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Review

Influence of Dental Prosthesis and Restorative Materials Interface on Oral Biofilms

1
State Key Laboratory of Oral Diseases, Sichuan University, Chengdu 610041, China
2
Department of Cariology and Endodontics, West China School of Stomatology, Sichuan University, Chengdu 610041, China
3
National Clinical Research Center for Oral Diseases, Sichuan University, Chengdu 610041, China
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Int. J. Mol. Sci. 2018, 19(10), 3157; https://doi.org/10.3390/ijms19103157
Submission received: 27 August 2018 / Revised: 29 September 2018 / Accepted: 10 October 2018 / Published: 14 October 2018
(This article belongs to the Special Issue Molecular Research on Dental Materials and Biomaterials 2018)

Abstract

:
Oral biofilms attach onto both teeth surfaces and dental material surfaces in oral cavities. In the meantime, oral biofilms are not only the pathogenesis of dental caries and periodontitis, but also secondary caries and peri-implantitis, which would lead to the failure of clinical treatments. The material surfaces exposed to oral conditions can influence pellicle coating, initial bacterial adhesion, and biofilm formation, due to their specific physical and chemical characteristics. To define the effect of physical and chemical characteristics of dental prosthesis and restorative material on oral biofilms, we discuss resin-based composites, glass ionomer cements, amalgams, dental alloys, ceramic, and dental implant material surface properties. In conclusion, each particular chemical composition (organic matrix, inorganic filler, fluoride, and various metallic ions) can enhance or inhibit biofilm formation. Irregular topography and rough surfaces provide favorable interface for bacterial colonization, protecting bacteria against shear forces during their initial reversible binding and biofilm formation. Moreover, the surface free energy, hydrophobicity, and surface-coating techniques, also have a significant influence on oral biofilms. However, controversies still exist in the current research for the different methods and models applied. In addition, more in situ studies are needed to clarify the role and mechanism of each surface parameter on oral biofilm development.

1. Introduction

From the widely applied dental amalgams [1] to esthetic resin-based composites [2,3] and ion-release glass ionomer cements [4], direct restorative materials are generally used to reconstruct the tooth when its structure is compromised by trauma or dental caries. Besides, indirect crown restorations and dental implants have been applied to tooth and dentition defect restorations for decades [5,6]. Although these restorative materials had significant evolvement in the past few decades, the failure rates of restorations are still problems to the dentists and investigators.
As it stands, direct restorations showed an annual failure rate up to 7.9% with the main reasons of secondary caries and bulk fracture [3,7,8]. It was reported that the 5-year failure rate of fixed dental prostheses was more than 10%, due to the common complications of caries and endodontic diseases [9,10,11]. Although the implant survival reached 92.8–97.1% over a follow-up period of 10 years, we cannot ignore peri-implantitis, which is mainly caused by biofilm accumulation [12,13]. The prevalence of peri-implantitis varies from 11% to 47%, because of the different threshold of bone loss [14]. However, Schwendicke’s study showed that an implant might cost more than 300 Euro when it comes to peri-implantitis, by comparison with a healthy implant [15]. Dental restorative materials placed in oral cavity are subjected to aggressive attack by bacteria. Components in materials will be biodegraded by the dental plaque, which will probably compromise the marginal integrity and induce the development and progression of secondary caries and peri-implantitis [12,16,17,18].
The oral cavity is a complex environment, where high humidity, moderate temperature, and abundance of nutrients promote the formation of differentiated microorganisms and microbial biofilms [19,20,21]. Biofilm formation in the oral cavity is a gradated process consisting of four stages (Figure 1) [22]:
1
acquired pellicle formation;
2
primary colonization;
3
coaggregation;
4
mature biofilm establishment.
To generate a biofilm, all surfaces exposed to the oral environment are steadily covered by a pellicle derived from the adsorption of organic and inorganic molecules in saliva. The receptors of salivary pellicle offer binding sites for floating initial bacteria cells to attach to these surfaces and form microcolonies. As time goes by, the bacteria cells aggregate, proliferate, and grow into a mushroom-shaped mature biofilm, firmly attaching to these surfaces [23,24]. Therefore, bacterial cells within the biofilm do not exist as independent entities but, rather, as a coordinated, metabolically integrated microbial community [22].
Since adhesion is the crucial step of biofilm formation, understanding bacteria–surface interaction is essential for biofilm control and survival rate of restorations. The physical and chemical characteristics of dental prosthesis and restorative materials can influence pellicle coating, initial bacterial adhesion, and biofilm formation. The growing application of dental materials has presented an ever-increasing need to better understand the interactions between biofilm and material surfaces in the oral cavity. Thus, in this review, we discuss the effects of physical and chemical characteristics of different dental prosthesis and restorative material surfaces on oral biofilms.

2. Physical Characteristics of Dental Materials

2.1. Surface Roughness

Nowadays, some clinical procedures, polishing and finishing, are usually applied for smoother surfaces. Among these polishing and finishing techniques, the lowest surface roughness (SR) values could be achieved by Mylar, and followed by Al2O3 discs, one-step rubber points, diamond bur, and multi-blade carbide bur [25].
Many researches have demonstrated that unpolished materials surfaces could accumulate more dental biofilm than polished ones, including resin-based composites, ceramics, implant abutments, and denture bases [22,26,27]. Kim [28] investigated the surface ultrastructure, roughness of four ceramic materials (Vita Enamic, Lava Ultimate, Vitablocs Mark II, and Wieland Reflex), and assessed their promotion of biofilm development following adjustments and simulated intraoral polishing methods. It was proved that surface roughness values (Ra) were greater in all materials following these methods, resulting in more biofilm accumulation, which implied the main cause of biofilm accumulation was surface roughness. A previous study evaluated the surface roughness of 20 commercial dental composite resins after abrasive wear, with the average roughness ranging from 0.49 to 0.79 μm [29]. According to Bollen’s study, the surface roughness above the threshold roughness (Ra = 0.2 μm) results in a simultaneous increase in biofilm accumulation, and no further reduction in bacterial adhesion could be observed under the threshold value [30]. In the same way, Yuan et al. demonstrated that the area of adherent bacteria was a highly linear correlation coefficient (r = 0.893, P < 0.01) when Ra < 0.80 μm, and weakly correlated with SR when Ra ≤ 0.20 μm (r = 0.643, P < 0.01) [31]. It indicated that factors other than SR influence biofilm formation when Ra ≤ 0.20 μm.
According to Ionescu et al., surface topography, the 3D characteristics of a surface with peaks and valleys distribution, could explain the crucial role of SR in biofilm formation [26]. The deeper and larger depressions may increase the contact area and provide more favorable interfaces for bacterial colonization and biofilm formation, protecting bacteria against shear forces (rinsing and brushing) during their initial reversible binding, leading to irreversible and stronger attachment [17,32]. Hence, it is difficult to eliminate microcolonies on the rough surfaces, resulting in the formation of mature biofilm [33].
The studies mentioned above were mostly done in vitro. All surfaces in the oral cavity are covered by the salivary pellicle, and the SR, one of the physical characteristics of material surfaces, is, in part, counterbalanced by the presence of the salivary pellicle [33]. Besides, as the biofilm maturing, the effect of SR on biofilm development is reduced, with the new bacteria adhering to the initial formed biofilm but not to the tested material surface [34,35,36]. Hence, the roughness of material surface mainly influences the initial bacterial colonization. Lorenzo [37] revealed that biofilms developed by single bacterial species or simple microbial associations are more readily influenced by surface roughness and topography than biofilm formed by complex communities. The different outcomes of the above research could be related to different methods and the development of the genetic technology.
Although improving implant osseointegration, the surface roughness has been proposed as the main feature inducing biofilm development [38]. Many studies showed that the increase of the SR could cause an exponential growth in bacterial cells [39] and facilitate biofilm formation [22]. However, compared to the resin-based composites (RBCs) and ceramic, SR is not always detrimental to the treatment because it is benefit for the attachment of osteoblast. Thus, the role of SR seems a little contradictory in this field.
With respect to the biofilm composition, Marcos [40] affirmed that there seems to be no reason to believe that implants with rough surfaces are more susceptive to fail, and his results are in accordance with the study [41] that showed a similar microbiota composition on titanium of different SR. The controversial views, above, may result from different kinds of biofilms, different incubation times and, most importantly, the different kind of titanium discs used. Some of these studies employed the commercially available ones provided by companies, and some of them employed titanium discs only for labs, which differed in more than just roughness. Marcos [40] also found no significant difference of succession kinetics of 23 microorganism species on titanium, with different Ra values, in 1, 3, 7, 14, and 21 days. Regardless, in manufacturing advanced implants, new surface treatment technology should be applied to establish a balance between osteoblast and oral bacterial attachment.

