Zinc-substituted structures of hydroxyapatite: Modeling and experiment

V. S. Bystrov ; E. V. Paramonova ; S. V. Filippov ; L. A. Avakyan ; M. V. Chaikina ; N. V. Eremina ; S. V. Makarova ; N. V. Bulina

Matematičeskaâ biologiâ i bioinformatika, Tome 18 (2023) no. 2, pp. 580-601.

Résumé

The results of calculations of the substitution of calcium atoms for zinc in the structure of hydroxyapatite using density functional theory methods using hybrid functionals in the supercell model are presented. Changes in the parameters and volume of the unit cell, energy bands and energy of formation of substitutions with increasing number of substitutions in different positions of calcium (Ca1 and Ca2) are analyzed in comparison with experimental data. A proportional decrease in the parameters and volume of the cell with an increase in the number of substitutions has been established, and a more complex behavior of various cell parameters has been revealed, which is a consequence of the violation of the original symmetry. Electronic energy levels were found to depend on the zinc concentration and the positions of the calcium ions being replaced. In this case, the band gap $Eg$ of hydroxyapatite experiences a jump of 0.6–0.8 eV with the introduction of one zinc ion per supercell, and then decreases and reaches values below the initial $Eg$ value by 0.5–0.6 eV for substitutions in Ca1 positions, and by 0.8–0.9 eV for substitutions in Ca2 positions. It has been shown that the energy of substitution has a complex dependence on the concentration of the substituent and the replacement of calcium ions with zinc occurs predominantly in the Ca2 position over the entire concentration range. An analysis of changes in interatomic distances during the process of relaxation to the equilibrium state at different zinc concentrations was carried out. We revealed formation of bonds between zinc atoms and nearby oxygen anions, which violates the original symmetry of hydroxypatite structures. The data obtained are important for understanding the structural changes that occur during substitution, as well as for understanding and predicting the properties of synthesized biocompatible materials.

Bibliographie

[1] M. Epple, K. Ganesan, R. Heumann, J. Klesing, A. Kovtun, S. Neumann, V. Sokolova, “Application of calcium phosphate nanoparticles in biomedicine”, Journal of Materials Chemistry, 20:1 (2010), 18–23 | DOI | MR

[2] Ducheyne P., K. Healy, D. E. Hutmacher, D. W. Grainger, C. J. Kirkpatrick (eds.), Comprehensive Biomaterials II, 2nd ed, Elsevier, Amsterdam, 2017

[3] T. Duminis, S. Shahid, R. G. Hill, “Apatite Glass-Ceramics: A Review”, Front. Mater, 3 (2017), 59 | DOI

[4] B. D. Ratner, A. S. Hoffman, F. J. Schoen, J. E. Lemons, Biomaterials Science, Academic Press, Oxford, 2013

[5] S. M. Barinov, V. S. Komlev, Biokeramika na osnove fosfatov kaltsiya, Nauka, M., 2005, 204 pp.

[6] S. V. Dorozhkin, “Calcium orthophosphate deposits: Preparation, properties and biomedical applications”, Mater. Sci. Eng. C Mater. Biol. Appl., 55 (2015), 272–326 | DOI

[7] J. T.B. Ratnayake, M. Mucalo, G. J. Dias, “Substituted hydroxyapatites for bone regeneration: A review of current trends”, J. Biomed. Mater. Res. B Appl. Biomater., 105 (2017), 1285–1299 | DOI

[8] J. C. Elliot, Structure and Chemistry of the Apatites and Other Calcium Orthophosphates, Elsevier, Amsterdam, 1994

[9] M. I. Kay, R. A. Young, A. S. Posner, “Crystal Structure of Hydroxyapatite”, Nature (London), 204 (1964), 1050–1052 | DOI

[10] M. Mucalo, Hydroxyapatite (HAp) for Biomedical Applications, Elsevier, Amsterdam, 2015

[11] M. Supova, “Substituted hydroxyapatites for biomedical applications: A review”, Ceram. Int., 41 (2015), 9203–9231 | DOI

[12] A. Fihri, C. Len, R. S. Varma, A. Solhy, “Hydroxyapatite: A review of syntheses, structure and applications in heterogeneous catalysis”, Coord. Chem. Rev., 347 (2017), 48–76 | DOI

