Review Article
Effect of hyaluronic acid in bone formation and its applications in dentistry
Ningbo Zhao,
Xin Wang,
Lei Qin,
Min Zhai,
Jing Yuan,
Ji Chen,
Dehua Li,
Ningbo Zhao
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorXin Wang
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorLei Qin
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorMin Zhai
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorJing Yuan
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorJi Chen
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorCorresponding Author
Dehua Li
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Correspondence to: D. Li; e-mail: [email protected]Search for more papers by this authorNingbo Zhao,
Xin Wang,
Lei Qin,
Min Zhai,
Jing Yuan,
Ji Chen,
Dehua Li,
Ningbo Zhao
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorXin Wang
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorLei Qin
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorMin Zhai
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorJing Yuan
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorJi Chen
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Search for more papers by this authorCorresponding Author
Dehua Li
State Key Laboratory of Military Stomatology, Department of Oral Implants, School of Stomatology, Fourth Military Medical University, No. 145 Changle West Road, Xi'an, Shaanxi, 710032 People's Republic of China
Correspondence to: D. Li; e-mail: [email protected]Search for more papers by this authorAbstract
Hyaluronic acid (HA), the simplest glycosaminoglycan, participates in several important biological procedures, including mediation of cellular signaling, regulation of cell adhesion and proliferation, and manipulation of cell differentiation. The effect of HA on cell proliferation and differentiation depends on its molecular weight (MW) and concentration. Moreover, the properties of high viscosity, elasticity, highly negative charge, biocompatibility, biodegradability, and nonimmunogenicity make HA attractive in tissue engineering and disease treatment. This review comprises an overview of the effect of HA on cell proliferation and differentiation in vitro, the role of HA in bone regeneration in vivo, and the clinical applications of HA in dentistry, focusing on the mechanism underlining the effect of MW and concentration of HA on cell proliferation and osteogenic differentiation. It is expected that practical progress of HA both in laboratory-based experiments and clinical applications will be achieved in the next few years. © 2016 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 104A: 1560–1569, 2016.
REFERENCES
- 1Fakhari A, Berkland C. Applications and emerging trends of hyaluronic acid in tissue engineering, as a dermal filler and in osteoarthritis treatment. Acta Biomater 2013; 9: 7081–7092.
- 2Zheng Shu X, Liu Y, Palumbo FS, Luo Y, Prestwich GD. In situ crosslinkable hyaluronan hydrogels for tissue engineering. Biomaterials 2004; 25: 1339–1348.
- 3Falcone SJ, Palmeri DM, Berg RA. Rheological and cohesive properties of hyaluronic acid. J Biomed Mater Res A 2006; 76: 721–728.
- 4Chen WY, Abatangelo G. Functions of hyaluronan in wound repair. Wound Repair Regen 1999; 7: 79–89.
- 5Prestwich GD. Hyaluronic acid-based clinical biomaterials derived for cell and molecule delivery in regenerative medicine. J Control Release 2011; 155: 193–199.
- 6Pirnazar P, Wolinsky L, Nachnani S, Haake S, Pilloni A, Bernard GW. Bacteriostatic effects of hyaluronic acid. J Periodontol 1999; 70: 370–374.
- 7Carlson GA, Dragoo JL, Samimi B, Bruckner DA, Bernard GW, Hedrick M, Benhaim P. Bacteriostatic properties of biomatrices against common orthopaedic pathogens. Biochem Biophys Res Commun 2004; 321: 472–478.
- 8Kang JH, Kim YY, Chang JY, Kho HS. Influences of hyaluronic acid on the anticandidal activities of lysozyme and the peroxidase system. Oral Dis 2011; 17: 577–583.
- 9Laurent TC, Laurent UB, Fraser JR. Functions of hyaluronan. Ann Rheum Dis 1995; 54: 429–432.
- 10Turley EA, Noble PW, Bourguignon LY. Signaling properties of hyaluronan receptors. J Biol Chem 2002; 277: 4589–4592.
- 11Dahiya P, Kamal R. Hyaluronic acid: A boon in periodontal therapy. N Am J Med Sci 2013; 5: 309–315.
