Ó 2014 Eur J Oral Sci
Eur J Oral Sci 2014; 122: 303–309 DOI: 10.1111/eos.12133 Printed in Singapore. All rights reserved
European Journal of Oral Sciences
Effect of implant design and bioactive glass coating on biomechanical properties of fiber-reinforced composite implants Ballo AM, Akca E, Ozen T, Moritz N, Lassila L, Vallittu P, N€ arhi T. Effect of implant design and bioactive glass coating on biomechanical properties of fiberreinforced composite implants. Eur J Oral Sci 2014; 122: 303–309. © 2014 Eur J Oral Sci This study aimed to evaluate the influence of implant design and bioactive glass (BAG) coating on the response of bone to fiber-reinforced composite (FRC) implants. Three different FRC implant types were manufactured for the study: nonthreaded implants with a BAG coating; threaded implants with a BAG coating; and threaded implants with a grit-blasted surface. Thirty-six implants (six implants for each group per time point) were installed in the tibiae of six pigs. After an implantation period of 4 and 12 wk, the implants were retrieved and prepared for micro-computed tomography (micro-CT), push-out testing, and scanning electron microscopy analysis. Micro-CT demonstrated that the screw-threads and implant structure remained undamaged during the installation. The threaded FRC/BAG implants had the highest bone volume after 12 wk of implantation. The push-out strengths of the threaded FRC/BAG implants after 4 and 12 wk (463°N and 676°N, respectively) were significantly higher than those of the threaded FRC implants (416°N and 549°N, respectively) and the nonthreaded FRC/BAG implants (219°N and 430°N, respectively). Statistically significant correlation was found between bone volume and push-out strength values. This study showed that osseointegrated FRC implants can withstand the static loading up to failure without fracture, and that the addition of BAG significantly improves the push-out strength of FRC implants.
The long-term clinical success of oral implants is based on the presence and maintenance of a proper bone response and a safe and effective load transfer from the prosthesis to the bone. Bone responses to implant materials can be characterized as connective tissue capsulation (1) or direct bone contact with the implant surface (osseointegration) (2–5). The long-term success of oral implants relies on direct anchorage to bone. Several factors can be considered as important for successful osseointegration (6): the material properties of an implant, the implant design, the surface configuration of the implant, host tissue, the surgical technique, and loading conditions. The first three factors are related to the choice of implant material. The most important surface properties are topography, chemistry, surface charge, and wettability (7). Poor primary stability and implant micromotion have been considered as the main causes for implant failure (8, 9). Good primary stability is usually obtained by using the proper surgical technique and appropriate hardware (10). Implant surface topography also plays an important role (11).
Ahmed M. Ballo1,2, Eralp Akca3, Tuncer Ozen3, Niko Moritz4, Lippo Lassila5, Pekka Vallittu5, €rhi6 Timo Na 1
Department of Oral Health Sciences, University of British Columbia Faculty of Dentistry, Vancouver, BC, Canada; 2Dental Implant and Osseointegration Research Chair, College of Dentistry, King Saud University, Riyadh, Saudi Arabia; 3 Department of Periodontology, Dental Sciences Center, Gulhane Military Medical Academy, Ankara, Turkey; 4Orthopedic Research Unit, Department of Orthopedic Surgery and Traumatology, University of Turku, Turku, Finland; 5Department of Biomaterials Science, Institute of Dentistry, University of Turku, Turku, Finland; 6 Department of Prosthetic Dentistry, Institute of Dentistry, University of Turku, Turku, Finland
Dr Ahmed Ballo, Department of Oral Health Sciences, University of British Columbia Faculty of Dentistry, JBM 256 - 2199 Wesbrook Mall, Vancouver, BC, Canada, V6T 1Z3 E-mail: [email protected] Key words: bioactive glass; biomechanics; dental implant; fiber-reinforced composite; osseointegration Accepted for publication April 2014
In the case of titanium implants, occlusal forces are transmitted from the rigid implant material to the bone of lower modulus of elasticity. None of the commercially available oral implants can adapt to occlusal loads in the same way as a natural tooth with a sound periodontal ligament. Several different implant designs have been introduced that aim to optimize mechanical loading conditions. In poor bone conditions, the mismatch of stiffness between bone and a metallic implant may lead to treatment failure (12). This occurs when the tensile or compressive load exceeds the physiological limit of bone tolerance, causing microfracture at the bone-to-implant interface or initiating bone resorption (13). Fiber-reinforced composites (FRC) are durable materials, with strength and modulus of elasticity that can be adapted to the physiological properties of bone (14). Fiber-reinforced composite materials have been used in restorative and prosthetic dentistry for many years. There has been interest in using FRC implants for load-bearing applications in orthopedic and head and
