Integrity of Implant Surface Modifications After Insertion Daniel Mints, MS1/Carlos Elias, PhD2/Paul Funkenbusch, PhD3/Luiz Meirelles, DDS, MS, PhD4 Purpose: The surface integrity associated with implant placement was examined to determine whether the topography of common implant surface modifications is retained after implant insertion. Materials and Methods: Turned (TU), acid-etched (AE), and anodized (AN) experimental implants prepared inhouse were inserted into polyurethane foam blocks using a standard drilling protocol at maximum torque of 37 Ncm. Qualitative analysis of the surfaces of preinserted and postinserted implants was done by scanning electron microscopy (SEM), and quantitative analysis of the implant threads was performed by interferometry. Among the roughness parameters calculated were average height deviation (Sa), peak height above core roughness (Spk), and maximum peak height (Sp). Results: SEM showed that TU implants exhibited similar morphology before and after implant insertion. The AE implants showed reduced peak height associated with flattened areas after insertion. AN implants demonstrated the most extensive damage associated with insertion; the entire porous oxide layer had been removed at the apical region and on the crests of the threads. Surface roughness evaluation was corroborated with the SEM findings. Roughness parameters were similar for TU implants, and reduced Sp and Spk values were observed for the AE implants after insertion. AN implants were more complex to measure quantitatively because of variations in the extent of damage to the oxide layer during insertion. In some cases, the AN layer had been completely removed, exposing the underlying material and clearly decreasing the roughness, and in other cases it remained intact and rough. Polyurethane foam blocks in contact with AN implants demonstrated loose titanium particles of different sizes. Conclusion: This preliminary study demonstrated surface damage after insertion of experimental anodized implants into polyurethane blocks associated with loose titanium particles at the interface. Future in vivo studies should investigate the relevance of such loose particles on the peri-implant bone response. Int J Oral Maxillofac Implants 2014;29:97–104. doi: 10.11607/jomi.3259 Key words: dental implants, osteolysis, surface characterization, surface roughness
T
he surfaces of modern dental implants have been treated to enhance osseointegration. Osseointegration can be characterized by primary and secondary
1Graduate
student, University of Rochester, Department of Biomedical Engineering, Division of Prosthodontics, Eastman Dental Center, University of Rochester, Rochester, New York, USA. 2Professor, Department of Biomaterials, Instituto Militar de Engenharia, Biomaterials Laboratory, Rio de Janeiro, RJ, Brazil. 3 Professor, University of Rochester, Department of Mechanical Engineering, Hajim School of Engineering and Applied Sciences, University of Rochester, Rochester, New York, USA. 4 Assistant Professor, University of Rochester, Eastman Institute for Oral Health, Rochester, New York, USA. Correspondence to: Prof Luiz Meirelles, Division of Prosthodontics, Eastman Dental Center, University of Rochester, 625 Elmwood Avenue, Rochester, NY 14620. Email: [email protected] This paper was presented at the Academy of Osseointegration annual meeting in Phoenix, Arizona, March 2, 2012. ©2014 by Quintessence Publishing Co Inc.
phases: Primary osseointegration is the physical contact between the implant and the surrounding bone, while secondary osseointegration is the biologic activity associated with bone healing that enhances the contact between the implant and the bone tissue.1 Following successful osseointegration, a dental implant will be secure and immobile in the surgical site. Micromovement within the surgical site can adversely affect the healing and remodeling of the bone tissue around the implant and can cause implant failure.2 Typically, surface treatments give the implant surface a higher degree of roughness than a turned implant, with the intent of increasing osseointegration. There are many different methods for increasing the surface roughness, which include grit blasting, acid etching, and anodization. Grit-blasted implants typically have irregular surfaces, with peaks and valleys measuring between 4 and 6 µm.3 Acid-etched implants have uniform roughness throughout their entire surface, with finer features between 1 and 3 µm.4 The oxide layer on the surface of an anodized implant can be 3 to 7 µm thick, along with a wide variety of surface features measuring 0.8 to 7 µm.5 The International Journal of Oral & Maxillofacial Implants 97
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15 mm
15
a
m m
20 mm
MATERIALS AND METHODS
b
c
d
e Fig 1 Polyurethane sample preparation. (a) Samples are cut to 15 × 15 × 20 mm. (b) Each sample is cut transversely. (c) A hole is drilled on the interface line. (d) The implant is placed in the interface line. (e) The sample is split in half for implant analysis.
It is unclear whether the increasingly complex surface features found on modern dental implants are retained after insertion. Dynamic finite element analysis was used to simulate the insertion process with an implant with a diameter of 4.5 mm and length of 11 mm into a construct of the mandible.6 While the simulation was in progress, the maximum von Mises stress concentrations appeared in different locations and at different magnitudes along the implant length and circumference. This dynamic shifting of stresses would indicate that not all of the implant is in contact with the bone material at the same time, or it is at least not experiencing the same degree of contact uniformly. Because of this nonuniform contact between bone and implant, it is possible that the insertion procedure itself could affect the integrity of an implant’s surface. With a smaller implant surface area in contact with bone material, stresses will be higher, which might increase the likelihood of a change in the surface. If the surface integrity is compromised, corresponding loose particles may be produced. This can have clinical implications, as it has been shown that, in sufficient quantities, titanium oxide debris can increase the activity of inflammatory cytokines such as interleukin-8 (IL-8), IL-6, and tumor necrosis factor alpha,7 which may inhibit new bone formation.8 Loose titanium particles released from turned surfaces were detected in periimplant bone9 and in regional lymph nodes released from plasma spray–coated implants.10 Furthermore, the surfaces of unloaded implants showed a slight reduction of roughness after healing periods of 12 weeks,11,12 indicating surface alterations after placement of the implants in bone. This study examined common types of dental implant surfaces and evaluated how they are affected by the insertion procedure. Comparisons between implants before and after insertion were made with scanning electron microscopy, and roughness analysis was performed with interferometry.