- 12de Brito Bezerra B, Mendes Brazao MA, de Campos ML, Casati MZ, Sallum EA, Sallum AW. Association of hyaluronic acid with a collagen scaffold may improve bone healing in critical-size bone defects. Clin Oral Implants Res 2012; 23: 938–942.
- 13Kawano M, Ariyoshi W, Iwanaga K, Okinaga T, Habu M, Yoshioka I, Tominaga K, Nishihara T. Mechanism involved in enhancement of osteoblast differentiation by hyaluronic acid. Biochem Biophys Res Commun 2011; 405: 575–580.
- 14Mendes RM, Silva GA, Lima MF, Calliari MV, Almeida AP, Alves JB, Ferreira AJ. Sodium hyaluronate accelerates the healing process in tooth sockets of rats. Arch Oral Biol 2008; 53: 1155–1162.
- 15Sasaki T, Watanabe C. Stimulation of osteoinduction in bone wound healing by high-molecular hyaluronic acid. Bone 1995; 16: 9–15.
- 16Deed R, Rooney P, Kumar P, Norton JD, Smith J, Freemont AJ, Kumar S. Early-response gene signalling is induced by angiogenic oligosaccharides of hyaluronan in endothelial cells. Inhibition by non-angiogenic, high-molecular-weight hyaluronan. Int J Cancer 1997; 71: 251–256.
10.1002/(SICI)1097-0215(19970410)71:2<251::AID-IJC21>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- 17Raines AL, Sunwoo M, Gertzman AA, Thacker K, Guldberg RE, Schwartz Z, Boyan BD. Hyaluronic acid stimulates neovascularization during the regeneration of bone marrow after ablation. J Biomed Mater Res A 2011; 96: 575–583.
- 18Toole BP. Hyaluronan: From extracellular glue to pericellular cue. Nat Rev Cancer 2004; 4: 528–539.
- 19Kim J, Kim IS, Cho TH, Lee KB, Hwang SJ, Tae G, Noh I, Lee SH, Park Y, Sun K. Bone regeneration using hyaluronic acid-based hydrogel with bone morphogenic protein-2 and human mesenchymal stem cells. Biomaterials 2007; 28: 1830–1837.
- 20Luo Y, Kirker KR, Prestwich GD. Cross-linked hyaluronic acid hydrogel films: New biomaterials for drug delivery. J Control Release 2000; 69: 169–184.
- 21Eng D, Caplan M, Preul M, Panitch A. Hyaluronan scaffolds: A balance between backbone functionalization and bioactivity. Acta Biomater 2010; 6: 2407–2414.
- 22Lee KY, Mooney DJ. Hydrogels for tissue engineering. Chem Rev 2001; 101: 1869–1879.
- 23Drury JL, Mooney DJ. Hydrogels for tissue engineering: Scaffold design variables and applications. Biomaterials 2003; 24: 4337–4351.
- 24Bastow ER, Byers S, Golub SB, Clarkin CE, Pitsillides AA, Fosang AJ. Hyaluronan synthesis and degradation in cartilage and bone. Cell Mol Life Sci 2008; 65: 395–413.
- 25Allison DD, Grande-Allen KJ. Review. Hyaluronan: A powerful tissue engineering tool. Tissue Eng 2006; 12: 2131–2140.
- 26Burdick JA, Prestwich GD. Hyaluronic acid hydrogels for biomedical applications. Adv Mater 2011; 23: H41–H56.
- 27Collins MN, Birkinshaw C. Hyaluronic acid based scaffolds for tissue engineering—A review. Carbohydr Polym 2013; 92: 1262–1279.
- 28Little CJ, Kulyk WM, Chen X. The effect of chondroitin sulphate and hyaluronic acid on chondrocytes cultured within a fibrin-alginate hydrogel. J Funct Biomater 2014; 5: 197–210.
- 29Pilloni A, Bernard GW. The effect of hyaluronan on mouse intramembranous osteogenesis in vitro. Cell Tissue Res 1998; 294: 323–333.
- 30Huang L, Cheng YY, Koo PL, Lee KM, Qin L, Cheng JC, Kumta SM. The effect of hyaluronan on osteoblast proliferation and differentiation in rat calvarial-derived cell cultures. J Biomed Mater Res A 2003; 66: 880–884.