2.2. Other Physical Characteristics

The surface free energy (SFE) is related to the wettability of the material surface as an equivalent to the surface of a fluid. To determine the SFE, the contact angles (θ) are measured by three liquids differing in hydrophobicity on a specific surface [26]. A smaller contact angle implies higher SFE and higher surface hydrophilia of the material [33]. It has been reported that less biofilm formation occurred on RBC surfaces with low SFE, probably because of the similar hydrophilic properties between salivary pellicle and substratum surfaces [26,30]. The effects of SFE on biofilm formation may be inaccurate when Ra > 0.1 μm, and SR plays the primary role in biofilm accumulation, indeed. In other words, SFE influenced early adhesion of Streptococcus mutans (S. mutans) on super smooth surfaces (Ra ≤ 0.06 μm) [31].
The parameters of clinical dental materials influence on oral biofilms are intricate and co-occurring. Higher surface hydrophilia implies higher SFE, which induces more microorganism accumulation [33]. Also, the SR partially depends on inorganic filler size. Nanofilled RBCs wear by breaking out of individual primary particles. However, for microhybrid RBCs, the relatively soft matrix is worn before the fillers plucked out [29]. It is essential to control variables to study single parameters of clinical dental materials influencing oral biofilms.

3. Chemical Characteristics of Dental Materials

3.1. Resin-Based Composite

Resin-based dental materials have substantially evolved since they have been brought into the market, more than 60 years ago [2,42]. Resin-based composites, as a kind of versatile direct restorative materials, are widely used due to their excellent esthetic properties, improved mechanical characteristics, and ease of clinical handling [2,3]. Conventional RBCs are composed of four major components: a polymeric matrix, inorganic fillers, a silane coupling agent to produce a strong interface between the two phases mentioned, and initiators that induce or modulate the polymerization reaction [2]. Although the composite resin has been widely used in recent years, it has more biofilm accumulation, more frequent replacement, and shorter longevity, when compared with amalgam [43,44]. The failure of RBCs, mainly on account of secondary caries along the tooth–composite interfaces, is frequently related to biofilm formation on dental restorations [3,8].
Different kinds of components imply that the surface of a RBC is not a homogeneous interface, because of the distribution of physical-chemical phases with different chemical properties. The main base monomers of polymeric matrix used in commercial dental composites are Bis-GMA (bis-phenyl glycidyl dimethacrylate), Bis-EMA (bisphenol A ethoxylated dimethacrylate), PEGDMA (polyethylene glycol dimethacrylate), and UDMA (urethane dimethacrylate) with high viscosity, mixed with TEGDMA (triethylene glycol dimethacrylate) for dilution [2,31]. By tailoring RBC surfaces with either high carbon (matrix-rich) or high silicon (filler-rich) content from several commercially available RBCs without any antimicrobial agent, Ionescu et al. suggested that minimization of resin-matrix exposure might reduce biofilm formation on RBC surfaces because of the correlation between RBC surface carbon content and viable S. mutans biomass [26]. Recently, it was discovered that RBCs with a UDMA/aliphatic dimethacrylate matrix blend showed significantly higher biofilm formation on the surfaces than specimens with a Bis-GMA/TEGDMA matrix blend and analogous filler fraction, except for nanosized filler particles [45]. Another matrix, the silorane-based composite, was demonstrated to be less prone to S. mutans biofilm development compared with a generally used methacrylate-based composite, due to the increased hydrophobicity by silorane [46]. It was investigated that a reduced light-curing time can significantly increase the amount of unpolymerized monomers on the material surface, which might be responsible for increasing in vitro colonization on resin composite surfaces by S. mutans [47]. Kawai et al. reported that the specific resin components, a diglycidyl methacrylate and TEGDMA, significantly promoted glucosyltransferase (GTF) enzymes activity [48]. The GTF enzymes involved in the synthesis of water-insoluble glucan in situ entail an extracellular slime layer that promotes adhesion and the formation of dental plaque biofilms [49,50]. Consistently, the biodegradation byproduct (BBP) triethylene glycol (TEG), derived from methacrylate monomers, promotes the growth of S. mutans via upregulating the expression of glucosyltransferase B (gtfB) (involved in biofilm formation) and yfiV (a putative transcription regulator) in S. mutans [49]. Meanwhile, another BBP bishydroxypropoxyphenyl propane (BisHPPP) of Bis-GMA can also enhance the GTF enzyme activity of S. mutans biofilms, and modulate genes and proteins involved in biofilm formation, carbohydrate transport, and acid tolerance [51]. In conclusion, further studies are needed to explore the appropriate proportions of resin matrix and filler particles on the surface of RBCs, as well as to explore better ways to prevent resin biodegradation.
There are different sized inorganic fillers of the resin composites, including macrofill, microfill, nanofill, and hybrids. The RBC’s strength and polishing ability mostly depend on the size and proportion of inorganic fillers [2]. Pereira et al. demonstrated the least biofilm formation on a nanofilled RBC (Filtek Z350TM) compared with nanohybrid, microhybrid, and bulk-filled RBCs. The nanosized inorganic fillers could obtain the extensive distribution of the fillers and smoother composite surfaces after the same finishing and polishing procedures, consequently decreasing S. mutans adhesion [25,29,52]. Resin composites containing surface pre-reacted glass ionomer (S-PRG) filler have been reported to show less biofilm accumulation and reduced bacterial attachment. The pre-reacted glass-ionomer bioactive fillers have been fabricated by the acid–base reaction between a fluoroaluminosilicate glass and polyalkenoic acid in the presence of water. The antibacterial effects of S-PRG filler-containing resin composite is mainly attributed to release of BO33− and F, and fluoride-recharging abilities [53,54]. Yoshihara et al. investigated that bioactive glass filler may promote bacterial adhesion because of the unstable surface integrity, releasing ions and dissolving, which results in rougher restoration surfaces [55].
Up to now, there is still a high secondary caries rate, probably because of relatively few commercially antibacterial resins materials applied in clinic. However, more and more experimental antibacterial components and materials have been produced in the lab [44,56,57,58], among which, 12-methacryloyloxydodecylpyridinium bromide (MDPB), fluoride, and nanoparticles, have been translated into clinical materials. Both experimental antibacterial materials and new commercial antibacterial materials will soon pioneer a new materials field [54,59,60].
These experimental findings (Table 1) suggest that biofilm formation is influenced by the surface chemical composition of the material, including filler size, shape, and distribution, as well as matrix composition.

3.2. Glass Ionomer Cements

Glass ionomer cements (GICs), applied as direct restorative materials and cements, feature some desirable characters, such as a chemical adhesion to enamel and dentin, and the ability to release fluoride over time [4]. It is well known that conventional GICs have biological effects and caries-inhibiting properties because of the release of surface fluoride ions [61].
Recently, many studies have reported that the fluoride of GICs can affect the acid production, acid tolerance, and extracellular polymetric substance (EPS) formation of dental plaques, especially cariogenic biofilms, such as S. mutans biofilms. The fluoride can reduce the proportion of S. mutans but increase S. oralis (Streptococcus oralis) in the dual-species biofilm, subsequently inhibiting the formation of cariogenic bacteria-dominant biofilms [62]. This phenomenon lasts during both the initial rapid and second slow release phases, which is called the biphasic pattern of fluoride release of GICs [63,64,65,66]. The release of fluoride showed a significant dependence on the experimental conditions applied, such as sterile broth, bacteria, and acid. The bacterial condition leads to the highest decrease in the release of fluoride, which can be explained by the extracellular matrix of biofilm serving as a layer that modulates the release of fluoride from the substratum materials. Furthermore, the acidic conditions can enhance the constant release of fluoride, due to its high bioavailability at low pH [67]. The result agreed with Jennifer’s study, that more fluoride is released at pH 4, the acidic and cariogenic pH, than at pH 5.5 or pH 7, when these ions are most needed to inhibit caries [68]. It can be concluded that the efficiency of fluoride ions depends not only on their amount, but also on the pH value of the material during setting.
Acidic conditions promote the free fluoride ions to be released and form a weak electrolyte, hydrogen fluoride (HF, unionized fluoride) [66], and the combination of F-/HF and enzymes can modulate bacterium metabolism [69]. Adjacent to GIC restorations, an anti-caries environment is established by the fluoride, which may inhibit acidic pH efficiently due to the relatively high pKa value, 3.15, of hydrogen fluoride (HF) in vivo [70], by affecting bacterial metabolism (Figure 2), both directly (e.g., inhibition of enolase and ATPase) and indirectly (e.g., intracellular acidification) [71]. In addition, the aluminum released from Vitremer plays a vital role in inhibiting bacterial metabolism and has a synergistic effect with fluoride [71,72].
Although the acid conditions of biofilms can promote fluoride release to inhibit biofilm formation, the microbial environment changes the morphology of GICs, and accelerates material aging (Figure 3). Meanwhile, the changed morphology and increased roughness can enhance the initial bacterial attachment and oral biofilm formation [17]. To demonstrate the actual effects on biofilm formation of dental material in a pragmatic way, the study models evolved consistently, from the previous water aging model to a biological aging model, from a primary caries animal model to a secondary caries animal model, and from in vitro to the in situ model used nowadays [73,74,75].

