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Pulsed laser deposition temperature effects on strontium-substituted hydroxyapatite thin films for biomedical implants

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Abstract

Substituting small molecule drugs with abundant and easily affordable ions may have positive effects on the way countless disease treatments are approached. The interest in strontium cation in bone therapies soared in the wake of the success of strontium ranelate in the treatment of osteoporosis. A new method for producing thin strontium-containing hydroxyapatite (Sr-HA, Ca9Sr(PO4)6(OH)2) films as coatings that render bioinert titanium implant bioactive is reported here. The method is based on the combination of a mechanochemical synthesis of Sr-HA targets and their deposition in form of thin films on top of titanium with the use of laser ablation at low pressure. The films were 1–2 μm in thickness and their formation was studied at different temperatures, including 25, 300, and 500 °C. Highly crystalline Sr-HA target transformed during pulsed laser deposition to a fully amorphous film, whose degree of long-range order recovered with temperature. Particle edges became somewhat sharper and surface roughness moderately increased with temperature, but the (Ca+Sr)/P atomic ratio, which increased 1.5 times during the film formation, remained approximately constant at different temperatures. Despite the mostly amorphous structure of the coatings, their affinity for capturing atmospheric carbon dioxide and accommodating it as carbonate ions that replace both phosphates and hydroxyls of HA was confirmed in an X-ray photoelectron spectroscopic analysis. As the film deposition temperature increased, the lattice voids got reduced in concentration and the structure gradually “closed,” becoming more compact and entailing a linear increase in microhardness with temperature, by 0.03 GPa/°C for the entire 25–500 °C range. Biocompatibility and bioactivity of Sr-HA thin films deposited on titanium were confirmed in an interaction with dental pulp stem cells, suggesting that these coatings, regardless of the processing temperature, may be viable candidates for the surface components of metallic bone implants.

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References

  • Aina V, Bergandi L, Lusvardi G, Malavasi G, Imrie FE, Gibson IR, et al. Sr containing hydroxyapatite: morphologies of HA crystals and bioactivity on osteoblast cells. Mater Sci Eng C. 2013;33:1132–4112.

    Article  CAS  Google Scholar 

  • Amiri A, Chahkandi M, Targhoo A. Synthesis of nano-hydroxyapatite sorbent for microextraction in packed syringe of phthalate esters in water samples. Anal Chim Acta. 2017;950:64–70.

    Article  CAS  PubMed  Google Scholar 

  • Avci M, Yilmaz B, Tezcanera A, Evis Z. Strontium doped hydroxyapatite biomimetic coatings on Ti6Al4V plates. Ceram Int. 2017;43:9431–6.

    Article  CAS  Google Scholar 

  • Azari A, Nikzad S, Yazdani A, Atri F, Fazel AYA. Deposition of crystalline hydroxyapatite nano-particle on zirconia ceramic: a potential solution for the poor bonding characteristic of zirconia ceramics to resin cement. J Mater Sci Mater Med. 2017;28(7):111.

  • Bastan FE, Erdogan C, Ustel F. Role of strontium substitution in spray drying of hydroxyapatite: a comparative study on physical properties. Int J Appl Ceram Technol. (in press. 2020. https://doi.org/10.1111/ijac.13422.

  • Behera RR, Das A, Pamu D, Pandey LM, Sankar MR. Mechano-tribological properties and in vitro bioactivity of biphasic calcium phosphate coating on Ti-6Al-4V. J Mech Behav Biomed Mater. 2018;86:143–57.

    Article  CAS  PubMed  Google Scholar 

  • Bohner M. Silicon-substituted calcium phosphates – a critical view. Biomaterials. 2009;30(32):6403–6.

    Article  CAS  PubMed  Google Scholar 

  • Boivin G, Deloffre P, Perrat B, Panczer G, Boudeulle M, Mauras Y, et al. Strontium distribution and interactions with bone mineral in monkey iliac bone after strontium salt (S 12911) administration. J Bone Miner Res. 1996;11:1302–11.

    Article  CAS  PubMed  Google Scholar 

  • Bonnelye E, Chabadel A, Saltel F, Jurdic P. Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone. 2008;42(1):129–38.

