A review: strategies to reduce infection in tantalum and its derivative applied to implants

Xiao Ge; Ti Li; Miao Yu; Hongguang Zhu; Qing Wang; Xiuting Bi; Tiantian Xi; Xiaoyan Wu; Yubin Gao

doi:10.1515/bmt-2022-0211

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A review: strategies to reduce infection in tantalum and its derivative applied to implants

Xiao Ge , Ti Li , Miao Yu , Hongguang Zhu , Qing Wang , Xiuting Bi , Tiantian Xi , Xiaoyan Wu und Yubin Gao

Veröffentlicht/Copyright: 3. Januar 2023

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Abstract

Implant-associated infection is the main reasons for implant failure. Titanium and titanium alloy are currently the most widely used implant materials. However, they have limited antibacterial performance. Therefore, enhancing the antibacterial ability of implants by surface modification technology has become a trend of research. Tantalum is a potential implant coating material with good biological properties. With the development of surface modification technology, tantalum coating becomes more functional through improvement. In addition to improving osseointegration, its antibacterial performance has also become the focus of attention. In this review, we provide an overview of the latest strategies to improve tantalum antibacterial properties. We demonstrate the potential of the clinical application of tantalum in reducing implant infections by stressing its advantageous properties.

Keywords: antibacterial; coating; tantalum

Introduction

The primary risk factors for implant failure are microbial colonization and biofilm formation [1]. Although preventive antibiotic therapy is the primary measure for preventing implant infection in clinics [2], systemic administration has low antibacterial efficacy [3]. It is debatable whether antibiotics should be prescribed as a preventative measure during implant insertion procedures because there is insufficient data to create definitive clinical guidelines. First of all, the area around the implant cannot accumulate enough antibiotics after surgery. Second, drug resistance is easily developed [4]. Thirdly, the body’s other tissues may suffer damage from systemic antibiotic doses that are too high [5].

Researchers have been expanding their research on the antimicrobial properties of implant materials to reduce orthopedic implant-related infections caused by antibiotic-susceptible microorganisms [6]. The surface morphology and chemical composition of the implant affect microorganism adhesion and biofilm formation [7].

The commonly used implants made of titanium and titanium alloy do not currently have particularly strong antibacterial properties [8]. The corrosion resistance of titanium and titanium alloys is limited, resulting in the dissociation of metal particles and ions from the implant surface into the surrounding tissue, which can cause inflammation and even toxic reactions [9]. As a result, in recent years, scientists have been searching for implant modification methods and titanium alternatives.

Tantalum metal has extremely strong corrosion resistance and stable physical and chemical properties [10], and previous research has shown that its osteogenic property is superior to that of titanium, making tantalum a promising implant material for clinical use [11]. In addition to its excellent osteogenic properties, some related studies have investigated and compared its antibacterial properties. Implants are becoming more functional and intelligent. With the advancement of implant surface engineering, there is some research being conducted to improve the bioactivity and antimicrobial properties of implants in conjunction with tantalum and other materials in order to increase the success rate of dental implant surgery [12, 13].

This review demonstrates the role of tantalum in the antimicrobial surface modification of implants, as well as recent research progress in tantalum-based antimicrobial coatings. We demonstrate the advantages of tantalum for clinical applications as an implant material, evaluate its potential to prevent implant-related infections, and discuss future trends for novel implants.

Properties advantages of tantalum

It was first recorded in 1940 that tantalum was utilized in surgery. Tantalum was developed by scientists into surgical sutures for tantalum nails and tantalum plates for fracture repair, and long-term clinical evidence has shown its reliability as a material for use in surgery [14]. Tantalum and its alloys have exceptional physicochemical and biological qualities; it can keep its original physical, chemical, mechanical, and biological properties while performing its duty without being rejected or injured by the host, and finally creates a favorable integration with the host [15]. Tantalum possesses antibacterial qualities in addition to its good osteogenesis induction when used as an implant material [16]. Tantalum has an advantage over other materials in reducing implant infections because of these properties. Tantalum’s highly stabilized physicochemical qualities serve as the preliminary and essential foundation for other properties, allowing it to maintain appropriate mechanical strength even after surface processing alterations and maximizing the physical properties of other implant materials. Its exceptional osteogenic qualities enhance host cell attachment, shield the implant surface from microbial growth, and hence support antimicrobial activity. Other tantalum characteristics, including photocatalytic and electrochemical characteristics, also hold significant promise for the creation of future intelligent and useful implant coatings.

Physicochemical properties

Implants are prone to wear and corrosion in the oral environment. Frictional forces might cause the coating to separate. Particles released from the implant surface contribute to implant failure [17]. Dental implants are more vulnerable to electrochemical reactions between the implant surface and the oral fluid because the presence of microbial metabolites may cause a decrease in the pH of the oral environment in the body. This can result in partial or complete dissolution of the metal and the release of metal ions and particles from the implant into the surrounding tissue. This can potentially result in serious complications like peri-implant disease or systemic toxicity [18]. Much of the current research tends to building functional implant surfaces. However, implants can only maintain their own physicochemical properties in vivo to ensure that functions such as antimicrobial properties and osteogenic properties can be performed steadily in the long term.

Hydroxyapatite is an excellent bioactive implant coating material, and researchers have been focused on the development of drug-loaded or antimicrobial ion-loaded implant coatings with antimicrobial capabilities. However, the application of hydroxyapatite in orthopedics has been constrained by its weak mechanical qualities [19]. In comparison, tantalum metal has a high mechanical strength and density. This enables it to satisfy the mechanical demands of an orthopedic or dental implant. It also exhibits a modulus of elasticity similar to natural cortical and cancellous bone when manufactured as a thin film or porous structure [20, 21].

Tantalum offers superior wear tolerance and corrosion resistance than titanium and titanium alloys [22]. As a result, researchers have created tantalum alloys or coated tantalum on the surface of other materials to improve the mechanical strength of the implant while also reducing corrosion of the underlying material.

