Simplified micrometric surface characterization of different implant surfaces available on the Brazilian market

Aim: This study characterized the implant surfaces available on the Brazilian market in terms of topography, chemical composition, and roughness. Methods: The following brands were selected according to their surfaces: Kopp (Ko), Signo Vinces (Sv), Neodent (Ne), Osseotite (Os), Nanotite (Nt), SIN (Si), Titanium Fix (Tf), conventional Straumann (Str), SLActive (SLA). The morphological analysis and the alloy impurities and implant surface contaminants were analyzed by SEM-EDS. Surface roughness parameters and 3-D reconstructions were obtained by laser microscopy (20x). Two distinct areas were evaluated: i) the cervical portion (no surface treatment), and ii) the middle third (treated surface). Results: The characterization of the implant surfaces by SEM showed morphological differences between the thread geometries and surface morphology at 800x and 2000x magnification. The EDS elemental analysis showed a predominance of titanium (Ti) for all implants. The SLA surface showed only peaks of Ti while other implants brands showed traces of impurities and contaminants including Al, C, PR, F, Mg, Na, Ni, O, P, and SR. The implant surface roughness in the cervical portion did not exceed Ra 0.5–1.0 μm, constituting a minimally rough surface and obtaining acceptable standards for this region. Only Nt, Str, and SLA presented Ra above 2 μm in the middle third area showing a rough surface favorable for osseointegration. Conclusion: This study concluded that there is no established standard for morphology, chemical composition and implant surface roughness that allows a safe comparison between the available dental implant surfaces. National implant brands generally contain more impurities and surface contaminants than their international counterparts and were consequently more sensitive to the surface treatment techniques.


Introduction
The discovery of osseointegration enabled treatment of totally and partially edentulous patients with dental implants 1 .In a previous study, Branemark (1977)  2 stated that direct contact between vital bone tissue and implant is totally predictable, safe and long-lasting, and thus constitutes an important parameter for clinical success 3 .Insights in healing and repair processes contributed to the modification of the implant surface treatments and designs.Surface roughness, macro, and microgeometry influence the cell proliferation and differentiation, extracellular matrix synthesis, local cell production factors, and even cell shape 4 .Therefore, the treatment used on the implant surface directly affects the implant's survival rate and has been the focus of intense study 3 .
When the osseointegration is triggered, the osteoblast adhesion to the implant surface is required for the cell to receive signals that induce osteoblastic proliferation 5 .Adopting rough implant surfaces can facilitate the retention of the osteogenic cells and can accelerate their migration through osseoconduction 6 .Consequently, a high quality bone-implant interface guarantees faster and stronger bone formation that in turn promotes greater stability during the repair process [7][8][9] .The primary stability is a predictor for successful osseointegration 10 .Geometry can also be factor, as spherical materials induce less fibrous encapsulation than cylindrical or sharp angles 11 .The quality of the bone-implant interface also depends on the implant's ability to support loading, mainly because overload biomechanics increase the bone density in the long-term and overloading might influence peri-implant tissue breakdown when plaque accumulation is present 12 .The systematic review of in vivo data evidenced a differential peri-implant bone tissue response to overloading, depending on the mucosal health: supra-occlusal contacts in a non-inflamed peri-implant environment did not negatively affect osseointegration and are even anabolic 12 .A combination of all the aforementioned factors can influence the clinical success of dental implants.
In recent years, some studies 5,7,13,14 have measured the dental implants surfaces at macro, micro, and nanometric scales, to investigate how the different surfaces influence the bone repair process.Although there are studies available that analyze the influence of surface roughness, little is known about the physico-chemical properties of the implant surfaces.This information is generally restricted to the implant package specifications and informational catalogs provided by the manufacturers 15 .Furthermore, the gold standard test to characterize the physical properties of implant surface treatments is interferometry, an expensive and time-consuming technique.This study aims to characterize the surface roughness of different commercial implant brands available in Brazil using scanning electron microscopy images in conjunction with laser microscopy, a simplified interferometrical technique that has been sucessfully applied in the material engineering sciences 16 .
In this study, we used the following parameters: Rp (maximum profile peak height / peak height of the highest roughness); Ry (maximum distance between peak and valley); Rz ( maximum height of profile / represents the arithmetic mean of the 5 values); Rt (total height of profile); Ra (arithmetic mean deviation of profile / represents the average profile roughness -amplitude parameter defined as integral and absolute value of the height of peaks and valleys, along the evaluated profile) 17 .In addition, the surfaces studied were reconstructed in a 3-D format using the OLS 4000 2.1 Software to process and obtain 20x magnified images (Figure 1).The implants surface morphologies and the elemental analysis were performed using a scanning electron microscopy (SEM) and energy dispersive X-ray spectrometry (EDS) (SSX-550; Shimadzu, Tokyo, Japan) to identify the elements present on the implant surface.Two regions of the implant were selected to perform the analyses: i) the cervical region (without surface treatment), and ii) the medium third (treated surface).

