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RESEARCH REPORT |
1 Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Berne, Freiburgstrasse 7, PO Box 64, 3010 Berne, Switzerland;
2 Institut Straumann AG, Waldenburg, Switzerland;
3 Department of Periodontics, University of Texas Health Science Center at San Antonio, San Antonio, USA; and
4 Division of Pediatric Dentistry and Structural Biology, Department of Operative Dentistry, School of Dental Medicine, University of Berne, Switzerland;
* corresponding author, daniel.buser{at}zmk.unibe.ch
| ABSTRACT |
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KEY WORDS: titanium surface sandblasted and acid-etched surface histomorphometric analysis surface topography surface chemistry
| INTRODUCTION |
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In the past 15 yrs, the topography of titanium surfaces has been investigated for dental implant applications (Buser, 2001). The main goal of these experimental studies was to determine whether bone apposition could be enhanced by new microrough titanium surfaces as compared with the original implant surfaces utilized in implant dentistry, such as machined or titanium-plasma-sprayed (TPS) surfaces. Various techniques have been used to produce microrough titanium surfaces, including sandblasting, acid-etching, or combinations thereof, to modify surface topography (Wieland et al., 2000). Among these new surfaces, the sandblasted and acid-etched (SLA) surface demonstrated enhanced bone apposition in histomorphometric studies (Buser et al., 1991; Cochran et al., 1998), and higher removal torque values in biomechanical testing (Wilke et al., 1990; Buser et al., 1999; Li et al., 2002). Based on these experimental results, clinical studies were initiated to load SLA implants after a reduced healing period of only 6 wks. The clinical examination up to 3 yrs demonstrated favorable results, with success rates around 99% (Roccuzzo et al., 2001; Cochran et al., 2002; Bornstein et al., 2003).
Besides surface topography, surface chemistry is another key variable for peri-implant bone apposition, since it influences surface charge and wettability (Kilpadi and Lemons, 1994). Surface wettability is largely dependent on surface energy, and influences the degree of contact with the physiologic environment. Increased wettability thus enhances interaction between the implant surface and the biologic environment (Kilpadi and Lemons, 1994). A certain similarity of clean hydrophilic titanium oxide surfaces to water can be assumed as a consequence of extensive hydroxylation/hydration of the oxide layer and a high wettability by water, leading to a gentle interaction of the surface with the water shell around delicate biomolecules such as proteins (Textor et al., 2001).
The aim of the present study was to examine bone apposition to a modified SLA (modSLA) surface in the maxillae of miniature pigs as compared with the standard SLA surface. Test and control implants had the same surface topography, but potentially differed in their surface chemistry due to different production protocols. The hypothesis of the study was that the modSLA surface would promote a faster bone apposition in comparison with the standard SLA surface.
| MATERIALS & METHODS |
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Surgical Procedure
The current study protocol was approved by the Committee for Animal Research, State of Berne, Switzerland (Approval no. 109/99), and utilized a study design that has been successfully used in previous studies (Buser et al., 1999; Li et al., 2002). In brief, two surgical interventions were performed in 6 adult miniature pigs. In the first surgery, the anterior teeth in the maxilla were carefully removed, while the animals were under general anesthesia (Surgical Research Unit ESI and Clinic for Large Animals, University of Berne), by means of flap elevation, careful osteotomy, and tooth separation. After wound closure, the sites were allowed to heal for at least 6 mos so that a fully healed edentulous alveolar crest in the maxilla could be achieved. In the second surgery, specially manufactured titanium implants were inserted according to a low-trauma surgical technique. The implants were placed, with good primary stability provided by the press-fit of the implants with the bone walls of the prepared implant beds.
Depending on the anatomical situation, 3 or 4 implants were inserted on either side of the maxilla, in a split-mouth design. Following irrigation, primary wound closure was achieved with interrupted sutures, and implants were left to heal in a submerged position. Sample sizes were based on those used in previously published studies, where the study design had allowed statistically significant differences to be observed.