Osseointegration properities of tantalum

The concept of “surface race” was introduced early on by Anthony Gristina [23]. According to this principle, host cells compete with invasive microorganisms to occupy the implant surface, and the victory of the latter usually leads to the formation of a microbial film on the implant surface and implant-related infection. So, the rapid integration of host cells and implant surfaces plays a key role in inhibiting pathogen adhesion and proliferation [24]. However, some popular implant coating materials do not have excellent osteogenic bioactivity. For example, polyether ether ketone (PEEK), which is widely used for dental and orthopedic implants because of its excellent mechanical strength and biocompatibility, is a biologically inert material that does not induce cell attachment, proliferation, differentiation, or bone regeneration [25]. In contrast, tantalum has osteogenesis-promoting properties compared to PEEK. In animal models of bone defects, tantalum implants have shown a superior promotion of new bone growth [26]. In vitro experiments have shown that the nanoporous structure of the tantalum-coated surface facilitates the adhesion and proliferation of osteoblasts [27]. Furthermore, it can induce osteogenesis through certain signaling pathways, such as Wnt/β-catenin, BMP, TGF-β, and integrin signaling pathways [28].

When applied to clinical hip arthroplasty, tantalum prostheses have been shown to have fewer postoperative infections than titanium prostheses. The main reason may be that Ta has a higher osseointegration potential, which facilitates osteoblast proliferation and occupies the surface of the implant, thus depriving it of space for bacterial invasion [29].

Tantalum’s superior osteogenic properties allow it to achieve good osseointegration. In addition to this, it has been shown that tantalum coatings can promote the proliferation of gingival cells [30], allowing them to bio-seal in close association with periodontal tissue, thereby preventing bacterial attack and greatly reducing the risk of infection.

Antibacterial properties

In 2006, Schildhauer et al. reported that Staphylococcus aureus and Staphylococcus epidermidis had lower adhesion rate on the surface of pure tantalum than titanium and ordinary steel alloy, suggesting that tantalum has superior antibacterial characteristics than titanium [31]. Zhang et al. produced tantalum coatings on titanium alloy surfaces and investigated the effects of different implant surfaces on osteoblasts, Streptococcus mutans, and Porphyromonas gingivalis, as well as in a cellular bacterial co-culture model. Ta-modified micro/nanostructured surfaces would encourage cell-surface interactions rather than bacterial-surface interactions. The adherence of S. mutans and P. gingivalis on the Ta-coated surface was much lower than on the titanium alloy surface (Figure 1a). Cell surface coverage on both surfaces decreased when bacteria were added to the cells in a co-culture. The decrease of Ta-coated samples, however, was significantly lower than that on SLA titanium surfaces (Figure 1b). Additionally, statistical analysis of the cell surface coverage consistently showed that the Ta coating decreased bacterial-caused cell damage (Figure 1c). In the experiment, the tantalum coating provided greater coverage for cells in the presence of pathogens [32]. This is an explanation of the “surface race” principle. As previously stated, osteoinductivity plays a function in enhancing antibacterial characteristics.

Figure 1:

(a) Confocal microscopic images of bacteria cultured on both groups for 6 and 12 h. The green fluorescent intensity on Ta-coated SLA was obviously lower than those on SLA. Scale bar=75 μm. (b) Cell-surface coverage on both groups in absence or presence of bacteria as visualized by using rhodamine phalloidin and DAPI staining. Scale bar=100 μm. (c) Statistical results for cell-surface coverage. Reproduced with permission [32]. Copyright 2017, Wiley.

Based on the improved performance of tantalum-coated samples compared to titanium samples in the experiment, Zhang et al. further described the antibacterial mechanism of tantalum coating. It was discovered that the implant surface modified by Ta coating had good antibacterial activity against Fusobacterium nucleatum and P. gingivalis, which was related to the micro-current produced between tantalum metal and titanium-based metal. The micro-current created between various metals can consume protons, increasing the generation of oxidative stress products in the environment around the implant and decreasing bacterial ATP synthesis, thereby having an antibacterial effect [33]. Shimabukuro et al. evaluated the antibacterial properties of Ti alloys, Ti, Nb, Ta, and Zr. Ag inhibited cell adherence the most, but Ta and Nb outperformed Ti and Zr in terms of antibacterial activity [34]. Tantalum oxides, nitrides, tellurides, and other compounds have also been shown to have antibacterial effects, inhibiting Escherichia coli, S. mutans, Enterococcus faecalis, and other bacteria [35], [36], [37]. The research comparing tantalum and its compounds’ antibacterial qualities to those of other minerals is shown in Table 1 of this article.

Table 1:

Tests for antibacterial properties of tantalum or its compounds.

