Osteoimmunology drives dental implant osseointegration: A new paradigm for implant dentistry

Japanese Dental Science Review - Tập 57 - Trang 12-19 - 2021
Luis Amengual-Peñafiel1, Luis A. Córdova2,3,4, M. Constanza Jara-Sepúlveda5, Manuel Brañes-Aroca6, Francisco Marchesani-Carrasco7, Ricardo Cartes-Velásquez8
1Dental Implantology Unit, Hospital Leonardo Guzmán, Antofagasta, Chile
2Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, University of Chile, Chile
3Department of Oral and Maxillofacial Surgery, Clínica Las Condes, Santiago, Chile
4Department of Oral and Maxillofacial Surgery, Complejo Hospitalario San José. Craneofacial Translational Research Laboratory, Faculty of Dentistry, University of Chile, Santiago, Chile
5Private Practice, Antofagasta, Chile
6Faculty of Sciences, University of Chile, Santiago, Chile
7Clínica Marchesani, Concepción, Chile
8Fundación Kimntrum, Concepción, Chile

Tài liệu tham khảo

Albrektsson, 2017, Osseointegration of implants- a biological and clinical overview, JSM Dent Surg, 2, 1022 Trindade, 2018, 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, 20, 82, 10.1111/cid.12578 Albrektsson, 2019, On inflammation-immunological balance theory-A critical apprehension of disease concepts around implants: mucositis and marginal bone loss may represent normal conditions and not necessarily a state of disease, Clin Implant Dent Relat Res, 21, 183, 10.1111/cid.12711 Albrektsson, 2014, Is marginal bone loss around oral implants the result of a provoked foreign body reaction?, Clin Implant Dent Relat Res, 16, 155, 10.1111/cid.12142 Iismaa, 2018, Comparative regenerative mechanisms across different mammalian tissues, NPJ Regen Med, 3, 6, 10.1038/s41536-018-0044-5 Godwin, 2013, Macrophages required for regeneration, Proc Natl Acad Sci U S A, 110, 9415, 10.1073/pnas.1300290110 Limmer, 2017, Osteoimmunology: influence of the immune system on bone regeneration and consumption, Z Orthop Unfall, 155, 273, 10.1055/s-0043-100100 Albrektsson, 1987, Osseointegration of bone implants: a review of an alternative mode of fixation, Acta Orthop Scand, 58, 567, 10.3109/17453678709146401 Rahal, 2000, Myelointegration of titanium implants: B lymphopoiesis and hemopoietic cell proliferation in mouse bone marrow exposed to titanium implants, Int J Oral Maxillofac Implants, 15, 175 Zhao, 2012, Bone marrow and the control of immunity, Cell Mol Immunol, 9, 11, 10.1038/cmi.2011.47 Amengual-Peñafiel, 2019, Coupling between Osseointegration and mechanotransduction to maintain foreign body equilibrium in the long-term: a comprehensive overview, J Clin Med, 8, 10.3390/jcm8020139 Tsukasaki, 2019, Osteoimmunology: evolving concepts in bone–immune interactions in health and disease, Nat Rev Immunol, 19, 626, 10.1038/s41577-019-0178-8 Kim, 2019, Intravital multiphoton imaging of the bone and bone marrow environment, Cytom Part A, 97, 496, 10.1002/cyto.a.23937 Furuya, 2018, Direct cell-cell contact between mature osteoblasts and osteoclasts dynamically controls their functions in vivo, Nat Commun, 9, 10.1038/s41467-017-02541-w Kumar, 2019, From crosstalk between immune and bone cells to bone erosion in infection, Int J Mol Sci, 20, 5154, 10.3390/ijms20205154 Ponzetti, 2019, Updates on osteoimmunology: what’s new on the cross-talk between bone and immune system, Front Endocrinol, 10, 236, 10.3389/fendo.2019.00236 Blin-Wakkach, 2019, Advances in osteoimmunology, Front Immunol, 10, 2595, 10.3389/fimmu.2019.02595 Trindade, 2015, Current concepts for the biological basis of dental implants: foreign body equilibrium and osseointegration dynamics, Oral Maxillofac Surg Clin North Am, 27, 175, 10.1016/j.coms.2015.01.004 Zetao, 2016, Osteoimmunomodulation for the development of advanced bone biomaterials, Mater