3.3. Amalgams

Over its long clinical history, dental amalgams have evolved and served the profession successfully and at low cost. Amalgam restorations are being phased out because of the environmental pollution and inferior esthetic appearance [1]. However, they cannot be replaced by other restoratives because of their perfect mechanical properties, longevity, and low cost [15]. The longevity of amalgam is inseparable from the lower incidence of secondary caries caused by oral biofilms.
After clinical placement, amalgam restorations undergo a series of corrosion to release a variety of metallic ions in oral cavities. It was discovered that the mercury of amalgams could deposit in the dental plaque for up to 2 μg in 24 h, whereas the aged amalgams released little mercury because of the presence of the formed passive tarnish layer on the surface of amalgams [76]. In the 1980s, the amalgam was proved to have bacteriostatic and bactericidal properties due to the metallic ions being released from the surface of the materials, such as Ag, Cu, Sn, and Hg [77]. The low biomass of oral biofilms on amalgam surfaces is probably a result of the release of toxic ions from amalgam, which mainly consists of Hg and Ag [69]. Specifically, amalgam showed lasting inhibition of both S. mutans and Actinomyces viscosus (A. viscosus) which played crucial roles in biofilm formation [78]. Morrier et al. investigated that the order of antimicrobial potential of elements in amalgams would be Hg > Cu > Zn, by testing a suspension of S. mutans and A. viscosus [79]. Among those metallic ions, Cu2+ and Zn2+ showed synergistic effects on the reduction in acid production in dental biofilm [80]. Amalgam also showed a robust acid-buffering ability, which can neutralize bacteria-produced acids of oral biofilm by increasing the start pH of all solutions to around 7 to 8. This should be attributed to the release of corrosion products on the amalgams surface. The tin and copper oxides are amphoteric compounds that react as a base in acidic conditions [81]. This can be related to the fact that biofilms accumulated more on composites than amalgams in the clinic. Even in the in situ study, the amalgam showed, visually, a prevalence of non-viable cells forming small clusters distributed by the biofilm compared to other materials [69]. However, no research has yet explored the mechanisms of bacteriostatic and bactericidal properties of amalgam clearly.

3.4. Dental Alloys of Indirect Restoration

After 1975, the alloys for full-cast restorations, porcelain-fused-to-metal restorations, and removable partial denture frameworks, can be divided into three kinds, high-noble alloys (Au–Pt, Au–Pd, Au–Cu–Ag–Pd), noble alloys (Au–Cu–Ag–Pd, Pd–Cu, Pd–Ag), and base-metal alloys (Ni–Cr, Co–Cr, Ti) [5]. Oral microbial metabolites, such as acids, sulfide, and ammonia, can induce the microbial corrosion of metallic materials [82]. Dental alloys corrode and release metal irons in the oral environment which may compromise material biocompatibility and mechanical properties, and lead to the esthetic loss of dental restorations, and influence health [83].
Among the noble alloys, a high gold content alloy (88% by weight), Captek™, showed a 71% reduction in total bacterial numbers when compared to natural tooth surfaces [84]. This could be attributed to the low porosity of high nobility gold inherent in the manufacturing process and the unique electrochemical corrosion resistance [85]. Besides, metallic copper and copper-containing alloys possess a strong and rapid bactericidal effect, named “contact killing”. This was induced by successive membrane damage, oxidative damage, cell death, and DNA degradation [20,86]. The surface-released free copper ions are toxic to bacteria because of their soft ionic character and their thiophilicity [86,87]. As for the base-metal alloys, a higher amount of viable microbial cells and biofilm density on prosthetic structures based on cobalt–chromium (Co–Cr) alloys was demonstrated, when compared to those based on titanium [21,88]. Mystkowska found that there were more corrosion pits on cobalt alloys than on titanium alloys [88], and that these corrosion pits increase the surfaces roughness of dental alloys, which may facilitate the subsequent accumulation of biofilm [82]. However, there was a significant increase in biofilm density and number of microbial cells of biofilm growing on both titanium and Co–Cr alloy, from 24 up to 48 h [21]. The acid produced by microorganisms induces the corrosion of Cr2O3 and TiO2, the passive films, which are responsible for corrosion resistance and biocompatibility of the alloys [82,89,90,91] (Table 2).
Zhang et al. discovered that corroded alloy surfaces could upregulate gene expression of the glucosyltransferase BCD, glucan-binding proteins B, fructosyltransferase, and lactate dehydrogenase in S. mutans, which play critical roles in bacteria adherence and biofilm accumulation [82]. Microorganisms of biofilm decrease the pH by producing acidic substances and dissolve the surface oxides of the dental alloys to reduce the corrosion resistance of the metal [92]. In turn, the changed surfaces of the dental alloys can accelerate the virulence gene expression and biofilm formation [82]. Therefore, this bacteria-adhesion and corrosion cycle can accelerate the corrosion process and, finally, induce failure of the dental alloys’ restoration.

3.5. Ceramic

In recent years, adhesively cemented ceramic restorations, such as inlays/onlays, veneers, and crowns, have been used as the main approach for minimally invasive esthetic restorations in anterior and posterior teeth [93]. However, its clinical failure is related to a lot of factors, such as marginal misfit, surface irregularities, and cement excess, which may favor the accumulation of microorganisms, compromising clinical restoration longevity [94].
Both surface roughness and surface free energy have been found to influence initial microbial adherence decisively [40], due to compositional and microstructural differences, and bacterial colonization was thought to differ from one ceramic material to another. Sebastian [95] employed different kind of ceramics, glass/lithium disilicate glass/glass-infiltrated zirconia/partially sintered zirconia/hipped zirconia ceramic as the specimens, and the glass plates were used as a control. He found that the lithium disilicate glass ceramic had the highest values for Ra, whereas the lowest values were found for the glass ceramic, the partially sintered zirconia, and the hipped zirconia ceramic. Furthermore, salivary protein coating caused a significant increase in surface free energy and the polarity of these ceramics, except for the control material. However, after salivary protein coating, only the control material showed higher values for streptococcal adhesion than all ceramic materials. The same study [96], which was performed in vivo, demonstrated significant differences in biofilm formation with various types of dental ceramics. In particular, zirconia exhibited low biofilm accumulation. Thus, except for its high intensity, low biofilm accumulation makes zirconia a promising material for various indications. The different results of the two studies [95,96] may be related to the different models (in vitro, in vivo) they applied (Table 3).

3.6. Dental Implant

Over the last decades, the use of dental implants has become a common way of restoring dentition defect [6]. The implant survival rate reaches to 92.8–97.1% over a follow-up period of 10 years, but dental implants easily become infectious, due to oral pathogenic bacteria [12,13,97]. Two main etiologies of peri-implantitis are oral biofilms and occlusal overload [98], among which, oral biofilms developed on dental implants play a significant role in peri-implantitis’ pathogenesis. The peri-implantitis can cause implant loss in the absence of prevention and therapy [99,100]. The implant may be attached by saliva, blood, and oral bacterial cells during and after the implant surgery, and bacterial cells attached to the abutment harm the surrounding gingiva. All the above-mentioned points would affect the healing and restoration following surgery [101].
We begin with the abutment, since pathogenic bacteria usually attach on it first, causing peri-implant mucositis [102]. Hence, peri-implant tissue inflammation, as a consequence of biofilms on abutments in the subgingival region, is currently considered as a major contributor to implant loss [103]. Avila [103] found that, in the case of saliva-derived biofilm, the number of cells and the density of the biofilm on ZrO2 were lower than on titanium materials. Zirconia abutments have a lower possibility for bacterial attachment, which is similar to the study above [104,105], and some researchers thought that the surface free energy is more critical on zirconia abutment surfaces [106]. Cássio’s [107] 16S rDNA sequencing results agreed with previous studies [108,109] that the titanium accumulated more biofilm and more species of microorganisms. Two studies [110,111] found that the early bacterial communities were low in genome counts at the very beginning of implant surgery for both the zirconia and titanium abutment materials. As time goes by, both materials showed similar microbial counts and diversity, the same as on teeth. The different results may be related to no criterion for these products and testing methods. Zirconia is used widely for its esthetic property nowadays, and maybe the zirconia abutment will replace the titanium abutment for the lower bacteria attachment. However, substantial evidence is needed to prove its excellent properties in microbiological field.
When the peri-implant mucositis progress to peri-implantitis, more attention should be paid to the implant surface (Figure 4). About implant surface treatment techniques, there are mainly four kinds of coating techniques: alumina coating, titanium plasma spraying (TPS), biomimetic calcium phosphate (CaP) coating and plasma sprayed hydroxyapatite (HA) coating [112]. The coating techniques contribute to critical positive effects of dental implant application. Most authors [113,114] agreed that a suitable coating technique may enhance the mechanical properties of the dental implants. However, these techniques have several limitations including poor long-term adherence of the coating to the substrate material [115], nonuniformity in thickness of the deposited layer, variations in crystallinity [116], and composition of the coating, which influence the biofilm formation on the surface [112] (Table 4). However, none of studies shows the single factor of different coating techniques so far, because different coating techniques are related to different surface characteristics, which we have discussed in other sections of this review, further studies about the coating techniques should be performed.
It has been found out that, except for surface roughness and surface free energy [119], the type of the biomaterial itself can also influence biofilm formation and subsequent plaque accumulation on implant surfaces [21]. Two investigations have shown less inflammatory cells in the peri-implant soft tissue of zirconia in comparison with titanium or other metals [104,105]. Additionally, Zhao’s [106] study showed that neither roughness nor hydrophobicity had a decisive influence on the biofilm formation that occurred on three different implant materials, comprising titanium (Ti, cold-worked, grade 4), titanium–zirconium alloy (TiZr, 15% (wt) Zr) and zirconium oxide (ZrO2, Y-TZP). Same as Zhao’s result, in the 3-species biofilm (Streptococcus sanguinis, Fusobacterium nucleatum, and Porphyromonas gingivalis), the analysis showed that there were no significant differences between titanium and zirconia in terms of total biofilm mass and metabolism. However, zirconia revealed significantly reduced plaque thickness. Regarding human plaque biofilms, microbiological techniques showed statistically significant reduction in biofilm formation for zirconia compared to titanium. The result suggested that not only surface roughness or surface hydrophilicity might be important factors for biofilm formation, but also material composition—metals compared to ceramics—suggesting a reduced disposition for peri-implant plaque and subsequent potential peri-implant infections on zirconia compared to titanium implant surfaces [32,120]. Nowadays, topography, surface charge, roughness, hydrophobicity, and chemistry have been investigated for many years. Besides, some new techniques have been studied, like nanoscale surface roughness, negatively charged surfaces, super hydrophilic surfaces and super hydrophobic surfaces, and they have all been demonstrated to reduce bacterial adhesion [32].