Tantalum or its compounds	Contrasting materials	Included bacteria species	Comparison of antibacterial effect	Reference
Ta	Ti	F. nucleatum	The Ta-coated surface had a stronger antibacterial effect on F. nucleatum than on P. gingivalis	Zhang et al. [33]
Ta	Ti	P. gingivalis		Zhang et al. [33]
Ta	Ti, Nb, Zr, Ag	S. aureus	Silver has the best antibacterial performance, Nb and Ta are better than Ti and Zr	Shimabukuro et al. [34]
Ta	Ti	S. mutans, P. gingivalis	The amounts of S. mutans and P. gingivalis adhered on Ta-coated surfaces were obviously fewer than those on titanium surfaces	Zhu et al. [32]
Ta	Tantalum-coated stainless steel, titanium, titanium alloy, grit-blasted and polished stainless steel	S. aureus, S. epidermidis	Bacterial adherence of S. aureus: Pure tantalum presented with significantly lower S. aureus adhesion compared to titanium alloy, polished stainless steel, and tantalum-coated stainless steel. Furthermore, pure tantalum had a lower, though not significantly, adhesion than commercially pure titanium and grit-blasted stainless steel. S. epidermidis adherence was not significantly different among the tested materials.	Schildhauer et al. [31]
TaN	Ti, TaN-Ag (with Ag content of 21.4 at.%)	S. aureus	TaN-Ag>TaN>Ti	Huang et al. [35]
Ta₂O₅, Ta	Ti, Ta	S. aureus, A. actinomycetemcomitans	Ta₂O₅ (amorphous) >Ta>Ti>Ta₂O₅ (crystalline)	Chang et al. [36]
Ta₂O₅	Ti	S. sanguinis	No significant difference	Beline et al. [38]
Ta-DLC (Tantalum containing diamond-like carbon)	Silver-DLC, cobalt-DLC, indium-DLC, tungsten-DLC, tin-DLC, aluminum-DLC, chromium-DLC, zinc-DLC, manganese, titanium-DLC	C. albicans, E. coli, P. aeruginosa, S. aureus, E. faecalis	Silver-DLC and cobalt-DLC have exhibited inhibition of growth of all tested strains.	Cazalini et al. [39]
			In-DLC thin film was not effective against any strain.
			Tungsten-DLC, tin-DLC and aluminum-DLC, zinc-DLC, manganese-DLC, tantalum-DLC inhibited the growth of some strains.
			Chromium-DLC and titanium-DLC weakly inhibited the growth of only one of the tested strains.
TaSe₃, TaTe₄	Nb₂Se₃, NbTe₄	E. coli, S. aureus.	Superior antibacterial efficacy was observed for telluride system compared with selenide system.	Altaf et al. [37]
TaSe₃, TaTe₄	Nb₂Se₃, NbTe₄	E. coli, S. aureus.	The antibacterial property of NbTe₄ is superior to that of TaTe₄.	Altaf et al. [37]

However, there are divergent views on the antibacterial properties of tantalum. Tantalum is not considered to be intrinsically antimicrobial as it is difficult to dissociate tantalum ions in vivo. Harrison et al. inoculated S. aureus and S. epidermidis into Ta and Ti acetabular prostheses in vitro. In comparison to the Ti control, Ta did not show sufficient intrinsic antibacterial activity or inhibition of biofilm formation [40]. Therefore, there is no consistent conclusion as to whether tantalum has inherent antibacterial ability.

Photocatalytic properties

Photodynamic therapy, as a minimally invasive and safe method of reducing biofilm formation, has been shown to significantly reduce the frequency of implant-related infections [41]. Metal ions can become catalytic centers for oxidative stress processes when exposed to light, resulting in the formation of reactive oxygen species (ROS). Reactive oxygen species are oxygen-containing molecules that are chemically reactive. The hydroxyl radicals and organic molecules generated are either directly or indirectly oxidized, altering the balance of the oxidation-antioxidation system and harming bacteria’s cell membranes, and preventing their reproduction [42, 43].

It is reported that tantalum oxide has certain photocatalytic activity. These oxides can promote electron transition under the excitation of certain spectral light, and the reactive oxygen free radicals produced can lead to oxidative stress reaction of bacteria, destroying the cell wall and cell membrane of bacteria and causing them to cleavage and die [44]. Cristal et al. showed that tantalum nitride films have good photocatalytic degradation ability and the inhibition of Salmonella by the films improved with the increase of oxynitride content [45]. In addition, according to the principle of photocatalysis, the implants can be pretreated with UV light to achieve better antimicrobial effect. Tantalum doping in titanium dioxide can improve its photocatalytic efficiency. Experiments by Gupta et al. showed that the 20 mol% Ta-doped titanium dioxide particles had the highest photocatalytic degradation rate and showed strong antibacterial ability [46].

Enhanced local innate immunity

If the study of antimicrobial qualities just focuses on the implant surface’s bactericidal potential, there is a risk of overlooking the material’s safety and causing harm to the host. An effective strategy is the use of biomaterials with immuno-compatible and immuno-protective qualities to improve host defensive mechanisms [47]. Some researchers believe that tantalum coating does not have direct antibacterial activity in vitro, but that it can attain antibacterial performance in vivo through immunological stimulation of neutrophils and macrophages. Tantalum coating can increase not just osteoblast growth and adhesion, but also macrophage proliferation. In the animal model of bone tissue infection, the tantalum nano-coating demonstrated good antibacterial capabilities in vivo. Its primary antibacterial mechanism is to enhance neutrophil phagocytosis of germs, minimize neutrophil lysis, and encourage macrophages to release pro-inflammatory cytokines. When the local host’s defensive ability accumulates, it will generate a stronger antibacterial effect [48]. Schildhauer et al. showed that leukocytes-mainly neutrophils and monocytes-in peripheral blood were activated upon contact with tantalum trabecular material. Tantalum trabeculae’s macroporous shape is an excellent precursor for leukocyte infiltration into the circulation quickly and for cell attachment, which may cause leukocyte activation and the release of cytokines. Cytokine release from leukocytes exposed to tantalum trabecular material was significantly increased compared to the response of other traditional materials used for orthopedic metal implants [49].

Advantages of application for infection-prone patients

There is an inherent susceptibility to infection in patients who are treated with dental implants. Their age distribution is mostly middle-aged and elderly, and they may be suffering from periodontal disease with poor oral hygiene, or from systemic diseases that lead to a decrease in immunity. These patients have more microorganisms inherent in the oral cavity or have a delayed bone healing process due to systemic factors that increase the risk of pathogen invasion [50]. Patients susceptible to infection are the main target group for antimicrobial performance implants. It is significantly more convincing and clinically relevant to target specific groups than studies based on healthy individuals. Several studies have already shown that tantalum implants have a higher success rate in susceptible patients.

The response of human osteoblasts to orthopedic and dental implant materials is related to the gender and age of the patient. It has been demonstrated that human osteoblasts from older female patients have a significantly reduced ability to form bone on implants [51]. Moreover, middle aged and elderly women are at high risk of osteoporosis. Sagomonyants et al. showed that porous tantalum has a superior effect on stimulating osteoblast proliferation in middle-aged and elderly women compared to titanium [52]. Osteoporosis is one of the most common bone metabolic disorders that can prolong the healing period and affect early implant stability. Lu et al. compared the osteoinductivity of polished tantalum and polished titanium in osteoporosis using ovariectomized rats to simulate the conditions of osteoporosis. The results showed that tantalum performed better in both in vitro and in vivo experiments compared to titanium [53].