Today, 19, 304, 10.1016/j.mattod.2015.11.004 Hoellwarth, 2020, Osseointegration for amputees: current implants, techniques, and future directions, JBJS Rev, 8, 10.2106/JBJS.RVW.19.00043 Simkin, 2017, Macrophages are necessary for epimorphic regeneration in African spiny mice, eLife, 16 Dimitriou, 2011, Bone regeneration: current concepts and future directions, BMC Med, 9 Shrivats, 2014, Bone tissue engineering: state of the union, Drug Discov Today, 19, 781, 10.1016/j.drudis.2014.04.010 Mescher, 2017, Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration, Regeneration, 4, 39, 10.1002/reg2.77 Oishi, 2018, Macrophages in inflammation, repair and regeneration, Int Immunol, 30, 511, 10.1093/intimm/dxy054 Mescher, 2017, Macrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration, Regeneration, 4, 39, 10.1002/reg2.77 Simkina, 2019, Healing power: the mammalian macrophage in skeletal regeneration, scar formation, and regenerative medicine, J Regen, 2, 93 Wu, 2020, The role of macrophages in osteoarthritis and cartilage repair, Osteoarthr Cartil, 28, 544, 10.1016/j.joca.2019.12.007 Goodman, 2014, Novel biological strategies for treatment of wear particle-induced periprosthetic osteolysis of orthopaedic implants for joint replacement, J R Soc Interface, 11, 10.1098/rsif.2013.0962 Trindade, 2018, Bone immune response to materials, part I: titanium, PEEK and copper in comparison to sham at 10 days in Rabbit Tibia, J Clin Med, 7, 526, 10.3390/jcm7120526 Trindade, 2019, Bone immune response to materials, part II: copper and polyetheretherketone (PEEK) compared to titanium at 10 and 28 days in rabbit tibia, J Clin Med, 8, 814, 10.3390/jcm8060814 Gong, 2016, The macrophage polarization regulates MSC osteoblast differentiation in vitro, Ann Clin Lab Sci Winter, 46, 65 Pajarinen, 2019, Mesenchymal stem cell-macrophage crosstalk and bone healing, Biomaterials, 196, 80, 10.1016/j.biomaterials.2017.12.025 Schlundt, 2018, Macrophages in bone fracture healing: their essential role in endochondral ossification, Bone, 106, 78, 10.1016/j.bone.2015.10.019 Zhang, 2018, M2 macrophages are closely associated with accelerated clavicle fracture healing in patients with traumatic brain injury: a retrospective cohort study, J Orthop Surg Res, 13, 213, 10.1186/s13018-018-0926-7 Wong, 2020, Parallels between wound healing, epimorphic regeneration and solid tumors, Development, 147, 10.1242/dev.181636 Wynn, 2013, Macrophage biology in development, homeostasis and disease, Nature, 496, 445, 10.1038/nature12034 Cosin-Roger, 2019, Macrophages as an emerging source of wnt ligands: relevance in mucosal integrity, Front Immunol, 10, 2297, 10.3389/fimmu.2019.02297 Li, 2017, Relationships among bone quality, implant osseointegration, and wnt signaling, J Dent Res, 96, 822, 10.1177/0022034517700131 Houschyar, 2019, Wnt pathway in bone repair and regeneration - what do we know so far, Front Cell Dev Biol, 6, 170, 10.3389/fcell.2018.00170 Stoick-Cooper, 2007, Distinct Wnt signaling pathways have opposing roles in appendage regeneration, Development, 134, 479, 10.1242/dev.001123 Wendler, 2019, Immune modulation to enhance bone Healing-A new concept to induce bone using prostacyclin to locally modulate immunity, Front Immunol, 10, 713, 10.3389/fimmu.2019.00713 Alexander, 2017, Resting and injury-induced inflamed periosteum contain multiple macrophage subsets that are located at sites of bone growth and regeneration, Immunol Cell Biol, 95, 7, 10.1038/icb.2016.74 Yang, 2019, The role of macrophage in the pathogenesis of osteoporosis, Int J Mol Sci, 20, 2093, 10.3390/ijms20092093 Miron, 2018, Multinucleated giant cells: good guys or bad guys, Tissue Eng Part B Rev, 24, 53, 10.1089/ten.teb.2017.0242 Rossi, 2014, Bone-healing pattern