Histological Preparation and Histomorphometric Analysis
Two miniature pigs were killed after 2, 4, and 8 wks of healing, respectively. Immediately following death, the soft tissues were removed to expose the edentulous areas of the maxilla with 3 or 4 integrated implants per side. In each animal, 2 bone blocks were produced with an oscillating saw. The details of the histological processing have been described in previous studies (Buser et al., 1991; Cochran et al., 1998). The block specimens with the implants were immersed in a solution of formaldehyde (4%) combined with CaCl2 (1%) for histological preparation (Schenk et al., 1984). The specimens were dehydrated and embedded in methylmethacrylate. Using a low-speed diamond saw with coolant (Leco Corporation, St. Joseph, MI, USA), we cut the specimens in the bucco-lingual direction and parallel to the axis of the implants, resulting in 3 undecalcified sections of ~ 500 µm in thickness per implant. Subsequently, the sections were glued with acrylic cement to opaque Plexiglas, ground to a final thickness of ~ 80 µm, and stained superficially with toluidine blue followed by basic fuchsin. Three specimens of each implant were analyzed by an experienced examiner (B.H.). We determined the percentage of direct contact between mineralized bone and the titanium surface by intersection counting, using an integrative eyepiece with parallel sampling lines at a magnification of 100x. The bone-implant interface was restricted to the peri-implant chamber as defined by the 3 rings and the bony wall of the implant site.
Statistical Analysis
We used analysis of variance (ANOVA) to identify the effects of surface wettabillity on surface roughness, described with the parameters Sa, Sq, St, and Sk. Mean bone-to-implant contact (BIC) per implant was calculated and used for further analysis. Using a split-mouth design, we matched implants and compared them according to their position in the maxillary arch, thus allowing for a location-dependent analysis using the Wilcoxon test for paired data (Systat 5.2, Systat Inc., Evanston, IL, USA). The significance level chosen in all statistical tests was 0.05.
To limit confounding factors, such as anatomical variations between anterior-posterior locations in the maxilla, we used the implant, rather than the animal, as the unit of analysis, to allow for a site-dependent comparison using the split-mouth design with test and control implants in the same position. Thus, each anterior-posterior position was considered independently, and the implant constituted the unit of analysis.
| RESULTS |
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| DISCUSSION |
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In the current study, the test surface demonstrated a significantly greater bone-to-implant contact at 2 and 4 wks of healing as compared with the standard SLA surface. At 8 wks, no differences were apparent. Both test and standard SLA surfaces possessed the same topography, as confirmed by topographical analyses. Therefore, the observed difference at 2 and 4 wks of healing could not have been caused by alterations in surface topography, but instead by alterations in surface chemistry. The modSLA surface was produced when the implants were stored in glass ampules containing isotonic NaCl solution following the acid-etching procedure, whereas standard SLA implants were stored in conventional glass ampules and, thus, were in contact with the surrounding atmosphere. Continuous submersion of an implant surface in isotonic solution appears to protect the pure Ti surface from contamination with carbonates and organic components naturally occurring in the atmosphere, thus preserving a chemically clean and reactive surface (Steinemann, 1998). This assumption is supported by the current XPS analysis, which detected a reduced carbon level on modSLA surfaces, typical for a chemically cleaned Ti surface (Textor et al., 2001). The carbon concentration measured on standard SLA surfaces is consistent with results reported in the literature which compared SLA with other commercially available implant surfaces which have been exposed to air for some time (Massaro et al., 2002). Furthermore, an increased oxygen value was determined on modSLA surfaces. The oxygen can be attributed to the titanium oxide layer (Textor et al., 2001). Another reason for the increased oxygen concentration is due to the increased hydroxylated/hydrated groups bound to the surface (Textor et al., 2001). The hydroxylated/hydrated surface has an additional characteristic. This oxide surface is hydrophilic, which is supported by the current DCA measurements. These measurements demonstrated that the modSLA surface is indeed characterized by increased wettability when compared with the standard SLA surface.