    Article  CAS  PubMed  Google Scholar 

  • Boyd AR, Rutledge L, Randolph LD, Mutreja I, Meenan BJ. The deposition of strontium substituted hydroxyapatite coatings. J Mater Sci Mater Med. 2015a;26(2):65.

    Article  PubMed  CAS  Google Scholar 

  • Boyd AR, Rutledge L, Randolph LD, Meenan BJ. Strontium-substituted hydroxyapatite coatings deposited via a co-deposition sputter technique. Mater Sci Eng C. 2015b;46:290–300.

    Article  CAS  Google Scholar 

  • Brodie J, Godber J. Bakery processes, chemical leavening agents. Kirk-Othmer Encyclopedia of Chemical Technology. New York: Wiley; 2008.

    Google Scholar 

  • Bulina NV, Chaikina MV, Prosanov IY. Mechanochemical synthesis of Sr. substituted hydroxyapatite. Inorg Mater. 2018;54:820–5.

    Article  CAS  Google Scholar 

  • Capuccini C, Torricelli P, Sima F, Boanini E, Ristoscu C, Bracci B, et al. Strontium-substituted hydroxyapatite coatings synthesized by pulsed-laser deposition: in vitro osteoblast and osteoclast response. Acta Biomater. 2008;4(6):1885–93.

    Article  CAS  PubMed  Google Scholar 

  • Caverzasio J. Strontium ranelate promotes osteoblastic cell replication through at least two different mechanisms. Bone. 2008;42(6):1131–6.

    Article  CAS  PubMed  Google Scholar 

  • Chadha RK, Singh KL, Sharma C, Singh AP, Naithani V. Effect of microwave and conventional processing techniques on mechanical properties of strontium substituted hydroxyapatite. Ceram Int. 2020;46:1091–8.

    Article  CAS  Google Scholar 

  • Chen JY, Duan YR, Deng CL, Zhang QY, Zhang XD. A comparative study between dynamic and static simulated body fluid methods. Key Eng Mater. 2006;309(311):271–4.

    Article  Google Scholar 

  • Chen FF, Zhu YJ, Xiong ZC, Dong LY, Chen F, Lu BQ, et al. Hydroxyapatite nanowire-based all-weather flexible electrically conductive paper with superhydrophobic and flame-retardant properties. ACS Appl Mater Interfaces. 2017;9:39534–48.

  • Coelho PG, Freire JN, Granato R, Marin C, Bonfante EA, Gil JN, et al. Bone mineral apposition rates at early implantation times around differently prepared titanium surfaces: a study in beagle dogs. Int J Oral Maxillofac Implants. 2011;26(1):63–9.

    PubMed  Google Scholar 

  • Combes C, Rey C. Amorphous calcium phosphates: synthesis, properties and uses in biomaterials. Acta Biomater. 2010;6:3362–78.

    Article  CAS  PubMed  Google Scholar 

  • Cook SD, Thomas KA, Kay JF, Jarcho M. Hydroxyapatite-coated titanium for orthopedic implant applications. Clin Orthop Relat Res. 1988;232:225–43.

    Article  CAS  Google Scholar 

  • Curcio M, De Bonis A, Fosca M, Santagata A, Teghil R, Rau JV. Pulsed laser-deposited composite carbon-glass-ceramic films with improved hardness. J Mater Sci. 2017;52:9140–250.

    Article  CAS  Google Scholar 

  • De Bruijn JD, Bovell YP, van Blitterswijk CA. Structural arrangements at the interface between plasma sprayed calcium phosphates and bone. Biomaterials. 1994;15:543–50.

  • Ding XX, Li X, Li CY, Qi ML, Zhang Z, Sun XL, et al. Chitosan/dextran hydrogel constructs containing strontium-doped hydroxyapatite with enhanced osteogenic potential in rat cranium. ACS Biomater Sci Eng. 2019;5:4574–86.