4. Conclusions

As discussed in this review, bacterial adhesion and biofilm formation can be strongly influenced by surface characteristics of dental materials, which include chemical compositions, surface roughness, surface free energy, surface topography, ions release, and others. In conclusion, every possible particular chemical composition (organic matrix, inorganic filler, fluoride, and various metallic ions) can enhance or inhibit biofilm formation. Irregular topography and rough surfaces provide favorable interfaces for bacterial colonization, protecting bacteria against shear forces during their initial reversible binding and biofilm formation. Besides, the surface free energy, hydrophobicity, surfaces coating techniques also have a significant influence on oral biofilm.
However, the “ideal” surface characteristics have not been identified yet, and results have varied from different methods and models. One of the major drawbacks of current research is the limitation of the in vitro study. In vitro studies are not always able to completely simulate the complicated conditions presented in the oral environment. Thus, further in situ studies are much needed to clarify the role and mechanism of each surface parameter on oral biofilm formation. Finally, the goal is to produce robust, long-lasting dental materials which will reduce costly replacements and significantly ameliorate oral health.

Author Contributions

Y.H. and X.H. drafted the manuscript. X.Z., M.L., B.R., X.P., L.C. edited and added valuable insights into the manuscript. All authors read and approved the final manuscript.

Acknowledgments

This research was supported by The National Key Research Program of China 2017YFC0840100 and 2017YFC0840107 (L.C.), National Natural Science Foundation of China (81870759), the Youth Grant of the Science and Technology Department of Sichuan Province, China 2017JQ0028 (L.C.), Innovative Research Team Program of Sichuan Province (L.C.)