[13] V. S. Bystrov, “Computational Studies of the Hydroxyapatite Nanostructures, Peculiarities and Properties”, Math. Biol. Bioinform., 12 (2017), 14–54 | DOI

[14] V. Bystrov, A. Bystrova, Y. Dekhtyar, I. A. Khlusov, V. Pichugin, K. Prosolov, Y. Sharkeev, “Electrical functionalization and fabrication of nanostructured hydroxyapatite coatings”, Bioceramics and Biocomposites: From Research to Clinical Practice, ed. A. Jiulian, John Wiley Sons, Inc., Hoboken, 2019, 149–190 | DOI

[15] B. Leon, J. A. Janson, Thin Calcium Phosphate Coatings for Medical Implants, Springer, Berkkin, 2009

[16] K. Baltacis, V. Bystrov, A. Bystrova, Y. Dekhtyar, T. Freivalds, J. Raines, K. Rozenberga, H. Sorokins, M. Zeidaks, “Physical fundamentals of biomaterials surface electrical functionalization”, Materials, 13 (2020), 4575 | DOI

[17] V. S. Bystrov, C. Piccirillo, D. M. Tobaldi, P. M.L. Castro, J. Coutinho, S. Kopyl, R. C. Pullar, “Oxygen vacancies, the optical band gap (Eg) and photocatalysis of hydroxyapatite: Comparing modelling with measured data”, Appl. Catal. B Environ., 196 (2016), 100–107 | DOI

[18] E. X. Figueroa-Rosales, J. Martinez-Juarez, E. Garcia-Diaz, D. Hernandez-Cruz, S. A. Sabinas-Hernandez, M. J. Robles-Aguila, “Photoluminescent Properties of Hydroxyapatite and Hydroxyapatite/Multi-Walled Carbon Nanotube Composites”, Crystals, 11 (2021), 832 | DOI

[19] A. Oulguidoum, K. Bouiahya, H. Bouyarmane, A. Talbaoui, J. M. Nunzi, A. Laghzizil, “Mesoporous nanocrystalline sulfonated hydroxyapatites enhance heavy metal removal and antimicrobial activity”, Sep. Purif. Technol., 255 (2020), 117777 | DOI

[20] P. Yang, P. Yang, X. Teng, J. Lin, L. Huang, “A novel luminescent mesoporous silica/apatite composite for controlled drug release”, J. Mater. Chem., 21 (2011), 5505–5510 | DOI

[21] Y. Wen, J. Li, H. Lin, H. Huang, K. Song, K. Duan, T. Guo, J. Weng, “Improvement of Drug-Loading Properties of Hydroxyapatite Particles Using Triethylamine as a Capping Agent: A Novel Approach”, Crystals, 11 (2021), 703 | DOI

[22] L. Degli Esposti, F. Carella, A. Adamiano, A. Tampieri, M. Iafisco, “Calcium phosphate based nanosystems for advanced targeted nanomedicine”, Drug Dev. Ind. Pharm., 44 (2018), 1223–1238 | DOI

[23] L. Avakyan, E. Paramonova, V. Bystrov, J. Coutinho, S. Gomes, G. Renaudin, Iron in Hydroxyapatite: Interstitial or Substitution Sites?, Nanomaterials, 11 (2021), 2978 | DOI

[24] S. Mondal, P. Manivasagan, S. Bharathiraja, M. Santha Moorthy, H. H. Kim, H. Seo, K. D. Lee, J. Oh, “Magnetic hydroxyapatite: A promising multifunctional platform for nanomedicine application”, Int. J. Nanomed., 12 (2017), 8389–8410 | DOI

[25] A. Tampieri, T. D'Alessandro, M. Sandri, S. Sprio, E. Landi, L. Bertinetti, S. Panseri, G. Pepponi, J. Goettlicher, M. Banobre-Lopez et al, “Intrinsic magnetism and hyperthermia in bioactive Fe-doped hydroxyapatite”, Acta Biomater., 8 (2012), 843–851 | DOI

[26] J. D. Currey, Bones Structures and Mechanics, 2nd ed., Princeton University Press, Princeton, 2002

