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Atkinson, I. Metal Ions and Bioactive Glasses. Encyclopedia. Available online: https://encyclopedia.pub/entry/28141 (accessed on 19 April 2024).
Atkinson I. Metal Ions and Bioactive Glasses. Encyclopedia. Available at: https://encyclopedia.pub/entry/28141. Accessed April 19, 2024.
Atkinson, Irina. "Metal Ions and Bioactive Glasses" Encyclopedia, https://encyclopedia.pub/entry/28141 (accessed April 19, 2024).
Atkinson, I. (2022, September 30). Metal Ions and Bioactive Glasses. In Encyclopedia. https://encyclopedia.pub/entry/28141
Atkinson, Irina. "Metal Ions and Bioactive Glasses." Encyclopedia. Web. 30 September, 2022.
Metal Ions and Bioactive Glasses
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This entry is adapted from the peer-reviewed paper 10.3390/bioengineering9100489

Bioactive glasses (BGs) are of great interest in the field of medical implants due to their osteoinductive, osteoproductive, osteoconductive, and antimicrobial properties. Metal ions with bactericidal action can be incorporated into the glass structure in order to improve the antibiofilm activity of the BGs.

bacterial biofilm bioactive glass metal ions

1. Bioactive Glasses

Bioactive glasses (BGs) are of great interest in the field of medical implants due to their osteoinductive, osteoproductive, osteoconductive, and antimicrobial properties [1]. L. Hench, who revolutionized the field of biomaterials with his invention of 45S5 BG, known as Bioglass® (wt. %: 45SiO2-24.5Na2O-24.5CaO-6P2O5), in the early 1970s, classified a bioactive material as one that causes a biological reaction at its interface and promotes a bond to develop between the tissues and the material [2]. He discovered that the composition of 45S5 bioactive glass bonded with the bone through the formation of hydroxyapatite (HAP), an analog to the mineral phase of bones when it was in contact with biological fluids. The Bioglass® composition has received the approval of the US Food and Drug Administration. Currently, it is used for middle ear treatment and periodontal repair and augmentation [3].
Since then, the research on BGs has provided very good results through the conversion of traditional glasses into glasses with added properties that address healthcare needs. BGs can bond to and integrate with the bone tissue without promoting inflammation and toxicity or forming fibrous tissue [4][5].
The main advantage of BGs for tissue engineering applications is their surface reactivity. The reaction products resulting from the interaction between BGs and the physiological fluids lead to the formation of the HAP-like phase, similar to the crystalline HAP of bones. When these glasses are exposed to an aqueous environment, they undergo several surface reactions that have been described as the bioactivity of BGs [6]:
I.
Rapid exchange of Ca2+ with a proton or hydrate proton;
II.
Generation of silanols (Si–OH) at the site of the breakdown of the silica network. Solution interface for BG. In this stage, soluble silica [Si(OH)4] is also produced and released to the bodily fluid;
III.
Condensation and repolymerization of the silica-rich layer take place on the BGs’surface. Consumption of Si–OH;
IV.
Ca2+ and PO43− migrate to the surface and form Ca–PO43− clusters on the top of the SiO2-rich layer, and the crystallization of the amorphous CaP takes place;
V.
Finally, the hydroxycarbonate apatite layer (HAC) is formed by the incorporation of OH– and CO32− anions from the solution.
Furthermore, the release of ions makes the surrounding environment hostile to microbial development through the generation of osmotic and acid-base imbalance without being dependent on antibiotics and without harming the host tissues.
BGs can be obtained either by the traditional melt-quenching or the modern sol-gel method [7].