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neck surgery (15–17), which make them interesting materials also as oral implants. In our earlier studies, FRC implants showed good mechanical performance in the laboratory environment (14, 18). Furthermore, it was found that FRC materials do not elicit cytotoxic responses with osteoblast-like cells (19, 20) and human gingival fibroblasts (21) in cell-culture conditions and can therefore be considered as cytocompatible. The smooth FRC surface was shown to increase cell adhesion, spreading, and proliferation after 4 d of culture when compared with tissue-culture polystyrene (20). Rough and porous FRC surfaces, on the other hand, seem to enhance osteoblast proliferation and the formation of mineralized extracellular matrix (19, 20). Bioactivity has been defined as the interaction of cells with the implant surface that facilitates peri-implant bone regeneration, allowing the implant to form a biologic bond with living tissue (22). Bioactive glass (BAG) facilitates biologic bone bonding (23–25). A good osteoconductive property has also been observed with BAG-coated FRC by enhancing bone healing in the close vicinity of the coated implants (16). Our previous histomorphometric study showed that the polymer surface allows equal bone formation with titanium after 4 and 12 wk of healing (26). Both gritblasted and BAG-coated FRC implants established direct bone contact and showed no toxicity during the 4- and 12-wk healing periods. The purpose of this study was to evaluate the effect of implant designs and surface modifications on the biomechanical responses of FRC implants in vivo.
Material and methods Preparation of experimental implants Three different groups of FRC implants with a length of 10 mm and a diameter of 4.1 mm were fabricated for the study: BAG-coated non-threaded FRC implants; gritblasted threaded FRC implants; and BAG-coated threaded FRC implants. Scanning electron microscopy images of threaded FRC implants are shown in Fig. 1. The implants were made of E-glass FRC. The fabrication process of FRC implants has been described in detail in our previous study (18).
A
Briefly, the implants consisted of five fiber-reinforcement bundles, each consisting of 4,000 continuous unidirectional E-glass fibers (approximately 15 lm in diameter). The fiber bundle was impregnated manually in light-polymerizable bisphenyl A glycidyl methacrylate-triethyleneglycol dimethacrylate (bisGMA-TEGDMA) Stick (Stich Tech, Turku, Finland) resin. The composition of fibers was: 55% SiO2, 15% Al2O3, 22% CaO, 6% B2O3, 0.5% MgO, and >1.0% Fe+Na+K. The implant threads were reinforced by adding bidirectional fiber weave around the threads. Commercially available BAG (S53P4; Vivoxid, Turku, Finland) granules, of 0.01). At 12 wk post-implantation, the bone volumes were 23% and 56%, respectively, with a significantly greater bone volume on FRC/BAG implants (P < 0.01). Push-out test
The results of the push-out test are shown in Fig. 7. The bonding forces of threaded FRC/BAG implants after 4 and 12 wk (463°N and 676°N, respectively) were significantly higher than those of threaded FRC implants (416°N and 549°N, respectively P < 0.0001) and non-threaded FRC/BAG implants (219°N and 430°N, respectively, P < 0.0001). No significant differences had occurred between the threaded experimental implants after 4 wk. Significant correlation was found between BV/TV and the push-out force (r = 0.83), which indicates that the BV/TV, at a higher push-out strength of FRC/ BAG, is closely linked to better peri-implant bone formation.
Fig. 6. Mean values of relative bone volume between the threads of experimental threaded fiber-reinforced composite (FRC) implants analyzed by micro-computed tomography (micro-CT), 4 and 12 wk after implantation. Light-grey bars, threaded FRC; dark-grey bars, threaded FRC/bioactive glass (BAG).
signs of delamination, breakdown, or change in thickness of the BAG coating were observed. In all threaded implants, fracture occurred at the level of the thread crests. In the FRC/BAG implants, newly formed bone had filled the thread areas and stayed in immediate contact with the BAG coating after the push-out test (Figs 8 and 9), whereas in nonthreaded FRC/BAG implants, fracture occurred at the implant–bone interface.