Results
The 3-D reconstructions showing the surface morphology of the 7 implant types are shown in Figure 1, while Figure 2 presents the SEM images showing the implant surface morphologies.Table 2 lists the results of the implant surface roughness analysis for the different commercial brands in their cervical and middle regions.The cervical portion of all implants can be considered minimally rough, while the middle region may range from minimally rough to rough (Ra> 2.0 μm).The EDS elemental analysis shows that only the SLA implant surface is composed of pure titanium; all other implant surfaces contained significant amounts of different elements, as described in Table 3 and Figure 3.

Discussion
The characteristics of the bone-implant interface and the methods to improve this relationship such as implant surface modifications have been intensely studied 18 .The average surface roughness of the implants, represented by Ra, is a widely investigated parameter by interferometry.Our study was the first that described a simplified laser methodology for implants surface roughness characterization.According to Albrektsson and Wennerberg 13 (2004), the surfaces can be classified according to the Ra value as: i) minimally coarse: Ra 0.5 -1.0 μm, present in machine turned implants; ii) moderately rough: Ra 1.0 -2.0 μm, found in implants with acid-conditioned, blasting or anodized surfaces; and iii) rough: Ra > 2.0 μm, as found in implants treated with plasma spray.However, the precise characterization of the surface morphologies is still a topic of discussion.Most implant surface studies ignore the chemical aspects 18 ; chemical characterization of commercially available products is extremely scarce in the literature 19,20 .In contrast, surface morphology and micrometer-scale topography are commonly used, but the optimal method to quantify microstructures remains a source of debate 21 .
The implant surface characteristics can influence the initial biofilm formation, because the adhesion of the microorganisms is directly proportional to the surface roughness.Therefore, the cervical portion of the implants ideally should have a smoother surface, because this region of the implant is most exposed to the buccal environment.
A smoother surface reduces bacterial adhesion and consequently reduces the incidence of peri-implant pathologies that can lead to implant failure 22 .The Ra values in the cervical portion of (Table 2) did not exceed 1.0 μm in the national implant brands, characterizing a minimally rough surface 13 .The latter implies that all brands presented acceptable micrometric patterns, capable of safely avoid biofilm accumulation in the peri-implant region.However, when other roughness parameters are included, a great disparity of values is observed, and all implants surfaces evaluated.The Nt surface  generally presented the highest roughness values in the middle portion of the implant (4 of 5 parameters evaluated) while the SLA surface presented the lowest roughness parameters in the cervical part, in accordance with the available literature 13,23 .In our study, Str and SLA surfaces presented similar roughness as described in previous studies, yet SLA surfaces presented greater bone-to-implant contact areas during the early stages of bone healing (2 and 4 weeks) 7,23 .
The surfaces Nt, Str and SLA presented mean Ra values above 2 μm in the middle third region.While high roughness promotes the retention of the osteogenic cells on the surface 5,6 , Ra values exceeding 2 μm can lead to an impaired and unenhanced bone response 5 .The SIN implant surface was characterized as minimally rough (Ra 0.7 μm) and presented the lowest values of roughness in the middle region compared to other commercial brands, mainly in terms of the Ry and Rz parameters.The Nt surface presented the highest Rp value (maximum height of the highest peak of the roughness) and the Tf surface presented a high value of Rt (the total height of the profile).These rough spots probably represent the locations where the first osteoblastic cells will attach.
The EDS analysis showed that only the implant with SLA surface is free of contaminations and impurities (Figure 1 and Table 3).This implant is immersed in water when sold, thus minimizing previous contamination.All other implants can be considered contaminated, and these impurities can determine the biological performance of the implant, and may be responsible for future osseointegration failures 24 .These results corroborate the study of Dohan Ehrenfest et al. 18 (2011) that detected inorganic contaminations, such as Na, P, Ca, F, and S in the evaluated implants.Therefore, even if dental implants are carefully manufactured, the results are not homogeneous; similar implant surface treatments do not necessarily yield identical results 7 .In addition, when the macrometric topography of an implant surface changes, its micrometric and chemical characteristics can also undergo changes, sometimes accidentally.Therefore, it is essential that each implant design has a suitable surface treatment to achieve an acceptable roughness 15 .
A large number of experimental investigations have clearly demonstrated that the bone response is influenced by the implant surface.Our study adopted a simplified methodology and showed that there is no pre-established roughness pattern that allows a safe comparison of different commercial brands available in Brazil.Therefore, it is necessary to perform more laboratory and clinical studies to investigate the ideal roughness characteristics that accelerate and maintain osseointegration.A limitation of this study is that only a qualitative analysis with one implant per brand was performed, precluding a statistical analysis.
In conclusion, dental implants are currently marketed without clearly defined surface characteristics.Our study was the first that described a simplified laser methodology for implants surface roughness characterization.The results indicate that there is no pre-established roughness pattern that easily allows a safe comparison of the available different dental implants brands.The SEM-EDS data indicate that national implant brands generally present higher amounts of impurities and elemental contamination than their international counterparts.

Table 1 .
Description of the type of surface treatment for the studied commercial brands.

Table 2 .
Roughness parameters of the studied implant surfaces in the cervical and middle third regions of the different commercial brands at the micrometric level (μm).

Table 3 .
Elemental composition of the studed implant surfaces (in weight %) measured with energy dispersive spectrometry (EDS).