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Material-related parameters

Surface properties

Similar to any material exposed to the oral cavity, the surface properties of a dental implant and its associated components may substantially impact the formation of biofilms on its surface. The surface parameters most commonly associated with microbial adhesion to solid surfaces in the oral cavity are surface roughness and surface free energy; however, the influence of surface roughness on microbial adhesion is generally regarded to overrule the impact of surface free energy (Teughels et al., 2006). For dental materials, numerous laboratory and clinical studies investigating the impact of substratum surface properties on the adhesion and proliferation of microorganisms have been published, and—at least for laboratory studies—contradictory results on the impact of these parameters have been reported. Thus, due to their more homogeneous results, the data gathered in clinical studies are usually preferred over the outcome of laboratory studies (Hannig and Hannig, 2009; Busscher et al., 2010), which is also why preferably data of clinical studies are included in the present review. However, with regard to biofilm formation on implant surfaces, the scientific data currently available has to be interpreted with caution. Very most studies addressing the influence of surface properties on biofilm formation investigated the adhesion and proliferation of microorganisms on a supragingival level, which is not fully representative of the subgingival conditions present in implants. For instance, microbial adhesion is significantly impacted by the presence of shear stresses, and it has been underlined that shear stresses in subgingival areas are markedly lower than in supragingival areas (Busscher et al., 2010). Investigating biofilm formation on titanium abutments, Heuer et al. (2007) showed that after 14 days of maturation, less than 1% of the available subgingival area of the abutments was covered by a biofilm, whereas more than 17% were covered in the supragingival areas. Thus it is clear that results gathered for dental materials from studies performed on a supragingival level cannot easily be transferred to the subclinical level. It has furthermore been reported that the impact of surface properties on biofilm formation is lower in subgingival than in supragingival areas (Quirynen and Bollen, 1995; Busscher et al., 2010), which further narrows the informative value of studies performed on a supragingival level.

Surface roughness and topography

With regard to the impact of surface roughness on biofilm formation, the conventional wisdom is that rough surfaces accumulate higher levels of biofilm than smooth surfaces. This phenomenon is attributed to the fact that irregularities in the substratum surface render protective areas for microorganisms against oral shear forces; in addition to that, some researchers have shown that the retention forces of microorganisms adherent to rough surfaces are higher than on smooth surfaces (Mei et al., 2011). For implant surfaces, some researchers have also identified that the surface roughness of implant surfaces affects the quantity and quality of proteins adsorbing to the implant surface during pellicle formation in vitro, suggesting that these phenomena might affect the subsequent adherence of microorganisms (Cavalcanti et al., 2015). However, for the improvement of osseointegration of dental implants, rough implant surfaces are required, which have been categorized by Albrektsson and Wennerberg (2004) to be either one of the following:

  • • smooth, with an arithmetic average of absolute surface roughness value (Ra) lower than 0.5 pm;
  • • minimally rough, with an Ra between 0.5 and 1.0 pm;
  • • moderately rough, with an Ra between 1.1 and 2.0 pm;
  • • rough, with an Ra exceeding 2.0 pm.

Particularly moderately rough surfaces are recommended for optimized osseointegration of the implant into the surrounding bone (Albrektsson and Wennerberg, 2004), which obviously interferes with the postulation of low surface roughness required for minimal biofilm formation. As a result of this dilemma, many commercially available dental implants feature a split design, which includes a roughened body for improved osseointegration, and a smooth and polished neck for minimization of biofilm formation in its transmucosal part. However, as some studies showed that marginal bone loss is lower in implants without a polished neck (Bratu et al., 2009; Bateli et al., 2011), many commercially available implant systems—particularly those ending at the crestal bone level—feature a completely rough surface. The surface roughness of a dental implant becomes increasingly important in cases where marginal bone loss has occurred, implying that—similar to periodontitis—parts of the roughened implant body are not any more covered by osseous tissues and can thus serve as a corridor for microbial invasion and subsequent adhesion and proliferation. In these cases, the formation of biofilms may increase, and the roughened surface makes it even harder to remove the biofilms from the implant surfaces.

As a result of the dilemma between osseointegrative and microbial considerations on the implant surface, the abutment and its surface properties have gained increasing importance. Particularly in implants ending at the crestal bone level, the abutment is—on a subgingival level—in close and direct contact with the periimplant soft tissues, which suggests that biofilms adherent to the implant abutment surface may instantaneously affect periimplant tissues and cause inflammation. For investigating the impact of abutment surface roughness on biofilm formation on the subgingival areas of implant abutments, Quirynen et al. employed a split-mouth design, using two types of titanium abutents with an Ra of either 0.3 or 0.8 pm. Although differences in plaque composition were limited, rough surfaces rendered up to 25 times more plaque than smooth surfaces (Quirynen et al., 1993). In later follow-up studies from the same group, no significant differences in quantitative and qualitative biofilm formation could be identified various abutments with different Ra which were all lower than 0.2 gm (Bollen et al., 1996; Quirynen et al., 1996). In contrast to these results, Wennerberg et al. (2003) failed to establish a correlation between the surface roughness of implant abutments ranging between 0.26 and 1.87 gm and plaque formation; however, other researchers attributed these observations to the insensitive analysis methods that had been applied in the Wennerberg study (Quirynen and Van Assche, 2012). Nevertheless, these results have been corroborated by Elter et al. (2008), who investigated the supra- and subgingival biofilm formation on titanium abutments with four distinct surfaces areas with Ra values ranging between 0.2 and 0.9 gm; this group identified significant differences in the percentage of available surface area covered by biofilms on a supragingival but not on a subgingival level. Burgers et al. (2010) supragingivally analyzed initial biofilm formation in vitro and in vivo using titanium specimens with different Ra values ranging from 0.15 to 0.95 gm, concluding that surface roughness significantly impacted biofilm formation and was significantly increased on the substratum with higher surface roughness.