    Article  CAS  PubMed  Google Scholar 

  • Dos Santos EA, Moldovan S, Mateescu M, Faerber J, Acosta M, Pelletier H, et al. Physical–chemical and biological behavior of an amorphous calcium phosphate thin film produced by RF-magnetron sputtering. Mater Sci Eng C. 2012;32:2086–95.

  • Duer M, Veis A. Bone mineralization: water brings order. Nat Mater. 2013;12:1081–2.

    Article  CAS  PubMed  Google Scholar 

  • Eftekharzadeh S, Sabetkish N, Sabetkish S, Kajbafzadeh AM. Comparing the bulking effect of calcium hydroxyapatite and Deflux injection into the bladder neck for improvement of urinary incontinence in bladder exstrophy-epispadias complex. Int Urol Nephrol. 2017;49(2):183–9.

    Article  CAS  PubMed  Google Scholar 

  • Essamlali Y, Amadine O, Larzek M, Len C, Zahouily M. Sodium modified hydroxyapatite: highly efficient and stable solid-base catalyst for biodiesel production. Energy Convers Manag. 2017;149:355–67.

    Article  CAS  Google Scholar 

  • Ferro D, Barinov SM, Rau JV, Latini A, Scandurra R, Brunetti B. Vickers and Knoop hardness of electron beam deposited ZrC and HfC thin films on titanium. Surf Coat Technol. 2006;200:4701–7.

    Article  CAS  Google Scholar 

  • Frasnelli M, Cristofaro F, Sglavo VM, Dire S, Callone E, Ceccato R, et al. Synthesis and characterization of strontium-substituted hydroxyapatite nanoparticles for bone regeneration. Mater Sci Eng C. 2017;71:653–62.

    Article  CAS  Google Scholar 

  • Fu DL, Jiang QH, He FM, Fu BP. Adhesion of bone marrow mesenchymal stem cells on porous titanium surfaces with strontium-doped hydroxyapatite coating. J Zheijang Univ Sci B. 2017;18:778–88.

    Article  CAS  Google Scholar 

  • Ge M, Ge K, Gao F, Yan W, Liu H, Xue L, et al. Biomimetic mineralized strontium-doped hydroxyapatite on porous poly(l-lactic acid) scaffolds for bone defect repair. Int J Nanomedicine. 2018;13:1707–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geng Z, Wang R, Zhuo X, Li Z, Huang Y, Ma L, et al. Incorporation of silver and strontium in hydroxyapatite coating on titanium surface for enhanced antibacterial and biological properties. Mater Sci Eng C Mater Biol Appl. 2017;71:852–61.

    Article  CAS  PubMed  Google Scholar 

  • Geng Z, Wang X, Zhao J, Li Z, Ma L, Zhu S, et al. The synergistic effect of strontium-substituted hydroxyapatite and microRNA-21 on improving bone remodeling and osseointegration. Biomater Sci. 2018;6(10):2694–703.

    Article  CAS  PubMed  Google Scholar 

  • Horiuchi M, Madokoro K, Nozaki K, Nakamura M, Katayama K, Nagai A, et al. Electrical conductivity of polycrystalline hydroxyapatite and its application to electret formation. Solid State Ionics. 2018;315:19–25.

    Article  CAS  Google Scholar 

  • Ignjatović N, Ajduković Z, Savić V, Najman S, Mihailović D, Vasiljević P, et al. Nanoparticles of cobalt-substituted hydroxyapatite in regeneration of mandibular osteoporotic bones. J Mater Sci Mater Med. 2013;24(2):343–54.

    Article  PubMed  CAS  Google Scholar 

  • Johnson A. The influence of strontium on characteristic factors of bone. Calcif Tissue Res. 1973;1:215–21.

    Article  Google Scholar 

  • Johnson AR, Armstrong WD, Singer L. The incorporation and removal of large amounts of strontium by physiologic mechanisms in mineralized tissues of the rat. Calcif Tissue Res. 1968;2:242–52.

