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Bivalent cationic ions doped bioactive glasses: the influence of magnesium, zinc, strontium and copper on the physical and biological properties

  • In Honor of Larry Hench
  • Published:
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Abstract

Bioactive glass and glass ceramic materials are widely used as substitutes for bone augmentation and restoration, in orthopaedic, dental and maxillofacial surgery and in the tissue engineering field. Indeed, these materials are bioactive, biocompatible, mechanically stable, biodegradable and favour osteointegration, being able to promote bone tissue formation at their surface and to bond to surrounding living tissues when implanted in the human body. It has been demonstrated that bioglass (BG) ionic dissolution products (e.g. Si, Ca, P and Na) are able to induce and stimulate the expressions of genes related to the osteoblastic differentiation and bone formation, to stimulate angiogenesis in vitro and in vivo, as well as to play possible antibacterial and anti-inflammatory actions. Thus, it is possible to tailor BGs properties properly formulating their chemical composition and adding selected ions with specific functional and biological role. In this perspective, Hench proposed a new generation of genetically designed glasses, on the basis of their ability to activate specific genes involved in in situ tissue regeneration, by doping silicate and phosphate glasses with several active ions, particularly metallic ions with therapeutic effects. In this framework, the present review is aimed to provide an overview about the effect of selected cationic substitutions (i.e. magnesium, zinc, strontium and copper), incorporated within the bioglasses structure, on the physical and biological properties of these materials, since the comprehension of the influence of the most employed metallic ions has to be considered pivotal to address the formulation of more promising and performing glasses.

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Figure 1

(adapted from Ref. [18] (a), [11] (b) with permission)

Figure 2

(adapted from Ref. [50] with permission)

Figure 3

(adapted from Ref. [80] with permission)

Figure 4

(reproduced from Ref. [10] with permission)

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References

  1. Dorozhkin SV (2010) Bioceramics of calcium orthophosphates. Biomaterials 31:1465–1485

    Article  Google Scholar 

  2. Bianco A, Cacciotti I, Lombardi M, Montanaro L, Gusmano G (2007) Thermal stability and sintering behaviour of hydroxyapatite nanopowders. J Thermal Anal Calor. 88:237–243

    Article  Google Scholar 

  3. Cacciotti I, Bianco A (2011) High thermally stable Mg-substituted tricalcium phosphate by precipitation. Ceram Inter 37:127–137

    Article  Google Scholar 

  4. Hench LL (1998) Bioceramics. J Am Ceram Soc 81:1705–1728

    Article  Google Scholar 

  5. Hench LL (1991) Bioceramics: from concept to clinic. J Am Ceram Soc 74(7):1487–1510

    Article  Google Scholar 

  6. Cacciotti I, Lombardi M, Bianco A, Ravaglioli A, Montanaro L (2012) Sol-gel derived 45S5 bioglass: synthesis, microstructural evolution and thermal behaviour. J Mater Sci Mater Med 23(8):1849–1866

    Article  Google Scholar 

  7. Hench LL, Xynos ID, Polak JM (2004) Bioactive glasses for in situ tissue regeneration. J Biomater Sci Polym Ed 15:543–562

    Article  Google Scholar 

  8. Day RM (2005) Bioactive glass stimulates the secretion of angiogenic growth factors and angiogenesis in vitro. Tissue Eng 11:768–777

    Article  Google Scholar 

  9. Hench LL (1993) Bioceramics. J Am Ceram Soc 81:1705–1728

    Article  Google Scholar 

  10. Bueno EM, Glowacki J (2009) Cell-free and cell-based approaches for bone regeneration. Nat Rev Rheumatol 5(12):685–697

    Article  Google Scholar 

  11. Jell G, Stevens MM (2006) Gene activation by bioactive glasses. J Mater Sci Mater Med 17:997–1002

    Article  Google Scholar 

  12. Cacciotti I. Cationic and Anionic substitutions in hydroxyapatite, In: Handbook of Bioceramics and Biocomposites, Iulian Vasile Antoniac Editor, Springer International Publishing 2016:145–211

  13. Saltman PD, Strause LG (1993) The role of trace minerals in osteoporosis. J Am Coll Nutr 12:384–389

    Article  Google Scholar 

  14. Cacciotti I, Bianco A, Lombardi M, Montanaro L (2009) Mg-substituted hydroxyapatite nanopowders: synthesis, thermal stability and sinterability. J Europ Ceram Soc 29(14):2969–2978

    Article  Google Scholar 

  15. Bianco A, Cacciotti I, Lombardi M, Montanaro L (2009) Si-substituted hydroxyapatite nanopowders: synthesis, thermal stability and sinterability. Mater Res Bull 44:345–354

    Article  Google Scholar 

  16. Bianco A, Cacciotti I, Lombardi M, Montanaro L, Bemporad E, Sebastiani M (2010) F-substituted hydroxyapatite nanopowders: thermal stability, sintering behavior and mechanical properties. Ceram Inter 36(1):313–322

    Article  Google Scholar 

  17. Hench LL (2009) Genetic design of bioactive glass. J Eur Ceram Soc 29:1257–1265

    Article  Google Scholar 

  18. Hoppe A, Güldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32:2757–2774

    Article  Google Scholar 

  19. Mourino V, Cattalini JP, Boccaccini AR (2012) Metallic ions as therapeutic agents in tissue engineering scaffolds: an overview of their biological applications and strategies for new developments. J R Soc Interface 9:401–419

    Article  Google Scholar 

  20. Hoppe A, Mouriño V, Boccaccini AR (2013) Therapeutic inorganic ions in bioactive glasses to enhance bone formation and beyond. Biomater Sci 1:254–256

    Article  Google Scholar 

  21. Abou Neel EA, Chrzanowski W, Pickup DM, O’Dell LA, Mordan NJ, Newport RJ, Smith ME, Knowles JC (2009) Structure and properties of strontium-doped phosphate-based glasses. J R Soc Interface 6:435–446