Titanium Implants A total of nine screw-shaped titanium implants (commercially pure titanium grade 3) with identical geometry (3.75 × 13 mm) were used for this investigation. Three implant groups were created: (1) acid-etched (AE), (2) anodized (AN), or (3) as turned (TU) (n = 3 implants in each group). Acid etching was done by immersion in a solution of sulfuric, nitric, and hydrofluoric acid. The surface of the anodized implant was modified by microarc oxidation treatment. A porous layer was formed on the titanium surface during the oxidation treatment. The experimental surface modifications were performed in the laboratory and may have different behavior during insertion compared to commercially available implants.
Polyurethane Foam Blocks
Polyurethane foam blocks (PFBs), grade 30 (SawBones) with a density of 0.48 g/cm3, were cut into smaller pieces measuring 15 × 15 × 20 mm with a diamondtipped band saw (Fig 1a). Grade 30 PFBs follow the guidelines of the American Society for Testing and Materials, with a compressive strength of 18 MPa and a compressive modulus of 445 MPa,11 and are widely used for mechanical testing of dental and orthopedic devices.12–14 Previous results suggested that grade 30 PFBs are similar to bone type 3 or 4, as observed in the anterior maxilla.14 Each piece was mounted on a cutting system (Model CP310, Exakt) and was sliced transversely to create a thin interface line between two halves. The two halves were then clamped tightly back together into the original configuration, creating a uniform block suitable for dismounting without any potential damage to the implant surface after insertion (Fig 1b).
Drilling and Implant Placement
The implantation site was prepared with an undersized drilling technique, as recommended by the manufacturers for types 3 and 4 bone. On the interface line, holes were drilled in sequence at 800 rpm, starting with a 2.0-mm pilot drill, followed by twist drills that were 2.0 mm, 3.0 mm, 3.15 mm, and 3.2 mm in diameter (Fig 1c). The implant was inserted at 25 rpm, and the torque never exceeded 37 Ncm during the procedure (Figs 1c and 1d). Samples were split into the two presectioned halves to retrieve the implant, which was easily removed (Fig 1e). Implants were sonicated for 15 minutes in acetone to remove any polyurethane debris from the surface that might compromise the roughness evaluation.
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a
b
Figs 2a and 2b Similar morphology of (a) preinserted and (b) postinserted TU implants (×1,500).
Surface Analysis
The surfaces were examined at the same locations before and after implant insertion. To evaluate which part of the implant was most susceptible to surface damage, the analyses were performed at three different areas: apical cutting edges, middle threads, and implant neck. Before and after insertion, the implants were examined in a scanning electron microscope (SEM) (Auriga SEM/FIB, Zeiss). Images were taken in secondary electron imaging mode at ×200 and ×1,500 with an accelerating voltage between 10 and 15 kV. Additionally, energy dispersive x-ray spectroscopy (EDX) mapping for titanium was performed on some polyurethane blocks to examine potential debris particles. Using an optical surface profilometer (Zygo 7100), the crest of threads of both pristine and postinsertion implants were measured using a ×20 lens in conjunction with an internal lens with ×0.75 magnification. Implant surface topography was measured as previously recommended,15 but in the present study this was limited to the crest of the threads. A Gaussian filter (size 50 × 50 µm) was selected to remove errors of form and waviness. All 20 threads of each implant were measured before and after implant insertion, for a total of 120 measurements/implant group. Extra care was taken to make sure that the thread surface was perpendicular to the light source to ensure the most accurate measurements of roughness parameters. The interferometric data were further processed (SPIP, Image Analysis A/S), and roughness parameters were calculated. The parameters were: • Sa, the average roughness of all heights present on the surface • Sdr, the percentage of additional surface area contributed by surface features when compared to a level plane
• Sds, the number of summits per square micron of a measured surface • Ssk, the symmetry of heights on the surface by the mean plane (positive values indicate a disproportionate amount of peaks, whereas negative values indicate the same for valleys) • Sku, the kurtosis or “peakedness” of the surface (Sku > 3.00 indicates the presence of extremes in height, while Sku < 3.00 indicates a lack of extremes and a more uniform surface) • Spk, a measurement of the peak heights above the core roughness (the higher the value, the higher probability the surface is made up of high peaks with small contact area and therefore high contact stress) • Sp, a measure of the height of the highest point on a surface
RESULTS SEM images of the TU implants showed no apparent changes in surface integrity after implant insertion (Figs 2a and 2b). At ×1,500, there were some finer marks related to the turning process that were not clearly affected, most likely attributable to individual peculiarities during manufacturing than from damage caused by insertion. The AE implants showed some surface damage at apical cutting threads (Figs 3a and 3b). At ×200, the crest of the cutting edge of the inserted implant was smoother than the rougher pristine implant’s cutting edge. At ×1,500, many of the smaller surface features were less prominent, indicating possible removal of material from the edge during implantation. The middle threads exhibited a minor degree of damage that was apparent only at ×1,500 (Figs 4a and 4b), and the neck region displayed almost no surface alterations. The International Journal of Oral & Maxillofacial Implants 99
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Mints et al
a
b
Figs 3a and 3b Apex region of (a) preinserted AE implant with intact surface and (b) flattened area, delimited by the arrows on the crest of the thread, revealing surface damage after insertion on the cutting edge (×1,500).
a
b
Figs 4a and 4b (a) Preinserted AE Implants with sharp peaks. (b) Postinserted implants with less prominent peaks associated with flattened areas on the crest of the threads (×1,500).
a
b
Figs 5a and 5b Apex region of (a) preinserted anodized implants with intact oxide layer and (b) clear damage after the insertion procedure (×1,500).
The AN implants exhibited the most evident surface damage. The apical cutting threads are subject to a particularly high amount of stress, and the damage was highly localized to this area. In the preinserted implants, the apical surfaces were intact with pores of
various diameters and depths. Postinserted implants exhibited a clear break in the oxide layer, exposing an underlying layer that had debris from the top layer (Figs 5a and 5b). In the middle threads, there were spots missing the oxide layer and an intensification of
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a
b
Figs 6a and 6b (a) Preinserted AN implant with intact oxide layer and (b) postinserted implant with clear damage to the oxide layer revealing the underlying bulk material of the crest of the threads (×1,500).