- 31Zhao N, Wang X, Qin L, Guo Z, Li D. Effect of molecular weight and concentration of hyaluronan on cell proliferation and osteogenic differentiation in vitro. Biochem Biophys Res Commun 2015; 465: 569–574.
- 32Yeom J, Hwang BW, Yang DJ, Shin H-I, Hahn SK. Effect of osteoconductive hyaluronate hydrogels on calvarial bone regeneration. Biomater Res 2014; 18: 1–6.
10.1186/2055-7124-18-8 Google Scholar
- 33Gu H, Huang L, Wong YP, Burd A. HA modulation of epidermal morphogenesis in an organotypic keratinocyte-fibroblast co-culture model. Exp Dermatol 2010; 19: E336–E339.
- 34Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M. Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels. J Cell Physiol 1999; 179: 142–148.
10.1002/(SICI)1097-4652(199905)179:2<142::AID-JCP4>3.0.CO;2-Q CAS PubMed Web of Science® Google Scholar
- 35Malaisse J, Pendaries V, Hontoir FD, Glas V, Van Vlaender D, Simon M, Lambert de Rouvroit C, Poumay Y, Flamion B. Hyaluronan does not regulate human epidermal keratinocyte proliferation and differentiation. J Biol Chem 2016; 291: 6347–6358.
- 36Zou L, Zou X, Chen L, Li H, Mygind T, Kassem M, Bunger C. Effect of hyaluronan on osteogenic differentiation of porcine bone marrow stromal cells in vitro. J Orthop Res 2008; 26: 713–720.
- 37Takeda K, Sakai N, Shiba H, Nagahara T, Fujita T, Kajiya M, Iwata T, Matsuda S, Kawahara K, Kawaguchi H, Kurihara H. Characteristics of high-molecular-weight hyaluronic acid as a brain-derived neurotrophic factor scaffold in periodontal tissue regeneration. Tissue Eng Part A 2011; 17: 955–967.
- 38Kaneko K, Higuchi C, Kunugiza Y, Yoshida K, Sakai T, Yoshikawa H, Nakata K. Hyaluronan inhibits BMP-induced osteoblast differentiation. FEBS Lett 2015; 589: 447–454.
- 39Boeckel DG, Shinkai RS, Grossi ML, Teixeira ER. In vitro evaluation of cytotoxicity of hyaluronic acid as an extracellular matrix on OFCOL II cells by the MTT assay. Oral Surg Oral Med Oral Pathol Oral Radiol 2014; 117: e423–e428.
- 40Lai JY, Tu IH. Adhesion, phenotypic expression, and biosynthetic capacity of corneal keratocytes on surfaces coated with hyaluronic acid of different molecular weights. Acta Biomater 2012; 8: 1068–1079.
- 41Villar-Suarez V, Colaco B, Calles-Venal I, Bravo IG, Fernandez-Alvarez JG, Fernandez-Caso M, Villar-Lacilla JM. Effects of extracellular matrix on the morphology and behaviour of rabbit auricular chondrocytes in culture. J Biomed Biotechnol 2005; 2005: 364–373.
- 42Amorim S, Martins A, Neves NM, Reis RL, Pires RA. Hyaluronic acid/poly-l-lysine bilayered silica nanoparticles enhance the osteogenic differentiation of human mesenchymal stem cells. J Mater Chem B 2014; 2: 6939–6946.
- 43Hempel U, Moller S, Noack C, Hintze V, Scharnweber D, Schnabelrauch M, Dieter P. Sulfated hyaluronan/collagen I matrices enhance the osteogenic differentiation of human mesenchymal stromal cells in vitro even in the absence of dexamethasone. Acta Biomater 2012; 8: 4064–4072.
- 44Knudson CB, Knudson W. Hyaluronan-binding proteins in development, tissue homeostasis, and disease. FASEB J 1993; 7: 1233–1241.
- 45Toole BP. Hyaluronan in morphogenesis. Semin Cell Dev Biol 2001; 12: 79–87.