at the surface of titanium implants: an experimental study in the dog, Clin Oral Implants Res, 25, 124, 10.1111/clr.12097 Ysander, 2001, Intramedullary osseointegration: development of a rodent model and study of histology and neuropeptide changes around titanium implants, J Rehabil Res Dev, 38, 183 Le, 2017, The components of bone and what they can teach us about regeneration, Materials (Basel), 11, 14, 10.3390/ma11010014 Li, 2016, The role of bone marrow microenvironment in governing the balance between Osteoblastogenesis and adipogenesis, Aging Dis, 7, 514, 10.14336/AD.2015.1206 Morelli, 2015, Influence of bone marrow on osseointegration in long bones: an experimental study in sheep, Clin Oral Implants Res, 26, 300, 10.1111/clr.12487 De Medeiros, 2018, Dental implants in patients with osteoporosis: a systematic review with meta-analysis, Int J Oral Maxillofac Surg, 47, 480, 10.1016/j.ijom.2017.05.021 Srivastava, 2018, Immunoporosis: immunology of osteoporosis-role of t cells, Front Immunol, 9, 657, 10.3389/fimmu.2018.00657 Chang, 2008, Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo, J Immunol, 181, 1232, 10.4049/jimmunol.181.2.1232 Stefanowski, 2019, Spatial distribution of macrophages during callus formation and maturation reveals close crosstalk between macrophages and newly forming vessels, Front Immunol, 10, 2588, 10.3389/fimmu.2019.02588 Batoon, 2017, Osteomacs and bone regeneration, Curr Osteoporos Rep, 15, 385, 10.1007/s11914-017-0384-x Miron, 2016, OsteoMacs: key players around bone biomaterials, Biomaterials, 82, 1, 10.1016/j.biomaterials.2015.12.017 Jennissen, 2016, A macrophage model of osseointegration, Curr Dir Biomed Eng, 2, 53, 10.1515/cdbme-2016-0015 Wang, 2020, The role of macrophages in osseointegration of dental implants: an experimental study in vivo, J Biomed Mater Res A, 10.1002/jbm.a.36978 Milde, 2015, Multinucleated giant cells are specialized for complement-mediated phagocytosis and large target destruction, Cell Rep, 13, 1937, 10.1016/j.celrep.2015.10.065 Anderson, 2008, Foreign body reaction to biomaterials, Semin Immunol, 20, 86, 10.1016/j.smim.2007.11.004 Dondossola, 2017, Examination of the foreign body response to biomaterials by nonlinear intravital microscopy, Nat Biomed Eng, 1, 0007, 10.1038/s41551-016-0007 Brodbeck, 2009, Giant cell formation and function, Curr Opin Hematol, 16, 53, 10.1097/MOH.0b013e32831ac52e Albrektsson, 2008, Hard tissue implant interface, Aust Dent J, 53, S34, 10.1111/j.1834-7819.2008.00039.x Miron, 2016, Giant cells around bone biomaterials: Osteoclasts or multi-nucleated giant cells?, Acta Biomater, 46, 15, 10.1016/j.actbio.2016.09.029 Anderson, 2015, Perspectives on the inflammatory, healing, and foreign body responses to biomaterials and medical devices, 13 Mariani, 2019, Biomaterials: foreign bodies or tuners for the immune response?, Int J Mol Sci, 20, 636, 10.3390/ijms20030636 Land, 2015, The role of damage-associated molecular patterns (DAMPs) in human diseases: part II: DAMPs as diagnostics, prognostics and therapeutics in clinical medicine, Sultan Qaboos Univ Med J, 15, e157 Biguetti, 2019, HGMB1 and RAGE as essential components of Ti osseointegration process in mice, Front Immunol, 10, 709, 10.3389/fimmu.2019.00709 Arasaki, 2020, The RNA-binding protein Cpeb4 is a novel positive regulator of osteoclast differentiation, Biochem Biophys Res Commun, 528, 621, 10.1016/j.bbrc.2020.05.089 Alvarez, 2019, Osteoimmunology of oral and maxillofacial diseases: translational applications based on biological mechanisms, Front Immunol, 10, 1664, 10.3389/fimmu.2019.01664 Hasséus, 2004, Langerhans cells from human oral epithelium are more effective at stimulating allogeneic T cells in vitro than Langerhans cells from skin, Clin Exp