    Article  Google Scholar 

  22. Miola M, Vitale Brovarone C, Maina G, Rossi F, Bergandi L, Ghigo D, Saracino S, Maggiora M, Canuto RA, Muzio G et al (2014) In vitro study of manganese-doped bioactive glasses for bone regeneration. Mater Sci Eng C 38:107–118

    Article  Google Scholar 

  23. Gomez-Vega J, Saiz E, Tomsia A, Marshall G, Marshall S (2000) Bioactive glass coatings with hydroxyapatite and Bioglass particles on Ti-based implants. 1. Processing. Biomaterials 21:105–111

    Article  Google Scholar 

  24. Rau JV, Teghil R, Fosca M, De Bonis A, Cacciotti I, Bianco A, Caminiti R, Rossi Albertini V, Ravaglioli A (2012) Bioactive glass-ceramic coatings deposited by pulsed laser deposition from RKKP targets (sol-gel vs melt-processing route). Mater Res Bull 47:1130–1137

    Article  Google Scholar 

  25. Ledda M, De Bonis A, Bertani FR, Cacciotti I, Teghil R, Lolli MG, Ravaglioli A, Lisi A, Rau JV (2015) Interdisciplinary Approach to Cell-Biomaterial Interactions: biocompatibility and Cell Friendly Characteristics of RKKP Glass-Ceramic Coatings on Titanium. Biomed Material 10(3):035005

    Article  Google Scholar 

  26. De Bonis A, Curcio M, Fosca M, Cacciotti I, Santagata A, Teghil R (2016) Rau JV RBP1 bioactive glass-ceramic films obtained by pulsed laser deposition. Mater Lett 175:195–198

    Article  Google Scholar 

  27. Gerhardt LC, Widdows KL, Erol MM, Burch CW, Sanz-Herrera JA, Ochoa I, Stämpfli R, Roqan IS, Gabe S, Ansari T et al (2011) The pro-angiogenic properties of multi-functional bioactive glass composite scaffolds. Biomaterials 32:4096–4108

    Article  Google Scholar 

  28. Rahaman MN, Day DE, Sonny Bal B, Fu Q, Jung SB, Bonewald LF et al (2011) Bioactive glass in tissue engineering. Acta Biomater 7:2355–2373

    Article  Google Scholar 

  29. Jones JR (2013) Review of bioactive glass: from Hench to hybrids. Acta Biomater 9:4457–4486

    Article  Google Scholar 

  30. Beattie JH, Avenell A (1992) Trace element nutrition and bone metabolism. Nutr Res Rev 5:167–188

    Article  Google Scholar 

  31. Nielsen F (1990) New essential trace elements for the life sciences. Biol Trace Elem Res 26–27:599–611

    Article  Google Scholar 

  32. Xynos ID, Edgar AJ, Buttery LDK, Hench LL, Polak JM (2001) Gene-expression profiling of human osteoblasts following treatment with the ionic products of Bioglass_ 45S5 dissolution. J Biomed Mater Res 55:151–157

    Article  Google Scholar 

  33. Gorustovich AA, Roether JA, Boccaccini AR (2010) Effect of bioactive glasses on angiogenesis: a review of in vitro and in vivo evidences. Tissue Eng Part B Rev 16:199–207

    Article  Google Scholar 

  34. Leu A, Leach J (2008) Proangiogenic potential of a collagen/bioactive glass substrate. Pharm Res 25:1222–1229

    Article  Google Scholar 

  35. Allan I, Newman H, Wilson M (2001) Antibacterial activity of particulate Bioglass_against supra- and subgingival bacteria. Biomaterials 2001(22):1683–1687

    Article  Google Scholar 

  36. Gorriti MF, López JMP, Boccaccini AR, Audisio C, Gorustovich AA (2009) In vitro study of the antibacterial activity of bioactive glass-ceramic scaffolds. Adv Eng Mater 11:B67–B70

    Article  Google Scholar 

  37. Zhang D, Lepparanta O, Munukka E, Ylanen H, Viljanen MK, Eerola E, Hupa M, Hupa L (2010) Antibacterial effects and dissolution behavior of six bioactive glasses. J Biomed Mater Res A 93:475–483

    Google Scholar 

  38. Stoor P, Söderling E, Salonen JI (1998) Antibacterial effects of a bioactive glass paste on oral microorganisms. Acta Odontol Scand 56:161–165

    Article  Google Scholar 

  39. Leppäranta O, Vaahtio M, Peltola T, Zhang D, Hupa L, Hupa M et al (2008) Antibacterial effect of bioactive glasses on clinically important anaerobic bacteria in vitro. J Mater Sci Mater Med 19:547–551

    Article  Google Scholar 

  40. Hu S, Chang J, Liu M, Ning C (2009) Study on antibacterial effect of 45S5 Bioglass. J Mater Sci Mater Med 20(1):281–286

    Article  Google Scholar 

  41. Jones J, Ehrenfried L, Saravanapavan P, Hench L (2006) Controlling ion release from bioactive glass foam scaffolds with antibacterial properties. J Mater Sci Mate Med 17:989–996

    Article  Google Scholar 

  42. Yli-Urpo H, Närhi T, Söderling E (2003) Antimicrobial effects of glass ionomer cements containing bioactive glass (S53P4) on oral micro-organisms in vitro. Acta Odontol Scand 61:241–246

    Article  Google Scholar 

  43. Munukka E, Leppäranta O, Korkeamäki M, Vaahtio M, Peltola T, Zhang D et al (2008) Bactericidal effects of bioactive glasses on clinically important aerobic bacteria. J Mater Sci Mater Med 19:27–32

    Article  Google Scholar 

  44. Day RM, Boccaccini AR (2005) Effect of particulate bioactive glasses on human macrophages and monocytes in vitro. J Biomed Mater Res A 73A:73–79

    Article  Google Scholar 

  45. Miguez-Pacheco V, Hench LL, Boccaccini AR (2015) Bioactive glasses beyond bone and teeth: emerging applications in contact with soft tissues. Acta Biomater 13:1–15