- 46David-Raoudi M, Tranchepain F, Deschrevel B, Vincent JC, Bogdanowicz P, Boumediene K, Pujol JP. Differential effects of hyaluronan and its fragments on fibroblasts: Relation to wound healing. Wound Repair Regen 2008; 16: 274–287.
- 47Kato Y, Nakamura S, Nishimura M. Beneficial actions of hyaluronan (HA) on arthritic joints: Effects of molecular weight of HA on elasticity of cartilage matrix. Biorheology 2006; 43: 347–354.
- 48Takahashi K, Goomer RS, Harwood F, Kubo T, Hirasawa Y, Amiel D. The effects of hyaluronan on matrix metalloproteinase-3 (MMP-3), interleukin-1beta (IL-1β), and tissue inhibitor of metalloproteinase-1 (TIMP-1) gene expression during the development of osteoarthritis. Osteoarthritis Cartilage 1999; 7: 182–190.
- 49Feinberg RN, Beebe DC. Hyaluronate in vasculogenesis. Science 1983; 220: 1177–1179.
- 50Mitsui Y, Gotoh M, Nakama K, Yamada T, Higuchi F, Nagata K. Hyaluronic acid inhibits mRNA expression of proinflammatory cytokines and cyclooxygenase-2/prostaglandin E(2) production via CD44 in interleukin-1-stimulated subacromial synovial fibroblasts from patients with rotator cuff disease. J Orthop Res 2008; 26: 1032–1037.
- 51West DC, Hampson IN, Arnold F, Kumar S. Angiogenesis induced by degradation products of hyaluronic acid. Science 1985; 228: 1324–1326.
- 52Itano N. Simple primary structure, complex turnover regulation and multiple roles of hyaluronan. J Biochem 2008; 144: 131–137.
- 53Bendall LJ, Gottlieb DJ. CD44 and adhesion of normal and leukemic CD34+ cells to bone marrow stroma. Leuk Lymphoma 1999; 32: 427–439.
- 54Noble PW. Hyaluronan and its catabolic products in tissue injury and repair. Matrix Biol 2002; 21: 25–29.
- 55Toole BP, Wight TN, Tammi MI. Hyaluronan–cell interactions in cancer and vascular disease. J Biol Chem 2002; 277: 4593–4596.
- 56Liotta F, Angeli R, Cosmi L, Fili L, Manuelli C, Frosali F, Mazzinghi B, Maggi L, Pasini A, Lisi V, Santarlasci V, Consoloni L, Angelotti ML, Romagnani P, Parronchi P, Krampera M, Maggi E, Romagnani S, Annunziato F. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells 2008; 26: 279–289.
- 57Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990; 61: 1303–1313.
- 58Laurent TC, Fraser JR. Hyaluronan. FASEB J 1992; 6: 2397–2404.
- 59Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143–147.
- 60Ishida O, Tanaka Y, Morimoto I, Takigawa M, Eto S. Chondrocytes are regulated by cellular adhesion through CD44 and hyaluronic acid pathway. J Bone Miner Res 1997; 12: 1657–1663.
- 61Cao JJ, Singleton PA, Majumdar S, Boudignon B, Burghardt A, Kurimoto P, Wronski TJ, Bourguignon LY, Halloran BP. Hyaluronan increases RANKL expression in bone marrow stromal cells through CD44. J Bone Miner Res 2005; 20: 30–40.
- 62Ponta H, Sherman L, Herrlich PA. CD44: From adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003; 4: 33–45.
- 63Entwistle J, Hall CL, Turley EA. HA receptors: Regulators of signalling to the cytoskeleton. J Cell Biochem 1996; 61: 569–577.
10.1002/(SICI)1097-4644(19960616)61:4<569::AID-JCB10>3.0.CO;2-B CAS PubMed Web of Science® Google Scholar
- 64Hall CL, Wang C, Lange LA, Turley EA. Hyaluronan and the hyaluronan receptor RHAMM promote focal adhesion turnover and transient tyrosine kinase activity. J Cell Biol 1994; 126: 575–588.
- 65Wang C, Entwistle J, Hou G, Li Q, Turley EA. The characterization of a human RHAMM cDNA: Conservation of the hyaluronan-binding domains. Gene 1996; 174: 299–306.