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Shenoy, A. Is it the end of the road for dental amalgam? A critical review. J. Conserv. Dent. 2008, 11, 99–107. [Google Scholar] [CrossRef] [PubMed]
  2. Ferracane, J.L. Resin composite—State of the art. Dent. Mater. 2011, 27, 29–38. [Google Scholar] [CrossRef] [PubMed]
  3. Demarco, F.F.; Correa, M.B.; Cenci, M.S. Longevity of posterior composite restorations: Not only a matter of materials. Dent. Mater. 2012, 28, 87–101. [Google Scholar] [CrossRef] [PubMed]
  4. Joel, H. Berg, Glass ionomer cements. Pediatr. Dent. 2002, 24, 430–438. [Google Scholar]
  5. Wataha, J.C. Alloys for prosthodontic restorations. J. Prosthet. Dent. 2002, 87, 351–363. [Google Scholar] [CrossRef] [PubMed]
  6. Renvert, S.; Quirynen, M. Risk indicators for peri-implantitis. A narrative review. Clin. Oral Implants Res. 2015, 26, 15–44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Laske, M.; Opdam, N.J.; Bronkhorst, E.M. Longevity of direct restorations in Dutch dental practices. Descriptive study out of a practice based research network. J. Dent. 2016, 46, 12–17. [Google Scholar] [CrossRef] [PubMed]
  8. Delaviz, Y.; Finer, Y.; Santerre, J.P. Biodegradation of resin composites and adhesives by oral bacteria and saliva: A rationale for new material designs that consider the clinical environment and treatment challenges. Dent. Mater. 2014, 30, 16–32. [Google Scholar] [CrossRef] [PubMed]
  9. Goodacre, C.J. Bernal, Guillermo, Rungcharassaeng, Kitichai,, Clinical complications in fixed prosthodontics. J. Prosthet. Dent. 2003, 90, 31–41. [Google Scholar] [CrossRef]
  10. Toman, M.; Toksavul, S. Clinical evaluation of 121 lithium disilicate all-ceramic crowns up to 9 years. Quintessence Int. 2015, 46, 189–197. [Google Scholar] [CrossRef] [PubMed]
  11. Layton, D. A critical appraisal of the survival and complication rates of tooth-supported all-ceramic and metal-ceramic fixed dental prostheses the application of evidence-based dentistry. Int. J. Prosthodont. 2011, 24, 417–427. [Google Scholar] [PubMed]
  12. Albrektsson, T.; Donos, N. Implant survival and complications. In Proceedings of the Third EAO Consensus Conference, Pfäffikon, Schwyz, Switzerland, 15–18 February 2012; pp. 63–65. [Google Scholar]
  13. Srinivasan, M.; Vazquez, L.; Rieder, P.; Moraguez, O. Survival rates of short (6 mm) micro-rough surface implants: A review of literature and meta-analysis. Clin. Oral Implants Res. 2014, 25, 539–545. [Google Scholar] [CrossRef] [PubMed]
  14. Robertson, K.; Shahbazian, T.; MacLeod, S. Treatment of peri-implantitis and the failing implant. Dent. Clin. N. Am. 2015, 59, 329–343. [Google Scholar] [CrossRef] [PubMed]
  15. Schwendicke, F.; Tu, Y.K.; Stolpe, M. Preventing and Treating Peri-Implantitis: A Cost-Effectiveness Analysis. J. Periodontol. 2015, 86, 1020–1029. [Google Scholar] [CrossRef] [PubMed]
  16. Li, Y.; Carrera, C.; Chen, R.; Li, J. Degradation in the dentin-composite interface subjected to multi-species biofilm challenges. Acta Biomater. 2014, 10, 375–383. [Google Scholar] [CrossRef] [PubMed]
  17. Park, J.W.; Song, C.W.; Jung, J.H. The effects of surface roughness of composite resin on biofilm formation of Streptococcus mutans in the presence of saliva. Oper. Dent. 2012, 37, 532–539. [Google Scholar] [CrossRef] [PubMed]
  18. Cheng, L.; Zhang, K.; Zhang, N.; Melo, M.A.S.; Weir, M.D.; Zhou, X.D.; Bai, Y.X.; Reynolds, M.A.; Xu, H.H.K. Developing a New Generation of Antimicrobial and Bioactive Dental Resins. J. Dent. Res. 2017, 96, 855–863. [Google Scholar] [CrossRef] [PubMed]
  19. Dewhirst, F.E.; Chen, T.; Izard, J. The human oral microbiome. J. Bacteriol. 2010, 192, 5002–5017. [Google Scholar] [CrossRef] [PubMed]
  20. Grass, G.; Rensing, C.; Solioz, M. Metallic copper as an antimicrobial surface. Appl. Environ. Microbiol. 2011, 77, 1541–1547. [Google Scholar] [CrossRef] [PubMed]
  21. Souza, J.; Mota, R.R.; Sordi, M.B.; Passoni, B.B. Biofilm Formation on Different Materials Used in Oral Rehabilitation. Braz. Dent. J. 2016, 27, 141–147. [Google Scholar] [CrossRef] [PubMed]
  22. Teughels, W.; Van Assche, N.; Sliepen, I.; Quirynen, M. Effect of material characteristics and/or surface topography on biofilm development. Clin. Oral Implants Res. 2006, 17, 68–81. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Wang, Z.; Shen, Y.; Haapasalo, M. Dental materials with antibiofilm properties. Dent. Mater. 2014, 30, e1–e16. [Google Scholar] [CrossRef] [PubMed]
  24. Teranaka, A.; Tomiyama, K.; Ohashi, K. Relevance of surface characteristics in the adhesiveness of polymicrobial biofilms to crown restoration materials. J. Oral Sci. 2017, 60, 129–136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Cazzaniga, G.; Ottobelli, M.; Ionescu, A.C. In vitro biofilm formation on resin-based composites after different finishing and polishing procedures. J. Dent. 2017, 67, 43–52. [Google Scholar] [CrossRef] [PubMed]
  26. Ionescu, A.; Wutscher, E.; Brambilla, E. Influence of surface properties of resin-based composites on in vitro Streptococcus mutans biofilm development. Eur. J. Oral Sci. 2012, 120, 458–465. [Google Scholar] [CrossRef] [PubMed]
  27. Haralur, S.B. Evaluation of efficiency of manual polishing over autoglazed and overglazed porcelain and its effect on plaque accumulation. J. Adv. Prosthodont. 2012, 4, 179–186. [Google Scholar] [CrossRef] [PubMed]
  28. Kim, K.H.; Loch, C.; Waddell, J.N.; Tompkins, G. Surface Characteristics and Biofilm Development on Selected Dental Ceramic Materials. Int. J. Dent. 2017, 2017, 7627945. [Google Scholar] [CrossRef] [PubMed]
  29. Han, J.M.; Zhang, H.; Choe, H.S.; Lin, H.; Zheng, G.; Hong, G. Abrasive wear and surface roughness of contemporary dental composite resin. Dent. Mater. J. 2014, 33, 725–732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Curd, M.L.; Bollen, P.L. Marc Quirynen Comparison of surface roughness of oral hard materials to the threshold surface roughness for bacterial plaque retention: A review of the literature. Dent. Mater. 1997, 13, 258. [Google Scholar] [CrossRef]
  31. Yuan, C.; Wang, X.; Gao, X. Effects of surface properties of polymer-based restorative materials on early adhesion of Streptococcus mutans in vitro. J. Dent. 2016, 54, 33–40. [Google Scholar] [CrossRef] [PubMed]
  32. Song, F.; Koo, H.; Ren, D. Effects of Material Properties on Bacterial Adhesion and Biofilm Formation. J. Dent. Res. 2015, 94, 1027–1034. [Google Scholar] [CrossRef] [PubMed]
  33. Cazzaniga, G.; Ottobelli, M.; Ionescu, A. Surface properties of resin-based composite materials and biofilm formation A review of the current literature. Am. J. Dent. 2015, 28, 311–320. [Google Scholar] [PubMed]
  34. Frojd, V.; Chavez de Paz, L. In situ analysis of multispecies biofilm formation on customized titanium surfaces. Mol. Oral Microbiol. 2011, 26, 241–252. [Google Scholar] [CrossRef] [PubMed]
  35. Al-Ahmad, A.; Wiedmann-Al-Ahmad, M.; Faust, J.; Bachle, M.; Follo, M.; Wolkewitz, M.; Hannig, C.; Hellwig, E.; Carvalho, C.; Kohal, R. Biofilm formation and composition on different implant materials in vivo. J. Biomed. Mater. Res. B Appl. Biomater. 2010, 95, 101–109. [Google Scholar] [CrossRef] [PubMed]
  36. Dezelic, T.G.B.; Schmidlin, P.R. Multi-species Biofilm Formation on Dental Materials and an Adhesive Patch. Oral Health Prev. Dent. 2009, 7, 47–53. [Google Scholar] [CrossRef] [PubMed]
  37. Bevilacqua, L.; Milan, A.; Del Lupo, V.; Maglione, M.; Dolzani, L. Biofilms Developed on Dental Implant Titanium Surfaces with Different Roughness: Comparison Between In Vitro and In Vivo Studies. Curr. Microbiol. 2018, 75, 766–772. [Google Scholar] [CrossRef] [PubMed]
  38. Wennerberg, A.; Albrektsson, T. Effects of titanium surface topography on bone integration: A systematic review. Clin. Oral Implants Res. 2009, 20 (Suppl. S4), 172–184. [Google Scholar] [CrossRef] [PubMed]
  39. Da Silva, C.H.F.P.; Vidigal, G.M., Jr.; de Uzeda, M.; de Almeida Soares, G. Influence of Titanium Surface Roughness on Attachment of Streptococcus Sanguis: An in vitro study. Implant Dent. 2005, 14, 88–93. [Google Scholar] [CrossRef]
  40. De Freitas, M.M.; da Silva, C.H.; Groisman, M.; Vidigal, G.M., Jr. Comparative analysis of microorganism species succession on three implant surfaces with different roughness: An in vivo study. Implant Dent. 2011, 20, e14–e23. [Google Scholar] [CrossRef] [PubMed]
  41. Größner-Schreiber, B.; Teichmann, J.; Hannig, M.; Dörfer, C.; Wenderoth, D.F.; Ott, S.J. Modified implant surfaces show different biofilm compositions under in vivo conditions. Clin. Oral Implants Res. 2009, 20, 817–826. [Google Scholar] [CrossRef] [PubMed]