Immunol, 136, 483, 10.1111/j.1365-2249.2004.02469.x Chomiczewska, 2009, The role of Langerhans cells in the skin immune system, Pol Merkur Lekarski, 26, 173 Plekhova, 2017, Responses of dendritic cells to different coatings of titanium, vol 186, 165 Segura, 2013, Inflammatory dendritic cells in mice and humans, Trends Immunol, 34, 440, 10.1016/j.it.2013.06.001 Babensee, 2008, Interaction of dendritic cells with biomaterials, Semin Immunol, 20, 101, 10.1016/j.smim.2007.10.013 Kou, 2011, Macrophage and dendritic cell phenotypic diversity in the context of biomaterials, J Biomed Mater Res A, 96, 239, 10.1002/jbm.a.32971 Lapérine, 2016, Dendritic-cell-derived osteoclasts: a new game changer in bone-resorption-associated diseases, Drug Discov Today, 21, 1345, 10.1016/j.drudis.2016.04.022 Rivollier, 2004, Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment, Blood, 104, 4029, 10.1182/blood-2004-01-0041 Shortman, 2002, Mouse and human dendritic cell subtypes, Nat Rev Immunol, 2, 151, 10.1038/nri746 Blum, 2013, Pathways of antigen processing, Annu Rev Immunol, 31, 443, 10.1146/annurev-immunol-032712-095910 Steinman, 1991, The dendritic cell system and its role in immunogenicity, Annu Rev Immunol, 9, 271, 10.1146/annurev.iy.09.040191.001415 Chen, 2017, Convergence of osteoimmunology and immunomodulation for the development and assessment of bone biomaterials McKee, 2016, Interplay of innate and adaptive immunity in metal-induced hypersensitivity, Curr Opin Immunol, 42, 25, 10.1016/j.coi.2016.05.001 Hallab, 2008, Th1 type lymphocyte reactivity to metals in patients with total hip arthroplasty, J Orthop Surg, 3, 6, 10.1186/1749-799X-3-6 Høl, 2018, Novel nanoparticulate and ionic titanium antigens for hypersensitivity testing, Int J Mol Sci, 19, 1101, 10.3390/ijms19041101 Chan, 2011, Influence of metal ions on human lymphocytes and the generation of titanium-specific T-lymphocytes, J Appl Biomater Biomech, 9, 137 Pogribna, 2020, Effect of titanium dioxide nanoparticles on DNA methylation in multiple human cell lines, Nanotoxicology, 14, 534, 10.1080/17435390.2020.1723730 Lucarelli, 2004, Innate defence functions of macrophages can be biased by nanosized ceramic and metallic particles, Eur Cytokine Netw, 15, 339 Teigen, 2012, Dental implant suprastructures using cobalt-chromium alloy compared with gold alloy framework veneered with ceramic or acrylic resin: a retrospective cohort study up to 18 years, Clin Oral Implants Res, 23, 853, 10.1111/j.1600-0501.2011.02211.x Adya, 2005, Corrosion in titanium dental implants: literature review, J Indian Prosthodont Soc, 5, 126, 10.4103/0972-4052.17104 Delgado-Ruiz, 2018, Potential causes of titanium particle and ion release in implant dentistry: a systematic review, Int J Mol Sci, 19, 3585, 10.3390/ijms19113585 Dohan Ehrenfest, 2014, 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, 2, 37 Christiansen, 2019, Cytokine profile in patients with aseptic loosening of total hip replacements and its relation to metal release and metal allergy, J Clin Med, 8, 1259, 10.3390/jcm8081259 Takayanagi, 2000, T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-γ, Nature, 408, 600, 10.1038/35046102 Pajarinen, 2014, Innate immune reactions in septic and aseptic osteolysis around hip implants, J Long Term Eff Med Implants, 24, 283, 10.1615/JLongTermEffMedImplants.2014010564 Kim, 2013, Influence of transmucosal designs of dental implant on tissue regeneration in beagle dogs, Tissue Eng Regen Med., 10, 25, 10.1007/s13770-013-0373-9 Kim, 2019, Influence of implant-abutment connection structure on peri-implant bone level in a second molar: a 1-year randomized controlled trial, J Adv Prosthodont, 11, 147, 10.4047/jap.2019.11.3.147 Kzhyshkowska, 2015, Macrophage responses to implants: prospects for personalized medicine, J Leukoc Biol, 98, 953, 10.1189/jlb.5VMR0415-166R Weszl, 2018, The overview of titanium and its crystalline phases the impact in biomedical applications, 71 Albrektsson, 2020, An imbalance of the immune system instead of a disease behind marginal bone loss around oral implants: position paper, Int J Oral Maxillofac Implants, 35, 495, 10.11607/jomi.8218 Aktaş, 2018, Osteoimmunomodulation with biomaterials, 161 Anderson, 2008, Foreign body reaction to biomaterials, Semin Immunol, 20, 86, 10.1016/j.smim.2007.11.004 Sridharan, 2015, Biomaterial based modulation of macrophage polarization: a review and suggested design principles, Mater Today, 18, 313, 10.1016/j.mattod.2015.01.019 Wang, 2018, Nanostructured titanium regulates osseointegration via influencing macrophage polarization in the osteogenic environment, Int J Nanomed, 13, 4029, 10.2147/IJN.S163956 Su, 2018, Effects of titanium nanotubes on the osseointegration, cell differentiation, mineralisation and antibacterial properties of orthopaedic implant surfaces, Bone Joint J, 100-B, 9, 10.1302/0301-620X.100B1.BJJ-2017-0551.R1 Latha, 2017, Immunomodulatory properties of titanium dioxide nanostructural materials, Indian J Pharmacol, 49, 458, 10.4103/ijp.IJP_536_16 Neacsua, 2014, Reduced inflammatory activity of RAW 264.7 macrophages on titania nanotube modified Ti surface, Int J Biochem Cell Biol, 55, 187, 10.1016/j.biocel.2014.09.006 Sun, 2013, Effects of TiO2 nanotube layers on RAW 264.7 macrophage behaviour and bone morphogenetic protein-2 expression, Cell Prolif, 46, 685, 10.1111/cpr.12072 Gao, 2020, Immune response of macrophages on super-hydrophilic TiO2 nanotube arrays, J Biomater Appl, 34, 1239, 10.1177/0885328220903249 Razzi, 2020, Immunomodulation of surface biofunctionalized 3D printed porous titanium implants, Biomed Mater, 15, 10.1088/1748-605X/ab7763 Hotchkiss, 2017, Dental implant surface chemistry and energy alter macrophage activation in vitro, Clin Oral Implants Res, 28, 414, 10.1111/clr.12814 Loi, 2016, Inflammation, fracture and bone repair, Bone, 86, 119, 10.1016/j.bone.2016.02.020 Vasconcelos, 2016, The two faces of metal ions: From implants rejection to tissue repair/regeneration, Biomaterials, 84, 262, 10.1016/j.biomaterials.2016.01.046 Yang, 2019, Lithium chloride with immunomodulatory function for regulating titanium nanoparticle-stimulated inflammatory response and accelerating osteogenesis through suppression of MAPK signaling pathway, Int J Nanomed, 14, 7475, 10.2147/IJN.S210834 Loi, 2016, The effects of immunomodulation by macrophage subsets on osteogenesis in vitro, Stem Cell Res Ther, 22, 7 Córdova, 2017, CCL2, CCL5, and IGF-1 participate in the immunomodulation of osteogenesis during M1/M2 transition in vitro, J Biomed Mater Res A, 105, 3069, 10.1002/jbm.a.36166 Viganò, 2016, Mesenchymal stem cells as therapeutic target of biophysical stimulation for the treatment of musculoskeletal disorders, J Orthop Surg Res, 11, 163, 10.1186/s13018-016-0496-5 Meirelles, 2009, Mechanisms involved in the therapeutic properties of mesenchymal stem cells, Cytokine Growth Factor Rev, 20, 419, 10.1016/j.cytogfr.2009.10.002 English, 2010, Mesenchymal stroman cell: Facilitators of successful transplantation?, Cell Stem Cell, 7, 431, 10.1016/j.stem.2010.09.009 Hou, 2017, Regulatory effect of bone marrow mesenchymal stem cells on polarization of macrophages, Zhonghua Gan Zang Bing Za Zhi, 25, 273 Amengual-Peñafiel, 2018, Immunomodulation of osseointegration through extracorporeal shock wave therapy, Dent Hypotheses, 9, 45, 10.4103/denthyp.denthyp_4_18 Shin, 2016, Improving Stem Cell Therapeutics With Mechanobiology, Cell Stem Cell, 18, 16, 10.1016/j.stem.2015.12.007 Ho, 2016, The impact of mechanical