[27] J. C. Crockett, M. J. Rogers, F. P. Coxon, L. J. Hocking, M. H. Helfrich, “Bone remodelling at a glance”, Journal of Cell Science, 124:7 (2011), 991–998 | DOI | MR

[28] K. J. Koester, J. W. Ager III, R. O. Ritchie, “The true toughness of human cortical bone measured with realistically short cracks”, Nat. Mater., 7 (2008), 672–677 | DOI

[29] S. Weiner, P. A. Price, “Disaggregation of bone into crystals”, Calcif. Tissue Int., 39 (1986), 365–375 | DOI

[30] N. Kanzaki, K. Onuma, A. Ito, K. Teraoka, T. Tateishi, S. Tsutsumi, “Direct growth rate measurement of hydroxyapatite single crystal by moire phase shift interferometry”, J. Phys. Chem. B, 102 (1998), 6471–6476 | DOI

[31] J. M. Hughes, M. Cameron, K. D. Crowley, “Structural variations in natural F, OH, and Cl apatites”, American Mineralogist, 74 (1989), 870–876 (accessed: 07.12.2023) http://rruff.geo.arizona.edu/AMS/result.php

[32] T. Tite, A. C. Popa, L. M. Balescu, I. M. Bogdan, I. Pasuk, J. M.F. Ferreira, G. E. Stan, “Cationic Substitutions in Hydroxyapatite: Current Status of the Derived Biofunctional Effects and Their In Vitro Interrogation Methods”, Materials, 11 (2018), 2081 | DOI

[33] S. P. Khanal, H. Mahfuz, A. J. Rondinone, T. Leventouri, “Improvement of the fracture toughness of hydroxyapatite (HAp) by incorporation of carboxyl functionalized single walled carbon nanotubes (CfSWCNTs) and nylon”, Mater. Sci. Eng. C Mater. Biol. Appl., 60 (2016), 204–210 | DOI

[34] I. Uysal, F. Severcan, A. Tezcaner, Z. Evis, “Co-doping of hydroxyapatite with zinc and fluoride improves mechanical and biological properties of hydroxyapatite”, Prog. Nat. Sci., 24 (2014), 340–349 | DOI

[35] M. V. Chaikina, N. V. Bulina, I. Yu. Prosanov, A. V. Ischenko, “Anionnye zamescheniya v protsesse mekhanokhimicheskogo sinteza gidroksiapatita”, Khimiya v interesakh ustoichivogo razvitiya, 27 (2019), 345–352 | DOI

[36] A. Bigi, E. Foresti, R. Gregorini, A. Ripamonti, N. Roveri, J. Shah, “The role of magnesium on the structure of biological apatites”, Calcif. Tissue Int., 50 (1992), 439–444 | DOI

[37] F. Ren, Y. Leng, R. Xin, X. Ge, “Synthesis, Characterization and Ab Initio Simulation of Magnesium-Substituted Hydroxyapatite”, Acta Biomater., 6 (2010), 2787–2796 | DOI

[38] W. Mroz, B. Budner, R. Syroka, K. Niedzielski, G. Golanski, A. Slosarczyk, D. Schwarze, T. E. Douglas, “In vivo implantation of porous titanium, alloy implants coated with magnesium-doped octacalcium phosphate and hydroxyapatite thin films using pulsed laser depostion”, Journal of Biomedical Materials Research Part B: Applied Biomaterials, 103:1 (2015), 151–158 | DOI

[39] W. Mroz, A. Bombalska, S. Burdynska, M. Jedynski, A. Prokopiuk, B. Budner, A. Slosarczyk, A. Zima, E. Menaszek, A. Scislowska-Czarnecka et al, “Structural studies of magnesium doped hydroxyapatite coatings after osteoblast culture”, J. Mol. Struct., 977 (2010), 145–152 | DOI

[40] L. M. Silva, D. S. Tavares, E. A. Santos, “Isolating the Effects of Mg$^{2+}$, Mn$^{2+}$ and Sr$^{2+}$ Ions on Osteoblast Behavior from those Caused by Hydroxyapatite Transformation”, Materials Research, 23:2 (2020) | DOI

[41] I. Fadeeva, V. Kalita, D. Komlev, A. Radiuk, A. Fomin, G. Davidova, N. Fursova, F. Murzakhanov, M. Gafurov, M. Fosca et al, “In Vitro Properties of Manganese Substituted Tricalcium Phosphate Coatings for Titanium Biomedical Implants Deposited by Arc Plasma”, Materials, 13 (2020), 4411 | DOI