    Article  CAS  PubMed  Google Scholar 

  • Kallistová A, Skála R, Šlouf M, Čejchan P, Matulková I, Horáček I. Enamel apatite crystallinity significantly contributes to mammalian dental adaptations. Sci Rep. 2018;8(1):5544.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim HM, Himeno T, Kokubo T, Nakamura T. Process and kinetics of bonelike apatite formation on sintered hydroxyapatite in a simulated body fluid. Biomaterials. 2005;26(21):4366–73.

    Article  CAS  PubMed  Google Scholar 

  • Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials. 2006;27:2907–15.

    Article  CAS  PubMed  Google Scholar 

  • Kottegoda N, Sandaruwan C, Priyadarshana G, Siriwardhana A, Rathnayake UA, Berugoda Arachchige DM, et al. Urea-hydroxyapatite nanohybrids for slow release of nitrogen. ACS Nano. 2017;11(2):1214–21.

    Article  CAS  PubMed  Google Scholar 

  • Kung KC, Lee TM, Lui TS. Bioactivity and corrosion properties of novel coatings containing strontium by micro-arc oxidation. J Alloys Compd. 2010;508:384–90.

    Article  CAS  Google Scholar 

  • Lee JH, Jang HL, Lee KM, Baek HR, Jin K, Noh JH. Cold-spray coating of hydroxyapatite on a three-dimensional polyetheretherketone implant and its biocompatibility evaluated by in vitro and in vivo mini pig model. J Biomed Mater Res B Appl Biomater. 2017;105(3):647–57.

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Ko YM, Choe HC. Electrochemical deposition of hydroxyapatite substituted with magnesium and strontium on Ti-6Al-4V alloy. J Nanosci Nanotechnol. 2018;18(2):1449–52.

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Thompson BC, Dong Z, Khor KA. Optical and biological properties of transparent nanocrystalline hydroxyapatite obtained through spark plasma sintering. Mater Sci Eng C Mater Biol Appl. 2016;69:956–66.

    Article  CAS  PubMed  Google Scholar 

  • Li H, Wu J, Dong LY, Zhu YJ, Wu D, Hu X. Flexible, high-wettability and fire-resistant separators based on hydroxyapatite nanowires for advanced lithium-ion batteries. Adv Mater. 2017;29:1703548.

  • Li J, Liu X, Park S, Miller AL 2nd, Terzic A, Lu L. Strontium-substituted hydroxyapatite stimulates osteogenesis on poly(propylene fumarate) nanocomposite scaffolds. J Biomed Mater Res A. 2019;107(3):631–42.

    Article  CAS  PubMed  Google Scholar 

  • Lincks J, Boyan BD, Blanchard CR, Lohmann CH, Liu Y, Cochran DL, et al. Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials. 1998;19(23):2219–32.

    Article  CAS  PubMed  Google Scholar 

  • Ling S, Qin Z, Huang W, Cao S, Kaplan DL, Buehler MJ. Design and function of biomimetic multilayer water purification membranes. Sci Adv. 2017;3(4):e1601939.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mao L, Xia L, Chang J, Liu J, Jiang L, Wu C, et al. The synergistic effects of Sr and Si bioactive ions on osteogenesis, osteoclastogenesis and angiogenesis for osteoporotic bone regeneration. Acta Biomater. 2017;61:217–32.

    Article  CAS  PubMed  Google Scholar 

  • Marie PJ, Hott M. Short-term effects of fluoride and strontium on bone formation and resorption in the mouse. Metabolism. 1986;35(6):547–51.

    Article  CAS  PubMed  Google Scholar 

  • McManamon C, De Silva JP, Power J, Ramirez-Garcia S, Morris MA, Cross GLW. Interfacial characteristics and determination of cohesive and adhesive strength of plasma-coated hydroxyapatite via nanoindentation and microscratch techniques. Langmuir. 2014;30:11412–20.

  • Meininger M, Wolf-Brandstetter C, Zerweck J, Wenninger F, Gbureck U, Groll J, et al. Electrochemically assisted deposition of strontium modified magnesium phosphate on titanium surfaces. Mater Sci Eng C Mater Biol Appl. 2016;67:65–71.

    Article  CAS  PubMed  Google Scholar 

  • Mishra VK, Rai SB, Asthana BP, Parkash O, Kumar D. Effect of annealing on nanoparticles of hydroxyapatite synthesized via microwave irradiation: structural and spectroscopic studies. Ceram Int. 2014;40:11319–28.