    Article  Google Scholar 

  46. Baino F, Novajra G, Miguez-Pacheco V, Boccaccini AR, Vitale-Brovarone C (2016) Bioactive glasses: special applications outside the skeletal system. J Non-Cryst Solids 432:15–30

    Article  Google Scholar 

  47. Miguez-Pacheco V, Greenspan D, Hench LL, Boccaccini AR (2015) Bioactive glasses in soft tissue repair. Am Ceram Soc Bull 94:27–31

    Google Scholar 

  48. Rath SN, Brandl A, Hiller D, Hoppe A, Gbureck U, Horch RE et al (2014) Bioactive copper-doped glass scaffolds can stimulate endothelial cells in co-culture in combination with mesenchymal stem cells. PLoS ONE 99(12):e113319

    Article  Google Scholar 

  49. Kingery WD, Bowen HK, Uhlmann DR (1976) Introduction to Ceramics, 2nd edn. Wiley, New York

    Google Scholar 

  50. Shelby JE (2005) Introduction to Glass Science and Technology, 2nd edn. The Royal Society of Chemistry, Cambridge

    Google Scholar 

  51. Kaur G, Pandey OP, Singh K, Homa D, Scott B, Pickrell G (2014) A review of bioactive glasses: their structure, properties, fabrication, and apatite formation. J Biomed Mater Res A. 102(1):254–274

    Article  Google Scholar 

  52. Tilocca A (2009) Structural models of bioactive glasses from molecular dynamics simulations. Proc R Soc A 465:1003–1027

    Article  Google Scholar 

  53. Wers E, Oudadesse H (2014) Thermal behaviour and excess entropy of bioactive glasses and Zn-doped glasses. J Therm Anal Calorim 115(3):2137–2144

    Article  Google Scholar 

  54. Cortizo AM, Molinuevo MS, Barrio DA, Bruzzone L (2006) Osteogenic activity of vanadyl(IV)-ascorbate complex: evaluation of its mechanism of action. Int J Biochem Cell Biol 38(7):1171–1180

    Article  Google Scholar 

  55. Marie PJ, Ammann P, Boivin G, Rey C (2001) Mechanisms of action and therapeutic potential of strontium in bone. Calcif Tissue Int 69(3):121–129

    Article  Google Scholar 

  56. Yamaguchi M (1998) Role of zinc in bone formation and bone resorption. J Trace Elem Exp Med 11(2–3):119–135

    Article  Google Scholar 

  57. Sun ZL, Wataha JC, Hanks CT (1997) Effects of metal ions on osteoblast-like cell metabolism and differentiation. J Biomed Mater Res 34(1):29–37

    Article  Google Scholar 

  58. LeGeros RZ (1991) Calcium phosphates in oral biology and medicine. Karger, Basel

    Book  Google Scholar 

  59. Zreiqat H, Howlett CR, Zannettino A, Evans P, Schulze-Tanzil G, Knabe C et al (2002) Mechanisms of magnesium-stimulated adhesion of osteoblastic cells to commonly used orthopaedic implants. J Biomed Mater Res 62(2):175–184

    Article  Google Scholar 

  60. Yamasaki Y, Yoshida Y, Okazaki M, Shimazu A, Uchida T, Kubo T et al (2002) Synthesis of functionally graded MgCO3 apatite accelerating osteoblast adhesion. J Biomed Mater Res 62(1):99–105

    Article  Google Scholar 

  61. Rude RK, Gruber HE, Norton HJ, Wei LY, Frausto A, Kilburn J (2005) Dietary magnesium reduction to 25% of nutrient requirement disrupts bone and mineral metabolism in the rat. Bone 37(2):211–219

    Article  Google Scholar 

  62. Percival M (1999) Bone health and Osteoporosis. Appl Nutr Sci Rep 5(4):1–5

    Google Scholar 

  63. Bigi A, Foresti B, Gregoriani R, Ripamonti A, Roveri N (1992) Shah JS The role of magnesium on the structure of biological apatites. Calcif Tissue Int 50:439–444

    Article  Google Scholar 

  64. Brown KH, Wuehler SE, Peerson JM (2001) The importance of zinc in human nutrition and estimation of the global prevalence of zinc deficiency. Food Nutr Bull 22:113–125

    Article  Google Scholar 

  65. Chasapis CT, Loutsidou AC, Spiliopoulou CA, Stefanidou ME (2012) Zinc and human health: an update. Arch Toxicol 86:521–534

    Article  Google Scholar 

  66. Yamaguchi M, Yamaguchi R (1986) Action of zinc on bone metabolism in rats. Increases in alkaline phosphatise activity and DNA content. Biochem Pharmacol 35:773–777

    Article  Google Scholar 

  67. Holloway WR, Collier FM, Herbt RE, Hodge JM, Nicolson GC (1996) Osteoblast-mediated effects of zinc on isolated rat osteoclasts: inhibition of bone resorption and enhancement of osteoclast number. Bone 19:137–142

    Article  Google Scholar 

  68. Lang C, Murgia C, Leong M, Tan LW, Perozzi G, Knight D et al (2007) Anti-inflammatory effects of zinc and alterations in zinc transporter mRNA in mouse models of allergic inflammation. Am J Physiol Lung Cell Mol Physiol 292(2):L577–L584

    Article  Google Scholar 

  69. Cousins RJ (1998) A role of zinc in the regulation of gene expression. Proc Nutr Soc 57:307–311

    Article  Google Scholar 

  70. Kwun IS, Cho YE, Lomeda RAR, Shin HI, Choi JY, Kang YH et al (2010) Zinc deficiency suppresses matrix mineralization and retards osteogenesis transiently with catch-up possibly through Runx 2 modulation. Bone 46(3):732–741

    Article  Google Scholar 

  71. Brandao NJ, Stefan V, Mendonca BB, Bloise W, Castro AVV (1995) The essential role of zinc in growth. Nutr. Res. 15:335–358