stress on stem cell properties: the link between cell shape and pluripotency, Histol Histopathol, 31, 41 Lee, 2011, Stem cell mechanobiology, J Cell Biochem, 112, 1, 10.1002/jcb.22758 Tummala, 2010, The role of primary cilia in mesenchymal stem cell differentiation: a pivotal switch in guiding lineage commitment, Cell Mol Bioeng, 3, 207, 10.1007/s12195-010-0127-x Corrigan, 2018, TRPV4-mediates oscillatory fluid shear mechanotransduction in mesenchymal stem cells in part via the primary cilium, Sci Rep, 8, 10.1038/s41598-018-22174-3 Mennens, 2017, Role for mechanotransduction in macrophage and dendritic cell immunobiology, Results Probl Cell Differ, 62, 209, 10.1007/978-3-319-54090-0_9 Fahy, 2019, Shear and dynamic compression modulates the inflammatory phenotype of human monocytes in vitro, Front Immunol, 10, 383, 10.3389/fimmu.2019.00383 Xie, 2019, Bench-to-bedside strategies for osteoporotic fracture: from osteoimmunology to mechanosensation, Bone Res, 7, 25, 10.1038/s41413-019-0066-7 Albrektsson, 2005, The impact of oral implants - past and future, 1966-2042, J Can Dent Assoc, 71, 327 Corpas Ldos, 2014, Peri-implant bone innervation: histological findings in humans, Eur J Oral Implantol, 7, 283 Cerutti-Kopplin, 2016, Tooth loss increases the risk of diminished cognitive function: a systematic review and meta-analysis, JDR Clin Trans Res, 1, 10 Ki, 2019, Association between dental implants and cognitive function in community-dwelling older adults in Korea, J Prev Med Public Health, 52, 333, 10.3961/jpmph.19.163 Habre-Hallage, 2012, Brain plasticity and cortical correlates of osseoperception revealed by punctate mechanical stimulation of osseointegrated oral implants during fMRI, Eur J Oral Implantol, 5, 175 Mishra, 2016, Osseoperception in dental implants: a systematic review, J Prosthodont, 25, 185, 10.1111/jopr.12310 Enkling, 2010, Osseoperception: active tactile sensibility of osseointegrated dental implants, Int J Oral Maxillofac Implants, 25, 1159 Roehling, 2015, Sandblasted and acid-etched implant surfaces with or without high surface free energy: experimental and clinical background, 93 Brazill, 2019, Nerves in bone: evolving concepts in pain and anabolism, J Bone Miner Res, 34, 1393, 10.1002/jbmr.3822 Jones, 2019, Skeletal stem cell-Schwann cell circuitry in mandibular repair, Cell Rep, 28, 2757, 10.1016/j.celrep.2019.08.021 Korsching, 1986, The role of nerve growth factor in the CNS, Trends Neurosci, 9, 570, 10.1016/0166-2236(86)90179-7 Eppley, 1999, Efficacy of nerve growth factor in regeneration of the mandibular nerve: a preliminary report, J Oral Maxillofac Surg, 49, 61, 10.1016/0278-2391(91)90268-Q He, 2012, 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, 18, 10.12659/MSM.883253 Zhang, 2020, The effects of the M2a macrophage-induced axonal regeneration of neurons by arginase 1, Biosci Rep, 40, 10.1042/BSR20193031 Naveau, 2019, Etiology and measurement of peri-implant crestal bone loss (CBL), J Clin Med, 8, 166, 10.3390/jcm8020166 Wada, 2001, Effect of loading on the development of nerve fibers around oral implants in the dog mandible, Clin Oral Implants Res, 12, 219, 10.1034/j.1600-0501.2001.012003219.x Dingle, 2020, Experimental basis for creating an osseointegrated neural interface for prosthetic control: a pilot study in rabbits, Mil Med, 185, 462, 10.1093/milmed/usz246 Li, 2019, Thumb amputations treated with osseointegrated percutaneous prostheses with up to 25 years of follow-up, J Am Acad Orthop Surg Glob Res Rev, 3, e097 Gallagher, 2008, Psychoprosthetics: an introduction, vol 1, 1 Ortiz-Catalan, 2014, An osseointegrated human-machine gateway for long-term sensory feedback and motor control of artificial limbs, Sci Transl Med, 6, 257re6, 10.1126/scitranslmed.3008933