[42] Fadeeva I.V., Fomin A.S., Barinov S.M., Davydova G.A., Selezneva I.I., Preobrazhenskii I.I., Rusakov M.K., Fomina A.A., Volchenkova V.A., “Synthesis and Properties of Manganese-Containing Calcium Phosphate Materials”, Inorganic Materials, 56:7 (2020), 700–706 | DOI | DOI

[43] H. Liu, X. Cui, X. Lu, X. Liu, L. Zhang, T. S. Chan, “Mechanism of Mn incorporation into hydroxyapatite: Insights from SR-XRD, Raman, XAS, and DFT calculation”, Chem. Geol., 579 (2021), 120354 | DOI

[44] S. Lala, T. Maity, M. Singha, K. Biswas, S. Pradhan, “Effect of doping (Mg, Mn, Zn) on the microstructure and mechanical properties of spark plasma sintered hydroxyapatites synthesized by mechanical alloying”, Ceram. Int., 43 (2017), 2389–2397 | DOI

[45] I. V. Fadeeva, N. V. Bakunova, V. S. Komlev, “Tsink- i serebrosoderzhaschie gidroksiapatity: sintez i svoistva”, Doklady Akademii nauk, 442:6 (2012), 780–783

[46] M. V. Chaikina, N. V. Bulina, I. Yu. Prosanov, O. B. Vinokurova, A. V. Ischenko, “Formirovanie struktury tsink-zameschennogo gidroksiapatita v protsesse mekhanokhimicheskogo sinteza”, Neorganicheskie materialy, 56:4 (2020), 422–428 | DOI

[47] N. V. Bulina, O. V. Vinokurova, N. V. Eremina, I. Y. Prosanov, V. R. Khusnutdinov, M. V. Chaikina, “Features of solid-phase mechanochemical synthesis of hydroxyapatite doped by copper and zinc ions”, Journal of Solid State Chemistry, 296 (2021), 121973 | DOI

[48] M. V. Chaikina, N. V. Bulina, I. Yu. Prosanov, O. V. Vinokurova, A. V. Ischenko, “Structure formation of zinc-substituted hydroxyapatite during mechanochemical synthesis”, Inorg. Mater., 56:4 (2020), 402–408 | DOI

[49] N. V. Bulina, M. V. Chaikina, A. S. Andreev, O. B. Lapina, A. V. Ishchenko, I. Yu. Prosanov, K. B. Gerasimov, L. A. Solovyov, “Mechanochemical Synthesis of SiO44-Substituted Hydroxyapatite, Part II - Reaction Mechanism, Structure, and Substitution Limit”, Eur. J. Inorg. Chem., 2014:28 (2014), 4810–4825 | DOI

[50] N. V. Bulina, M. V. Chaikina, I. Y. Prosanov, “Mechanochemical Synthesis of Sr Substituted Hydroxyapatite”, Inorg. Mater., 54 (2018), 820–825 | DOI

[51] N. V. Bulina, S. V. Makarova, I. Y. Prosanov, O. B. Vinokurova, N. Z. Lyakhov, “Structure and thermal stability of fluorhydroxyapatite and fluorapatite obtained by mechanochemical method”, J. Solid State Chem., 282 (2020), 121076 | DOI

[52] N. V. Bulina, S. V. Makarova, S. G. Baev, A. A. Matvienko, K. B. Gerasimov, O. A. Logutenko, V. S. Bystrov, “A Study of Thermal Stability of Hydroxyapatite”, Minerals, 11 (2021), 1310 | DOI

[53] S. Aryal, K. Matsunaga, W. Y. Ching, “Ab initio simulation of elastic and mechanical properties of Zn- and Mg-doped hydroxyapatite (HAP)”, J. Mech. Behav. Biomed. Mater., 47 (2015), 135–146 | DOI

[54] K. Matsunaga, A. Kuwabara, “First-principles study of vacancy formation in hydroxyapatite”, Phys. Rev. B, 75 (2007), 014102 | DOI