The current clinical evidence suggests a high failure rate of titanium implants in diabetic patients [54], [55], [56]. High blood glucose levels reduce osteoblast adhesion to titanium surfaces,which adversely affect the healing process in the surgical area and lead to an increased susceptibility to infection [57]. The diabetes leads to overproduction of reactive oxygen species (ROS), which may affect the viability of the cells surrounding the implant surface [58]. Wang found that the diabetes-induced ROS-mediated p38 MAPK signaling pathway caused significant osteoblast dysfunction and apoptotic damage on implants. Meanwhile, their experimental results showed that tantalum coating could reduce the overproduction of ROS and decrease the phosphorylation of MAPK pathway. Moreover, in diabetic animal models, the tantalum coating significantly promoted the osteogenic performance of the implants [59].

Patients suffering from maxillofacial tumors with bone loss or tooth loss need implants to restore oral and maxillofacial function. But the radiation therapy negatively affects the cells of the hard and soft tissues of the oral and maxillofacial region in patients with head and neck cancer, putting them at greater risk of dental implant failure. Vuletić et al. reported a case in which Porous tantalum trabecular metal implants were used in the mandible of an oropharyngeal cancer patient undergoing radiotherapy. After 1 year of follow-up, no complications were observed [60]. In addition, a study by Ding et al. found that tantalum coatings treated with thermal oxidation have photothermal conversion properties [61]. Photothermal therapy is a non-invasive and efficient treatment strategy for bone cancer, and biomaterials with photothermal conversion properties are a good choice for repairing bone defects in patients with bone malignancies [62]. Therefore, tantalum has the potential to be used as a bifunctional coating material with both bone defect regeneration and photothermal conversion functions to kill residual tumor cells [63].

Re-implantation in patients with failed dental implants is challenging. Because the majority of these patients are middle-aged or elderly, smokers or have a history of moderate to severe periodontal disease [64]. The Dimaira trial evaluated 16 tantalum trabecular implants in 14 patients who underwent immediate implant placement at the site of initial implant failure. Follow-up results showed that 15 implants were still functional after five years and showed success in clinical signs and imaging assessment [65]. This suggests that tantalum implants are better choices for reimplant treatment after initial implant failure.

Strategies to enhance the antimicrobial properties of tantalum

Although there are previous clinical reports that indicate a low infection risk for tantalum implants, some research has shown that tantalum does not have significant antimicrobial properties in vitro. In recent years, researchers have begun to improve the antimicrobial properties of tantalum-coated or tantalum-based implants through surface modification techniques.

Currently, antibacterial surface modification strategies for implants are classified into two types based on their antibacterial mechanism: “passive” antibacterial, which aims to avoid bacterial adhesion or biofilm formation, and “active” antibacterial, which kills bacteria in direct contact with or near the implant surface [66, 67]. The microorganisms around the implant exist in the form of attachment or free, and antiadhesion and contact bactericidal strategies mostly target adhesive bacteria, while bactericidal release strategies are applied to suspension bacteria. For this reason, it is difficult to accomplish long-lasting antimicrobial effects using a single antimicrobial strategy, while a combination of passive and active strategies can maximize antimicrobial performance [68]. However, there are limitations to each material, and it is difficult to achieve excellent antimicrobial performance with tantalum alone. It must be combined with other metallic or non-metallic materials to achieve antimicrobial purposes and to provide for other needs of the implant. Methods to enhance the antimicrobial ability of tantalum can be divided into two categories, namely the synthesis of alloys that release antimicrobial metal ions and the preparation of coatings with antimicrobial properties.

Antibacterial alloy

Tantalum alloys for implant applications include tantalum-niobium alloys, tantalum-zirconium alloys, and novel titanium alloys with additional elements [69, 70]. Antimicrobial tantalum alloys, all of which are produced by adding metals with potent antibacterial properties to the alloy, have received relatively little attention. Cui et al. combined mechanical alloying and spark plasma sintering technology to prepare bulk Ta-5Cu alloy. It was found that the addition of copper had a significant effect on the antibacterial activity, hardness, corrosion resistance and wear resistance of Ta. Due to the continuous release of copper ions, Ta-5Cu alloy has strong antibacterial activity against E. coli. However, the addition of copper can cause mild cytotoxicity and reduce the corrosion resistance of Ta [71]. Zhang et al. prepared a titanium-tantalum-silver alloy and experimentally demonstrated that low Ag content can significantly improve the hardness, deformation resistance and hardness of the alloy, but decreases the plasticity and brittleness of the alloy significantly [72]. Lin et al. developed an osseocompatible β-type Ti-28Nb-11Ta-8Zr (TNTZ) alloy with an elastic modulus close to that of human bone and a superior corrosion resistance compared with commercial pure titanium. In terms of bioavailability, the crystalline nanoporous oxide layer on the surface of this alloy promoted the adhesion and proliferation of bone cells on the surface of the material. And the presence of nano-silver enhanced the antibacterial effect against Pseudomonas aeruginosa, S. aureus and E. coli [73]. Therefore, the comprehensive performance of the alloy in clinical application is not as good as that of the coating, and the future focus should still be on the surface modification technology.

Antibacterial coatings

Tantalum is a rare metal with a high melting point and mechanical strength, resulting in processing challenges, expensive costs, and mismatches with the elastic modulus of bone. Tantalum is typically produced in the form of coatings for practical application to address these issues [74]. The consumption and expense can be greatly decreased by preparing tantalum as a coating. More importantly, the coating can optimize the properties of the substrate material, such as improving corrosion resistance, enhancing surface hardness, changing surface morphology, changing wettability, hydrophobicity, etc. [75]. A variety of tantalum-based composite coatings have been designed. These coatings have good durability and corrosion resistance because of the existence of tantalum metal, which can provide effective support for tissue growth [11].

Tantalum coatings can be used not only for the modification of titanium and titanium alloy implants, but also for other implant materials, such as polyetherketoneketone (PEKK) and polyetheretherketone (PEEK), which have become popular in recent years [76, 77].

