapy. Clin. Orthop. Relat. Res. 2001, 387, 8–17. [Google Scholar] [CrossRef]
- Van der Jagt, O.P.; Waarsing, J.H.; Kops, N.; Schaden, W.; Jahr, H.; Verhaar, J.A.; Weinans, H. Unfocused extracorporeal shock waves induce anabolic effects in osteoporotic rats. JBJS 2011, 93, 38–48. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.J. Extracorporeal shockwave therapy in musculoskeletal disorders. J. Orthop. Surg. Res. 2012, 7, 11. [Google Scholar] [CrossRef] [PubMed]
- Iro, H.; Schneider, H.T.; Födra, C.; Waitz, G.; Nitsche, N.; Heinritz, H.H.; Benninger, J.; Ell, C. Shockwave lithotripsy of salivary duct stones. Lancet 1992, 339, 1333–1336. [Google Scholar] [CrossRef]
- Kraus, M.; Reinhart, E.; Krause, H.; Reuther, J. Low energy extracorporeal shockwave therapy [ESWT] for treatment of myogelosis of the masseter muscle. Mund-Kiefer Gesichtschir. 1999, 3, 20–23. [Google Scholar] [CrossRef]
- Falkensammer, F.; Rausch-Fan, X.; Schaden, W.; Kivaranovic, D.; Freudenthaler, J. Impact of extracorporeal shockwave therapy on tooth mobility in adult orthodontic patients: A randomized singlecenter placebo-controlled clinical trial. J. Clin. Periodontol. 2015, 42, 294–301. [Google Scholar] [CrossRef]
- Falkensammer, F.; Schaden, W.; Krall, C.; Freudenthaler, J.; Bantleon, H.P. Effect of extracorporeal shockwave therapy [ESWT] on pulpal blood flow after orthodontic treatment: A randomized clinical trial. Clin. Oral Investig. 2016, 20, 373–379. [Google Scholar] [CrossRef]
- Holfeld, J.; Tepeköylü, C.; Reissig, C.; Lobenwein, D.; Scheller, B.; Kirchmair, E.; Kozaryn, R.; Albrecht-Schgoer, K.; Krapf, C.; Zins, K.; et al. Toll-like receptor 3 signalling mediates angiogenic response upon shock wave treatment of ischaemic muscle. Cardiovasc. Res. 2016, 109, 331–343. [Google Scholar] [CrossRef]
- Goiato, M.C.; dos Santos, D.M.; Santiago, J.F.; Moreno, A.; Pellizzer, E.P. Longevity of dental implants in type IV bone: A systematic review. Int. J. Oral Maxillofac. Surg. 2014, 43, 1108–1116. [Google Scholar] [CrossRef] [PubMed]
- De Medeiros, F.C.F.L.; Kudo, G.A.H.; Leme, B.G.; Saraiva, P.P.; Verri, F.R.; Honório, H.M.; Pellizzer, E.P.; Santiago, J.F. Dental implants in patients with osteoporosis: A systematic review with meta-analysis. Int. J. Oral Maxillofac. Surg. 2018, 47, 480–491. [Google Scholar] [CrossRef] [PubMed]
- Koolen, M.K.E.; Kruyt, M.C.; Zadpoor, A.A.; Öner, F.C.; Weinans, H.; van der Jagt, O.P. Optimization of screw fixation in rat bone with extracorporeal shock waves. J. Orthop. Res. 2018, 36, 76–84. [Google Scholar] [CrossRef] [PubMed]
- Van der Jagt, O.P.; Piscaer, T.M.; Schaden, W.; Li, J.; Kops, N.; Jahr, H.; van der Linden, J.C.; Waarsing, J.H.; Verhaar, J.A.; de Jong, M.; Weinans, H. Unfocused extracorporeal shock waves induce anabolic effects in rat bone. J. Bone Jt. Surg. Am. 2011, 93, 38–48. [Google Scholar] [CrossRef] [PubMed]
- Koolen, M.K.E.; Pouran, B.; Öner, F.C.; Zadpoor, A.A.; van der Jagt, O.P.; Weinans, H. Unfocused shockwaves for osteoinduction in bone substitutes in rat cortical bone defects. PLoS ONE 2018, 13, e0200020. [Google Scholar] [CrossRef] [PubMed]
- Loske, A.M. Extracorporeal Shock Wave Therapy, Shock Wave and High Pressure Phenomena. Bone Healing. In Medical and Biomedical Applications of Shock Waves; Loske, A.M., Ed.; Springer International Publishing: New York, NY, USA, 2017; p. 222. ISBN 978-3-319-47570-7. [Google Scholar]