Scanning electron microscopy
Scanning electron microscopy analysis revealed that all FRC implants remained sound after the push-out test, the screw-threads and implant configuration being well maintained. Regardless of the study time point, no
Discussion Implant fixation in the surrounding bone is basically a result of friction, mechanical interlock, and chemical
A
B
C
D
E
F
Fig. 5. Micro-computed tomography images illustrate bone growth in close contact with bioactive glass (BAG)-coated non-threaded fiber-reinforced composite (FRC) implants (A, D), with sandblasted threaded FRC implants (B, E) and with BAG-coated threaded FRC implants (C, F), 4 wk (upper row) and 12 wk (lower row) after implantation.
Bone response of fiber-reinforced composite implants
307
A
Fig. 7. Mean push-out strength values of experimental fiberreinforced composite (FRC) implants. The horizontal line above the bars represents homogeneous subsets (Tukey’s posthoc test). Dark-grey bars, 4 wk after implantation; light-grey bars, 12 wk after implantation.
bonding. Macro- and microtexture are other factors that determine shear movement. Macrotexture, for example, is provided by screw threads, whereas microtexture is related to dimensions that are created by surface-treatment procedures. Besides the surface condition of the implant material, specific bulk mechanical properties can affect the push-out strength. The mechanical properties of FRCs resemble the modulus of bone. However, despite the encouraging in vitro mechanical and histological results, the bone-bonding strength of BAG-coated and non-coated FRC implants were not known. The fact that new-bone apposition was detected between the implant threads suggests good biocompatibility of the FRC implants. The enhanced bone anchorage of BAG-coated FRC implants was not surprising as the BAG used in this study has been shown to promote bone formation in many previous investigations (25–29). However, with the exception of measuring direct bone-to-implant contact, investigation of trabecular bone structure around implants with micro-CT alone is not a very reliable method for the characterization of bone structure.
Fig. 8. Photograph (inset) and scanning electron microscopy micrograph of the fracture surface of a threaded and sandblasted fiber-reinforced composite (FRC) implant after the push-out test. Fracture occurred through the crestal level of FRC threads, suggesting that the main cause of failure was low cohesive shear strength of bone.
B
Fig. 9. Scanning electron microscopy micrographs of the fracture surface of the threaded fiber-reinforced composite (FRC) implants, with and without bioactive glass (BAG) coating, after the push-out test. Fracture occurred within the bone and not at the bone–implant interface. In the FRC/ BAG implants, newly formed bone filled the thread areas in immediate contact with the BAG coating.
et al. (30) noted that pull-out and pushBRANEMARK out tests measure peri-implant bone quality, as, by definition, the bone surrounding the implant fractures during the experiment. Although the push-out test is a better measure of the mechanical properties of bone around the implant and the strength of the coating– implant interface than of the shear strength of the bone–implant interface, from a clinical perspective, push-out data still provide valid information about how strongly an implant is anchored in the bone. The present study showed a significant improvement in the interfacial bond strength of the FRC/BAG implant with increasing healing time. In this study, statistical unit was an implant. Having an animal as a statistical unit would have required more experimental animals and the results of this study must be considered by bearing in mind that only three animals were used per time point. It is unlikely that the difference in bone bonding between the threaded FRC implants found in this study is related to differences in surface topographies and surface volume as the non-coated FRC implants were moderately roughened with grit-blasting. The better bonding strength of the BAG-coated FRC implant is rather related to the surface activity of BAG and ionic exchange at the implant–bone interface. The BAG is