According to the surface structure, tantalum coatings can be categorized as smooth tantalum, porous tantalum and nanostructured tantalum coatings [12, 78]. In addition to pure tantalum coatings, its non-metallic coatings have also attracted attention, such as tantalum oxide, tantalum nitride, tantalum boride, tantalum carbide, etc. [79].

But the coating remains a weakness compared to the alloy and deserves our consideration. With long-term mechanical stress and loading wear, metal nanoparticles will inevitably detach from the implant surface, and these particles may adversely affect the surrounding tissues. Wang et al. explored the effects of tantalum nanoparticles on osteoblasts and found that tantalum nanoparticles had an autophagy-inducing effect, and low concentrations of tantalum nanoparticles promoted the proliferation of osteoblasts, while at ≥25 g/mL, tantalum nanoparticles began to cause a decrease in osteoblast viability [80]. So we can consider that low doses of tantalum nanoparticles are not harmful to organizations.

With the development of surface modification technologies, increasingly more coating fabrication methods are being used to improve the surface properties of implants. The commonly used fabrication methods of tantalum coatings include plasma spraying, chemical vapor deposition, laser cladding, magnetron-sputtering technology, sol-gel technique, etc. [30, 81], [82], [83], [84], [85] Researches nowadays began to focus on the combination of multiple surface modification techniques, and the coating structure gradually evolved from monolithic to complex. Functional and intelligent antibacterial surfaces are the development direction of implant coating technology.

The antibacterial coating material on the surface of implant has important clinical significance for reducing implant-associated infection [86]. Tantalum antimicrobial coatings can be modified by changing their surface morphology to create a surface that is adverse to bacterial adhesion. Or the surface can be loaded with antimicrobial agents that release metal ions, antibiotics, antimicrobial polymers and other biocides that act directly on bacteria [87] (Figure 2). The presence of tantalum improves the mechanical properties and corrosion resistance of the coating and plays a role in regulating the release of antimicrobial agents, thus influencing the final antimicrobial effect [88].

Figure 2:

Main types of tantalum-based antimicrobial coatings.

Surface morphology of tantalum-based coating with reduced microbial adhesion

The surface characteristics of implants, such as surface charge, wettability, roughness, and surface morphology, are thought to be important factors limiting the initial adhesion of bacteria to the implant surface [89, 90].

Although the surface chemistry of bacteria is different, most bacteria have a negative total surface charge. Under the effect of Coulombic forces, negatively charged bacteria were attracted to the positively charged implant surface, which accelerated the adhesion of microorganisms. Lawrence et al. prepared poly (amino acid) polyelectrolytes coatings on the surface of tantalum oxide by layer-by-layer deposition. It was shown that the adhesion of bacteria increased when the top layer was positively charged poly (amino acid) layers and the coverage of bacteria decreased sharply if it was negatively charged poly (amino acid) layers. Moreover, it was found that the polyelectrolyte coating is more favorable on the surface of high-k dielectric bioceramics like tantalum oxide and zirconium oxide to form a dense polyelectrolyte coating, which can enhance the attraction and repulsion of the coating to bacteria. This demonstrates the significance of surface charge density in regulating bacterial adhesion to the implant surface [91].

Surface wettability, roughness, topography are correlated and representative surface properties. Surface wettability has a significant effect on bacterial adhesion, and the inherent wettability of a surface depends on its surface energy and roughness. Huang et al. treated tantalum oxide coatings on titanium surfaces by plasma electrolytic oxidation (PEO) to increase their wettability. The results of antibacterial performance tests showed that both the tantalum oxide coating group and the PEO-treated tantalum oxide coating group were superior to the titanium group, while the PEO-treated tantalum oxide was slightly less effective than tantalum oxide in inhibiting S. aureus and associated actinomycetes, probably because it has a superhydrophilic surface [92]. Chang et al. prepared crystalline and amorphous tantalum oxide coatings and found that amorphous tantalum oxide with low surface energy hydrophobicity showed better antibacterial activity against S. aureus and Actinomyces. While crystalline tantalum oxide coatings exhibit hydrophilicity and excellent cellular biocompatibility to human skin fibroblasts [36]. Horandghadim et al. compounded multi-walled carbon nanotubes with hydroxyapatite-tantalum pentoxide (HA-Ta₂O₅) to prepare a coating on the surface of nickel-titanium metal. As the content of multi-walled carbon nanotubes increased, the surface wettability decreased and the bactericidal effect became better. In addition, the multi-walled carbon nanotubes induced the antimicrobial properties of HA-Ta₂O₅ coating through direct contact with bacteria leading to the degradation of the film [93]. Huang et al. found that TaN-coated titanium had a lower amount of bacteria adhesion compared to uncoated titanium, which was related to its increased roughness and hydrophobicity [35]. Zhang et al. found that TaN coatings had significant antibacterial activity against S. mutans, S. aureus, Pseudomonas gingivalis, and Actinomyces owing to the modified surface roughness and hydrophilicity, which is consistent with the findings of Huang et al. However, the real reason why increasing the TaN amount can improve the antibacterial performance of titanium-based implant materials is not well clarified. In addition, TaN was found to be able to resist the microbial corrosion caused by oral bacteria on the implant surface [94].

Surface topography affects roughness, and higher roughness results in higher wettability. But the surface morphology of material surfaces with similar roughness can be completely different. The three-dimensional details of the surface topography, such as geometry, density or hierarchy, were important for bacterial adhesion. In Sopata et al.’s experiments, micro-arc oxidized (MAO) treated nanocrystalline tantalum had a higher roughness and hydrophilicity than microcrystalline tantalum, but it showed a higher bacterial inhibition ability, which may be related to the fact that it has a thicker oxide layer [95]. Therefore we should pay more attention to the effects associated with the surface morphology. Specific surface nanostructures, such as nanotubes, nanopores and nanotubes, have been shown to have certain antimicrobial properties [96]. A number of studies have been published the effect of morphological modifications of tantalum coatings on osteoblast adhesion, proliferation and differentiation, but no studies have yet been conducted to improve the antimicrobial properties of tantalum coatings simply by modifying their topography [87, 97, 98].