    Article  Google Scholar 

  72. Williams C, McBride S, Mostler K, Petrone DM, Simone AJ, Crawford R, Patel S, Petrone ME, Chaknis P, DeVizio W, Volpe AR, Proskin HM (1998) Efficacy of a dentifrice containing zinc citrate for the control of plaque and gingivitis: a 6-month clinical study in adults. Compend Contin Educ Dent 19(2):4–15

    Google Scholar 

  73. D’Haese PC, Van Landeghem GF, Lamberts LV, Bekaert VA, Schrooten I, De Broe ME (1997) Measurement of strontium in serum, urine, bone, and soft tissues by Zeeman atomic absorption spectrometry. Clin Chem 43(1):121–128

    Google Scholar 

  74. Dahl SG, Allain P, Marie PJ, Mauras Y, Boivin G, Ammann P, Tsouderos Y, Delmas PD, Christiansen C (2001) Incorporation and distribution of strontium in bone. Bone 28(4):446–453

    Article  Google Scholar 

  75. Meunier PJ, Roux C, Seeman E, Ortolani S, Badurski JE, Spector TD et al (2004) The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. N Engl J Med 350(5):459–468

    Article  Google Scholar 

  76. Bonnelye E, Chabadel A, Saltel F, Jurdic P (2008) Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone 42(1):129–138

    Article  Google Scholar 

  77. Sila-asna M, Bunyaratvej A (2007) Kobe University Repository: kernel. Kobe J Med Sci 53(1):25–35

    Google Scholar 

  78. Marie PJ (2006) Strontium ranelate: a physiological approach for optimizing bone formation and resorption. Bone 38(2):S10–S14

    Article  Google Scholar 

  79. Brauer DS, Karpukhina N, Kedia G, Bhat A, Law RV, Radecka I, Hill RG (2012) Bactericidal strontium-releasing injectable bone cements based on bioactive glasses. J R Soc Interfac 10(78):1–8

    Article  Google Scholar 

  80. Saidak Z, Marie PJ (2012) Strontium signaling: molecular mechanisms and therapeutic implications in osteoporosis. Pharmacol Ther 136(2):216–226

    Article  Google Scholar 

  81. Reginster JY (2002) Strontium ranelate in osteoporosis. Curr Pharm Design 8(21):1907–1916

    Article  Google Scholar 

  82. Peng SL, Zhou GQ, Luk KDK, Cheung KMC, Li ZY, Lam WM, Zhou ZJ, Lu WW (2009) Strontium promotes osteogenic differentiation of mesenchymal stem cells through the Ras/MAPK signaling pathway. Cell Physiol Biochem 23(1–3):165–174

    Article  Google Scholar 

  83. Buehler J, Chappuis P, Saffar JL, Tsouderos Y, Vignery A (2001) Strontium ranelate inhibits bone resorption while maintaining bone formation in alveolar bone in monkeys (Macaca fascicularis). Bone 29(2):176–179

    Article  Google Scholar 

  84. Dollwet H, Sorenso J (1985) Historic uses of copper compounds in medicine. Trace Elements in Medicine 2(2):80–87

    Google Scholar 

  85. Stanic V, Dimitrijevic S, Antic-Stankovic J, Mitric M, Jokic B, Plecas IB, Raicevic S (2010) Synthesis, characterization and antimicrobial activity of copper and zinc-doped hydroxyapatite nanopowders. Appl Surf Sci 256(20):6083–6089

    Article  Google Scholar 

  86. Hu GF (1998) Copper stimulates proliferation of human endothelial cells under culture. J Cell Biochem 69(3):326–335

    Article  Google Scholar 

  87. Rodríguez JP, Ríos S, González M (2002) Modulation of the proliferation and differentiation of human mesenchymal stem cells by copper. J Cell Biochem 85(1):92–100

    Article  Google Scholar 

  88. Zhang JC, Huang JA, Xu SJ, Wang K, Yu SF (2003) Effects of Cu2+ and pH on osteoclastic bone resorption in vitro. Prog Nat Sci 13(4):266–270

    Google Scholar 

  89. Kothapalli CR, Ramamurthi A (2009) Copper nanoparticle cues for biomimetic cellular assembly of crosslinked elastin fibers. Acta Biomater 5:541–553

    Article  Google Scholar 

  90. Finney L, Vogt S, Fukai T, Glesne D (2009) Copper and angiogenesis: unravelling a relationship key to cancer progression. Clin Exp Pharmacol Physiol 36(1):88–94

    Article  Google Scholar 

  91. Gérard C, Bordeleau L-J, Barralet J, Doillon CJ (2010) The stimulation of angiogenesis and collagen deposition by copper. Biomaterials 31(5):824–831

    Article  Google Scholar 

  92. Feng W (2009) YeF, Xue W, Zhou Z, Kang YJ. Copper regulation of hypoxia-inducible factor-1 activity. Mol Pharmacol 75:174–182

    Article  Google Scholar 

  93. Sen CK, Khanna S, Venojarvi M, Trikha P, Ellison EC, Hunt TK et al (2002) Copper-induced vascular endothelial growth factor expression and wound healing. Am J Physiol Heart Circ Physiol 282:H1821–H1827

    Article  Google Scholar 

  94. Li S, Xie H, Li S, Kang YJ (2012) Copper stimulates growth of human umbilical vein endothelial cells in a vascular endothelial growth factor-independent pathway. Exp Biol Med 237:77–82

    Article  Google Scholar 

  95. Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163

    Article  Google Scholar 

  96. Hung YH, Bush AI, Cherny RA (2010) Copper in the brain and Alzheimer’s disease. J Biol Inorg Chem 15:61–76

    Article  Google Scholar 

  97. Bejarano J, Caviedes P, Palza H (2015) Sol–gel synthesis and in vitro bioactivity of copper and zinc-doped silicate bioactive glasses and glass-ceramics. Biomed Mater 10(2):025001

    Article  Google Scholar 

  98. Bini M, Grandi S, Capsoni D, Mustarelli P, Saino E, Visai L (2009) SiO2–P2O5–CaO glasses and glass-ceramics with and without ZnO: relationships among composition, microstructure, and bioactivity. J Phys Chem C 113:8821–8828