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known to be osseoconductive and also to improve bone quality in the close vicinity of the coated implant (31). The differences in bonding strength between nonthreaded and threaded FRC/BAG implants are obviously related to implant design (32). Furthermore, the total bioactive surface area was larger in threaded FRC implants as a result of the larger implant surface, which could have further improved bone quality at the implant–bone interface. The push-out failure of threaded FRC/BAG and FRC implants occurred in the bone tissue, not in the interfacial region, indicating that the bonding strength between bone and the implant surface was stronger than the newly formed bone tissue itself. This provided further evidence of good fixation between the FRC surface and bone tissue. However, in non-threaded BAGcoated implants, failure occurred at the coating–bone interface, which can be related to poor initial stability and the fact that in the FRC/BAG implant, the interface is assumed to be able to resist compressive stress but not high shear stress. However, in the threaded FRC specimens, with or without BAG coating, the interface was partly compressed with respect to the FRC surface, thus providing a better environment for the establishment of bone–implant integration. It should be noted that all the experimental implants were inserted using the press-fit protocol. Thus, the implants had poor primary stability, and their push-out strength was derived from bone apposition at the bone–implant interface. It is noteworthy that, after 12 wk, nonthreaded FRC/BAG implants had achieved bond strength similar to that of non-coated threaded FRC implants after 4 wk. With longer healing time the non-threaded FRC/BAG implants can establish better bone-to-implant integration. There was no evidence of breakdown or change in thickness of the BAG coating. The good mechanical and biologic responses suggest that the BAG embedded in the composite resin enhances the biologic performance of FRC implants. The interesting finding that uncoated and grit-blasted FRC implants also showed good osseointegration corresponds to the results obtained in a previous cellculture study (19), which revealed good osteoblast proliferation and bone formation on both uncoated and BAG-coated FRC specimens. However, the data presented here are based on micro-CT and mechanical push-out strength analyses, in which implants were integrated on unloaded conditions. More information is needed under loaded conditions before any definitive statements can be made about the integration of the FRC oral implants into bone. In conclusion, the findings of this study suggest that the threaded design of FRC implants can withstand static loading until failure without fracture. The strong relationship of maximum force with BV/ TV of BAG-coated FRC implants demonstrates that increased bone formation around the BAG coating plays an important role in the osseointegration of FRC implants.
Acknowledgements – Study was carried out in BioCity Turku Biomaterials Reserach Program (www.biomaterials.utu.fi) and its support is greatly appreciated. Conflicts of interest – In particular to the subject matter authors do not have conflicts of interests. Author Vallittu is a Board Member of and owner of calvarial implant producing company Skulle Implants Corporation and consults Stick Tech Ltd - Member of the GC Group.
References 1. WEISS CM. Tissue integration of dental endosseous implants: description and comparative analysis of the fibro-osseous integration and osseous integration systems. J Oral Implantol 1986; 12: 169–214. 2. LINDER L. Osseointegration of metallic implants. I. Light microscopy in the rabbit. Acta Orthop Scand 1989; 60: 129– 134. 3. BRANEMARK PI. Introduction to osseointegration. In: BRANEMARK PI, ZARB GA, ALBREKTSSON T, eds. Tissue integrated prostheses. Osseointegration in clinical dentistry. Chicago: Quintessence, 1985; 11–76. 4. BRANEMARK PI. Osseointegration and its experimental background. J Prosthet Dent 1983; 50: 399–410. 5. BRANEMARK PI, ADELL R, BREINE U, HANSSON BO, LINDSTROM J, OHLSSON A. Intra-osseous anchorage of dental prostheses. I. Experimental studies. Scand J Plast Reconstr Surg 1969; 3: 81–100. 6. ALBREKTSSON T, BRANEMARK 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. 7. PARK JB, BRONZINO JD, KIM YK. Metallic Biomaterials. In: PARK JB, BRONZINO JD, eds. Ceramic biomaterials. Boca Raton, USA: CRC Press, 2003; 1–45. 8. SZMUKLER-MONCLER S, SALAMA H, REINGEWIRTZ Y, DUBRUILLE JH. Timing of loading and effect of micromotion on bone-dental implant interface: review of experimental literature. J Biomed Mater Res 1998; 43: 192–203. 