Surface wettability is known to influence the interactions between the implant surface and the surrounding milieu (Kilpadi and Lemons, 1994). Inorganic molecules, such as calcium and phosphate ions, are readily adsorbed from the blood onto the hydroxylated/hydrated TiO2 surface. Of equal importance are interactions that lead to the adsorption of organic molecules, such as proteins, lipoproteins, and peptides, to the TiO2 surface. These interactions may occur electrostatically between positively charged amino acid groups (e.g., -NH3+) and the negatively charged TiO2 surface, or between negatively charged amino acid groups (COO) and Ca++ bridges which have been previously adsorbed to a negatively charged TiO2 surface. In addition, a direct attachment of a COO group onto the Ti cations can take place by replacement of hydroxy groups (Steinemann, 1998; Textor et al., 2001). It has been reported that a fibrin network is laid upon the titanium dioxide surface and its associated adsorbed molecules, which facilitates the attachment of local osteoblasts (Sodek and Cheifetz, 2000). By maintaining a hydroxylated oxide surface, the modSLA surface could enhance surface reactivity with surrounding ions, amino acids, and proteins in the tissue fluid. Further studies are required to elucidate this speculation and the exact mechanisms of molecular interaction.
The observed significant enhancement of new bone apposition to the modSLA surface during the initial stages of bone regeneration is promising. The standard SLA surface has already led to a reduction of healing periods in patients from 3 mos to 6 wks in implant sites with regular bone density (Roccuzzo et al., 2001; Cochran et al., 2002; Bornstein et al., 2003). The modSLA surface could offer a further reduction of the healing period following implant placement. Before clinical testing of this new implant surface in patients can be initiated, further in vivo studies would be of help to demonstrate whether the observed improved bone apposition in the present study represents superior bone anchorage at earlier time points. Such confirmation could allow for a further reduction in the healing period as a routine procedure in patients.
| ACKNOWLEDGMENTS |
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Received July 24, 2003; Last revision April 19, 2004; Accepted May 6, 2004
| REFERENCES |
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Bico J, Thiele M, Quéré D (2002). Wetting of textured surfaces. Colloids Surf A 206:4146.
Bornstein MM, Lussi A, Schmid B, Belser UC, Buser D (2003). Early loading of titanium implants with a sandblasted and acid-etched (SLA) surface. 3-year results of a prospective study in partially edentulous patients. Int J Oral Maxillofac Implants 18:659666.[Medline]
Boyan BD, Schwartz Z (2000). Modulation of osteogenesis via implant surface design. In: Bone engineering. Davies JE, editor. Toronto: em squared inc., pp. 232239.
Buser D (2001). Titanium for dental applications (II): implants with roughened surfaces. In: Titanium in medicine. Brunette DM, Tengvall P, Textor M, Thomson P, editors. Berlin: Springer, pp. 876888.
Buser D, Schenk RK, Steinemann S, Fiorellini J, Fox C, Stich H (1991). Influence of surface characteristics on bone integration of titanium implants. A histomorphometric study in miniature pigs. J Biomed Mater Res 25:889902.[ISI][Medline]
Buser D, Nydegger T, Oxland T, Cochran DL, Schenk RK, Hirt HP, et al. (1999). The interface shear strength of titanium implants with a sandblasted and acid-etched surface. A biomechanical study in the maxilla of miniature pigs. J Biomed Mater Res 45:7583.[Medline]
Cochran DL, Schenk RK, Lussi A, Higginbottom FL, Buser D (1998). Bone response to unloaded and loaded titanium implants with a sandblasted and acid-etched surface. A histometric study in the canine mandible. J Biomed Mater Res 40:111.[ISI][Medline]
Cochran DL, Buser D, ten Bruggenkate CM, Weingart D, Taylor TM, Bernard JP, et al. (2002). The use of reduced healing times on ITI implants with a sandblasted and acid-etched (SLA) surface: early results from clinical trials on ITI SLA implants. Clin Oral Implants Res 13:144153.[Medline]
Gotfredsen K, Nimb L, Hjørting-Hansen E, Jensen JS, Holmen A (1992). Histomorphometric and removal torque analysis for TiO2-blasted titanium implants. Clin Oral Implants Res 3:7784.[Medline]
Jordan H, Brodmann R, Grigat M, Valentin J (2001). Quality assurance of HARMS and MOEMS surface structures using confocal white light microscopy. In: Lithographic and micromachining techniques for optical component fabrication. Proceedings of the SPIE (International Society for Optical Engineering) Conference, July 2930, 2001, San Diego, CA. Kley E, Herzig HP, editors. 4440:5158.