    Article  Google Scholar 

  99. Aina V, Cerrato G, Martra G, Malavasi G, Lusvardi G, Menabue L (2013) Towards the controlled release of metal nanoparticles from biomaterials: physico-chemical, morphological and bioactivity features of Cu-containing sol–gel glasses. Appl Surf Sci 283:240–248

    Article  Google Scholar 

  100. Aina V, Malavasi G, Fiorio Pla A, Munaron L, Morterra C (2009) Zinc-containing bioactive glasses: surface reactivity and behaviour towards endothelial cells. Acta Biomater 5:1211–1222

    Article  Google Scholar 

  101. Lusvardi G, Malavasi G, Menabue L, Menziani MC (2002) Synthesis, characterization, and molecular dynamics simulation of Na2O–CaO–SiO2–ZnO glasses. J Phys Chem B 106:9753–9760

    Article  Google Scholar 

  102. Srivastava AK, Pyare R (2012) Characterization of CuO substituted 45S5 bioactive glasses and glass-ceramics. Int J Sci Technol Res 1:28–41

    Google Scholar 

  103. Wu C, Zhou Y, Xu M, Han P, Chen L, Chang J, Xiao Y (2013) Copper-containing mesoporous bioactive glass scaffolds with multifunctional properties of angiogenesis capacity, osteostimulation and antibacterial activity. Biomaterials 34:422–433

    Article  Google Scholar 

  104. Watts SJ, Hill RG, O’Donnell MD, Law RV (2010) Influence of magnesia on the structure and properties of bioactive glasses. J Non-Cryst Solids 356:517–524

    Article  Google Scholar 

  105. El-Kady AM, Ali AF (2012) Fabrication and characterization of ZnO modified bioactive glass nanoparticles. Ceram Int 38:1195–1204

    Article  Google Scholar 

  106. Fredholm YC, Karpukhina N, Law RV, Hill RG (2010) Strontium containing bioactive glasses: glass structure and physical properties. J Non-Cryst Solids 356(44):2546–2551

    Article  Google Scholar 

  107. Anand V, Singh KJ, Kaur K (2014) Evaluation of zinc and magnesium doped 45S5 mesoporous bioactive glass system for the growth of hydroxyl apatite layer. J Non-Cryst Solids 406:88–94

    Article  Google Scholar 

  108. Kaur G, Pickrell G, Kimsawatde G, Homa D, Allbee HA, Sriranganathan N (2014) Synthesis, cytotoxicity, and hydroxyapatite formation in 27-Tris-SBF for sol-gel based CaO-P2O5-SiO2-B2O3-ZnO bioactive glasses. Sci Rep 4:4392

    Article  Google Scholar 

  109. McMillan P (1964) Glass-Ceramics. Academic Press, London

    Google Scholar 

  110. Pereira D, Cachinho S, Ferro MC, Fernandes MHV (2004) Surface behaviour of high MgO-containing glasses of the Si–Ca–P–Mg system in a synthetic physiological fluid. J Eur Ceram Soc 24:3693–3701

    Article  Google Scholar 

  111. Karakassids MA, Sranti A, Koutselas I (2004) Preparation and structural study of binary phosphate glasses with high calcium and/or magnesium content. J Non-Cryst Solids 347:69–79

    Article  Google Scholar 

  112. Hoppe A, Meszaros R, Stähli C, Romeis S, Schmidt J et al (2013) In vitro reactivity of Cu doped 45S5 Bioglass derived scaffolds for bone tissue engineering. J Mater Chem B 1:5659–5674

    Article  Google Scholar 

  113. Shahrabi S, Hesaraki S, Moemeni S, Khorami M (2011) Structural discrepancies and in vitro nanoapatite formation ability of sol–gel derived glasses doped with different bone stimulator ions. Ceram Inter 37(7):2737–2746

    Article  Google Scholar 

  114. Wers E, Oudadesse H, Lefeuvre B, Lucas-Girot A, Rocherullé J, Lebullenger R (2014) Excess entropy and thermal behavior of Cu- and Ti-doped bioactive glasses. J Therm Anal Calorim 117:579–588

    Article  Google Scholar 

  115. Kokubo T (1990) Surface chemistry of bioactive glass-ceramics. J Non-Cryst Solids 120:138–151

    Article  Google Scholar 

  116. Dubok VA (2000) Bioceramics: yesterday, Today, Tomorrow. Powder Metall Metal Ceram 39(7–8):381–394

    Article  Google Scholar 

  117. Rawlings RD (1993) Bioactive glasses and glass-ceramics. Clin Mater 14:155–179

    Article  Google Scholar 

  118. Strnad Z (1992) Role of the glass phase in bioactive glass-ceramics, glass phase in bioactive glass-ceramics. Biomaterials 13:317–321

    Article  Google Scholar 

  119. Hill R (1996) An alternative view of the degradation of bioglass. J Mater Sci Lett 15:1122–1125

    Article  Google Scholar 

  120. Al-Noamana A, Rawlinson SCF, Hill RG (2012) The role of MgO on thermal properties, structure and bioactivity of bioactive glass coating for dental implants. J Non-Cryst Solids 358:3019–3027

    Article  Google Scholar 

  121. Branda F, Arcobello-Varlese F, Costantini A, Luciani G (2002) Effect of the substitution of M2O3 (M = La, Y, In, Ga, Al) for CaO on the bioactivity of 2.5CaO–2SiO2 glass. Biomaterials 23:711–716

    Article  Google Scholar 

  122. Balamurugan A, Balossier G, Michel J, Kannan S, Benhayoune H, Rebelo AHS, Ferreira JMF (2007) Sol gel derived SiO2–CaO–MgO–P2O5 bioglass system-preparation and in vitro characterization. J Biomed Mater Res Part B Appl Biomater 83:546–553

    Article  Google Scholar 

  123. Dietrich E, Oudadesse H, Lucas-Girot A, Mami M (2009) In vitro bioactivity of melt derived glass 46S6 doped with magnesium. J Biomed Mater Res A 88A(4):1087–1096