- 66Entwistle J, Zhang S, Yang B, Wong C, Li Q, Hall CL, A J, Mowat M, Greenberg AH, Turley EA. Characterization of the murine gene encoding the hyaluronan receptor RHAMM. Gene 1995; 163: 233–238.
- 67Assmann V, Jenkinson D, Marshall JF, Hart IR. The intracellular hyaluronan receptor RHAMM/IHABP interacts with microtubules and actin filaments. J Cell Sci 1999; 112: 3943–3954.
- 68Choudhary M, Zhang X, Stojkovic P, Hyslop L, Anyfantis G, Herbert M, Murdoch AP, Stojkovic M, Lako M. Putative role of hyaluronan and its related genes, HAS2 and RHAMM, in human early preimplantation embryogenesis and embryonic stem cell characterization. Stem Cells 2007; 25: 3045–3057.
- 69Nedvetzki S, Gonen E, Assayag N, Reich R, Williams RO, Thurmond RL, Huang JF, Neudecker BA, Wang FS, Turley EA, Naor D. RHAMM, a receptor for hyaluronan-mediated motility, compensates for CD44 in inflamed CD44-knockout mice: A different interpretation of redundancy. Proc Natl Acad Sci USA 2004; 101: 18081–18086.
- 70Tomchuck SL, Zwezdaryk KJ, Coffelt SB, Waterman RS, Danka ES, Scandurro AB. Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cells 2008; 26: 99–107.
- 71Takeda K, Akira S. Toll-like receptors. Curr Protoc Immunol 2007; Chapter 14: Unit 14.2.
- 72Akira S, Takeda K, Kaisho T. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2: 675–680.
- 73McKee CM, Penno MB, Cowman M, Burdick MD, Strieter RM, Bao C, Noble PW. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest 1996; 98: 2403–2413.
- 74Tzircotis G, Thorne RF, Isacke CM. Chemotaxis towards hyaluronan is dependent on CD44 expression and modulated by cell type variation in CD44–hyaluronan binding. J Cell Sci 2005; 118: 5119–5128.
- 75Cichy J, Pure E. Cytokines regulate the affinity of soluble CD44 for hyaluronan. FEBS Lett 2004; 556: 69–74.
- 76Hascall VC, Heinegard D. Aggregation of cartilage proteoglycans. II. Oligosaccharide competitors of the proteoglycan–hyaluronic acid interaction. J Biol Chem 1974; 249: 4242–4249.
- 77Ghatak S, Misra S, Toole BP. Hyaluronan oligosaccharides inhibit anchorage-independent growth of tumor cells by suppressing the phosphoinositide 3-kinase/Akt cell survival pathway. J Biol Chem 2002; 277: 38013–38020.
- 78Astachov L, Vago R, Aviv M, Nevo Z. Hyaluronan and mesenchymal stem cells: From germ layer to cartilage and bone. Front Biosci (Landmark Ed) 2011; 16: 261–276.
- 79Gonzalez-Garcia C, Sousa SR, Moratal D, Rico P, Salmeron-Sanchez M. Effect of nanoscale topography on fibronectin adsorption, focal adhesion size and matrix organisation. Colloids Surf B Biointerfaces 2010; 77: 181–190.
- 80Polimeni G, Xiropaidis AV, Wikesjo UM. Biology and principles of periodontal wound healing/regeneration. Periodontol 2000 2006; 41: 30–47.
- 81Bhakta G, Lim ZX, Rai B, Lin T, Hui JH, Prestwich GD, van Wijnen AJ, Nurcombe V, Cool SM. The influence of collagen and hyaluronan matrices on the delivery and bioactivity of bone morphogenetic protein-2 and ectopic bone formation. Acta Biomater 2013; 9: 9098–9106.
- 82Kisiel M, Klar AS, Martino MM, Ventura M, Hilborn J. Evaluation of injectable constructs for bone repair with a subperiosteal cranial model in the rat. PLoS One 2013; 8: e71683.
- 83Patterson J, Siew R, Herring SW, Lin AS, Guldberg R, Stayton PS. Hyaluronic acid hydrogels with controlled degradation properties for oriented bone regeneration. Biomaterials 2010; 31: 6772–6781.