  42. Pfeifer, C.S. Polymer-Based Direct Filling Materials. Dent. Clin. N. Am. 2017, 61, 733–750. [Google Scholar] [CrossRef] [PubMed]
  43. Spencer, P.; Ye, Q.; Misra, A. Proteins, pathogens, and failure at the composite-tooth interface. J. Dent. Res. 2014, 93, 1243–1249. [Google Scholar] [CrossRef] [PubMed]
  44. Zhang, N.; Melo, M.A.S.; Weir, M.D. Do Dental Resin Composites Accumulate More Oral Biofilms and Plaque than Amalgam and Glass Ionomer Materials? Materials 2016, 9, 888. [Google Scholar] [CrossRef] [PubMed]
  45. Ionescu, A.; Brambilla, E.; Wastl, D.S. Influence of matrix and filler fraction on biofilm formation on the surface of experimental resin-based composites. J. Mater. Sci. Mater. Med. 2015, 26, 1–7. [Google Scholar] [CrossRef] [PubMed]
  46. Brambilla, E.; Ionescu, A.; Cazzaniga, G.; Ottobelli, M. Influence of Light-curing Parameters on Biofilm Development and Flexural Strength of a Silorane-based Composite. Oper. Dent. 2016, 41, 219–227. [Google Scholar] [CrossRef] [PubMed]
  47. Brambilla, E.; Gagliani, M.; Ionescu, A. The influence of light-curing time on the bacterial colonization of resin composite surfaces. Dent. Mater. 2009, 25, 1067–1072. [Google Scholar] [CrossRef] [PubMed]
  48. Kawai, K.; Tsuchitani, Y. Effects of resin composite components on glucosyltransferase of cariogenic bacterium. J. Biomed. Mater. Res. 2000, 51, 123–127. [Google Scholar] [CrossRef]
  49. Khalichi, P.; Singh, J.; Cvitkovitch, D.G. The influence of triethylene glycol derived from dental composite resins on the regulation of Streptococcus mutans gene expression. Biomaterials 2009, 30, 452–459. [Google Scholar] [CrossRef] [PubMed]
  50. Bowen, W.H.; Koo, H. Biology of Streptococcus mutans-derived glucosyltransferases: Role in extracellular matrix formation of cariogenic biofilms. Caries Res. 2011, 45, 69–86. [Google Scholar] [CrossRef] [PubMed]
  51. Sadeghinejad, L.; Cvitkovitch, D.G.; Siqueira, W.L. Mechanistic, genomic and proteomic study on the effects of BisGMA-derived biodegradation product on cariogenic bacteria. Dent. Mater. 2017, 33, 175–190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Pereira, C.A.; Eskelson, E.; Cavalli, V. Streptococcus mutansBiofilm Adhesion on Composite Resin Surfaces After Different Finishing and Polishing Techniques. Oper. Dent. 2011, 36, 311–317. [Google Scholar] [CrossRef] [PubMed]
  53. Hahnel, S.; Wastl, D.S. Streptococcus mutans biofilm formation and release of fluoride from experimental resin-based composites depending on surface treatment and S-PRG filler particle fraction. J. Adhes. Dent. 2014, 16, 313–321. [Google Scholar] [CrossRef] [PubMed]
  54. Miki, S.; Kitagawa, H.; Kitagawa, R. Antibacterial activity of resin composites containing surface pre-reacted glass-ionomer (S-PRG) filler. Dent. Mater. 2016, 32, 1095–1102. [Google Scholar] [CrossRef] [PubMed]
  55. Yoshihara, K.; Nagaoka, N.; Maruo, Y. Bacterial adhesion not inhibited by ion-releasing bioactive glass filler. Dent. Mater. 2017, 33, 723–734. [Google Scholar] [CrossRef] [PubMed]
  56. Liang, J.; Li, M.; Ren, B.; Wu, T. The anti-caries effects of dental adhesive resin influenced by the position of functional groups in quaternary ammonium monomers. Dent. Mater. 2018, 34, 400–411. [Google Scholar] [CrossRef] [PubMed]
  57. Khurshid, Z.; Naseem, M.; Sheikh, Z.; Najeeb, S. Oral antimicrobial peptides: Types and role in the oral cavity. Saudi Pharm. J. 2016, 24, 515–524. [Google Scholar] [CrossRef] [PubMed]
  58. Ge, Y.; Wang, S.; Zhou, X.; Wang, H.; Xu, H.H.; Cheng, L. The Use of Quaternary Ammonium to Combat Dental Caries. Materials 2015, 8, 3532–3549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  59. Carlo, H.L.; Bonan, P.R.F.; Franklin, G.G. In vitro effect of S. mutans biofilm on fluoride/MDPB-containing adhesive system bonded to caries-affected primary dentin. Am. J. Dent. 2014, 37, 227–232. [Google Scholar]
  60. Khurshid, Z.; Zafar, M.; Qasim, S.; Shahab, S. Advances in Nanotechnology for Restorative Dentistry. Materials 2015, 8, 717–731. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Kramer, N.; Schmidt, M.; Lücker, S. Glass ionomer cement inhibits secondary caries in an in vitro biofilm model. Clin. Oral Investig. 2018, 22, 1019–1031. [Google Scholar] [CrossRef] [PubMed]
  62. Jung, J.E.; Cai, J.N.; Cho, S.D. Influence of fluoride on the bacterial composition of a dual-species biofilm composed of Streptococcus mutans and Streptococcus oralis. Biofouling 2016, 32, 1079–1087. [Google Scholar] [CrossRef] [PubMed]
  63. Neilands, J.; Troedsson, U.; Sjodin, T.; Davies, J.R. The effect of delmopinol and fluoride on acid adaptation and acid production in dental plaque biofilms. Arch. Oral Biol. 2014, 59, 318–323. [Google Scholar] [CrossRef] [PubMed]
  64. Pandit, S.; Kim, H.J.; Song, K.Y.; Jeon, J.G. Relationship between fluoride concentration and activity against virulence factors and viability of a cariogenic biofilm: In vitro study. Caries Res. 2013, 47, 539–547. [Google Scholar] [CrossRef] [PubMed]
  65. Chau, N.P.; Pandit, S.; Jung, J.-E. Long-term anti-cariogenic biofilm activity of glass ionomers related to fluoride release. J. Dent. 2016, 47, 34–40. [Google Scholar] [CrossRef] [PubMed]
  66. Mayanagi, G.; Igarashi, K.; Washio, J.; Domon-Tawaraya, H.; Takahashi, N. Effect of fluoride-releasing restorative materials on bacteria-induced pH fall at the bacteria–material interface: An in vitro model study. J. Dent. 2014, 42, 15–20. [Google Scholar] [CrossRef] [PubMed]
  67. Hahnel, S.; Ionescu, A.C.; Cazzaniga, G.; Ottobelli, M.; Brambilla, E. Biofilm formation and release of fluoride from dental restorative materials in relation to their surface properties. J. Dent. 2017, 60, 14–24. [Google Scholar] [CrossRef] [PubMed]
  68. Moreau, J.L.; Xu, H.H. Fluoride releasing restorative materials: Effects of pH on mechanical properties and ion release. Dent. Mater. 2010, 26, e227–e235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Padovani, G.C.; Fucio, S.B.; Ambrosano, G.M.; Correr-Sobrinho, L.; Puppin-Rontani, R.M. In situ bacterial accumulation on dental restorative materials. CLSMCOMSTAT analysis. Am. J. Dent. 2016, 28, 3–8. [Google Scholar]
  70. Nakajo, K.; Takahashi, Y.; Kiba, W.; Imazato, S.; Takahashi, N. Fluoride ion released from glass-ionomer cement is responsible to inhibit the acid production of caries-related oral streptococci. Interface Oral Health Sci. 2007, 25, 263–264. [Google Scholar] [CrossRef]
  71. Hayacibara, M.F.; Rosa, O.P.; Koo, H. Effects of fluoride and aluminum from ionomeric materials on S. mutans biofilm. J. Dent. Res. 2003, 82, 267–271. [Google Scholar] [CrossRef] [PubMed]
  72. Fucio, S.B.; Paula, A.B.; Sardi, J.C.O. Streptococcus Mutans Biofilm Influences on the Antimicrobial Properties of Glass Ionomer Cements. Braz. Dent. J. 2016, 27, 681–687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Zhou, X.; Wang, S.; Peng, X.; Hu, Y.; Ren, B. Effects of water and microbial-based aging on the performance of three dental restorative materials. J. Mech. Behav. Biomed. Mater. 2018, 80, 42–50. [Google Scholar] [CrossRef] [PubMed]
  74. Wu, T.; Li, B.; Zhou, X.; Hu, Y.; Zhang, H. Evaluation of Novel Anticaries Adhesive in a Secondary Caries Animal Model. Caries Res. 2018, 52, 14–21. [Google Scholar] [CrossRef] [PubMed]
  75. Xue, Y.; Lu, Q.; Tian, Y.; Zhou, X. Effect of toothpaste containing arginine on dental plaque-A randomized controlled in situ study. J. Dent. 2017, 67, 88–93. [Google Scholar] [CrossRef] [PubMed]
  76. Lyttle, H.A.; Bowden, G.H. The level of mercury in human dental plaque and interaction in vitro between biofilms of Streptococcus mutans and dental amalgam. J. Dent. Res. 1993, 72, 1320–1324. [Google Scholar] [CrossRef] [PubMed]
  77. Morrier, J.J.; Barsotti, O.; Blanc-Benon, J.; Rocca, J.P.; Dumont, J. Antibacterial properties of five dental amalgams an in vitro study. Dent. Mater. 1989, 5, 310–313. [Google Scholar] [CrossRef]
  78. Beyth, N.; Domb, A.J.; Weiss, E.I. An in vitro quantitative antibacterial analysis of amalgam and composite resins. J. Dent. 2007, 35, 201–206. [Google Scholar] [CrossRef] [PubMed]
  79. Morrier, J.J.; Suchett-Kaye, G.; Nguyen, D.; Rocca, J.P.; Blanc-Benon, J.; Barsotti, O. Antimicrobial activity of amalgams, alloys and their elements and phases. Dent. Mater. 1998, 5, 310–313. [Google Scholar] [CrossRef]
  80. Afseth, J.; Oppermann, R.V.; Rolla, G. Thein vivoeffect of glucose solutions containing Cu++ and Zn++ on the acidogenicity of dental plaque. Acta Odontol. Scand. 2009, 38, 229–233. [Google Scholar] [CrossRef]