    Article  CAS  Google Scholar 

  • Mondal S, Manivasagan P, Bharathiraja S, Santha Moorthy M, Kim HH, Seo H, et al. Magnetic hydroxyapatite: a promising multifunctional platform for nanomedicine application. Int J Nanomedicine. 2017;12:8389–410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montesi M, Panseri S, Dapporto M, Tampieri A, Sprio S. Sr-substituted bone cements direct mesenchymal stem cells, osteoblasts and osteoclasts fate. PLoS One. 2017;12(2):e0172100.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nagano M, Nakamura T, Kokubo T, Tanahashi M, Ogawa M. Differences of bone bonding ability and degradation behaviour in vivo between amorphous calcium phosphate and highly crystalline hydroxyapatite coating. Biomaterials. 1996;17:1771–7.

    Article  CAS  PubMed  Google Scholar 

  • Nelson BK, Deniro MK, Schoeninger MJ, De Paolo DJ. Effects of diagenesis on strontium, carbon, nitrogen and oxygen concentration and isotopic composition of bone. Geochim Cosmochim Acta. 1986;50:1941–9.

    Article  CAS  Google Scholar 

  • Ni GX, Chiu KY, Lu WW, Wang Y, Zhang YG, Hao LB, et al. Strontium-containing hydroxyapatite bioactive bone cement in revision hip arthroplasty. Biomaterials. 2006;27(24):4348–55.

    Article  CAS  PubMed  Google Scholar 

  • Nieh TG, Jankowski AF, Koike J. Processing and characterization of hydroxyapatite coatings on titanium produced by magnetron sputtering. J Mater Res. 2001;16:3238–45.

    Article  CAS  Google Scholar 

  • Omdahl JL, Deluca HF. Rachitogenic activity of dietary strontium: inhibition of intestinal calcium absorption and 1,25 dihydroxycholecalciferol synthesis. J Biol Chem. 1972;247:5520–6.

    Article  CAS  PubMed  Google Scholar 

  • Palchik NA, Grigoreva TN, Stolpovskaya VN, Arkhipenko DK, Moroz TN. Effect of synthetic conditions on structural characteristics of hydroxylapatite. Russ J Appl Chem. 1997;70:1513–6.

    Google Scholar 

  • Petrakova NV, Ashmarin AA, Baranov OV, Fedotov AY, Barinov SM, Komlev VS. High-temperature solid-phase interaction of hydroxyapatite with mg, Sr, and Zn nitrates. Dokl Chem. 2018;483:283–6.

    Article  CAS  Google Scholar 

  • Quade M, Schumacher M, Bernhardt A, Lode A, Kampschulte M, Voß A, et al. Strontium-modification of porous scaffolds from mineralized collagen for potential use in bone defect therapy. Mater Sci Eng C Mater Biol Appl. 2018;84:159–67.

    Article  CAS  PubMed  Google Scholar 

  • Querido W, Farina M. Strontium ranelate increases the formation of bone-like mineralized nodules in osteoblast cell cultures and leads to Sr incorporation into the intact nodules. Cell Tissue Res. 2013;354(2):573–80.

    Article  CAS  PubMed  Google Scholar 

  • Querido W, Rossi AL, Farina M. The effects of strontium on bone mineral: a review on current knowledge and microanalytical approaches. Micron. 2016;80:122–34.

    Article  CAS  PubMed  Google Scholar 

  • Rau JV, Cesaro SN, Ferro D, Barinov SM, Fadeeva IV. FTIR study of carbonate loss from carbonated apatites in the wide temperature range. J Biomed Mater Res B Appl Biomater. 2004;71B:441–7.

    Article  CAS  Google Scholar 

  • Rau JV, Ferro D, Falcone MB, Generosi A, Rossi Albertini V, Latini A, et al. Hardness of zirconium diboride films deposited on titanium substrates. Mater Chem Phys. 2008;112:504–9.