- 84Bae MS, Ohe JY, Lee JB, Heo DN, Byun W, Bae H, Kwon YD, Kwon IK. Photo-cured hyaluronic acid-based hydrogels containing growth and differentiation factor 5 (GDF-5) for bone tissue regeneration. Bone 2014; 59: 189–198.
- 85Bae MS, Yang DH, Lee JB, Heo DN, Kwon YD, Youn IC, Choi K, Hong JH, Kim GT, Choi YS, Hwang EH, Kwon IK. Photo-cured hyaluronic acid-based hydrogels containing simvastatin as a bone tissue regeneration scaffold. Biomaterials 2011; 32: 8161–8171.
- 86Maus U, Andereya S, Niedhart C. Lack of effect on bone healing of injectable BMP-2 augmented hyaluronic acid. Arch Orthop Trauma Surg 2008; 128:1461–1466.
- 87Kim J, Kim IS, Cho TH, Kim HC, Yoon SJ, Choi J, Park Y, Sun K, Hwang SJ. In vivo evaluation of MMP sensitive high-molecular weight HA-based hydrogels for bone tissue engineering. J Biomed Mater Res A 2010; 95: 673–681.
- 88Lisignoli G, Fini M, Giavaresi G, Nicoli AN, Toneguzzi S, Facchini A. Osteogenesis of large segmental radius defects enhanced by basic fibroblast growth factor activated bone marrow stromal cells grown on non-woven hyaluronic acid-based polymer scaffold. Biomaterials 2002; 23: 1043–1051.
- 89Docherty-Skogh AC, Bergman K, Waern MJ, Ekman S, Hultenby K, Ossipov D, Hilborn J, Bowden T, Engstrand T. Bone morphogenetic protein-2 delivered by hyaluronan-based hydrogel induces massive bone formation and healing of cranial defects in minipigs. Plast Reconstr Surg 2010; 125: 1383–1392.
- 90Segari WAO, Radwan DAEK, El Hamid MAA. The effect of adding hyaluronic acid to calcium phosphate on periapical tissue healing following periradicular surgery in dogs. Tanta Dent J 2014; 11: 122–129.
10.1016/j.tdj.2014.07.001 Google Scholar
- 91Suzuki K, Anada T, Suzuki O. Effect of addition of hyaluronic acids on the osteoconductivity and biodegradability of synthetic octacalcium phosphate. Acta Biomater 2014; 10:531–543.
- 92Mendes RM, Silva GA, Caliari MV, Silva EE, Ladeira LO, Ferreira AJ. Effects of single wall carbon nanotubes and its functionalization with sodium hyaluronate on bone repair. Life Sci 2010; 87: 215–222.
- 93Lee JH, Kim J, Baek HR, Lee KM, Seo JH, Lee HK, Lee AY, Zheng GB, Chang BS, Lee CK. Fabrication of an rhBMP-2 loaded porous β-TCP microsphere-hyaluronic acid-based powder gel composite and evaluation of implant osseointegration. J Mater Sci Mater Med 2014; 25: 2141–2151.
- 94Chen JP, Tsai MJ, Liao HT. Incorporation of biphasic calcium phosphate microparticles in injectable thermoresponsive hydrogel modulates bone cell proliferation and differentiation. Colloids Surf B Biointerfaces 2013; 110: 120–129.
- 95Martinez-Sanz E, Varghese OP, Kisiel M, Engstrand T, Reich KM, Bohner M, Jonsson KB, Kohler T, Muller R, Ossipov DA, Hilborn J. Minimally invasive mandibular bone augmentation using injectable hydrogels. J Tissue Eng Regen Med 2012; 6(Suppl 3): s15–s23.
- 96Hulsart-Billstrom G, Piskounova S, Gedda L, Andersson BM, Bergman K, Hilborn J, Larsson S, Bowden T. Morphological differences in BMP-2-induced ectopic bone between solid and crushed hyaluronan hydrogel templates. J Mater Sci Mater Med 2013; 24: 1201–1209.