9. JASTY M, BRAGDON C, BURKE D, O’CONNOR D, LOWENSTEIN J, HARRIS WH. In vivo skeletal responses to porous-surfaced implants subjected to small induced motions. J Bone Joint Surg Am 1997; 79: 707–714. 10. HENRY PJ. Clinical experiences with dental implants. Adv Dent Res 1999; 13: 147–152. 11. ELLINGSEN JE, LYNGSTADAAS SP. Bio-implant interface: improving biomaterials and tissue reactions, 1st edn. Boca Raton, USA: CRC Press, 2003. 12. LEMONS JE. Unanticipated outcomes: dental implants. Implant Dent 1998; 7: 351–354. 13. BRUNSKI JB. In vivo bone response to biomechanical loading at the bone/dental-implant interface. Adv Dent Res 1999; 13: 99–119. € TO, VALLITTU PK. In vitro 14. BALLO AM, LASSILA L, NARHI mechanical testing of glass fiber-reinforced composite as dental implants. J Contemp Dent Pract 2008; 9: 41–48. 15. FREILICH MA, DUNCAN JP, ALARCON EK, ECKROTE KA. The design and fabrication of fiber-reinforced implant prostheses. J Prosthet Dent 2002; 88: 449–454. 16. TUUSA SM, PELTOLA MJ, TIRRI T, LASSILA LV, VALLITTU PK. Frontal bone defect repair with experimental glass-fiberreinforced composite with bioactive glass granule coating. J Biomed Mater Res B Appl Biomater 2007; 82: 149–155. € M, MATTILA R, ALANDER P, 17. AHO AJ, HAUTAMAKI STRANDBERG N, REKOLA J, GUNN J, LASSILA LV, VALLITTU PK. Surface porous fiber-reinforced composite bulk bone substitute. Cell Tissue Bank 2004; 5: 213–221. € TO. Load bear18. BALLO AM, LASSILA VJ, VALLITTU P, NARHI ing capacity of bone anchored fiber-reinforced composite device. J Mater Sci Mater Med 2007; 18: 2025–2031.
Bone response of fiber-reinforced composite implants 19. BALLO AM, KOKKARI AK, MERETOJA VV, LASSILA VJ, € TO. Osteoblast proliferation and maturaVALLITTU P, NARHI tion on fiber-reinforced composite surface. J Mater Sci Mater Med 2008; 19: 3169–3177. € M, MERETOJA VV, MATTILA RH, AHO AJ, 20. HAUTAMAKI VALLITTU PK. Osteoblast response to polymethyl methacrylate bioactive glass composite. J Mater Sci Mater Med 2010; 21: 1685–1692. 21. ABDULMAJEED AA, WALBOOMERS XF, MASSERA J, KOKKARI € AK, VALLITTU PK, NARHI TO. Blood and fibroblast responses to thermoset BisGMA-TEGDMA/glass fiber-reinforced composite implants in vitro. Clin Oral Implants Res 2013; doi: 10.1111/clr.12151. [Epub ahead of print]. 22. LEE JH, RYU HS, LEE DS, HONG KS, CHANG BS, LEE CK. Biomechanical and histomorphometric study on the bone-screw interface of bioactive ceramic-coated titanium screws. Biomaterials, 2005; 26: 3249–3257. 23. HENCH LL, WEST JK. Biological applications of bioactive glasses. Life Chem Rep 1996; 13: 187–241. € YLI-URPO A, 24. HEIKKILA€ JT, MATTILA KT, ANDERSSON OH, AHO AJ. Behaviour of bioactive glass in human bone. In: WILSON J, HENCH LL, GREENSPAN D, eds. Bioceramics, Vol. 8: Proceedings of the 8th international symposium on ceramics in medicine, Oxford, Florida: Elsevier, 1995; 35–40. 25. AITASALO K, KINNUNEN I, PALMGREN J, VARPULA M. Repair of orbital floor fractures with bioactive glass implants. J Oral Maxillofac Surg 2001; 59: 1390–1395. 26. BALLO AM, AKCA EA, OZEN T, LASSILA L, VALLITTU PK, € TO. Bone tissue responses to glass fiber-reinforced NARHI
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composite implants – a histomorphometric study. Clin Oral Implants Res 2009; 20: 608–615. € MORITZ N, BALLO AM, NARHI TO. Micro-CT application in oral implant research. In: BALLO AM, ed. Implant dentistry research guide: basic, translational and clinical research. Hauppauge, NY: Nova Publishers, 2012; 325–342. CORDIOLI G, MAZZOCCO C, SCHEPERS E, BRUGNOLO E, MAJZOUB Z. Maxillary sinus floor augmentation using bioactive glass granules and autogenous bone with simultaneous implant placement. Clinical and histological findings. Clin Oral Implants Res 2001; 12: 270–278. NORTON MR, WILSON J. Dental implants placed in extraction sites implanted with bioactive glass: human histology and clinical outcome. Int J Oral Maxillofac Implants 2002; 17: 249–257. R, OHRNELL LO, SKALAK R, CARLSSON L, BRANEBRANEMARK MARK PI. Biomechanical characterization of osseointegration: an experimental in vivo investigation in the beagle dog. J Orthop Res 1998; 16: 61–69. € H, ARO H, MORITZ N, ROSSI S, VEDEL E, TIRRI T, YLANEN € TO. Implants coated with bioactive glass by CO2NARHI laser, an in vivo study. J Mater Sci Mater Med 2004; 15: 795–802. BOLIND PK, JOHANSSON CB, BECKER W, LANGER L, SEVETZ EB, ALBREKTSSON TO. A descriptive study on retrieved nonthreaded and threaded implant designs. Clin Oral Implants Res 2005; 16: 447–455.