[55] A. Slepko, A. A. Demkov, “First-principles study of the biomineral hydroxyapatite”, Phys. Rev. B Condens. Matter Mater. Phys., 84. (2011), 134108 | DOI

[56] A. V. Sadetskaya, N. P. Bobrysheva, M. G. Osmolowsky, O. M. Osmolovskaya, M. A. Voznesenskiy, “Correlative experimental and theoretical characterization of transition metal doped hydroxyapatite nanoparticles fabricated by hydrothermal method”, Mater. Charact., 173 (2021), 110911 | DOI

[57] V. S. Bystrov, J. Coutinho, A. V. Bystrova, Y. D. Dekhtyar, R. C. Pullar, A. Poronin, E. Palcevskis, A. Dindune, B. Alkan, C. Durucan, “Computational study of the hydroxyapatite structures, properties and defects”, J. Phys. D Appl. Phys., 48 (2015), 195302 | DOI

[58] V. Bystrov, E. Paramonova, L. Avakyan, J. Coutinho, N. Bulina, “Simulation and Computer Study of Structures and Physical Properties of Hydroxyapatite with Various Defects”, Nanomaterials, 11 (2021), 2752 | DOI

[59] L. A. Avakyan, E. V. Paramonova, J. Coutinho, S. Oberg, V. S. Bystrov, L. A. Bugaev, “Optoelectronics and defect levels in hydroxyapatite by first-principles”, J. Chem. Phys, 148 (2018), 154706 | DOI

[60] V. S. Bystrov, L. A. Avakyan, E. V. Paramonova, J. Coutinho, “Sub-Band Gap Absorption Mechanisms Involving Oxygen Vacancies in Hydroxyapatite”, J. Chem. Phys., 123 (2019), 4856–4865 | DOI

[61] V. S. Bystrov, E. V. Paramonova, L. A. Avakyan, N. V. Eremina, S. V. Makarova, N. V. Bulina, “Effect of Magnesium Substitution on Structural Features and Properties of Hydroxyapatite”, Materials, 16 (2023), 5945 | DOI

[62] V. S. Bystrov, E. V. Paramonova, A. V. Bystrova, L. A. Avakyan, S. V. Makarova, D. D. Isaev, N. V. Bulina, “Vliyanie zameschenii atomov Ca na atomy Sr, Mg, Mn, Fe v strukture gidroksiapatita i izmenenii elektricheskogo polya na ego fizicheskie svoistva, vazhnye dlya biomeditsiny”, Sbornik nauchnykh trudov VII s'ezda biofizikov Rossii, v. 1, KubGTU, Krasnodar, 2023, 278–279 | DOI

[63] J. P. Perdew, K. Burke, M. Ernzerhof, “Generalized Gradient Approximation Made Simple”, Phys. Rev. Lett., 77 (1996), 3865–3868 | DOI

[64] J. Heyd, G. E. Scuseria, M. Ernzerhof, “Hybrid functionals based on a screened Coulomb potential”, J. Chem. Phys., 118 (2003), 8207–8215 | DOI

[65] A. V. Krukau, O. A. Vydrov, A. F. Izmaylov, G. E. Scuseria, “Influence of the exchange screening parameter on the performance of screened hybrid functionals”, J. Chem. Phys., 125 (2006), 224106 | DOI

[66] Quantum ESPRESSO, (accessed: 07.12.2023) https://www.quantum-espresso.org/

[67] M. Schlipf, F. Gygi, “Optimization algorithm for the generation of ONCV pseudopotentials”, Computer Phys. Commun., 196 (2015), 36–44 | DOI | Zbl

[68] D. R. Hamann, “Optimized norm-conserving Vanderbilt pseudopotentials”, Phys. Rev., B88 (2013), 085117 | DOI

[69] J. Nocedal, S. J. Wright, Numerical Optimization, Springer, New York, 2006 | MR | Zbl

[70] M. Avriel, Nonlinear Programming: Analysis and Methods, Dover Publishing, 2003 | MR | Zbl

[71] S. V. Filippov, R. V. Polozov, V. S. Sivozhelezov, “Vizualizatsiya prostranstvennykh struktur (bio)makromolekul v vide podobnykh gipsometricheskim kart”, Preprinty IPM im. M.V. Keldysha, 2019, 061, 14 pp. | DOI