    Article  CAS  Google Scholar 

  • Rau JV, Generosi A, Laureti S, Komlev VS, Ferro D, Nunziante Cesaro S, et al. Physicochemical investigation of pulsed laser deposited carbonated hydroxyapatite films on titanium. ACS Appl Mater Interfaces. 2009;1:1813–20.

    Article  CAS  PubMed  Google Scholar 

  • Rau JV, Smirnov VV, Laureti S, Generosi A, Varvaro G, Fosca M, et al. Properties of pulsed laser deposited fluorinated hydroxyapatite films on titanium. Mater Res Bull. 2010;45:1304–10.

    Article  CAS  Google Scholar 

  • Reginster JY, Brandi ML, Cannata-Andía J, Cooper C, Cortet B, Feron JM, et al. The position of strontium ranelate in today’s management of osteoporosis. Osteoporos Int. 2015;26:1667–71.

    Article  CAS  PubMed  Google Scholar 

  • Robinson L, Salma-Ancane K, Stipniece L, Meenan BJ, Boyd AR. The deposition of strontium and zinc Co-substituted hydroxyapatite coatings. J Mater Sci Mater Med. 2017;28(3):51.

    Article  CAS  PubMed  Google Scholar 

  • Saidak Z, Marie PJ. Strontium signaling: molecular mechanisms and therapeutic implications in osteoporosis. Pharmacol Ther. 2012;136(2):216–26.

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Qi Y, Jin B, Wang X, Hu Y, Jiang Q. Control of hydroxyapatite coating by self-assembled monolayers on titanium and improvement of osteoblast adhesion. J Biomed Mater Res B Appl Biomater. 2017;105(1):124–35.

    Article  CAS  PubMed  Google Scholar 

  • Shorr E, Carter AC. The usefulness of strontium as an adjuvant to calcium in the remineralization of the skeleton in man. Bull Hosp Joint Dis. 1952;13:59–66.

    CAS  PubMed  Google Scholar 

  • Stepan JJ. Strontium ranelate: in search of the mechanism of action. J Bone Miner Metab. 2013;31:606–12.

    Article  CAS  PubMed  Google Scholar 

  • Teng HP, Lin HY, Huang YH, Lu FH. Formation of strontium-substituted hydroxyapatite coatings on bulk Ti and TiN-coated substrates by plasma electrolytic oxidation. Surf Coat Technol. 2018;350:1112–9.

  • Terra J, Dourado ER, Eon JG, Ellis DE, Gonzalez G, Rossi AM. The structure of strontium-doped hydroxyapatite: an experimental and theoretical study. Phys Chem Chem Phys. 2009;11:568–77.

    Article  CAS  PubMed  Google Scholar 

  • Tite T, Popa AC, Balescu LM, Bogdan IM, Pasuk I, Ferreira JMF, et al. Cationic substitutions in hydroxyapatite: current status of the derived biofunctional effects and their in vitro interrogation methods. Materials. 2018;11:2081.

    Article  PubMed Central  CAS  Google Scholar 

  • Tlotleng M, Akinlabi E, Shukla M, Pityana S. Microstructures, hardness and bioactivity of hydroxyapatite coatings deposited by direct laser melting process. Mater Sci Eng C. 2014;43:189–98.

    Article  CAS  Google Scholar 

  • Tsui YC, Doyle C, Clyne TW. Plasma sprayed hydroxyapatite coatings on titanium substrates part 1: mechanical properties and residual stress levels. Biomaterials. 1998;19:2015–29.

    Article  CAS  PubMed  Google Scholar 

  • Tuukkanen J, Nakamura M. Hydroxyapatite as a nanomaterial for advanced tissue engineering and drug therapy. Curr Pharm Des. 2017;23(26):3786–93.

    Article  CAS  PubMed  Google Scholar 

  • Uskoković V. Disordering the disorder as the route to a higher order: incoherent crystallization of calcium phosphate through amorphous precursors. Cryst Growth Des. 2019;19(8):4340–57.