    Article  Google Scholar 

  124. Oliveira JM, Correia RN, Fernandes MH (2002) Effects of Si speciation on the in vitro bioactivity of glasses. Biomaterials 23:371–379

    Article  Google Scholar 

  125. Moya JS, Tomsia AP, Pazo A, Santos C, Guitian F (1994) In vitro formation of hydroxylapatite layer in a MgO-containing glass. J Mater Sci Mater Med 5:529–532

    Article  Google Scholar 

  126. Ma J, Chen CZ, Wang DG, Jiao Y, Shi JZ (2010) Effect of magnesia on the degradability and bioactivity of sol–gel derived SiO2–CaO–MgO–P2O5 system glasses. Colloids Surf B Biointerfaces 81:87–95

    Article  Google Scholar 

  127. Ma J, Chen CZ, Wang DG, Shao X, Wang CZ, Zhang HM (2012) Effect of MgO addition on the crystallization and in vitro bioactivity of glass ceramics in the CaO–MgO–SiO2–P2O5 system. Ceram Int 38:6677–6684

    Article  Google Scholar 

  128. Massera J, Hupa L, Hupa M (2012) Influence of the partial substitution of CaO with MgO on the thermal properties and in vitro reactivity of the bioactive glass S53P4. J Non-Cryst Solids 358:2701–2707

    Article  Google Scholar 

  129. Vallet-Regi M, Salinas AJ, Roman J, Gil M (1999) Effect of magnesium content on the in vitrobioactivity of CaO–MgO–SiO2–P2O5 sol-gel glasses. J Mater Chem 9:515–518

    Article  Google Scholar 

  130. Courthéoux L, Lao J, Nedelec JM, Jallot E (2008) Controlled bioactivity in zincdoped sol_gel-derived binary bioactive glasses. J Phys Chem C 112(35):13663–13667

    Article  Google Scholar 

  131. Singh RK, Srinivasan A (2010) Bioactivity of SiO2-CaO-P2O5-Na2O glasses containing zinc-iron oxide. Appl Surf Sci 256(6):1725–1730

    Article  Google Scholar 

  132. Lusvardi G, Malavasi G, Menabue L, Menziani MC, Pedone A, Segre U, Aina V, Perardi A, Morterra C, Boccafoschi F, Gatti S, Bosetti M, Cannas M (2008) Properties of zinc releasing surfaces for clinical applications. J Biomater Appl 22(6):505–526

    Article  Google Scholar 

  133. Oki A, Parveen B, Hossain S, Adeniji S, Donahue H (2004) Preparation and in vitro bioactivity of zinc containing sol-gel-derived bioglass materials. J Biomed Mater Res A 69A(2):216–221

    Article  Google Scholar 

  134. Aina V, Perardi A, Bergandi L, Malavasi G, Menabue L, Morterra C, Ghigo D (2007) Cytotoxicity of zinc-containing bioactive glasses in contact with human osteoblasts. Chem Biol Interact 167(3):207–218

    Article  Google Scholar 

  135. Haimi S, Gorianc G, Moimas L, Lindroos B, Huhtala H, Räty S, Kuokkanen H, Sándor GK, Schmid C, Miettinen S, Suuronen R (2009) Characterization of zinc-releasing three-dimensional bioactive glass scaffolds and their effect on human adipose stem cell proliferation and osteogenic differentiation. Acta Biomater 5(8):3122–3131

    Article  Google Scholar 

  136. Balamurugan A, Balossier G, Kannan S, Michel J, Rebelo AH, Ferreira JM (2007) Development and in vitro characterization of sol-gel derived CaO–P2O5–SiO2–ZnO bioglass. Acta Biomater 3:255–262

    Article  Google Scholar 

  137. Atkinson I, Anghel EM, Predoana L, Mocioiu OC, Jecu L, Raut I, Munteanu C, Culita D, Zaharescu M (2016) Influence of ZnO addition on the structural, in vitro behavior and antimicrobial activity of sol–gel derived CaO–P2O5–SiO2 bioactive glasses. Ceram Inter 42(2):3033–3045

    Article  Google Scholar 

  138. Fujita Y, Yamamuro T, Nakamura T, Kotani S, Ohtsuki C, Kokubo T (1991) The bonding behavior of calcite to bone. J Biomed Mater Res 25(8):991–1003

    Article  Google Scholar 

  139. Du RL, Chang J, Ni SY, Zhai WY, Wang JY (2006) Characterization and in vitro bioactivity of zinc-containing bioactive glass and glass-ceramics. J Biomater Appl 20(4):341–360

    Article  Google Scholar 

  140. Lao J, Jallot E (2008) Nedelec J- M. Strontium-delivering glasses with enhanced bioactivity: a new biomaterial for antiosteoporotic applications? Chem Mater 20(15):4969–4973

    Article  Google Scholar 

  141. Lao J, Nedelec JM, Jallot E (2009) New strontium-based bioactive glasses: physicochemical reactivity and delivering capability of biologically active dissolution products. J Mater Chem 19(19):2940–2949

    Article  Google Scholar 

  142. Hesaraki S, Gholami M, Vazehrad S, Shahrabi S (2010) The effect of Sr concentration on bioactivity and biocompatibility of sol-gel derived glasses based on CaO–SrO–SiO2–P2O5 quaternary system. Mater Sci Eng C 30(3):383–390

    Article  Google Scholar 

  143. Fredholm YC, Karpukhina N, Brauer DS, Jones JR, Law RV, Hill RG (2012) Influence of strontium for calcium substitution in bioactive glasses on degradation, ion release and apatite formation. J R Soc Interf 9(70):880–889

    Article  Google Scholar 

  144. Zhang J, Zhao S, Zhu Y, Huang Y, Zhu M, Tao C, Zhang C (2014) Three-dimensional printing of strontium-containing mesoporous bioactive glass scaffolds for bone regeneration. Acta Biomater 10(5):2269–2281