Eur J Oral Sci 2014; 122: 303–309 DOI: 10.1111/eos.12133 Printed in Singapore. All rights reserved
European Journal of Oral Sciences
Effect of implant design and bioactive glass coating on biomechanical properties of fiber-reinforced composite implants Ballo AM, Akca E, Ozen T, Moritz N, Lassila L, Vallittu P, N€ arhi T. Effect of implant design and bioactive glass coating on biomechanical properties of fiberreinforced composite implants. Eur J Oral Sci 2014; 122: 303–309. © 2014 Eur J Oral Sci This study aimed to evaluate the influence of implant design and bioactive glass (BAG) coating on the response of bone to fiber-reinforced composite (FRC) implants. Three different FRC implant types were manufactured for the study: nonthreaded implants with a BAG coating; threaded implants with a BAG coating; and threaded implants with a grit-blasted surface. Thirty-six implants (six implants for each group per time point) were installed in the tibiae of six pigs. After an implantation period of 4 and 12 wk, the implants were retrieved and prepared for micro-computed tomography (micro-CT), push-out testing, and scanning electron microscopy analysis. Micro-CT demonstrated that the screw-threads and implant structure remained undamaged during the installation. The threaded FRC/BAG implants had the highest bone volume after 12 wk of implantation. The push-out strengths of the threaded FRC/BAG implants after 4 and 12 wk (463°N and 676°N, respectively) were significantly higher than those of the threaded FRC implants (416°N and 549°N, respectively) and the nonthreaded FRC/BAG implants (219°N and 430°N, respectively). Statistically significant correlation was found between bone volume and push-out strength values. This study showed that osseointegrated FRC implants can withstand the static loading up to failure without fracture, and that the addition of BAG significantly improves the push-out strength of FRC implants.
The long-term clinical success of oral implants is based on the presence and maintenance of a proper bone response and a safe and effective load transfer from the prosthesis to the bone. Bone responses to implant materials can be characterized as connective tissue capsulation (1) or direct bone contact with the implant surface (osseointegration) (2–5). The long-term success of oral implants relies on direct anchorage to bone. Several factors can be considered as important for successful osseointegration (6): the material properties of an implant, the implant design, the surface configuration of the implant, host tissue, the surgical technique, and loading conditions. The first three factors are related to the choice of implant material. The most important surface properties are topography, chemistry, surface charge, and wettability (7). Poor primary stability and implant micromotion have been considered as the main causes for implant failure (8, 9). Good primary stability is usually obtained by using the proper surgical technique and appropriate hardware (10). Implant surface topography also plays an important role (11).
