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Understanding Composition–Structure– Bioactivity Correlations Understanding Composition–Structure– Bioactivity Correlations in Bioactive Glasses Yang Yu Academic dissertation for the Degree of Doctor of Philosophy in Physical Chemistry at Stockholm University to be publicly defended on Wednesday 12 December 2018 at 13.00 in De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 14. Abstract Bioactive glasses integrate with bone/tooth tissues by forming a layer of hydroxy-carbonate apatite (HCA), which mimics the composition of bone mineral. In the current thesis, we investigated composition–structure–bioactivity correlations of phosphosilicate and borophosphosilicate (BPS) glasses. Bioactive phosphosilicate glasses extend the compositional space of the ”45S5 Bioglass®”, which has been in clinical use for decades. Recently developed bioactive BPS glasses with SiO2→B2O3 substitutions transform more completely into HCA and their glass dissolution behaviors can be tuned by varying the relative contents of B and Si. It is known that the average silicate network connectivity NSi and the phosphate content (x(P2O5)) affect the apatite formation (in vitro bioactivity) of phosphosilicate glasses, but the details remain poorly explored. Three series of phosphosilicate glasses were designed by independently varying NSi and x(P2O5). After immersion of the glasses in a simulated body fluid (SBF) for 24 hours, different degrees of their apatite formation were quantified by Fourier-transform infrared (FTIR) spectroscopy. The results revealed that a high P content widened the NSi range that generated optimum amounts of apatite and also mitigated the detrimental effects associated with using glass particles with < 50 μm. The amounts of apatite derived from FTIR agreed with those from 31P magic angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy. The growth of apatite at bioactive glass surfaces was found to follow a sigmoidal growth model, in which the precursor phase, amorphous calcium phosphate (ACP), formed in the induction period and then crystallized into HCA in the following proliferation period, with an improvement in the structural ordering of HCA in the maturation period. This formation process closely resembles the apatite precipitated spontaneously from supersaturated Ca/P-containing solutions. The simultaneous growth of ACP and HCA is discussed in conjunction with a previously proposed mechanism for explaining in vitro bioactivity and apatite growth from bioactive glasses. The short- and medium- range structures of bioactive borophosphosilicate (BPS) glasses were investigated by solid-state MAS NMR. Two series of BPS glasses were designed by gradually replacing SiO2 with B2O3 in the 45S5 glass, as well as another base glass featuring a more condensed glass network. As the B2O3 content is increased, the glass networks become more polymerized, together with decreased fractions of the dominating BO3 and orthophosphate units. Borate groups are homogeneously mixed with the isolated orthophosphate groups, while the remaining phosphate groups exhibit a slight [3] [4] preference for bonding to BO4 over SiO4 units. Linkages among borate groups are dominated by B –O–B linkages at the expenses of B[3]–O–B[3] and B[4]–O–B[4] linkages, with the latter B[4]–O–B[4] motifs disfavored yet abundant. A similar fashion of borate mixing was observed in P-free Na/Ca-based borosilicate glasses that span a large compositional space. [4] [4] The content of B –O–B linkages was found to be controlled by the relative fractions of BO4 groups and non-bridging oxygen ions. Keywords: Bioactive glasses, Phosphosilicate glasses, Borophosphosilicate glasses, Solid-state NMR spectroscopy, Glass structure, Fourier-transform infrared spectroscopy, Hydroxyapatite, Amorphous calcium phosphate, Apatite formation, In vitro bioactivity testing. Stockholm 2018 http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-161477 ISBN 978-91-7797-458-1 ISBN 978-91-7797-459-8 Department of Materials and Environmental Chemistry (MMK) Stockholm University, 106 91 Stockholm UNDERSTANDING COMPOSITION–STRUCTURE–BIOACTIVITY CORRELATIONS IN BIOACTIVE GLASSES Yang Yu Understanding Composition– Structure–Bioactivity Correlations in Bioactive Glasses Yang Yu ©Yang Yu, Stockholm University 2018 ISBN print 978-91-7797-458-1 ISBN PDF 978-91-7797-459-8 Printed in Sweden by Universitetsservice US-AB, Stockholm 2018 To my beloved families and in memory of my father (以dº文.给我²1的Ͳ和已Ç世近A 二t的6²！ Abstract Bioactive glasses integrate with bone/tooth tissues by forming a layer of hydroxy- carbonate apatite (HCA), which mimics the composition of bone mineral. In the current thesis, we investigated composition–structure–bioactivity corre- lations of phosphosilicate and borophosphosilicate (BPS) glasses. Bioactive phosphosilicate glasses extend the compositional space of the “45S5 Bioglassr”, which has been in clinical use for decades. Recently developed bioactive BPS glasses with SiO2!B2O3 substitutions transform more completely into HCA and their glass dissolution behaviors can be tuned by varying the relative con- tents of B and Si. Si It is known that the average silicate network connectivity NBO and the phosphate content (x(P2O5)) affect the apatite formation (in vitro bioactivity) of phosphosilicate glasses, but the details remain poorly explored. Three series Si of phosphosilicate glasses were designed by independently varying NBO and x(P2O5). After immersion of the glasses in a simulated body fluid (SBF) for 24 hours, different degrees of their apatite formation were quantified by Fourier- transform infrared (FTIR) spectroscopy. The results revealed that a high P Si content widened the NBO range that generated optimum amounts of apatite and also mitigated the detrimental effects associated with using glass particles with < 50 mm. The amounts of apatite derived from FTIR agreed with those from 31P magic angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy. The growth of apatite at bioactive glass surfaces was found to follow a sigmoidal growth model, in which the precursor phase, amorphous calcium phosphate (ACP), formed in the induction period and then crystal- lized into HCA in the following proliferation period, with an improvement in the structural ordering of HCA in the maturation period. This formation process closely resembles the apatite precipitated spontaneously from super- saturated Ca/P-containing solutions. The simultaneous growth of ACP and HCA is discussed in conjunction with a previously proposed mechanism for explaining in vitro bioactivity and apatite growth from bioactive glasses. The short- and medium- range structures of bioactive borophosphosili- cate (BPS) glasses were investigated by solid-state MAS NMR. Two series of BPS glasses were designed by gradually replacing SiO2 with B2O3 in the 45S5 glass, as well as another base glass featuring a more condensed glass network. As the B2O3 content is increased, the glass networks become more polymerized, together with decreased fractions of the dominating BO3 and orthophosphate units. Borate groups are homogeneously mixed with the iso- lated orthophosphate groups, while the remaining phosphate groups exhibit a slight preference for bonding to BO4 over SiO4 units. Linkages among borate groups are dominated by B[3] O B[4] linkages at the expenses of B[3] O B[3] and B[4] O B[4] linkages, with the latter B[4] O B[4] motifs disfavored yet abundant. A similar fashion of borate mixing was observed in P-free Na/Ca- based borosilicate glasses that span a large compositional space. The content of B[4] O B[4] linkages was found to be controlled by the relative fractions of BO4 groups and non-bridging oxygen ions. Key Words: Bioactive glasses, Phosphosilicate glasses, Borophosphosili- cate glasses, Solid-state NMR spectroscopy, Glass structure, Fourier-transform infrared spectroscopy, Hydroxyapatite, Amorphous calcium phosphate, Ap- atite formation, in vitro bioactivity testing List of Papers The following papers, referred to in the text by their Roman numerals, are in- cluded in this thesis. Reprints were made with permission from the publishers. PAPER I: Quantitative Composition-Bioactivity Relationships of Phos- phosilicate Glasses: Bearings From the Phosphorus Content and Network Polymerization. Y. Yu, R. Mathew, and M. Edén, J. Non-Cryst. Solids, 502, 106– 117 (2018). DOI: 10.1016/j.jnoncrysol.2018.07.060 PAPER II: Contrasting In Vitro Apatite Growth From Bioactive Glass Surfaces with that of Spontaneous Precipitation. Y. Yu, Z. Bacsik, and M. Edén, Materials, 11, 1690 (2018). DOI: 10.3390/ma11091690 PAPER III: Structure-composition Relationships of Bioactive Borophos- phosilicate Glasses Probed by Multinuclear 11B, 29Si, and 31P Solid State NMR. Y. Yu, and M. Edén, RSC Adv., 6, 101288–101303 (2016). DOI: 10.1039/c6ra15275a PAPER IV: Medium-Range Structural Organization of Phosphorus-Bearing Borosilicate Glasses Revealed by Advanced Solid-State NMR Experiments and MD Simulations: Consequences of B/Si Substitutions. Y. Yu, B. Stevenson, and M. Edén, J. Phys Chem. B, 121, 9737– 9752 (2017). DOI: 10.1021/acs.jpcb.7b06654 PAPER V: Direct Experimental Evidence for Abundant BO4–BO4 Mo- tifs in Borosilicate Glasses From Double-Quantum 11B NMR Spectroscopy. Y. Yu, B. Stevenson, and M. Edén, J. Phys. Chem. Lett., 9, 6372–6376 (2018). DOI: 10.1021/acs.jpclett.8b02907 The following papers are not included in this thesis. PAPER VI: Two Heteronuclear Dipolar Results at the Price of One: Quan- tifying Na/P Contacts in Phosphosilicate Glasses and Biomimetic Hydroxy-Apatite. B. Stevensson, R.
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