    Article  Google Scholar 

  145. O’Donnell MD, Hill RG (2010) Influence of strontium and the importance of glass chemistry and structure when designing bioactive glasses for bone regeneration. Acta Biomater 6(7):2382–2385

    Article  Google Scholar 

  146. Sriranganathan D, Kanwal N, Hing KA, Hill RG (2016) Strontium substituted bioactive glasses for tissue engineered scaffolds: the importance of octacalcium phosphate. J Mater Sci Mater Med 27(2):1–10

    Article  Google Scholar 

  147. Pan HB, Zhao XL, Zhang X, Zhang KB, Li LC, Li ZY, Lam WM, Lu WW, Wang DP, Huang WH, Lin KL, Chang J (2010) Strontium borate glass: potential biomaterial for bone regeneration. J Royal Soc Interf 7(48):1025–1031

    Article  Google Scholar 

  148. Li ZY, Lam WM, Yang C, Xu B, Ni GX, Abbah SA, Cheung KM, Luk KD, Lu WW (2007) Chemical composition, crystal size and lattice structural changes after incorporation of strontium into biomimetic apatite. Biomaterials 28:1452–1460

    Article  Google Scholar 

  149. Wers E, Bunetel L, Oudadesse H, Lefeuvre B, Lucas-Girot A, Mostafa A, Pellen P (2013) Effect of copper and zinc on the bioactivity and cells viability of bioactive glasses. Bioceram Dev Appl. S1:013

    Google Scholar 

  150. Varanasi VG, Saiz E, Loomer PM, Ancheta B, Uritani N, Ho SP, Tomsia AP, Marshall SJ, Marshall GW (2009) Enhanced osteocalcin expression by osteoblast-like cells (MC3T3-E1) exposed to bioactive coating glass (SiO2-CaO-P2O5-MgO-K2O-Na2O system) ions. Acta Biomater 5(9):3536–3547

    Article  Google Scholar 

  151. Chen X, Liao X, Huang Z, You P, Chen C, Kang Y, Yin G (2010) Synthesis and characterization of novel multiphase bioactive glass-ceramics in the CaO-MgO-SiO2 system. J Biomed Mater Res B Appl Biomater 93B(1):194–202

    Google Scholar 

  152. Saboori A, Rabiee M, Moztarzadeh F, Sheikhi M, Tahriri M, Karimi M (2009) Synthesis, characterization and in vitro bioactivity of sol-gel-derived SiO2eCaOeP2O5eMgO bioglass. Mater Sci Eng C 29(1):335–340

    Article  Google Scholar 

  153. Knabe C, Stiller M, Berger G, Reif D, Gildenhaar R, Howlett CR, Zreiqat H (2005) The effect of bioactive glass ceramics on the expression of bone-related genes and proteins in vitro. Clin Oral Implants Res 16(1):119–127

    Article  Google Scholar 

  154. Isaac J, Nohra J, Lao J, Jallot E, Nedelec JM, Berdal A, Sautier JM (2011) Effects of strontium-doped bioactive glass on the differentiation of cultured osteogenic cells. Eur Cell Mater 21:130–143

    Article  Google Scholar 

  155. Gentleman E, Fredholm YC, Jell G, Lotfibakhshaiesh N, O’Donnell MD, Hill RG et al (2010) The effects of strontium-substituted bioactive glasses on osteoblasts and osteoclasts in vitro. Biomaterials 31(14):3949–3956

    Article  Google Scholar 

  156. Hesaraki S, Alizadeh M, Nazarian H, Sharifi D (2010) Physico-chemical and in vitro biological evaluation of strontium/calcium silicophosphate glass. J Mater Sci Mater Med 21(2):695–705

    Article  Google Scholar 

  157. Gorustovich AA, Steimetz T, Cabrini RL, López JMP (2010) Osteoconductivity of strontium-doped bioactive glass particles: a histomorphometric study in rats. J Biomed Mater Res A 92A(1):232–237

    Article  Google Scholar 

  158. Zhao S, Zhang J, Zhu M, Zhang Y, Liu Z, Tao C, Zhu Y, Zhang C (2015) Three-dimensional printed strontium-containing mesoporous bioactive glass scaffolds for repairing rat criticalsized calvarial defects. Acta Biomater 12:270–280

    Article  Google Scholar 

  159. Kong N, Lin K, Li H, Chang J (2014) Synergy effects of copper and silicon ions on stimulation of vascularization by copper-doped calcium silicate. J Mater Chem B 2:1100–1110

    Article  Google Scholar 

  160. Zhao S, Wang H, Zhang Y, Huang W, Rahaman MN, Liu Z, Wang D, Zhang C (2015) Copper-doped borosilicate bioactive glass scaffolds with improved angiogenic and osteogenic capacity for repairing osseous defects. Acta Biomater 14:185–196

    Article  Google Scholar 

  161. Wang H, Zhao SC, Zhou J, Shen YQ, Huang WH, Zhang CQ, Rahaman MN, Wang D (2014) Evaluation of borate bioactive glass scaffolds as a controlled delivery system for copper ions in stimulating osteogenesis and angiogenesis in bone healing. J Mater Chem B 2:8547–8557

    Article  Google Scholar 

  162. Varmette EA, Nowalk JR, Flick LM, Hall MM (2009) Abrogation of the inflammatory response in LPS-stimulated RAW 264.7 murine macrophages by Zn- and Cu- doped bioactive sol-gel glasses. J Biomed Mater Res A 90A(2):317–325

    Article  Google Scholar 

  163. Balamurugan A, Balossier G, Laurent-Maquin D, Pina S, Rebelo AHS, Faure J, Ferreira JM (2008) An in vitro biological and anti-bacterial study on a sol-gel derived silver-incorporated bioglass system. Dental Mater 24(10):1343–1351

    Article  Google Scholar 

  164. Palza H, Escobar B, Bejarano J, Bravo D, Diaz-Dosque M, Pereza J (2013) Designing antimicrobial bioactive glass materials with embedded metal ions synthesized by the sol-gel method. J Mater Sci Eng C 33:3795–3801