  81. Nedeljkovic, I.; De Munck, J.; Slomka, V. Lack of Buffering by Composites Promotes Shift to More Cariogenic Bacteria. J. Dent. Res. 2016, 95, 875–881. [Google Scholar] [CrossRef] [PubMed]
  82. Zhang, S.; Qiu, J.; Ren, Y. Reciprocal interaction between dental alloy biocorrosion and Streptococcus mutans virulent gene expression. J. Mater. Sci. Mater. Med. 2016, 27, 78. [Google Scholar] [CrossRef] [PubMed]
  83. Lu, C.; Zheng, Y.; Zhong, Q. Corrosion of dental alloys in artificial saliva with Streptococcus mutans. PLoS ONE 2017, 12, e0174440. [Google Scholar] [CrossRef] [PubMed]
  84. Goodson, J.M.; Shoher, I.; Imber, S.; Som, S.; Nathanson, D. Reduced dental plaque accumulation on composite gold alloy margins. J. Periodontal Res. 2001, 36, 252–259. [Google Scholar] [CrossRef] [PubMed]
  85. Zappala, C.; Shoher, I.; Battaini, P. Microstructural Aspects of the Captek™ Alloy for PorcelainFused-to-Metal Restorations. J. Esthet. Dent. 1996, 8, 151. [Google Scholar] [CrossRef] [PubMed]
  86. HansSalima, M. Physicochemical properties of copper important for its antibacterial activity and development of a unified model. Biointerphases 2016, 11, 018902. [Google Scholar] [CrossRef]
  87. Molteni, C.; Abicht, H.K.; Solioz, M. Killing of bacteria by copper surfaces involves dissolved copper. Appl. Environ. Microbiol. 2010, 76, 4099–4101. [Google Scholar] [CrossRef] [PubMed]
  88. Mystkowska, J. Biocorrosion of dental alloys due to Desulfotomaculum nigrificans bacteria. Acta Bioeng. Biomech. 2016, 18, 87–96. [Google Scholar] [CrossRef] [PubMed]
  89. Ward, B.C.; Webster, T.J. The effect of nanotopography on calcium and phosphorus deposition on metallic materials in vitro. Clin. Oral Implants Res. 2006, 27, 3064–3074. [Google Scholar] [CrossRef] [PubMed]
  90. Souza, J.C.; Ponthiaux, P. Corrosion behaviour of titanium in the presence of Streptococcus mutans. J. Dent. 2013, 41, 528–534. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  91. McGinley, E.L.; Dowling, A.H.; Moran, G.P. Influence of S. mutans on base-metal dental casting alloy toxicity. J. Dent. Res. 2013, 92, 92–97. [Google Scholar] [CrossRef] [PubMed]
  92. Lucchetti, M.C.; Fratto, G.; Valeriani, F. Cobalt-chromium alloys in dentistry: An evaluation of metal ion release. J. Prosthet. Dent. 2015, 114, 602–608. [Google Scholar] [CrossRef] [PubMed]
  93. Pereira, S.; Anami, L.C.; Pereira, C.A. Bacterial Colonization in the Marginal Region of Ceramic Restorations: Effects of Different Cement Removal Methods and Polishing. Oper. Dent. 2016, 41, 642–654. [Google Scholar] [CrossRef] [PubMed]
  94. Anami, L.C.; Pereira, C.A.; Guerra, E. Morphology and bacterial colonisation of tooth/ceramic restoration interface after different cement excess removal techniques. J. Dent. 2012, 40, 742–749. [Google Scholar] [CrossRef] [PubMed]
  95. Hahnel, S.; Rosentritt, M.; Handel, G. Surface characterization of dental ceramics and initial streptococcal adhesion in vitro. Dent. Mater. 2009, 25, 969–975. [Google Scholar] [CrossRef] [PubMed]
  96. Bremer, F.; Grade, S.; Kohorst, P.; Stiesch, M. In vivo biofilm formation on different dental ceramics. Quintessence Int. 2011, 42, 565. [Google Scholar] [PubMed]
  97. Klinge, B.; Meyle, J. Peri-implant tissue destruction. The Third EAO Consensus Conference 2012. Clin. Oral Implants Res. 2012, 23 (Suppl. S6), 108–110. [Google Scholar] [CrossRef] [PubMed]
  98. Serino, G.; Strom, C. Peri-implantitis in partially edentulous patients: Association with inadequate plaque control. Clin. Oral Implants Res. 2009, 20, 169–174. [Google Scholar] [CrossRef] [PubMed]
  99. Lindhe, J.; Meyle, J.; Group, D. Peri-implant diseases: Consensus Report of the Sixth European Workshop on Periodontology. J. Clin. Periodontol. 2008, 35, 282–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Zitzmann, N.U.; Berglundh, T. Definition and prevalence of peri-implant diseases. J. Clin. Periodontol. 2008, 35, 286–291. [Google Scholar] [CrossRef] [PubMed]
  101. Subramani, K.; Jung, R.E.; Molenberg, A.; Hämmerle, C.H. Biofilm on dental implants: A review of the literature. Int. J. Oral Maxillofac. Implants 2009. [Google Scholar] [CrossRef]
  102. De Avila, E.D.; Avila-Campos, M.J.; Vergani, C.E.; Spolidorio, D.M.; Mollo Fde, A., Jr. Structural and quantitative analysis of a mature anaerobic biofilm on different implant abutment surfaces. J. Prosthet. Dent. 2016, 115, 428–436. [Google Scholar] [CrossRef] [PubMed]
  103. Elter, C.; Heuer, W.; Demling, A.; Hannig, M.; Heidenblut, T.; Bach, F.W.; Stiesch-Scholz, M. Supra- and subgingival biofilm formation on implant abutments with different surface characteristics. Int. J. Oral Maxillofac. Implants 2008, 23, 327–334. [Google Scholar] [PubMed]
  104. Degidi, M.; Artese, L.; Scarano, A.; Perrotti, V.; Gehrke, P.; Piattelli, A. Inflammatory Infiltrate, Microvessel Density, Nitric Oxide Synthase Expression, Vascular Endothelial Growth Factor Expression, and Proliferative Activity in Peri-Implant Soft Tissues Around Titanium and Zirconium Oxide Healing Caps. J. Periodontol. 2006, 77, 73–80. [Google Scholar] [CrossRef] [PubMed]
  105. Welander, M.; Abrahamsson, I.; Berglundh, T. The mucosal barrier at implant abutments of different materials. Clin. Oral Implants Res. 2008, 19, 635–641. [Google Scholar] [CrossRef] [PubMed]
  106. Zhao, B.; van der Mei, H.C.; Subbiahdoss, G.; de Vries, J.; Rustema-Abbing, M.; Kuijer, R.; Busscher, H.J.; Ren, Y. Soft tissue integration versus early biofilm formation on different dental implant materials. Dent. Mater. 2014, 30, 716–727. [Google Scholar] [CrossRef] [PubMed]
  107. Nascimento, C.; Pita, M.S.; Santos Ede, S.; Monesi, N.; Pedrazzi, V.; Albuquerque Junior, R.F.; Ribeiro, R.F. Microbiome of titanium and zirconia dental implants abutments. Dent. Mater. 2016, 32, 93–101. [Google Scholar] [CrossRef] [PubMed]
  108. Do Nascimento, C.; Pita, M.S.; Pedrazzi, V. In vivo evaluation of Candida spp. adhesion on titanium or zirconia abutment surfaces. Arch. Oral Biol. 2013, 58, 853–861. [Google Scholar] [CrossRef] [PubMed]
  109. Nascimento, C.D.; Pita, M.S.; Fernandes, F.H.N.C.; Pedrazzi, V.; de Albuquerque Junior, R.F.; Ribeiro, R.F. Bacterial adhesion on the titanium and zirconia abutment surfaces. Clin. Oral Implants Res. 2014, 25, 337–343. [Google Scholar] [CrossRef] [PubMed]
  110. De Freitas, A.R.; Silva, T.S.O.; Ribeiro, R.F.; de Albuquerque Junior, R.F.; Pedrazzi, V.; do Nascimento, C. Oral bacterial colonization on dental implants restored with titanium or zirconia abutments: 6-month follow-up. Clin. Oral Investig. 2018. [Google Scholar] [CrossRef] [PubMed]
  111. Raffaini, F.C.; Freitas, A.R.; Silva, T.S.O.; Cavagioni, T.; Oliveira, J.F.; Albuquerque Junior, R.F.; Pedrazzi, V.; Ribeiro, R.F.; do Nascimento, C. Genome analysis and clinical implications of the bacterial communities in early biofilm formation on dental implants restored with titanium or zirconia abutments. Biofouling 2018, 34, 173–182. [Google Scholar] [CrossRef] [PubMed]
  112. Jemat, A.; Ghazali, M.J.; Razali, M.; Otsuka, Y. Surface Modifications and Their Effects on Titanium Dental Implants. Biomed. Res. Int. 2015, 2015, 791725. [Google Scholar] [CrossRef] [PubMed]
  113. Aparicio, C.; Rodriguez, D.; Gil, F.J. Variation of roughness and adhesion strength of deposited apatite layers on titanium dental implants. Mater. Sci. Eng. C Mater. Biol. Appl. 2011, 31, 320–324. [Google Scholar] [CrossRef]
  114. San Thian, E.; Huang, J.; Barber, Z.H.; Best, S.M.; Bonfield, W. Surface modification of magnetron-sputtered hydroxyapatite thin films via silicon substitution for orthopaedic and dental applications. Surf. Coat. Technol. 2011, 205, 3472–3477. [Google Scholar] [CrossRef]
  115. He, F.M.; Yang, G.L.; Li, Y.N. Early bone response to sandblasted, dual acid-etched and H2O2/HCl treated titanium implants: An experimental study in the rabbit. Int. J. Oral Maxillofac. Surg. 2009, 38, 677–681. [Google Scholar] [CrossRef] [PubMed]
  116. Yang, C.Y.; Lee, T.M.; Lu, Y.Z.; Yang, C.W.; Lui, T.S.; Kuo, A.; Huang, B.W. The influence of plasma spraying parameters on the characteristics of fluorapatite coatings. J. Med. Biol. Eng. 2010, 30, 91–98. [Google Scholar]
  117. Schmidlin, P.R.; Mueller, P.; Attin, T.; Wieland, M.; Hofer, D.; Guggenheim, B. Polyspecies biofilm formation on implant surfaces with different surface characteristics. J. Appl. Oral Sci. 2013, 21, 48–55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  118. Matos, A.O.; Ricomini-Filho, A.P.; Beline, T.; Ogawa, E.S.; Costa-Oliveira, B.E.; de Almeida, A.B.; Nociti Junior, F.H.; Rangel, E.C.; da Cruz, N.C.; Sukotjo, C.; et al. Three-species biofilm model onto plasma-treated titanium implant surface. Colloids Surf. B Biointerfaces 2017, 152, 354–366. [Google Scholar] [CrossRef] [PubMed]