Figs 7a and 7b (a) The PFB surface after removal of an AN implant and (b) titanium elemental EDX mapping showing the titanium debris in the implantation site after removal of an AN implant (×1,500).
a
the cracks seen on the surface (Figs 6a and 6b). In the neck region, the oxide layer on both preinserted and postinserted implants was completely intact. SEM-EDX mapping was performed on one PFB block per group that had been in contact with the implants. No metal particles were detected on the PFB blocks that had been in contact with TU and AE implants. Titanium debris ranging from nano- to microparticles was found along the implantation site of the AN implant. A higher concentration of smaller particles was observed in the crestal region, and a few larger particles were observed in the midapical regions (Figs 7a and 7b). Surface roughness values processed from the interferometric measurements are summarized in Table 1. In the preinserted and postinserted groups, certain roughness parameters decreased, which coincided with the smoother images seen under SEM. The values that indicated surface damage during insertion of AE and AN implants were represented by a decrease of Sku (number of extreme peaks), Spk (peak heights above core roughness), and Sp (height of the highest peak).
b
DISCUSSION Modifying the surface of a dental implant has become common in modern oral rehabilitation. The rationale for the use of modified rather than machined surfaces is to increase implant primary stability and improve osseointegration. Higher primary stability is desirable, as it is conducive to osseointegration. Osteoblasts, the cells that govern bone formation, have been shown to be particularly attracted to rough surfaces.16 These surfaces seem to increase the differentiation of precursor cells into osteoblasts that have a superior ability to lay down bone matrix.17 It has been shown that, after 6 weeks of healing, AN implants show bone-implant contact (BIC) superior to that of machined implants.18 Similarly, AE implants showed a higher BIC than machined implants after 8 weeks of healing.19 High BIC is essential for extending the useful life span of implants.1 These properties make surface-modified implants ideal for clinical use. One group studied bone tissue that had been damaged by implantation and found that microcracks had The International Journal of Oral & Maxillofacial Implants 101
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Table 1 Preinsertion and Postinsertion Roughness Parameters for the Three Implant Groups Group/ measurement
Preinsertion
Postinsertion
TU Sa Sdr Sds Ssk Sku Spk Sp
0.15 (0.01) 0.32 (0.12) 0.029 (0.01) –0.35 (0.43) 4.25 (1.27) 0.21 (0.05) 0.79 (0.12)
0.13 (0.02) 0.26 (0.08) 0.025 (0.004) –0.47 (0.29) 4.46 (0.75) 0.18 (0.03) 0.68 (0.08)
AE Sa Sdr Sds Ssk Sku Spk Sp
0.32 (0.04) 3.98 (1.91) 0.047 (0.002) –0.20 (0.42) 4.20 (1.45) 0.47 (0.23) 2.20 (1.56)
0.36 (0.02) 8.92 (0.93) 0.062 (0.01) –0.33 (0.15) 3.45 (0.22) 0.39 (0.07) 1.69 (0.34) Stripped
Intact
AN Sa Sdr Sds Ssk Sku Spk Sp
0.45 (0.02) 12.75 (1.99) 0.039 (0.002) –0.32 (0.13) 4.87 (0.34) 0.73 (0.07) 3.60 (0.85)
0.36 (0.02) 10.91 (1.14) 0.051 (0.01) 0.18 (0.36) 3.98 (1.49) 0.53 (0.26) 2.30 (0.72)
0.47 (0.03) 13.07 (1.44) 0.041 (0.01) –0.01 (0.02) 4.60 (0.42) 0.76 (0.018) 3.45 (0.49)
TU implants demonstrated similar roughness values before and after implant insertion. AE implants showed a Sku that decreased by 0.75, Spk that decreased by 0.8, and Sp that was reduced by approximately 0.5 µm. These values indicate that the highest features of an implant have been affected by implantation and that the overall surface has fewer extremes in height, with all features closer to the mean height plane than before implantation. The parameters of the AN surfaces presented a more complicated scenario, as multiple layers of the surface were present for characterization. In the preinserted group, the original layer was characterized. In the postinserted group, there were some threads with intact surfaces and some threads that had the tops of threads almost completely stripped off. Where the original layer of the implant remained intact, the values calculated were similar. Where the bottom layer was exposed, parameters show a different surface, as indicated by a reduction of the number (Sku) and the height of the peaks (Spk and Sp). Units: Sa, Spk, and Sp (µm); Sdr (%),Sds (1/µm²). Ssk and Sku are unitless.
formed in the surrounding tissue when drilling with a maximum torque of 45 Ncm.20 Depending on the quality of bone and the number of cracks present, this could lead to osteolysis in the bone tissue and reduced stability. As can be seen by the damage done to the AN implant’s surface in the present study, it can be inferred that titanium debris may be present after implant placement. In addition, it has been shown that damage to the implant surface is not equal in all regions. Especially with AN implants, the apical region shows the most damage, while the middle region shows less and the neck is untouched. This result points to different stresses caused by dynamic contact with the
implant surface during insertion. As shown by Guan et al, different areas of the implant are in contact with bone material at different times, as opposed to the expected uniform contact.6 With all the torque concentrated on a smaller contact area versus the entire implant surface, higher localized stresses will result. A correlation between high stress and surface removal can be made, suggesting that more debris will be created in areas of higher stress. Wear particles of sufficient quantity have been shown to elicit a chronic inflammatory response, one of the leading causes of aseptic loosening of total hip replacements. Titanium particles have been shown to enhance the release of inflammatory cytokines, such as IL-6, IL-8, and tumor necrosis factor alpha.21,22 Thus, implant surface damage can adversely affect the healing of the surgical site. There is precedent for measuring the surface of dental implants with an interferometer.15 Previous studies have characterized the surfaces of many commercial implants, attempting to correlate findings with osseointegrative ability and other biologic activity. Studies have shown that increased roughness leads to an increase in BIC. Optimal average roughness of 1 to 2 µm has been suggested based on studies performed in rabbits23 and in humans.24 Given this wide range, the small changes in surface roughness caused by implant insertion should not significantly influence an implant’s potential for bone formation. Both the TU and AE implants showed a change in average roughness on the order of 10–2 µm, while the AN implants had a change on the order of 10–1 µm. What is of particular concern are the peak height measurements for these surfaces. Insertion yielded large decreases in peak heights for both AE (∆Sp = 0.51 µm) and AN implants (∆Sp = 1.3 µm), in contrast to the small change for TU implants (∆Sp = 0.12 µm). In addition, the surface damage to the AN implants was confirmed by the decrease of the peak heights above core roughness (SpK) of 0.2 µm, compared to 0.06 and 0.03 µm for AE and TU implants, respectively. These large changes, especially in the case of AN implants, indicate loose particles at the bone-implant interface, as demonstrated in Fig 7. Previous results indicated the presence of titanium particles up to 30 µm at the bone-implant interface of turned implants, as observed with SEM/ EDX, associated with higher titanium concentrations in the kidneys, liver, and lungs.9 In the present study, no loose titanium particles were seen on the polyurethane foams of TU and AE implants, but the minor differences observed in the roughness parameters could indicate that some titanium particles detached during insertion.