Kilpadi DV, Lemons JE (1994). Surface energy characterization of unalloyed titanium implants. J Biomed Mater Res 28:14191425.[Medline]
Li D, Ferguson SJ, Beutler T, Cochran DL, Sittig C, Hirt HP, et al. (2002). Biomechanical comparison of the sandblasted and acid-etched and the machined and acid-etched titanium surface for dental implants. J Biomed Mater Res 60:325332.[Medline]
Martin JY, Schwartz Z, Hummert TW, Schraub DM, Simpson J, Lankford J, et al. (1995). Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res 29:389401.[ISI][Medline]
Massaro C, Rotolo P, DeRiccardis F, Milella E, Napoli A, Wieland M, et al. (2002). Comparative investigation of the properties of commercial titanium dental implants. Part I: Chemical composition. J Mater Sci: Mater Med 13:535548.[Medline]
Ratner BD, Porter SC (1996). Surfaces in biology and biomaterials; description and characterization. In: Interfacial phenomena and bioproducts. Brash JLW, editor. New York: Marcel Dekker, pp. 5783.
Roccuzzo M, Bunino M, Prioglio F, Bianchi SD (2001). Early loading of sandblasted and acid-etched (SLA) implants: a prospective split-mouth comparative study. Clin Oral Implants Res 12:572578.[Medline]
Schenk RK, Olah AJ, Hermann W (1984). Preparation of calcified tissues for light microscopy. In: Methods of calcified tissue preparation. Vol. 1. Dickson GR, editor. Amsterdam: Elsevier Science Publishers B.V., pp. 156.
Sodek J, Cheifetz S (2000). Molecular regulation of osteogenesis. In: Bone engineering. Davies JE, editor. Toronto: em squared inc., pp. 3143.
Steinemann SG (1998). Titaniumthe material of choice? Periodontol 2000 17:721.
Textor M, Sittig C, Frauchiger V, Tosatti S, Brunette DM (2001). Properties and biological significance of natural oxide films on titanium and its alloys. In: Titanium in medicine. Brunette DM, Tengvall P, Textor M, Thomsen P, editors. Berlin: Springer, pp. 171230.
Vörös J, Wieland M, Ruiz-Taylor L, Textor M, Brunette DM (2001). Characterization of titanium surfaces. In: Titanium in medicine. Brunette DM, Tengvall P, Textor M, Thomsen P, editors. Berlin: Springer, pp. 87144.
Wennerberg A, Albrektsson T, Andersson B, Krol JJ (1995). A histomorphometric and removal torque study of screw-shaped titanium implants with three different surface topographies. Clin Oral Implants Res 6:2430.[Medline]
Wieland M, Sittig C, Brunette DM, Textor M, Spencer ND (2000). Measurement and evaluation of the chemical composition and topography of titanium implant surfaces. In: Bone engineering. Davies JE, editor. Toronto: em squared inc., pp. 163182.
Wilke HJ, Claes L, Steinemann S (1990). The influence of various titanium surfaces on the interface shear strength between implants and bone. In: Clinical implant materials. Adv Biomater. Vol. 9. Heimke G, Soltesz U, Lee AJC, editors. Amsterdam: Elsevier Science Publishers B.V., pp. 309314.
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