Ahmed M. Ballo1,2, Eralp Akca3, Tuncer Ozen3, Niko Moritz4, Lippo Lassila5, Pekka Vallittu5, €rhi6 Timo Na 1
Department of Oral Health Sciences, University of British Columbia Faculty of Dentistry, Vancouver, BC, Canada; 2Dental Implant and Osseointegration Research Chair, College of Dentistry, King Saud University, Riyadh, Saudi Arabia; 3 Department of Periodontology, Dental Sciences Center, Gulhane Military Medical Academy, Ankara, Turkey; 4Orthopedic Research Unit, Department of Orthopedic Surgery and Traumatology, University of Turku, Turku, Finland; 5Department of Biomaterials Science, Institute of Dentistry, University of Turku, Turku, Finland; 6 Department of Prosthetic Dentistry, Institute of Dentistry, University of Turku, Turku, Finland
Dr Ahmed Ballo, Department of Oral Health Sciences, University of British Columbia Faculty of Dentistry, JBM 256 - 2199 Wesbrook Mall, Vancouver, BC, Canada, V6T 1Z3 E-mail: [email protected] Key words: bioactive glass; biomechanics; dental implant; fiber-reinforced composite; osseointegration Accepted for publication April 2014
In the case of titanium implants, occlusal forces are transmitted from the rigid implant material to the bone of lower modulus of elasticity. None of the commercially available oral implants can adapt to occlusal loads in the same way as a natural tooth with a sound periodontal ligament. Several different implant designs have been introduced that aim to optimize mechanical loading conditions. In poor bone conditions, the mismatch of stiffness between bone and a metallic implant may lead to treatment failure (12). This occurs when the tensile or compressive load exceeds the physiological limit of bone tolerance, causing microfracture at the bone-to-implant interface or initiating bone resorption (13). Fiber-reinforced composites (FRC) are durable materials, with strength and modulus of elasticity that can be adapted to the physiological properties of bone (14). Fiber-reinforced composite materials have been used in restorative and prosthetic dentistry for many years. There has been interest in using FRC implants for load-bearing applications in orthopedic and head and
304
Ballo et al.
neck surgery (15–17), which make them interesting materials also as oral implants. In our earlier studies, FRC implants showed good mechanical performance in the laboratory environment (14, 18). Furthermore, it was found that FRC materials do not elicit cytotoxic responses with osteoblast-like cells (19, 20) and human gingival fibroblasts (21) in cell-culture conditions and can therefore be considered as cytocompatible. The smooth FRC surface was shown to increase cell adhesion, spreading, and proliferation after 4 d of culture when compared with tissue-culture polystyrene (20). Rough and porous FRC surfaces, on the other hand, seem to enhance osteoblast proliferation and the formation of mineralized extracellular matrix (19, 20). Bioactivity has been defined as the interaction of cells with the implant surface that facilitates peri-implant bone regeneration, allowing the implant to form a biologic bond with living tissue (22). Bioactive glass (BAG) facilitates biologic bone bonding (23–25). A good osteoconductive property has also been observed with BAG-coated FRC by enhancing bone healing in the close vicinity of the coated implants (16). Our previous histomorphometric study showed that the polymer surface allows equal bone formation with titanium after 4 and 12 wk of healing (26). Both gritblasted and BAG-coated FRC implants established direct bone contact and showed no toxicity during the 4- and 12-wk healing periods. The purpose of this study was to evaluate the effect of implant designs and surface modifications on the biomechanical responses of FRC implants in vivo.
Material and methods Preparation of experimental implants Three different groups of FRC implants with a length of 10 mm and a diameter of 4.1 mm were fabricated for the study: BAG-coated non-threaded FRC implants; gritblasted threaded FRC implants; and BAG-coated threaded FRC implants. Scanning electron microscopy images of threaded FRC implants are shown in Fig. 1. The implants were made of E-glass FRC. The fabrication process of FRC implants has been described in detail in our previous study (18).
A
Briefly, the implants consisted of five fiber-reinforcement bundles, each consisting of 4,000 continuous unidirectional E-glass fibers (approximately 15 lm in diameter). The fiber bundle was impregnated manually in light-polymerizable bisphenyl A glycidyl methacrylate-triethyleneglycol dimethacrylate (bisGMA-TEGDMA) Stick (Stich Tech, Turku, Finland) resin. The composition of fibers was: 55% SiO2, 15% Al2O3, 22% CaO, 6% B2O3, 0.5% MgO, and >1.0% Fe+Na+K. The implant threads were reinforced by adding bidirectional fiber weave around the threads. Commercially available BAG (S53P4; Vivoxid, Turku, Finland) granules, of 0.01). At 12 wk post-implantation, the bone volumes were 23% and 56%, respectively, with a significantly greater bone volume on FRC/BAG implants (P < 0.01). Push-out test
The results of the push-out test are shown in Fig. 7. The bonding forces of threaded FRC/BAG implants after 4 and 12 wk (463°N and 676°N, respectively) were significantly higher than those of threaded FRC implants (416°N and 549°N, respectively P < 0.0001) and non-threaded FRC/BAG implants (219°N and 430°N, respectively, P < 0.0001). No significant differences had occurred between the threaded experimental implants after 4 wk. Significant correlation was found between BV/TV and the push-out force (r = 0.83), which indicates that the BV/TV, at a higher push-out strength of FRC/ BAG, is closely linked to better peri-implant bone formation.