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In agreement with the present results, the roughness evaluation of two alumina-blasted (25- and 75-µm particles) implant groups before and after insertion demonstrated an overall decrease in the Sz (absolute values of the five highest peaks and deepest valleys) and St (distance between the highest peak and lowest valley) after 12 weeks in rabbits.25 One important observation was that the rough-blasted implant (75-µm particles) was more affected by the insertion/ removal torque procedure compared to the smoothblasted (25-µm particles) implant.25 There are a few limitations to the design of the current study. Whereas the polyurethane used as a substitute for bone exhibits a stress/strain curve similar to that of cancellous bone under compression, it is important to emphasize that this material is not meant to fully reproduce all aspects of bone tissue.26 The structural complexity of bone precludes accurate polymer re-creation. Despite this, polyurethane foam is commonly used to test dental implants and orthopedic devices; according to the American Society for Testing and Materials, PFB provides consistent and reproducible results for device testing.11 Other groups have used polyurethane for studies on dental implants. Tabassum et al carefully chose grade 30 polyurethane foam with a density of 0.48 g/cm3 to correspond with bone densities found in the anterior and posterior maxilla of 0.55 g/cm3 and 0.31 g/cm3, respectively.14 These approximately simulate types 3 and 4 bone and are common areas for implant placement. Future studies should continue examining the effects of insertion on the surface of implants. Implants used in a current clinical setting, which have not only micron-sized features but nanometer-sized features as well, undergo a similar insertion procedure. The nanosized structures could introduce more initial contact stress points and friction, increasing the amount of surface damage done to the implant. Furthermore, the clinical implications of nanometer-sized debris particles from these structures, along with micron-sized debris, may possibly include a significant increase in monocyte and neutrophil proliferation in the surgical site, leading to an intensified inflammatory reaction.
CONCLUSION As evidenced from the present in vitro study, the surfaces of treated dental implants demonstrated damage as a result of the insertion process. Acid-etched implants showed slight decreases of the peak height measurements. Surface changes were clearly found only on anodized implants, as sections of the thick oxide layer were stripped off, mostly on the tops of threads and the apical region, associated with loose titanium particles.
However, it is unclear whether the amount of oxide lost would be sufficient to affect bone formation and longterm success of the implant rehabilitation.
Acknowledgments The authors reported no conflicts of interest related to this study.
REFERENCES 1. Albrektsson T, Brånemark PI, Hansson HA, Lindstrom J. Osseointegrated titanium implants. Requirements for ensuring a long-lasting, direct bone-to-implant anchorage in man. Acta Orthop Scand 1981; 52:155–170. 2. Schatzker JMD, Horne JG , Sumner-Smith GB. The effect of movement on the holding power of screws in bone. Clin Orthop Relat Res 1975;111:257–262. 3. Ruger M, Gensior TJ, Herren C, et al. The removal of Al2O3 particles from grit-blasted titanium implant surfaces: Effects on biocompatibility, osseointegration and interface strength in vivo. Acta Biomater 2010;6:2852–2861. 4. Mata A, Su X, Fleischman AJ, et al. Osteoblast attachment to a textured surface in the absence of exogenous adhesion proteins. IEEE Trans Nanobiosci 2003;2:287–294. 5. Choi JW, Heo SJ, Koak JY, et al. Biological responses of anodized titanium implants under different current voltages. J Oral Rehabil 2006;33:889–897. 6. Guan H, van Staden RC, Johnson NW, Loo YC. Dynamic modelling and simulation of dental implant insertion process—A finite element study. Finite Elem Anal Des 2011;47:886–897. 7. Blaine TA, Rosier RN, Puzas JE, et al. Increased levels of tumor necrosis factor-alpha and interleukin-6 protein and messenger RNA in human peripheral blood monocytes due to titanium particles. J Bone Joint Surg Am 1996;78:1181–1192. 8. Tsutsui T, Kawaguchi H, Fujino A, Sakai A, Kaji H, Nakamura T. Exposure of macrophage-like cells to titanium particles does not affect bone resorption, but inhibits bone formation. J Orthop Sci 1999;4:32–38. 9. Schliephake H, Reiss G, Urban R, Neukam FW, Guckel S. Metal release from titanium fixtures during placement in the mandible: An experimental study. Int J Oral Maxillofac Implants 1993;8:502–511. 10. Weingart D, Steinemann S, Schilli W, et al. Titanium deposition in regional lymph nodes after insertion of titanium screw implants in maxillofacial region. Int J Oral Maxillofac Surg 1994;23:450–452. 11. American Society for Testing and Materials. ASTM F543. Standard Specification and Test Methods for Metallic Medical Bone Screws. West Conshohocken, PA: ASTM International, 2007. 12. Dos Santos MV, Elias CN, Cavalcanti Lima JH. The effects of superficial roughness and design on the primary stability of dental implants. Clin Implant Dent Relat Res 2011;13:215–223. 13. Gokce V, Oflaz H, Dulgeroglu A, Bora A, Gunal I. Kirschner wire fixation for scaphoid fractures: An experimental study in synthetic bones. J Hand Surg (Eur) 2011;36:325–328. 14. Tabassum A, Meijer GJ, Wolke JG, Jansen JA. Influence of surgical technique and surface roughness on the primary stability of an implant in artificial bone with different cortical thickness: A laboratory study. Clin Oral Implants Res 2010;21:213–220. 15. Wennerberg A, Albrektsson T. Suggested guidelines for the topographic evaluation of implant surfaces. Int J Oral Maxillofac Implants 2000;15:331–344. 16. Cooper LF. A role for surface topography in creating and maintaining bone at titanium endosseous implants. J Prosthet Dent 2000;84: 522–534. 17. Alves SF, Wassall T. In vitro evaluation of osteoblastic cell adhesion on machined osseointegrated implants. Braz Oral Res 2009;23:131–136.