Tantalum-based coating with antibacterial metallic nanoparticles or ions

Metal and metal derivative nanomaterials have potential for antimicrobial applications in implants [99]. The antimicrobial properties of nanomaterials are clinically relevant in the fight against drug resistance caused by systemic antibiotic use [100]. When metal-based nanomaterials are used without a substrate material, they have limitations that reduce antimicrobial efficiency. Furthermore, biomaterials are frequently used as substrates in conjunction with metal ions or nanoparticles to improve antimicrobial properties. Because of its stable physicochemical properties and excellent biological properties, the tantalum-based coating is an ideal substrate material for antimicrobial agents [101]. A common method for improving the antimicrobial properties of tantalum is to load metallic nanoparticles or ion antimicrobial agents on the coating surface. Some metal ions can inhibit bacteria by causing cell membrane damage, protein inactivation, and oxidative stress. Silver (Ag), copper (Cu), and zinc (Zn) are the most frequently used antibacterial metal elements, though others like gallium (Ga), gold (Au), tin (Sn), and strontium (Sr) also possess some antibacterial qualities [102]. We present research on the antimicrobial properties of tantalum-based coatings loaded with metal nanoparticles or metal ions (Table 2).

Table 2:

Recent development of tantalum-based coating with antibacterial metallic nanoparticles or ions.

Main anti-infection agent	Mentioned synthesis method	Main forms of tantalum	Included bacteria species	Antibacterial effects	References
Ag nanoparticles	Silver plasma immersion ion implantation technique	Ta₂O₅	Staphylococcus epidermidis	Demonstrated antibacterial property	Cao et al. [103]
Ag nanoparticles	Silver plasma immersion ion implantation technique	Ta₂O₅	Staphylococcus epidermidis	Better antimicrobial performance for samples treated with plasma immersion technique for 1.5 h	Cao et al. [103]
Ag	Magnetron sputtering technique	Ta coating	E. coli	Demonstrated antibacterial activities	Wu et al. [104]
Ag	Magnetron sputtering technique	Ta₂O₅	E. coli, S. aureus	Samples via thermal treatment at 400 °C demonstrated antibacterial activities	Alias et al. [105]
Ag₂O nanoparticles	Physical vapor deposition	Tantalum oxide nanotubes	E. coli	Antibacterial property↑	Sarraf et al. [106]
Cu	Magnetron sputtering technology	Ta₂O₅ multilayer coating	S. aureus	Antibacterial property↑	Ding et al. [107]
Cu	Magnetron sputtering technology	Ta₂O₅ multilayer coating	S. aureus	Antibacterial property↑	Ding et al. [108]
Cu	Magnetron sputtering technology	Ta₂O₅ multilayer coating	S. aureus	The sample with Cu incorporation of 18.76 at % has better antibacterial properties	Ding et al. [108]
Cu	Magnetron sputtering technology, Anodization	Tantalum nanotubes	E. coli, S. aureus	Antibacterial property↑	Wu et al. [109]
Cu	Magnetron sputtering technology, Anodization	Tantalum nanotubes	E. coli, S. aureus	The sample TaCu2-NT (Ta: Cu=1:1 at %) has better antibacterial properties	Wu et al. [109]
Cu	Photolithography	Bilayered Ta\|TaCu thin films	E. coli, S. aureus	Antibacterial property↑	Zhu et al. [110]
	Inductively coupled plasma (ICP)-based dry etching			Promotes proliferation and osteogenic differentiation of preosteoblasts in the presence of bacterial infection
	Electron beam evaporation (EBE)
ZnO	Hydrothermal process	Ta foils	E. coli, S. aureus	Antibacterial property↑	Liao et al. [111]
ZnO	Hydrothermal process	Ta foils	E. coli, S. aureus	The antibacterial activity of the ZnO nanorods-nanoslices hierarchical structure could last for more than 2 weeks in animal experiments	Liao et al. [111]
Zn	Micro-arc oxidation (MAO)	Ta₂O₅	S. aureus	Antibacterial property↑	Fialho et al. [112]
Zn	Magnetron sputtering technology	Ta₂O₅	S. aureus	Antibacterial property↑	Fialho et al. [112]
ZnO	Magnetron sputtering technology	TaxOy	S. aureus	Antibacterial property↑	Ding et al. [113]

Ag ions are currently considered to have the best antibacterial properties, with long-lasting effects and less susceptible to drug resistance. Silver and silver compounds can destroy cell membranes, impair the function of intracellular enzymes and interfere with the respiration of microorganisms, thereby inhibiting their reproduction. The addition of Ta to the implant coating can effectively inhibit the dissolution of the coating to effectively control the release of silver ions [104]. Alias et al. prepared silver (Ag) and tantalum oxide (Ta₂O₅) nanocomposite layers on SS 316L steel surface by magnetron sputtering technique. Different heat treatment temperatures affect the morphology and bond strength of the coating surface. The composite coatings under heat treatment at 400 °C demonstrated excellent antibacterial activity, hBMSCs attachment and proliferation activity [105, 114]. The study by Sarraf et al. found that the coating of Ta₂O₅ NTs decorated with Ag2O NPs showed sufficient antibacterial effect against E. coli and that the Ta₂O₅ nanotube structure had a synergistic effect on silver ion release [115]. Cao et al. modified silver nanoparticles on tantalum oxide coating by plasma immersion ion implantation technique, and this composite coating had a killing effect on S. epidermidis and had no inhibitory effect on the adhesion and differentiation of bone marrow mesenchymal stem cells [116].