    Article  Google Scholar 

  165. Guida A, Towler MR, Wall JG, Hill RG, Eramo S (2003) Preliminary work on the antibacterial effect of strontium in glass ionomer cements. J Mater Sci Lett 22(20):1401–1403

    Article  Google Scholar 

  166. Gough JE, Notingher I, Hench LL (2004) Osteoblast attachment and mineralized nodule formation on rough and smooth 45S5 bioactive glass monoliths. J Biomed Mater Res A 68(4):640–650

    Article  Google Scholar 

  167. Karageorgiou V, Kaplan D (2005) Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26(27):5474–5491

    Article  Google Scholar 

  168. Hutmacher DW (2000) Scaffolds in tissue engineering bone and cartilage. Biomaterials 21(24):2529–2543

    Article  Google Scholar 

  169. Li R, Clark AE, Hench LL (1991) An investigation of bioactive glass powders by sol–gel processing. J Appl Biomater 2:231–239

    Article  Google Scholar 

  170. Hench LL (1997) Sol-gel materials for bioceramic applications. Curr Opin Solid State Mater Sci 2:604–610

    Article  Google Scholar 

  171. Dimitriev Y, Ivanova Y, Iordanova R (2008) History of sol-gel science and technology. J Uni Chem Tech Metall 43:181–192

    Google Scholar 

  172. Lombardi M, Gremillard L, Chevalier J, Lefebvre L, Cacciotti I, Bianco A, Montanaro L (2013) A comparative study between melt-derived and sol-gel synthesized 45S5 bioactive glasses. Key Eng Mater 541:15–30

    Article  Google Scholar 

  173. Saravanapavan P, Hench LL (2001) Low-temperature synthesis, structure, and bioactivity of gel-derived glasses in the binary CaO-SiO2 system. J Biomed Mater Res 54:608–618

    Article  Google Scholar 

  174. Kau G, Pandey OP, Singh K, Homa D, Scott B, Pickrell G (2014) A review of bioactive glasses: their structure, properties, fabrication, and apatite formation. J Biomed Mater Res A 102:254–274

    Article  Google Scholar 

  175. Sepulveda P, Jones JR, Hench LL (2002) In vitro dissolution of melt-derived 45S5 and sol-gel derived 58S bioactive glasses. J Biomed Mater Res 61(2):301–311

    Article  Google Scholar 

  176. Berger G, Gildenhaar R (1992) Long-term stable bioactive glass ceramic as implant material: ten years of clinical experience. In: Fourth world biomaterials congress, Federal Republic of Germany, Berlin, 24–28 April, p 33

  177. Cacciotti I, Lehmann G, Camaioni A, Bianco A (2013) AP40 bioactive glass ceramic by sol-gel synthesis: in vitro dissolution and cell-mediated bioresorption. Key Eng Mater 541:41–50

    Article  Google Scholar 

  178. Covani U, Giacomelli L, Krajewski A, Ravaglioli A, Spotorno L, Loria P, Das S, Nicolini C (2007) Biomaterials for orthopedics: a roughness analysis by atomic force microscopy. J Biomed Mater Res A 82(3):723–730

    Article  Google Scholar 

  179. Krajewski A, Ravaglioli A, Tinti A, Taddei P, Mazzocchi M, Martinetti R, Fagnano C, Fini M (2005) Comparison between the in vitro surface transformations of AP40 and RKKP bioactive glasses. J Mater Sci Mater Med 16:119–128

    Article  Google Scholar 

  180. Lombardi M, Cacciotti I, Bianco A, Montanaro L (2015) RKKP bioactive glass-ceramic material via an aqueous sol-gel process. Ceram Inter 41(3):3371–3380

    Article  Google Scholar 

  181. Boyd D, Carroll G, Towler MR, Freeman C, Farthing P, Brook IM (2009) Preliminary investigation of novel bone graft substitutes based on strontium-calcium-zinc- silicate glasses. J Mater Sci Mater Med 20(1):413–420

    Article  Google Scholar 

  182. Murphy S, Boyd D, Moane S, Bennett M (2009) The effect of composition on ion release from CaeSreNaeZneSi glass bone grafts. J Mater Sci Mater Med 20(11):2207–2214

    Article  Google Scholar 

  183. Murphy S, Wren A, Towler M, Boyd D (2010) The effect of ionic dissolution products of CaSrNaZnSi bioactive glass on in vitro cytocompatibility. J Mater Sci Mater Med 21(10):2827–2834

    Article  Google Scholar 

  184. Baghbani F, Moztarzadeh F, Hajibaki L, Mozafari M (2013) Synthesis, characterization and evaluation of bioactivity and antibacterial activity of quinary glass system (SiO2–CaO–P2O5–MgO–ZnO): in vitro study. Bull Mater Sci 36(7):1339–1346

    Article  Google Scholar 

  185. Rezaei Y, Moztarzadeh F, Shahabi S, Tahriri M (2014) Synthesis, Characterization, and In Vitro Bioactivity of Sol-Gel-Derived SiO2–CaO–P2O5–MgO-SrO Bioactive Glass. Synth React Inorg Met-Org Nano-Met Chem 44(5):692–701

    Article  Google Scholar 

  186. Azevedo MM, Jell G, O’Donnell MD, Law RV, Hill RG, Stevens MM (2010) Synthesis and characterization of hypoxia-mimicking bioactive glasses for skeletal regeneration. J Mater Chem 20(40):8854–8864

    Article  Google Scholar 

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  1. Engineering Department, University of Rome “Niccolò Cusano”, Via Don Carlo Gnocchi 3, 00166, Rome, Italy

    Ilaria Cacciotti

  2. Italian Interuniversity Consortium on Materials Science and Technology (INSTM), Rome, Italy

    Ilaria Cacciotti

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Cacciotti, I. Bivalent cationic ions doped bioactive glasses: the influence of magnesium, zinc, strontium and copper on the physical and biological properties. J Mater Sci 52, 8812–8831 (2017). https://doi.org/10.1007/s10853-017-1010-0

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