The International Journal of Oral & Maxillofacial Implants 103 © 2014 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
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18. Pak HS, Yeo IS, Yang JH. A histomorphometric study of dental implants with different surface characteristics. J Adv Prosthodont 2010;2:142–147. 19. Trisi P, Lazzara R, Rebaudi A, Rao W, Testori T, Porter SS. Bone-implant contact on machined and dual acid-etched surfaces after 2 months of healing in the human maxilla. J Periodontol 2003;74:945–956. 20. Bartold PM, Kuliwaba JS, Lee V, Shah S, Marino V, Fazzalari NL. Influence of surface roughness and shape on microdamage of the osseous surface adjacent to titanium dental implants. Clin Oral Implants Res 2011;22:613–618. 21. Bukata SV, Gelinas J, Wei X, et al. PGE2 and IL-6 production by fibroblasts in response to titanium wear debris particles is mediated through a Cox-2 dependent pathway. J Orthop Res 2004;22:6–12. 22. Goodman SB, Ma T. Cellular chemotaxis induced by wear particles from joint replacements. Biomaterials 2010;31:5045–5050.
23. Wennerberg A, Albrektsson T, Andersson B, Krol JJ. A histomorphometric and removal torque study of screw-shaped titanium implants with three different surface topographies. Clin Oral Implants Res 1995;6:24–30. 24. Ivanoff CJ, Widmark G, Johansson C, Wennerberg A. Histologic evaluation of bone response to oxidized and turned titanium microimplants in human jawbone. Int J Oral Maxillofac Implants 2003;18: 341–348. 25. Wennerberg A, Albrektsson T, Lausmaa J. Torque and histomorphometric evaluation of c.p. titanium screws blasted with 25- and 75-microns-sized particles of Al2O3. J Biomed Mater Res 1996;30:251–260. 26. Szivek JA, Thomas M, Benjamin JB. Characterization of a synthetic foam as a model for human cancellous bone. J Appl Biomater 1993; 4:269–272.
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T
he surfaces of modern dental implants have been treated to enhance osseointegration. Osseointegration can be characterized by primary and secondary
1Graduate
student, University of Rochester, Department of Biomedical Engineering, Division of Prosthodontics, Eastman Dental Center, University of Rochester, Rochester, New York, USA. 2Professor, Department of Biomaterials, Instituto Militar de Engenharia, Biomaterials Laboratory, Rio de Janeiro, RJ, Brazil. 3 Professor, University of Rochester, Department of Mechanical Engineering, Hajim School of Engineering and Applied Sciences, University of Rochester, Rochester, New York, USA. 4 Assistant Professor, University of Rochester, Eastman Institute for Oral Health, Rochester, New York, USA. Correspondence to: Prof Luiz Meirelles, Division of Prosthodontics, Eastman Dental Center, University of Rochester, 625 Elmwood Avenue, Rochester, NY 14620. Email: [email protected] This paper was presented at the Academy of Osseointegration annual meeting in Phoenix, Arizona, March 2, 2012. ©2014 by Quintessence Publishing Co Inc.
phases: Primary osseointegration is the physical contact between the implant and the surrounding bone, while secondary osseointegration is the biologic activity associated with bone healing that enhances the contact between the implant and the bone tissue.1 Following successful osseointegration, a dental implant will be secure and immobile in the surgical site. Micromovement within the surgical site can adversely affect the healing and remodeling of the bone tissue around the implant and can cause implant failure.2 Typically, surface treatments give the implant surface a higher degree of roughness than a turned implant, with the intent of increasing osseointegration. There are many different methods for increasing the surface roughness, which include grit blasting, acid etching, and anodization. Grit-blasted implants typically have irregular surfaces, with peaks and valleys measuring between 4 and 6 µm.3 Acid-etched implants have uniform roughness throughout their entire surface, with finer features between 1 and 3 µm.4 The oxide layer on the surface of an anodized implant can be 3 to 7 µm thick, along with a wide variety of surface features measuring 0.8 to 7 µm.5 The International Journal of Oral & Maxillofacial Implants 97
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Mints et al
15 mm
15
a
m m
20 mm
MATERIALS AND METHODS
b
c
d
e Fig 1 Polyurethane sample preparation. (a) Samples are cut to 15 × 15 × 20 mm. (b) Each sample is cut transversely. (c) A hole is drilled on the interface line. (d) The implant is placed in the interface line. (e) The sample is split in half for implant analysis.
It is unclear whether the increasingly complex surface features found on modern dental implants are retained after insertion. Dynamic finite element analysis was used to simulate the insertion process with an implant with a diameter of 4.5 mm and length of 11 mm into a construct of the mandible.6 While the simulation was in progress, the maximum von Mises stress concentrations appeared in different locations and at different magnitudes along the implant length and circumference. This dynamic shifting of stresses would indicate that not all of the implant is in contact with the bone material at the same time, or it is at least not experiencing the same degree of contact uniformly. Because of this nonuniform contact between bone and implant, it is possible that the insertion procedure itself could affect the integrity of an implant’s surface. With a smaller implant surface area in contact with bone material, stresses will be higher, which might increase the likelihood of a change in the surface. If the surface integrity is compromised, corresponding loose particles may be produced. This can have clinical implications, as it has been shown that, in sufficient quantities, titanium oxide debris can increase the activity of inflammatory cytokines such as interleukin-8 (IL-8), IL-6, and tumor necrosis factor alpha,7 which may inhibit new bone formation.8 Loose titanium particles released from turned surfaces were detected in periimplant bone9 and in regional lymph nodes released from plasma spray–coated implants.10 Furthermore, the surfaces of unloaded implants showed a slight reduction of roughness after healing periods of 12 weeks,11,12 indicating surface alterations after placement of the implants in bone. This study examined common types of dental implant surfaces and evaluated how they are affected by the insertion procedure. Comparisons between implants before and after insertion were made with scanning electron microscopy, and roughness analysis was performed with interferometry.