    Article  CAS  Google Scholar 

  • Uskoković V, Desai TA. Phase composition control of calcium phosphate nanoparticles for tunable drug delivery kinetics and treatment of osteomyelitis. II. Antibacterial and osteoblastic response. J Biomed Mater Res A. 2013;01(5):1427–36.

    Article  CAS  Google Scholar 

  • Uskoković V, Uskoković DP. Nanosized hydroxyapatite and other calcium phosphates: chemistry of formation and application as drug and gene delivery agents. J Biomed Mater Res B Appl Biomater. 2011;96B:152–91.

    Article  CAS  Google Scholar 

  • Uskoković V, Wu VM. Calcium phosphate as a key material for socially responsible tissue engineering. Materials. 2016;9:434–60.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uskoković V, Iyer MA, Wu VM. One ion to rule them all: combined antibacterial, osteoinductive and anticancer properties of selenite-incorporated hydroxyapatite. J Mater Chem B. 2017;5:1430–45.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uskoković V, Janković-Častvan I, Wu VM. Bone mineral crystallinity governs the orchestration of ossification and resorption during bone remodeling. ACS Biomater Sci Eng. 2019;5:3483–98.

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Von Euw S, Fernandes FM, Cassaignon S, Selmane M, Laurent G, et al. Water mediated structuring of bone apatite. Nat Mater. 2013;12(12):1144–53.

    Article  CAS  PubMed  Google Scholar 

  • Wang TL, Yang GZ, Zhou WC, Hu JZ, Jia WW, Lu W. One-pot hydrothermal synthesis, in vitro biodegradation and biocompatibility of Sr-doped nanorod/nanowire hydroxyapatite coatings on ZK60 magnesium alloy. J Alloys Compd. 2019;799:71–82.

    Article  CAS  Google Scholar 

  • Wopenka B, Pasteris JD. A mineralogical perspective on the apatite in bone. Mater Sci Eng C. 2005;25(2):131–43.

    Article  CAS  Google Scholar 

  • Yang F, Yang D, Tu J, Zheng Q, Cai L, Wang L. Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin signaling. Stem Cells. 2011;29(6):981–91.

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Li L, Xiao L, Zhang D. Recycle the dental fairy’s package: overview of dental pulp stem cells. Stem Cell Res Ther. 2018;9(1):347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu DG, Ding HF, Mao YQ, Liu M, Yu B, Zhao X, et al. Strontium ranelate reduces cartilage degeneration and subchondral bone remodeling in rat osteoarthritis model. Acta Pharmacol Sin. 2013;34(3):393–402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The technical assistance of Mr. Massimo Di Menno Di Bucchianico, Mr. Luca Imperatori, and Mr. Marco Ortenzi is gratefully acknowledged.

Funding

The present research was partially supported by the Italian Ministry of Health, grant codes IZS LT 02/15 RC and IZS LT 01/17 RC.

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Authors and Affiliations

  1. Dipartimento di Scienze, Università della Basilicata, Via dell’Ateneo Lucano, 10, 85100, Potenza, Italy

    Angela De Bonis, Mariangela Curcio & Roberto Teghil

  2. Department of Mechanical and Aerospace Engineering, University of California Irvine, Engineering Gateway 4200, Irvine, CA, 92697, USA

    Vuk Uskoković

  3. Istituto Zooprofilattico Sperimentale Lazio e Toscana “M. Aleandri”, Via Appia Nuova, 1411, 00178, Rome, Italy

    Katia Barbaro

  4. AA Baikov Institute of Metallurgy and Materials Science, Russian Academy of Sciences, Leninsky prospect 49, Moscow, Russia, 119991

    Inna Fadeeva

  5. Istituto di Struttura della Materia, Consiglio Nazionale delle Ricerche (ISM-CNR), Via del Fosso del Cavaliere 100, 00133, Rome, Italy

    Luca Imperatori & Julietta V. Rau

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  1. Angela De Bonis
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De Bonis, A., Uskoković, V., Barbaro, K. et al. Pulsed laser deposition temperature effects on strontium-substituted hydroxyapatite thin films for biomedical implants. Cell Biol Toxicol 36, 537–551 (2020). https://doi.org/10.1007/s10565-020-09527-3

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