- 97Xu C, Su P, Wang Y, Chen X, Meng Y, Liu C, Yu X, Yang X, Yu W, Zhang X, Xiang AP. A novel biomimetic composite scaffold hybridized with mesenchymal stem cells in repair of rat bone defects models. J Biomed Mater Res A 2010; 95:495–503.
- 98Kang SW, Kim JS, Park KS, Cha BH, Shim JH, Kim JY, Cho DW, Rhie JW, Lee SH. Surface modification with fibrin/hyaluronic acid hydrogel on solid-free form-based scaffolds followed by BMP-2 loading to enhance bone regeneration. Bone 2011; 48: 298–306.
- 99Neumayer T, Prinz A, Findl O. Effect of a new cohesive ophthalmic viscosurgical device on corneal protection and intraocular pressure in small-incision cataract surgery. J Cataract Refract Surg 2008; 34: 1362–1366.
- 100Migliore A, Granata M. Intra-articular use of hyaluronic acid in the treatment of osteoarthritis. Clin Interv Aging 2008; 3: 365–369.
- 101Adams ME, Atkinson MH, Lussier AJ, Schulz JI, Siminovitch KA, Wade JP, Zummer M. The role of viscosupplementation with hylan G-F 20 (Synvisc) in the treatment of osteoarthritis of the knee: A Canadian multicenter trial comparing hylan G-F 20 alone, hylan G-F 20 with non-steroidal anti-inflammatory drugs (NSAIDs) and NSAIDs alone. Osteoarthritis Cartilage 1995; 3: 213–225.
- 102Balazs EA, Denlinger JL. Viscosupplementation: A new concept in the treatment of osteoarthritis. J Rheumatol Suppl 1993; 39: 3–9.
- 103Colen S, van den Bekerom MP, Mulier M, Haverkamp D. Hyaluronic acid in the treatment of knee osteoarthritis: A systematic review and meta-analysis with emphasis on the efficacy of different products. BioDrugs 2012; 26: 257–268.
- 104Andre P. New trends in face rejuvenation by hyaluronic acid injections. J Cosmet Dermatol 2008; 7: 251–258.
- 105Brandt FS, Cazzaniga A. Hyaluronic acid gel fillers in the management of facial aging. Clin Interv Aging 2008; 3: 153–159.
- 106Liguori V, Guillemin C, Pesce GF, Mirimanoff RO, Bernier J. Double-blind, randomized clinical study comparing hyaluronic acid cream to placebo in patients treated with radiotherapy. Radiother Oncol 1997; 42: 155–161.
- 107Sapna N, Vandana KL. Evaluation of hyaluronan gel (Gengigel®) as a topical applicant in the treatment of gingivitis. J Investig Clin Dent 2011; 2: 162–170.
- 108Jentsch H, Pomowski R, Kundt G, Gocke R. Treatment of gingivitis with hyaluronan. J Clin Periodontol 2003; 30: 159–164.
- 109Engstrom PE, Shi XQ, Tronje G, Larsson A, Welander U, Frithiof L, Engstrom GN. The effect of hyaluronan on bone and soft tissue and immune response in wound healing. J Periodontol 2001; 72: 1192–1200.
- 110Gontiya G, Galgali SR. Effect of hyaluronan on periodontitis: A clinical and histological study. J Indian Soc Periodontol 2012; 16: 184–192.
- 111Ballini A, Cantore S, Capodiferro S, Grassi FR. Esterified hyaluronic acid and autologous bone in the surgical correction of the infra-bone defects. Int J Med Sci 2009; 6: 65–71.
- 112Rajan P, Baramappa R, Rao NM, Pavaluri AK, P I, Rahaman SM. Hyaluronic acid as an adjunct to scaling and root planing in chronic periodontitis. A randomized clinical trial. J Clin Diagn Res 2014; 8: ZC11–ZC14.
- 113Fawzy El-Sayed KM, Dahaba MA, Aboul-Ela S, Darhous MS. Local application of hyaluronan gel in conjunction with periodontal surgery: A randomized controlled trial. Clin Oral Investig 2012; 16: 1229–1236.
- 114Johannsen A, Tellefsen M, Wikesjo U, Johannsen G. Local delivery of hyaluronan as an adjunct to scaling and root planing in the treatment of chronic periodontitis. J Periodontol 2009; 80: 1493–1497.