Titanium Implants A total of nine screw-shaped titanium implants (commercially pure titanium grade 3) with identical geometry (3.75 × 13 mm) were used for this investigation. Three implant groups were created: (1) acid-etched (AE), (2) anodized (AN), or (3) as turned (TU) (n = 3 implants in each group). Acid etching was done by immersion in a solution of sulfuric, nitric, and hydrofluoric acid. The surface of the anodized implant was modified by microarc oxidation treatment. A porous layer was formed on the titanium surface during the oxidation treatment. The experimental surface modifications were performed in the laboratory and may have different behavior during insertion compared to commercially available implants.
Polyurethane Foam Blocks
Polyurethane foam blocks (PFBs), grade 30 (SawBones) with a density of 0.48 g/cm3, were cut into smaller pieces measuring 15 × 15 × 20 mm with a diamondtipped band saw (Fig 1a). Grade 30 PFBs follow the guidelines of the American Society for Testing and Materials, with a compressive strength of 18 MPa and a compressive modulus of 445 MPa,11 and are widely used for mechanical testing of dental and orthopedic devices.12–14 Previous results suggested that grade 30 PFBs are similar to bone type 3 or 4, as observed in the anterior maxilla.14 Each piece was mounted on a cutting system (Model CP310, Exakt) and was sliced transversely to create a thin interface line between two halves. The two halves were then clamped tightly back together into the original configuration, creating a uniform block suitable for dismounting without any potential damage to the implant surface after insertion (Fig 1b).
Drilling and Implant Placement
The implantation site was prepared with an undersized drilling technique, as recommended by the manufacturers for types 3 and 4 bone. On the interface line, holes were drilled in sequence at 800 rpm, starting with a 2.0-mm pilot drill, followed by twist drills that were 2.0 mm, 3.0 mm, 3.15 mm, and 3.2 mm in diameter (Fig 1c). The implant was inserted at 25 rpm, and the torque never exceeded 37 Ncm during the procedure (Figs 1c and 1d). Samples were split into the two presectioned halves to retrieve the implant, which was easily removed (Fig 1e). Implants were sonicated for 15 minutes in acetone to remove any polyurethane debris from the surface that might compromise the roughness evaluation.
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a
b
Figs 2a and 2b Similar morphology of (a) preinserted and (b) postinserted TU implants (×1,500).
Surface Analysis
The surfaces were examined at the same locations before and after implant insertion. To evaluate which part of the implant was most susceptible to surface damage, the analyses were performed at three different areas: apical cutting edges, middle threads, and implant neck. Before and after insertion, the implants were examined in a scanning electron microscope (SEM) (Auriga SEM/FIB, Zeiss). Images were taken in secondary electron imaging mode at ×200 and ×1,500 with an accelerating voltage between 10 and 15 kV. Additionally, energy dispersive x-ray spectroscopy (EDX) mapping for titanium was performed on some polyurethane blocks to examine potential debris particles. Using an optical surface profilometer (Zygo 7100), the crest of threads of both pristine and postinsertion implants were measured using a ×20 lens in conjunction with an internal lens with ×0.75 magnification. Implant surface topography was measured as previously recommended,15 but in the present study this was limited to the crest of the threads. A Gaussian filter (size 50 × 50 µm) was selected to remove errors of form and waviness. All 20 threads of each implant were measured before and after implant insertion, for a total of 120 measurements/implant group. Extra care was taken to make sure that the thread surface was perpendicular to the light source to ensure the most accurate measurements of roughness parameters. The interferometric data were further processed (SPIP, Image Analysis A/S), and roughness parameters were calculated. The parameters were: • Sa, the average roughness of all heights present on the surface • Sdr, the percentage of additional surface area contributed by surface features when compared to a level plane
• Sds, the number of summits per square micron of a measured surface • Ssk, the symmetry of heights on the surface by the mean plane (positive values indicate a disproportionate amount of peaks, whereas negative values indicate the same for valleys) • Sku, the kurtosis or “peakedness” of the surface (Sku > 3.00 indicates the presence of extremes in height, while Sku < 3.00 indicates a lack of extremes and a more uniform surface) • Spk, a measurement of the peak heights above the core roughness (the higher the value, the higher probability the surface is made up of high peaks with small contact area and therefore high contact stress) • Sp, a measure of the height of the highest point on a surface
RESULTS SEM images of the TU implants showed no apparent changes in surface integrity after implant insertion (Figs 2a and 2b). At ×1,500, there were some finer marks related to the turning process that were not clearly affected, most likely attributable to individual peculiarities during manufacturing than from damage caused by insertion. The AE implants showed some surface damage at apical cutting threads (Figs 3a and 3b). At ×200, the crest of the cutting edge of the inserted implant was smoother than the rougher pristine implant’s cutting edge. At ×1,500, many of the smaller surface features were less prominent, indicating possible removal of material from the edge during implantation. The middle threads exhibited a minor degree of damage that was apparent only at ×1,500 (Figs 4a and 4b), and the neck region displayed almost no surface alterations. The International Journal of Oral & Maxillofacial Implants 99
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b
Figs 3a and 3b Apex region of (a) preinserted AE implant with intact surface and (b) flattened area, delimited by the arrows on the crest of the thread, revealing surface damage after insertion on the cutting edge (×1,500).
a
b
Figs 4a and 4b (a) Preinserted AE Implants with sharp peaks. (b) Postinserted implants with less prominent peaks associated with flattened areas on the crest of the threads (×1,500).
a
b
Figs 5a and 5b Apex region of (a) preinserted anodized implants with intact oxide layer and (b) clear damage after the insertion procedure (×1,500).