Melt-derived BGs are prepared at temperatures higher than 1000 °C, with a procedure analogous to that used to melt common window glasses. The resulting material does not have any porosity at all, and the surface area depends only on the particle size obtained by grinding up the powders.
In the 1990s, the sol–gel method, which involves the hydrolysis and polymerization of metal hydroxides, alkoxides, and/or inorganic salts, was used for the first time to create BGs [8]. Contrary to the melt-derived BGs, the sol–gel glasses are not prepared at elevated processing temperatures. The surface and structural properties (such as the surface area and porosity) can be finely modulated depending on the composition and synthesis conditions. The BGs obtained by the sol–gel method can have different types of pores, such as nanopores, macropores, or mesopores [9]. At the very end, controlled nanostructured materials can be obtained. Due to their outstanding textural properties, HAP is deposited much faster on the sol–gel BGs than on the melt-derived ones, and the materials exhibit higher bone-bonding rates, together with excellent degradation/resorption properties [10][11][12].
Furthermore, the sol–gel processes can be combined with the supramolecular chemistry of surfactants, resulting in the third-generation class of BGs referred to as ordered mesoporous bioactive glasses (MBGs), with the values of the surface and porosity up to five times higher than those obtained by the sol–gel method [13][14]. The surfactants for preparing MBGs mainly include CTAB, P123 (EO20-PO70-EO20), and F127 (EO106-PO70-EO106) [15]. MBGs exhibit the highest in vitro bioactivity and their ordered mesoporous structure allows for the incorporation of antimicrobial agents, etc., thereby having a huge potential in the therapy of bacteria-associated infection.
Moreover, BGs can be used to produce three-dimensional scaffolds, which are an advantage in tissue-engineering applications. Thus, a bioactive, biodegradable, and highly porous matrix that could resemble the cancellous bone is obtained.
The introduction of the sol–gel method opened the research to new types of materials for medical applications. One of the advantages of this method, in comparison with the conventional melting technique, is the possibility of easy chemical doping. Moreover, the traditional melting method’s higher processing temperature causes some components, including P2O5, to evaporate throughout the process, decreasing the overall bioactive potential of the glass, as well as other properties [16].
The antibacterial property of the BGs is an intriguing characteristic. In some cases, BG compositions have demonstrated antibacterial properties without any addition to their composition of metal ions or antibiotics.
Zhou et al. [17] compared the efficacy of 45S5 and S53P4 (53SiO2-23Na2O-20%CaO- 4% P2O5, wt. %) BGs against the biofilm generated by MRSA and V. parvula. They found that 45S5 BG particles exhibited a higher reduction of the biofilm than the S53P4 BG particles, suggesting the potential of 45S5 BG for eradicating mature biofilm. They emphasized the influence of the BGs particle size on the effectiveness against biofilms. Smaller particles reduced biofilms significantly more than larger particles across the experiment. Other researchers have demonstrated the strong activity of S53P4 BG to reduce the biofilm produced by a wide variety of bacteria, including S. aureus, P. aeruginosa, K. pneumoniae, and S. epidermidis [18][19].
Considering that bacteria can evolve defensive mechanisms against antibiotics through mutation and selection, an alternative to treating bone infections is the use of biocide metal ions. Low-bacterial resistance is one of the advantages of these ions.
Moreover, the concentration of the dopant should be determined, because the low dopant concentrations sometimes may not produce the desired properties, and on the contrary, high dopant concentrations may have cytotoxic and carcinogenic effects [20].