- Deb, S.; Chana, S. Biomaterials in Relation to Dentistry. Front. Oral Biol. 2015, 17, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Hou, Y.; Zhou, X.; Cai, W.L.; Guo, C.C.; Han, Y. Regulatory effect of bone marrow mesenchymal stem cells on polarization of macrophages. Zhonghua Gan Zang Bing Za Zhi 2017, 25, 273–278. [Google Scholar] [CrossRef]
- English, K.; French, A.; Wood, K.J. Mesenchymal stromal cells: Facilitators of successful transplantation? Cell Stem Cell 2010, 7, 431–442. [Google Scholar] [CrossRef]
- Suhr, F.; Delhasse, Y.; Bungartz, G.; Schmidt, A.; Pfannkuche, K.; Bloch, W. Cell biological effects of mechanical stimulations generated by focused extracorporeal shock wave applications on cultured human bone marrow stromal cells. Stem Cell Res. 2013, 11, 951–964. [Google Scholar] [CrossRef]
- Leu, S.; Huang, T.H.; Chen, Y.L.; Yip, H.K. Effect of Extracorporeal Shockwave on Angiogenesis and Anti-Inflammation: Molecular-Cellular Signaling Pathways. In Shockwave Medicine; Wang, C.J., Schaden, W., Ko, J.Y., Eds.; Karger: Basel, Switzerland, 2018; Volume 6, pp. 109–116. [Google Scholar] [CrossRef]
- Sukubo, N.G.; Tibalt, E.; Respizzi, S.; Locati, M.; d’Agostino, M.C. Effect of shock waves on macrophages: A possible role in tissue regeneration and remodeling. Int. J. Surg. 2015, 24, 124–130. [Google Scholar] [CrossRef]
- Godwin, J.W.; Pinto, A.R.; Rosenthal, N.A. Macrophages required for regeneration. Proc. Natl. Acad. Sci. USA 2013, 110, 9415–9420. [Google Scholar] [CrossRef] [PubMed]
- Mishra, S.K.; Chowdhary, R.; Chrcanovic, B.R.; Brånemark, P.I. Osseoperception in Dental Implants: A Systematic Review. J. Prosthodont. 2016, 25, 185–195. [Google Scholar] [CrossRef] [PubMed]
- He, H.; Yao, Y.; Wang, Y.; Wu, Y.; Yang, Y.; Gong, P. A novel bionic design of dental implant for promoting its long-term success using nerve growth factor [NGF]: Utilizing nano-springs to construct a stress-cushioning structure inside the implant. Med. Sci. Monit. 2012, 18, HY42–HY46. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Lee, J.H.; Sung, Y.B.; Jang, S.H. Nerve growth factor expression in stroke induced rats after shock wave. J. Phys. Ther. Sci. 2016, 28, 3451–3453. [Google Scholar] [CrossRef] [PubMed]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Amengual-Peñafiel, L.; Brañes-Aroca, M.; Marchesani-Carrasco, F.; Jara-Sepúlveda, M.C.; Parada-Pozas, L.; Cartes-Velásquez, R. Coupling between Osseointegration and Mechanotransduction to Maintain Foreign Body Equilibrium in the Long-Term: A Comprehensive Overview. J. Clin. Med. 2019, 8, 139. https://doi.org/10.3390/jcm8020139
Amengual-Peñafiel L, Brañes-Aroca M, Marchesani-Carrasco F, Jara-Sepúlveda MC, Parada-Pozas L, Cartes-Velásquez R. Coupling between Osseointegration and Mechanotransduction to Maintain Foreign Body Equilibrium in the Long-Term: A Comprehensive Overview. Journal of Clinical Medicine. 2019; 8(2):139. https://doi.org/10.3390/jcm8020139
Chicago/Turabian StyleAmengual-Peñafiel, Luis, Manuel Brañes-Aroca, Francisco Marchesani-Carrasco, María Costanza Jara-Sepúlveda, Leopoldo Parada-Pozas, and Ricardo Cartes-Velásquez. 2019. "Coupling between Osseointegration and Mechanotransduction to Maintain Foreign Body Equilibrium in the Long-Term: A Comprehensive Overview" Journal of Clinical Medicine 8, no. 2: 139. https://doi.org/10.3390/jcm8020139
APA StyleAmengual-Peñafiel, L., Brañes-Aroca, M., Marchesani-Carrasco, F., Jara-Sepúlveda, M. C., Parada-Pozas, L., & Cartes-Velásquez, R. (2019). Coupling between Osseointegration and Mechanotransduction to Maintain Foreign Body Equilibrium in the Long-Term: A Comprehensive Overview. Journal of Clinical Medicine, 8(2), 139. https://doi.org/10.3390/jcm8020139