  119. Al-Ahmad, A.; Wiedmann-Al-Ahmad, M.; Fackler, A.; Follo, M.; Hellwig, E.; Bachle, M.; Hannig, C.; Han, J.S.; Wolkewitz, M.; Kohal, R. In vivo study of the initial bacterial adhesion on different implant materials. Arch. Oral Biol. 2013, 58, 1139–1147. [Google Scholar] [CrossRef] [PubMed]
  120. Roehling, S.; Astasov-Frauenhoffer, M.; Hauser-Gerspach, I.; Braissant, O.; Woelfler, H.; Waltimo, T.; Kniha, H.; Gahlert, M. In Vitro Biofilm Formation on Titanium and Zirconia Implant Surfaces. J. Periodontol. 2017, 88, 298–307. [Google Scholar] [CrossRef] [PubMed]
Figure 1. The process of biofilm formation in the oral cavity is divided into four stages: 1. acquired pellicle formation; 2. initial adhesion; 3. coaggregation; 4. maturation and diffusion.
Figure 1. The process of biofilm formation in the oral cavity is divided into four stages: 1. acquired pellicle formation; 2. initial adhesion; 3. coaggregation; 4. maturation and diffusion.
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Figure 2. The relationship between fluoride of glass ionomer cements and bacterial metabolism.
Figure 2. The relationship between fluoride of glass ionomer cements and bacterial metabolism.
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Figure 3. Representative SEM images of glass ionomer cement (GIC) surfaces before and after aging treatments. A: without any aging treatments; B: the GICs were immersed in water; C: S. mutans suspensions; D: salivary microbes’ suspensions.
Figure 3. Representative SEM images of glass ionomer cement (GIC) surfaces before and after aging treatments. A: without any aging treatments; B: the GICs were immersed in water; C: S. mutans suspensions; D: salivary microbes’ suspensions.
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Figure 4. Four kinds of titanium implant surface treatment show different SEM imagines. A: Sandblasting and acid etching technique (SLA); B: plasma sprayed hydroxyapatite coating (HA); C: machined treatment (machined); D: microarc oxidation (MAO).
Figure 4. Four kinds of titanium implant surface treatment show different SEM imagines. A: Sandblasting and acid etching technique (SLA); B: plasma sprayed hydroxyapatite coating (HA); C: machined treatment (machined); D: microarc oxidation (MAO).
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Table 1. The effect of the resin-based composites on biofilm formation.
Table 1. The effect of the resin-based composites on biofilm formation.
Author, YearResin-Based CompositeBriefRef.
Ionescu et al., 2012Filtek Supreme XT; Filtek SiloraneTM; Grandio The proportions of resin matrix and filler particles on the surface of resin-based composite strongly influence biofilm formation in vitro.[26]
Brambilla et al., 2016Filtek SiloraneTM; Filtek Z250TMSilorane-based composite is less prone to S. mutans biofilm development.[46]
Brambilla et al., 2009Filtek Z250TMUnpolymerized monomers on the material surface are responsible for increasing in vitro colonization by S. mutans.[47]
Kawai et al., 2000Clearfil F II; SiluxThe diglycidyl methacrylate and TEGDMA significantly promoted GTF enzymes activity[48]
Pereira et al., 2011Filtek Z 350TM; Esthet XTM; Vit-l-escenceTMThe least biofilm forms on a nanofilled RBC compared with nanohybrid, microhybrid, and bulk-filled RBCs. [52]
Hahnel et al., 2014Beautifil IIThe inclusion of S-PRG fillers may reduce biofilm formation on resin composite.[53]
Yoshihara et al., 2017Beautifil ll; Herculite XRV UltraBioactive glass filler may promote bacterial adhesion because of unstable surface integrity, releasing ions and dissolving.[53]
Table 2. The influence of different dental alloys on the biofilm formation.
Table 2. The influence of different dental alloys on the biofilm formation.
Author, YearResin-Based CompositeBriefRef.
Zappala et al., 1996Gold alloyHigh-noble alloys showed a significant reduction in biofilm because of the low porosity and unique electrochemical corrosion resistance.[85]
Grass et al., 2011Metallic copperMetallic copper processes strong and rapid bactericidal effect, named “contact killing”.[20]
Mystkowska et al., 2016Co–Cr-based alloyCo–Cr alloys developed more pits and viable microbial cells than titanium alloys after degradation.[88]
McGinley et al., 2013Ni-based alloyNi-based dental casting alloys induced elevated levels of cellular toxicity compared with S. mutans-treated Co–Cr-based dental casting alloys.[91]
Souza et al., 2013TitaniumThe presence of S. mutans colonies on the titanium negatively affected its corrosion resistance due to the titanium-passive film.[21]
Table 3. The influence of different ceramic on the biofilm formation.
Table 3. The influence of different ceramic on the biofilm formation.
Author, YearCeramicBriefRef.
Hahnel et al., 2009Glass, lithium disilicate glass, glass-infiltrated zirconia, partially sintered zirconia, hipped zirconia ceramicOnly slight and random differences in streptococcal adhesion were found between the various ceramic materials, and control material showed higher values for streptococcal adhesion than all ceramic materials.[95]
Bremer et al., 2011Veneering glass-ceramic, lithium disilicate glass-ceramic, yttrium-stabilized zirconia (Y-TZP), hot isostatically pressed (HIP) Y-TZP ceramic, and HIP Y-TZP ceramic with 25% aluminaThe study in vivo showed significant difference in biofilm formation with various types of dental ceramics; especially zirconia exhibited low biofilm accumulation.[96]
Kim et al., 2017Commercially available ceramic materials: Vita Enamic, Lava Ultimate, Vitablocs Mark II, and Wieland ReflexAll materials, except for Vitablocs Mark II, promoted significantly greater biofilm growth.[28]
Table 4. The influence of different titanium surface treatments on the biofilm formation.
Table 4. The influence of different titanium surface treatments on the biofilm formation.
Author, YearDifferent Titanium SurfacesBriefRef.
Patrick et al., 2013Machined, stained, acid-etched, or sandblasted/acid-etched (SLA)After the colonization for 2, 4, and 8 h, there seems no difference between these titanium discs. Up to 16.5 h, the SLA surface showed the highest trend for the bacterial colonization[117]
Matos et al., 2011Micro-arc oxidation (MAO), glow discharge plasma (GDP), machined, and sandblasted surfacesThe counts of F. nucleatum were lower for MAO treatment at early biofilm phase (16.5 h), while the plasma treatment did not affect the viable microorganism counts. Biofilm extracellular matrix was similar among these groups, except for GDP, with the lowest protein content.[118]
Al-Ahmad et al., 2010Machined titanium (Tim), modified titanium (TiUnite)No significant differences in biofilm composition on the implant surfaces. Besides, the influence of roughness and material on biofilm formation was compensated by biofilm maturation[35]
de Freitas et al., 2011Machined, blasted, HA-coated The titanium discs were put into volunteers’ oral cavity and were tested after 1, 3, 7, 14, and 21 days. There was no statistically significant difference between the kinetics of bacterial species succession and the different surfaces.[40]
Bevilacqua et al., 2018Machined surface(M), laser-treated surface (LT), sandblasted surface (SB)The biofilm developed in vivo for 1 day and 4 days showed no statistical difference between 3 kinds of discs. In vitro, when the biofilm was formed by P. aeruginosa, M showed less biomass and biofilm average thickness. As for the biofilm developed by mixed salivary bacteria, SB showed less biomass and average biofilm thickness.[37]

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Hao, Y.; Huang, X.; Zhou, X.; Li, M.; Ren, B.; Peng, X.; Cheng, L. Influence of Dental Prosthesis and Restorative Materials Interface on Oral Biofilms. Int. J. Mol. Sci. 2018, 19, 3157. https://doi.org/10.3390/ijms19103157

AMA Style

Hao Y, Huang X, Zhou X, Li M, Ren B, Peng X, Cheng L. Influence of Dental Prosthesis and Restorative Materials Interface on Oral Biofilms. International Journal of Molecular Sciences. 2018; 19(10):3157. https://doi.org/10.3390/ijms19103157

Chicago/Turabian Style

Hao, Yu, Xiaoyu Huang, Xuedong Zhou, Mingyun Li, Biao Ren, Xian Peng, and Lei Cheng. 2018. "Influence of Dental Prosthesis and Restorative Materials Interface on Oral Biofilms" International Journal of Molecular Sciences 19, no. 10: 3157. https://doi.org/10.3390/ijms19103157

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