2. Metal Ions Incorporated Bioactive Glasses with Antibiofilm Efficiency

In recent years, several studies have demonstrated the effective antibiofilm activity of different formulations of BGs. Ag+, Cu2+/+, Ga3+, Ti4+, and Zn2+ are some examples of ions that can be used in doped BGs to target the inhibition and disruption of bacterial biofilm [21][22][23][24].
A recent study [25] reported that F18 glass, synthesized by the melting method, belonging to the SiO2-Na2O-K2O-MgO-CaO-P2O5 system, is a promising material for preventing and controlling bacterial biofilm. The bacterial strains S. aureus and methicillin-resistant S. aureus (MRSA) were used to evaluate the reduction of the biofilm. 
One of the most efficient ions against bacterial biofilm is zinc (Zn) [26][27]. Zn is a multifunctional therapeutic ion. Zn can stimulate bone formation because it is a cofactor in many enzymes and is involved in DNA replication [26]. Zn can also leak from the BG, causing oxidative stress in the intracellular medium or damage to cell membranes [28].
Zn-containing BGs have been shown to have antimicrobial properties against S. aureus and E. coli in the planktonic form [29].
In their investigation, Esfahanizadeh et al. [22] discovered that BG doped with 5 mol % of Zn significantly reduced the ability of Gram-negative anaerobic periodontal pathogens such as P. gingivalis, A. actinomycetemcomitans, and P. intermedia to develop a biofilm.
Zn (2.39 wt. %)-doped nano-BG particles (55SiO2-40CaO-5P2O5 mol %) were obtained by Paramita et al. [30] using the sol–gel method.
Silver (Ag) exhibits powerful antibacterial activity against a range of bacterial species [31][32][33], including antibiotic-resistant strains [34]. Incorporating Ag into BG has been proposed as a possible alternative to antibiotics for reducing infection in clinical applications [35][36][37]. Wilkinson et al. [35] aimed to elucidate the antibiofilm efficacy of Ag-doped BG (TheraGlassTM) against the opportunistic pathogens P. aeruginosa and S. aureus. 
In a recent publication [38], the antibacterial activity of Ag-doped borate glasses with compositions of 60B2O3-36CaO-(4-x)P2O5-(x)Ag2O, where x = 0.0, 0.3, 0.5, and 1 (mol %), was examined in vitro.The dose-dependent antibacterial activity of the Ag-doped BG was demonstrated against P. aeruginosa preformed biofilms, with up to a 99.7% reduction in the bacterial cell counts.
Additionally, several studies [39][40] proved that Ag has an antimicrobial activity only against bacteria and fungus, but not against epithelial cells, indicating its clinical use without adverse side effects on human health.
Fan et al. [41] showed that Ag-containing MBGs (molar ratio Si:Ca:P = 80:15:5) presented an antibacterial activity against E. faecalis biofilm in the root canal of human teeth.
Copper (Cu) has also been used as a therapeutic ion due to its biocidal action against Gram-positive and Gram-negative bacteria and its low cytotoxicity to human cells. It is a necessary element for both human and animal existence [42]. Additionally, by enhancing angiogenesis and promoting osteogenesis, it plays a significant role in the metabolism of bone formation [42]. 
In 2008, the United States Environmental Protection Agency classified Cu as a metallic antimicrobial agent against many disease-causing bacteria [43].
Using poly(styrene)-block-poly(acrylic acid) (PS-b-PAA) and hexadecyltrimethylammonium bromide (CTAB) as structure-directing agents, Holquin et al. [44] produced Cu-doped hallo BG nanoparticles with the following composition: 79.5SiO2-(18-x)CaO-2.5P2O5-xCuO (x = 0, 2.5 or 5 mol % of CuO).
Their study showed that the composition with a greater amount of Cu was able to degrade the biofilm formed by S. aureus at a minimal concentration, indicating its suitability as a bactericide agent [44].
Furthermore, Bari et al. [24], demonstrated that Cu-containing MBG (2 mol %) prepared by an ultrasound-assisted one-pot synthesis inhibited bacterial growth and was also able to restrain the formation of a biofilm produced by S. epidermidis, and even favored its dispersion. It is known that S. epidermidis produces considerable quantities of polysaccharide intercellular adhesions that induce biofilm formation [45]. 
Gallium (Ga) is another interesting element to be used as a therapeutic ion due to its broad-spectrum activity and immunity to the conventional resistance mechanism of bacteria associated with antibiotics. All these characteristics are linked with gallium’s pathway in bacteria metabolism. Ga acts as a “Trojan horse”, disrupting the bacterial Fe metabolism. Since the ionic radii of Ga3+ and Fe3+ are nearly identical, many biologic systems cannot discriminate between them [46]. 
According to the study [21], melt-derived Ag- and Ga-doped phosphate glass with the following composition 10CaO-37Na2O-45P2O5-3Ga2O3-5Ag2O (mol %) contributed to the biofilm growth inhibitory effect on P. aeruginosa (up to 2.68 reductions in log10 values of the viable counts compared with controls). The composition may offer a successful choice to combat opportunistic pathogens such as P. aeruginosa-associated infections due to the controlled release of antibacterial Ga and Ag ions at the site of infection. The melt-derived Ag- and Ga-doped phosphate glass was also tested in terms of the inhibition of biofilm formation against P. gingivalis and S. gordonii periodontal pathogens [47]. The glass developed in the study [47] reduced biofilm formation of P. gingivalis after 7 days of exposure by combining the actions of Ga and Ag synergistically. Ag ions destabilize the biofilm matrix to increase the biofilm’s contact area, hence enhancing the chances of the Ag and Ga ions subsequently killing the bacteria.
Recently, Tellurium (Te), an element from the chalcogens group that exhibits several oxidation states, has been studied for biological applications due to its antimicrobial, antioxidant, and antitumoral properties [48][49][50][51]. Telluride (Te2−)→elemental tellurium (Te0)→tellurite (TeO32−)→tellurate (TeO42−) are only a few of the redox states in which Tellurium can be found. The tellurite (TeO32−) is highly toxic for most bacteria (e.g., Escherichia coli) even at concentrations of 1 μg mL−1 [52].
This opens a new perspective for the Te element in terms of biomaterials to prevent bacterial infections in tissue engineering applications.
A recent study [48] analyzed the antibacterial activity against bacterial biofilm of Te-doped BGs. The investigated Te-doped BG showed a significant biofilm metabolic reduction for both S. aureus and S. epidermidis, the most frequent strains involved in orthopedics infections [53].
The antibacterial activity of Te is due to a combination of different mechanisms that are likely not yet fully disclosed. Turner et al. [54] gave an explanation of some events. Briefly, tellurite can exceed the outer membrane due to the environmental pH variation and then exert its toxic action in the cytoplasmic compartment by triggering an increase in the generation of reactive oxygen species (ROS) [55]. The tellurite influences the activity of the superoxide dismutase (SOD) that is necessary to counteract the oxygen species (ROS) formed.

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