The AN implants exhibited the most evident surface damage. The apical cutting threads are subject to a particularly high amount of stress, and the damage was highly localized to this area. In the preinserted implants, the apical surfaces were intact with pores of
various diameters and depths. Postinserted implants exhibited a clear break in the oxide layer, exposing an underlying layer that had debris from the top layer (Figs 5a and 5b). In the middle threads, there were spots missing the oxide layer and an intensification of
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Figs 6a and 6b (a) Preinserted AN implant with intact oxide layer and (b) postinserted implant with clear damage to the oxide layer revealing the underlying bulk material of the crest of the threads (×1,500).
Figs 7a and 7b (a) The PFB surface after removal of an AN implant and (b) titanium elemental EDX mapping showing the titanium debris in the implantation site after removal of an AN implant (×1,500).
a
the cracks seen on the surface (Figs 6a and 6b). In the neck region, the oxide layer on both preinserted and postinserted implants was completely intact. SEM-EDX mapping was performed on one PFB block per group that had been in contact with the implants. No metal particles were detected on the PFB blocks that had been in contact with TU and AE implants. Titanium debris ranging from nano- to microparticles was found along the implantation site of the AN implant. A higher concentration of smaller particles was observed in the crestal region, and a few larger particles were observed in the midapical regions (Figs 7a and 7b). Surface roughness values processed from the interferometric measurements are summarized in Table 1. In the preinserted and postinserted groups, certain roughness parameters decreased, which coincided with the smoother images seen under SEM. The values that indicated surface damage during insertion of AE and AN implants were represented by a decrease of Sku (number of extreme peaks), Spk (peak heights above core roughness), and Sp (height of the highest peak).
b
DISCUSSION Modifying the surface of a dental implant has become common in modern oral rehabilitation. The rationale for the use of modified rather than machined surfaces is to increase implant primary stability and improve osseointegration. Higher primary stability is desirable, as it is conducive to osseointegration. Osteoblasts, the cells that govern bone formation, have been shown to be particularly attracted to rough surfaces.16 These surfaces seem to increase the differentiation of precursor cells into osteoblasts that have a superior ability to lay down bone matrix.17 It has been shown that, after 6 weeks of healing, AN implants show bone-implant contact (BIC) superior to that of machined implants.18 Similarly, AE implants showed a higher BIC than machined implants after 8 weeks of healing.19 High BIC is essential for extending the useful life span of implants.1 These properties make surface-modified implants ideal for clinical use. One group studied bone tissue that had been damaged by implantation and found that microcracks had The International Journal of Oral & Maxillofacial Implants 101
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Table 1 Preinsertion and Postinsertion Roughness Parameters for the Three Implant Groups Group/ measurement
Preinsertion
Postinsertion
TU Sa Sdr Sds Ssk Sku Spk Sp
0.15 (0.01) 0.32 (0.12) 0.029 (0.01) –0.35 (0.43) 4.25 (1.27) 0.21 (0.05) 0.79 (0.12)
0.13 (0.02) 0.26 (0.08) 0.025 (0.004) –0.47 (0.29) 4.46 (0.75) 0.18 (0.03) 0.68 (0.08)
AE Sa Sdr Sds Ssk Sku Spk Sp
0.32 (0.04) 3.98 (1.91) 0.047 (0.002) –0.20 (0.42) 4.20 (1.45) 0.47 (0.23) 2.20 (1.56)
0.36 (0.02) 8.92 (0.93) 0.062 (0.01) –0.33 (0.15) 3.45 (0.22) 0.39 (0.07) 1.69 (0.34) Stripped
Intact
AN Sa Sdr Sds Ssk Sku Spk Sp
0.45 (0.02) 12.75 (1.99) 0.039 (0.002) –0.32 (0.13) 4.87 (0.34) 0.73 (0.07) 3.60 (0.85)
0.36 (0.02) 10.91 (1.14) 0.051 (0.01) 0.18 (0.36) 3.98 (1.49) 0.53 (0.26) 2.30 (0.72)
0.47 (0.03) 13.07 (1.44) 0.041 (0.01) –0.01 (0.02) 4.60 (0.42) 0.76 (0.018) 3.45 (0.49)
TU implants demonstrated similar roughness values before and after implant insertion. AE implants showed a Sku that decreased by 0.75, Spk that decreased by 0.8, and Sp that was reduced by approximately 0.5 µm. These values indicate that the highest features of an implant have been affected by implantation and that the overall surface has fewer extremes in height, with all features closer to the mean height plane than before implantation. The parameters of the AN surfaces presented a more complicated scenario, as multiple layers of the surface were present for characterization. In the preinserted group, the original layer was characterized. In the postinserted group, there were some threads with intact surfaces and some threads that had the tops of threads almost completely stripped off. Where the original layer of the implant remained intact, the values calculated were similar. Where the bottom layer was exposed, parameters show a different surface, as indicated by a reduction of the number (Sku) and the height of the peaks (Spk and Sp). Units: Sa, Spk, and Sp (µm); Sdr (%),Sds (1/µm²). Ssk and Sku are unitless.