Copper is a widely used antimicrobial agent because of its low toxicity and low costs [103]. Copper ions released by antibacterial coatings act directly or indirectly on bacteria by promoting the formation of superoxide [117], which disrupts the enzyme system of bacteria, leading to the cessation of bacterial respiration and the degradation of DNA [106]. Copper-doped Ta₂O₅ multilayer composite coatings on the surface of Ti6Al4V alloy showed inhibition of colonization after co-culture with E. coli. Moreover, the antimicrobial properties of the Ta₂O₅ coating increased significantly with the increase of Cu²⁺ content [107, 108]. Wu et al. successfully fabricated Cu and Ta nanotubes on Ti substrates by magnetron sputtering and anodizing technology, they have good osteogenesis and antibacterial properties, and Ta nanotubes can stabilize the slow release of bioactive copper and has good antibacterial effect [109]. Zhu et al. fabricated microgroove-patterned Ti surface and the bilayered Ta|TaCu nanostructured thin film, which not only further promoted osteogenesis, but also created smart surfaces capable of continuous copper ion transport on a local scale with high antibacterial capacity [110].

Previous studies have reported that zinc oxide has good antibacterial activity against S. aureus, Salmonella, E. coli and other bacteria. The addition of low dosages of zinc oxide to the coating of implants can significantly improve the antimicrobial properties of the material. In addition, the adding of zinc oxide to the implant material can promote the proliferation and differentiation of osteoblasts, thus promoting osteogenesis. Ding et al. prepared a multilayer ZnO-TaxOy composite coating on titanium implants, which inhibited S. aureus up to 90.65%, while the single TaxOy coating inhibited nearly 19.78% [113]. Inspired by deciduous leaves, Liao et al. for the first time constructed a bilayer ZnO nanorod-nanosheet layered structure, and modified the surface of Ta to make tantalum possess good antibacterial properties [111]. Fialho et al. used micro-arc oxidation technology to obtain bone-like micro-nano-porous Ta₂O₅ layer with biomimetic Ca/P ratio. Zn/ZnO nanoparticles and carbon were deposited on the sample surface by DC magnetron sputtering technology to prepare TaCaP-Zn and TaCaP-ZnC composite coatings. Both of the two structures had inhibitory effect on S. aureus, but only TaCaP-Zn could inhibit the colonization of attached bacteria. The combination of the two techniques changed the surface morphology of the original tantalum implant, promoted the initial cell adhesion and proliferation, and had bactericidal effect due to the addition of Zn. This composite structure has a controlled effect on the release of Zn ions. And it reduces cytotoxicity because direct contact of Zn ions with the tissue is avoided [112].

However, there are still challenges for the application of metal ions and nanoparticles. On the first, metal ions and nanoparticles have negative effects on normal tissue cells. Secondly, bacteria may acquire drug resistance to nanoparticles. The antimicrobial activity of nanomaterials is not sufficient to eliminate all microorganisms, and the pathogens remaining on implant surfaces are likely to acquire antimicrobial resistance through long-term exposure to nanobacterial agents [118].

Tantalum-based coating with antibiotic

Antibiotic-loaded coating is a promising strategy for biofilm control [119, 120]. Porous tantalum is known as a “bone trabecular” metal due to its elastic modulus, which is similar to that of cancellous bone. The surface morphology of porous tantalum supports not only the formation of excellent integration with bone tissue, but also the adhesion of drugs and cytokines. It is an ideal loading scaffold material and with controlled degradation of bioactive molecules. The surface morphology of porous tantalum enhances the adherence of cytokines and medicines, in addition to the establishment of excellent integration with bone tissue. It is an excellent loading scaffold material with regulated bioactive molecule degradation.

A drug delivery hypothesis for artificial implants has been proposed, in which a particular structure on the implant surface is produced using surface modification technology to load antibacterial medications onto the implant surface. The medicine can be released into the surrounding bone tissue once the implant has been placed. This enables the medicine to act locally and efficiently, while also minimizing resistance and adverse responses induced by systemic drug administration. It has been shown that porous tantalum may release vancomycin for a very long time, allowing for the local release of significant doses of antibiotics [121]. Hua et al. placed anti-tuberculosis medicines on porous tantalum surfaces and discovered that slow drug release in vitro and in vivo can considerably extend antibacterial activity duration. The composite coating prevented bacterial growth while encouraging bone marrow mesenchymal stem cell osteogenic differentiation [122]. Liu et al. exhibited better biocompatibility and resistance to bacteria and biofilm in vitro and in vivo investigations after using chemical grafting to create a porous tantalum composite scaffold capable of locally slow-releasing vancomycin for the first time [123]. A study examined the antibacterial characteristics of tantalum, 3D-printed porous titanium, antibiotic-loaded bone cement, and titanium alloys. Porous tantalum implants were found to have the equivalent antimicrobial potential as antibiotic-loaded bone cements in the treatment of methicillin-sensitive S. aureus. Moreover, the porous tantalum implants inhibited staphylococcal adhesion over a longer period of time than the 3D-printed antibiotic-loaded porous titanium implants [124].

However, tantalum-based drug-loaded coatings continue to have issues with drug release rates, trouble regulating the quantity of release, and difficulty maintaining long-term antibacterial action. There have also been no studies to determine if the use of tantalum-coated antibiotic-loaded implants leads to drug resistance.

Composite coatings consisting of tantalum combined with polymers

Organic/inorganic biocomposites have been extensively studied in the last few decades. Incorporation of bioactive materials into polymers for bone repair materials has shown significantly enhanced mechanical and biological properties of biocomposites compared to polymers alone. Recently, researches have been conducted to combine polymers with tantalum to form composite coatings with antimicrobial and osteogenic induction properties (Table 3).

Table 3:

Recent development of composites of tantalum-associated polymers with improved antimicrobial properties.