- 115Bertl K, Bruckmann C, Isberg PE, Klinge B, Gotfredsen K, Stavropoulos A. Hyaluronan in non-surgical and surgical periodontal therapy: A systematic review. J Clin Periodontol 2015; 42: 236–246.
- 116Guarda-Nardini L, Masiero S, Marioni G. Conservative treatment of temporomandibular joint osteoarthrosis: Intra-articular injection of sodium hyaluronate. J Oral Rehabil 2005; 32: 729–734.
- 117Bjornland T, Gjaerum AA, Moystad A. Osteoarthritis of the temporomandibular joint: An evaluation of the effects and complications of corticosteroid injection compared with injection with sodium hyaluronate. J Oral Rehabil 2007; 34: 583–589.
- 118Long X, Chen G, Cheng AH, Cheng Y, Deng M, Cai H, Meng Q. A randomized controlled trial of superior and inferior temporomandibular joint space injection with hyaluronic acid in treatment of anterior disc displacement without reduction. J Oral Maxillofac Surg 2009; 67: 357–361.
- 119Escoda-Francoli J, Vazquez-Delgado E, Gay-Escoda C. Scientific evidence on the usefulness of intraarticular hyaluronic acid injection in the management of temporomandibular dysfunction. Med Oral Patol Oral Cir Bucal 2010; 15: e644–e648.
- 120Manfredini D, Bonnini S, Arboretti R, Guarda-Nardini L. Temporomandibular joint osteoarthritis: An open label trial of 76 patients treated with arthrocentesis plus hyaluronic acid injections. Int J Oral Maxillofac Surg 2009; 38: 827–834.
- 121Manfredini D, Piccotti F, Guarda-Nardini L. Hyaluronic acid in the treatment of TMJ disorders: A systematic review of the literature. Cranio 2010; 28: 166–176.
- 122Nolan A, Baillie C, Badminton J, Rudralingham M, Seymour RA. The efficacy of topical hyaluronic acid in the management of recurrent aphthous ulceration. J Oral Pathol Med 2006; 35: 461–465.
- 123Lee JH, Jung JY, Bang D. The efficacy of topical 0.2% hyaluronic acid gel on recurrent oral ulcers: Comparison between recurrent aphthous ulcers and the oral ulcers of Behcet's disease. J Eur Acad Dermatol Venereol 2008; 22: 590–595.
- 124Joeris A, Ondrus S, Planka L, Gal P, Slongo T. ChronOS inject in children with benign bone lesions—Does it increase the healing rate? Eur J Pediatr Surg 2010; 20: 24–28.
- 125Gal P, Ondrus S, Skvaril J, Straka M, Jochymek J, Planka L. Synthetic biocompatible degradable material for juvenile bone cyst treatment. Acta Chir Orthop Traumatol Cech 2009; 76: 495–500.
- 126Baldini A, Zaffe D, Nicolini G. Bone-defects healing by high-molecular hyaluronic acid: Preliminary results. Ann Stomatol (Roma) 2010; 1: 2–7.
- 127Galli F, Zuffetti F, Capelli M, Fumagalli L, Parenti A, Testori T, Esposito M. Hyaluronic acid to improve healing of surgical incisions in the oral cavity: A pilot multicentre placebo-controlled randomised clinical trial. Eur J Oral Implantol 2008; 1: 199–206.
- 128Moran SL, Duymaz A, Karabekmez FE. The efficacy of hyaluronic acid in the treatment of osteoarthritis of the trapeziometacarpal joint. J Hand Surg Am 2009; 34: 942–944.
- 129Zhao N, Wu Z, Qin L, Guo Z, Li D. Characteristics and tissue regeneration properties of gingiva-derived mesenchymal stem cells. Crit Rev Eukaryot Gene Expr 2015; 25: 135–144.
- 130Kreeger K. From bench to bedside. Nature 2003; 424: 1090–1091.
- 131Moore DR. Reverse translation: Clearing a path from bedside to bench. Nature 2008; 454: 274.
- 132Archer R, Williams DJ. Why tissue engineering needs process engineering. Nat Biotechnol 2005; 23: 1353–1355.
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