formed in the surrounding tissue when drilling with a maximum torque of 45 Ncm.20 Depending on the quality of bone and the number of cracks present, this could lead to osteolysis in the bone tissue and reduced stability. As can be seen by the damage done to the AN implant’s surface in the present study, it can be inferred that titanium debris may be present after implant placement. In addition, it has been shown that damage to the implant surface is not equal in all regions. Especially with AN implants, the apical region shows the most damage, while the middle region shows less and the neck is untouched. This result points to different stresses caused by dynamic contact with the
implant surface during insertion. As shown by Guan et al, different areas of the implant are in contact with bone material at different times, as opposed to the expected uniform contact.6 With all the torque concentrated on a smaller contact area versus the entire implant surface, higher localized stresses will result. A correlation between high stress and surface removal can be made, suggesting that more debris will be created in areas of higher stress. Wear particles of sufficient quantity have been shown to elicit a chronic inflammatory response, one of the leading causes of aseptic loosening of total hip replacements. Titanium particles have been shown to enhance the release of inflammatory cytokines, such as IL-6, IL-8, and tumor necrosis factor alpha.21,22 Thus, implant surface damage can adversely affect the healing of the surgical site. There is precedent for measuring the surface of dental implants with an interferometer.15 Previous studies have characterized the surfaces of many commercial implants, attempting to correlate findings with osseointegrative ability and other biologic activity. Studies have shown that increased roughness leads to an increase in BIC. Optimal average roughness of 1 to 2 µm has been suggested based on studies performed in rabbits23 and in humans.24 Given this wide range, the small changes in surface roughness caused by implant insertion should not significantly influence an implant’s potential for bone formation. Both the TU and AE implants showed a change in average roughness on the order of 10–2 µm, while the AN implants had a change on the order of 10–1 µm. What is of particular concern are the peak height measurements for these surfaces. Insertion yielded large decreases in peak heights for both AE (∆Sp = 0.51 µm) and AN implants (∆Sp = 1.3 µm), in contrast to the small change for TU implants (∆Sp = 0.12 µm). In addition, the surface damage to the AN implants was confirmed by the decrease of the peak heights above core roughness (SpK) of 0.2 µm, compared to 0.06 and 0.03 µm for AE and TU implants, respectively. These large changes, especially in the case of AN implants, indicate loose particles at the bone-implant interface, as demonstrated in Fig 7. Previous results indicated the presence of titanium particles up to 30 µm at the bone-implant interface of turned implants, as observed with SEM/ EDX, associated with higher titanium concentrations in the kidneys, liver, and lungs.9 In the present study, no loose titanium particles were seen on the polyurethane foams of TU and AE implants, but the minor differences observed in the roughness parameters could indicate that some titanium particles detached during insertion.
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In agreement with the present results, the roughness evaluation of two alumina-blasted (25- and 75-µm particles) implant groups before and after insertion demonstrated an overall decrease in the Sz (absolute values of the five highest peaks and deepest valleys) and St (distance between the highest peak and lowest valley) after 12 weeks in rabbits.25 One important observation was that the rough-blasted implant (75-µm particles) was more affected by the insertion/ removal torque procedure compared to the smoothblasted (25-µm particles) implant.25 There are a few limitations to the design of the current study. Whereas the polyurethane used as a substitute for bone exhibits a stress/strain curve similar to that of cancellous bone under compression, it is important to emphasize that this material is not meant to fully reproduce all aspects of bone tissue.26 The structural complexity of bone precludes accurate polymer re-creation. Despite this, polyurethane foam is commonly used to test dental implants and orthopedic devices; according to the American Society for Testing and Materials, PFB provides consistent and reproducible results for device testing.11 Other groups have used polyurethane for studies on dental implants. Tabassum et al carefully chose grade 30 polyurethane foam with a density of 0.48 g/cm3 to correspond with bone densities found in the anterior and posterior maxilla of 0.55 g/cm3 and 0.31 g/cm3, respectively.14 These approximately simulate types 3 and 4 bone and are common areas for implant placement. Future studies should continue examining the effects of insertion on the surface of implants. Implants used in a current clinical setting, which have not only micron-sized features but nanometer-sized features as well, undergo a similar insertion procedure. The nanosized structures could introduce more initial contact stress points and friction, increasing the amount of surface damage done to the implant. Furthermore, the clinical implications of nanometer-sized debris particles from these structures, along with micron-sized debris, may possibly include a significant increase in monocyte and neutrophil proliferation in the surgical site, leading to an intensified inflammatory reaction.
CONCLUSION As evidenced from the present in vitro study, the surfaces of treated dental implants demonstrated damage as a result of the insertion process. Acid-etched implants showed slight decreases of the peak height measurements. Surface changes were clearly found only on anodized implants, as sections of the thick oxide layer were stripped off, mostly on the tops of threads and the apical region, associated with loose titanium particles.
However, it is unclear whether the amount of oxide lost would be sufficient to affect bone formation and longterm success of the implant rehabilitation.
Acknowledgments The authors reported no conflicts of interest related to this study.
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18. Pak HS, Yeo IS, Yang JH. A histomorphometric study of dental implants with different surface characteristics. J Adv Prosthodont 2010;2:142–147. 19. Trisi P, Lazzara R, Rebaudi A, Rao W, Testori T, Porter SS. Bone-implant contact on machined and dual acid-etched surfaces after 2 months of healing in the human maxilla. J Periodontol 2003;74:945–956. 20. Bartold PM, Kuliwaba JS, Lee V, Shah S, Marino V, Fazzalari NL. Influence of surface roughness and shape on microdamage of the osseous surface adjacent to titanium dental implants. Clin Oral Implants Res 2011;22:613–618. 21. Bukata SV, Gelinas J, Wei X, et al. PGE2 and IL-6 production by fibroblasts in response to titanium wear debris particles is mediated through a Cox-2 dependent pathway. J Orthop Res 2004;22:6–12. 22. Goodman SB, Ma T. Cellular chemotaxis induced by wear particles from joint replacements. Biomaterials 2010;31:5045–5050.
23. Wennerberg A, Albrektsson T, Andersson B, Krol JJ. A histomorphometric and removal torque study of screw-shaped titanium implants with three different surface topographies. Clin Oral Implants Res 1995;6:24–30. 24. Ivanoff CJ, Widmark G, Johansson C, Wennerberg A. Histologic evaluation of bone response to oxidized and turned titanium microimplants in human jawbone. Int J Oral Maxillofac Implants 2003;18: 341–348. 25. Wennerberg A, Albrektsson T, Lausmaa J. Torque and histomorphometric evaluation of c.p. titanium screws blasted with 25- and 75-microns-sized particles of Al2O3. J Biomed Mater Res 1996;30:251–260. 26. Szivek JA, Thomas M, Benjamin JB. Characterization of a synthetic foam as a model for human cancellous bone. J Appl Biomater 1993; 4:269–272.
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