From the data gathered from in vivo studies on biofilm formation on surfaces differing in surface roughness, thresholds for surface roughness have been derived, suggesting that Ra values lower than the threshold do not lead to a further decrease in biofilm formation. Depending on the study methodology and substratum applied, these threshold values range around 0.088 gm (derived from an assay analyzing biofilm formation on titanium specimens that were supragingivally exposed to the oral cavity) (Rimondini et al., 1997) and 0.2 gm (Bollen et al., 1997). These considerations indicate that—from a microbiological point of view—an ideal implant and implant abutment surface should yield a Ra value that is lower than the threshold values published by the Rimondini and Bollen groups. However, Xing et al. in 2015 identified a positive correlation between biofilm formation and the surface roughness of TiZr specimens with Ra values ranging between 29 and 214 nm, which suggests that even differences in surface roughness that are lower than the threshold value might have an impact on biofilm formation. Thus due to the previous considerations, implant abutments are usually polished to high gloss for minimizing biofilm formation on their surface. Although the outcome of the study by Xing et al. (2015) has to be interpreted with caution as it was performed on a supragingival level, the authors also showed that biofilm formation was not only impacted by surface roughness but also surface topography, as biofilm formation was lower on surfaces with flat and grooved topography than on surfaces with irregular topography. A similar phenomenon is well known from biological systems, and some derivatives from these biological phenomena have already been applied in biomaterial science (Bixler and Bhushan, 2014; Bixler et al., 2014). With regard to this aspect, it has also been reported that the attachment of soft tissues to implant and abutment surfaces is enhanced by texturing surfaces on a submicrometer level (Quirynen et al., 2002). However, Zhao et al. (2014) simultaneously simulated adhesion of bacteria and human gingival fibroblasts in a coculture model, and proved that the smooth titanium surfaces provided the best conditions for the adherence of human gingival fibroblasts. This phenomenon has been attributed to the larger size of the human gingival fibroblasts, which boasts an advantage over the smaller bacteria on smooth surfaces. Thus, current scientific approaches for minimizing biofilm formation on implants and implant abutments and for improving the attachment of periimplant soft tissues as a further barrier for biofilm formation include surface texturing techniques to supply exposed implant surfaces with distinct and regularly shaped micro- and nanotopographic patterns; however, to date, no clinical data regarding a potential effect of defined-patterned surfaces in implants and implant abutments have yet been published.

Surface free energy

Though frequently overruled by surface roughness, surface free energy belongs to the most important surface parameters determining the initial adherence of microorganisms to solid surfaces in the oral cavity. However, laboratory studies investigating microbial adhesion to substrata differing in surface free energy regularly reported conflicting results. Nevertheless, clinical data have shown that substrata with hydrophobic surface properties, which is usually also referred to as substrata with low surface free energy, feature lower biofilm formation on their surface than hydrophilic surfaces (i.e., high surface free energy). These mechanisms are well-known phenomena and have been proven in a broad number of studies for a range of different materials. With regard to this aspect, surface free energy appears to be a crucial parameter determining the biofilm formation in supragingival areas, where fluctuating shear forces thwart microbial adhesion and proliferation (Quirynen and Bollen, 1995; Busscher et al.,

2010). However, for subgingival areas, the effect of substratum surface hydrophobic- ity or surface free energy appears to be decisively lower (Quirynen and Bollen, 1995). Using a supragingival approach and implant surfaces with distinct surface roughness and surface hydrophilicity ranging from rough and hydrophobic (sandblasted and acid-etched (SLA), Ra 1.022 gm), hydrophobic and smooth (machined, Ra 0.069 gm), and hydrophilic and intermediate roughness (chemically modified and acid etched, Ra 0.186 gm), John et al. (2015) identified highest biofilm formation on the SLA surface featuring highest Ra, yet lowest values on the hydrophilic surface with intermediate surface roughness. Within the limitations of a supragingival approach, these results suggest that surface hydrophilicity and surface free energy may impact biofilm formation on implant surfaces.

For implant abutment surfaces, Quirynen et al. (1994) investigated biofilm formation on the surface of implant abutments featuring marked differences in surface free energy (pure titanium and fluor-ethylene-propylene-coated) after three months of insertion and, on a subgingival level, identified no statistically significant differences in the number of colony-forming units (cfu) on the different abutment surfaces. Though performed on a supragingival level, these observations were supported by other groups, who identified a significant impact of surface roughness but not surface free energy on the formation of biofilms on the surface of titanium and TiZr specimens differing in surface roughness, surface topography, and surface free energy (Burgers et al., 2010; Xing et al., 2015). In addition to these findings, laboratory studies employing complex biofilm models have also identified few differences in biofilm formation on the surface of several modified titanium materials despite of distinct differences in surface roughness and surface free energy (Schmidlin et al., 2013).

Although clinical data are limited, the existing knowledge on the impact of surface free energy on biofilm formation on implant surfaces indicates that the impact of surface free energy is limited.

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