Main forms of tantalum	Main anti-infection agent	Polymers	Mentioned synthesis method	Included bacteria species	Antibacterial effects	References
Ta₂O₅	–SO₃H g r o u p s, Ta₂O₅	PI (polyimide)	Physical mixing, cold-pressuring and sintering methods, sulfonated modification	E. coli, S. aureus	Antibacterial activity↑	Mei et al. [120]
Solid Ta discs, porous Ta	Genistein	PHAs (polyhydroxyalkanoates)	Dip-coating technique, PHAs emulsion flow process	E. coli, S. aureus	Antibacterial activity↑	Rodríguez-Contreras et al. [125]
Solid Ta discs, porous Ta	Genistein	PHAs (polyhydroxyalkanoates)	Dip-coating technique, PHAs emulsion flow process	E. coli, S. aureus	Less antibacterial activity against E. coli compared to S. aureus	Rodríguez-Contreras et al. [125]
Ta₂O₅	MgO, Ag	PCL (polycaprolactone)	Magnetron sputtering, electrospinning	E. coli, S. aureus	Antibacterial activity↑	Bakhsheshi-Rad et al. [126]
Ta₂O₅	MgO, Ag	PCL (polycaprolactone)	Magnetron sputtering, electrospinning	E. coli, S. aureus	Less antibacterial activity against E. coli compared to S. aureus	Bakhsheshi-Rad et al. [126]
Ta₂O₅	Genistein, –SO₃H group	PEEK (polyetheretherketone)	Cold-pressing and sintering, Sulfonated modification	E. coli, S. aureus	Antibacterial activity↑	Mei et al. [127]
Ta₂O₅	Genistein, –SO₃H group	PEEK (polyetheretherketone)	Cold-pressing and sintering, Sulfonated modification	E. coli, S. aureus	Similar inhibition of E. coli and S. aureus	Mei et al. [127]
Ta oxide submicro-particles	Ta oxide submicro-particles, –SO₃H group	PI (polyimide)	Cold-pressing and sintering, Sulfonated modification	E. coli, S. aureus	Antibacterial activity↑	Asadullah et al. [128]
Nano tantalum	Genistein, –SO₃H group	PEEK (polyetheretherketone)	Cold-pressing and sintering, Sulfonated modification	E. coli, S. aureus	Antibacterial activity↑	Luo et al. [129]
Nano tantalum	Genistein, –SO₃H group	PEEK (polyetheretherketone)	Cold-pressing and sintering, Sulfonated modification	E. coli, S. aureus	Similar inhibition of E. coli and S. aureus	Luo et al. [129]

Bakhsheshi-Rad et al. successfully prepared novel anticorrosive and antimicrobial Ta₂O₅-PCL/MgO–Ag coatings on magnesium alloys. The Ta₂O₅ films were prepared by reactive magnetron sputtering and were enabled to improve the corrosion resistance as well as the adhesive strength of the substrates. The results also show that the single Ta₂O₅ coating has little antimicrobial activity, while the PCL/MgO–Ag nanofiber coating contributes to a significant decrease in bacterial proliferation [126].

Rodríguez-Contreras et al. prepared antibiotic-carrying PHA coatings on the surfaces of solid and porous tantalum implants. The coating of PHAs containing Genta was shown to provide an antimicrobial effect on the Ta surface, protecting the implant from Gram-positive and negative bacteria. Moreover, as a degradable material, the PHA coating degraded after the initial antibiotic release was achieved, and the exposed surface of the tantalum implant would facilitate osseointegration [130]. Asadullah et al. prepared tantalum pentoxide/polyimide composites, and the antibacterial properties significantly increased with the increase of Ta₂O₅ content, indicating that Ta₂O₅ plays a critical role in improving the antibacterial properties [125, 128]. Mei et al. prepared PEEK/NTP composite material with submicron particles of Ta₂O₅ and PEEK. The surface was sulfonated to form a layered micro-nano pore surface. Then the bacteriostatic genistein was loaded on the porous surface, which showed high genistein loading and sustained release, and could inhibit the growth of E. coli and S. aureus in vitro [127]. Luo et al. blended Ta nanoparticles with PEEK to prepare Ta/PEEK composites and loaded genistein on the surface, and tested their antibacterial and osteogenic activity. The conclusion is consistent with the conclusion of Mei et al. [129].

Summary and outlook

With the development of Oral Implantology, creating a new type of materials with good biocompatibility, osseoinductivity, antibacterial properties has become a challenge. As the demand for dental implants increases, more and more researchers are trying to improve the antimicrobial properties of implant materials to improve the success of dental implants, which is an aspect of interest for both material engineers and clinicians. The antimicrobial strategies of biomaterials are mainly divided into prevention of bacterial adhesion, contact killing, and release killing. However, anti-adhesive surfaces may hinder the attachment of normal tissue cells, and the addition of bactericidal components has some potential affects on the human body. Therefore, it might be the safest way to inhibit bacterial colonization by targeting biomaterial surfaces to promote rapid colonization or integration of tissue cells.

There is no consensus on whether tantalum is inherently antimicrobial. We presented a large variety of Strategies to enhance the antimicrobial properties of tantalum in this review. The physicochemical properties and biocompatibility of tantalum and its derivatives provide them with the advantage of acting as implant coating materials, which can not only load antibacterial agents such as drugs and metal ions, but also control the release of drugs, which is conducive to the construction of more individualized and intelligent antibacterial implants.

What needs to be emphasized is that the ultimate purpose of any implant surface modification is to promote the osseointegration of the implant, so any research on changing the antibacterial properties of materials should be based on ensuring that its biocompatibility and osteogenic properties are not affected. Fabricating a multifunctional surface coating that integrates bone and antibacterial functions is a future direction of development. Coating materials with a single structure and composition are difficult to meet clinical needs. At present, most of the research on tantalum-based coatings is in the stage of in vitro experiments, the long-term effect remains to be seen.

Corresponding author: Ti Li, Department of Stomatology, Weifang People’s Hospital, Weifang, China, Phone: +96 15906368098, E-mail:15906368098@163.com

Research funding: None declared.
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: Authors state no conflict of interest.
Informed consent: Informed consent was obtained from all individuals included in this study.
Ethical approval: The local Institutional Review Board deemed the study exempt from review.

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Received: 2022-05-28

Accepted: 2022-12-21

Published Online: 2023-01-03

Published in Print: 2023-06-27

Artikel in diesem Heft

https://doi.org/10.1515/bmt-2022-0211

Schlagwörter für diesen Artikel

antibacterial; coating; tantalum