Fig. 6. Mean values of relative bone volume between the threads of experimental threaded fiber-reinforced composite (FRC) implants analyzed by micro-computed tomography (micro-CT), 4 and 12 wk after implantation. Light-grey bars, threaded FRC; dark-grey bars, threaded FRC/bioactive glass (BAG).
signs of delamination, breakdown, or change in thickness of the BAG coating were observed. In all threaded implants, fracture occurred at the level of the thread crests. In the FRC/BAG implants, newly formed bone had filled the thread areas and stayed in immediate contact with the BAG coating after the push-out test (Figs 8 and 9), whereas in nonthreaded FRC/BAG implants, fracture occurred at the implant–bone interface.
Scanning electron microscopy
Scanning electron microscopy analysis revealed that all FRC implants remained sound after the push-out test, the screw-threads and implant configuration being well maintained. Regardless of the study time point, no
Discussion Implant fixation in the surrounding bone is basically a result of friction, mechanical interlock, and chemical
A
B
C
D
E
F
Fig. 5. Micro-computed tomography images illustrate bone growth in close contact with bioactive glass (BAG)-coated non-threaded fiber-reinforced composite (FRC) implants (A, D), with sandblasted threaded FRC implants (B, E) and with BAG-coated threaded FRC implants (C, F), 4 wk (upper row) and 12 wk (lower row) after implantation.
Bone response of fiber-reinforced composite implants
307
A
Fig. 7. Mean push-out strength values of experimental fiberreinforced composite (FRC) implants. The horizontal line above the bars represents homogeneous subsets (Tukey’s posthoc test). Dark-grey bars, 4 wk after implantation; light-grey bars, 12 wk after implantation.
bonding. Macro- and microtexture are other factors that determine shear movement. Macrotexture, for example, is provided by screw threads, whereas microtexture is related to dimensions that are created by surface-treatment procedures. Besides the surface condition of the implant material, specific bulk mechanical properties can affect the push-out strength. The mechanical properties of FRCs resemble the modulus of bone. However, despite the encouraging in vitro mechanical and histological results, the bone-bonding strength of BAG-coated and non-coated FRC implants were not known. The fact that new-bone apposition was detected between the implant threads suggests good biocompatibility of the FRC implants. The enhanced bone anchorage of BAG-coated FRC implants was not surprising as the BAG used in this study has been shown to promote bone formation in many previous investigations (25–29). However, with the exception of measuring direct bone-to-implant contact, investigation of trabecular bone structure around implants with micro-CT alone is not a very reliable method for the characterization of bone structure.
Fig. 8. Photograph (inset) and scanning electron microscopy micrograph of the fracture surface of a threaded and sandblasted fiber-reinforced composite (FRC) implant after the push-out test. Fracture occurred through the crestal level of FRC threads, suggesting that the main cause of failure was low cohesive shear strength of bone.
B
Fig. 9. Scanning electron microscopy micrographs of the fracture surface of the threaded fiber-reinforced composite (FRC) implants, with and without bioactive glass (BAG) coating, after the push-out test. Fracture occurred within the bone and not at the bone–implant interface. In the FRC/ BAG implants, newly formed bone filled the thread areas in immediate contact with the BAG coating.
et al. (30) noted that pull-out and pushBRANEMARK out tests measure peri-implant bone quality, as, by definition, the bone surrounding the implant fractures during the experiment. Although the push-out test is a better measure of the mechanical properties of bone around the implant and the strength of the coating– implant interface than of the shear strength of the bone–implant interface, from a clinical perspective, push-out data still provide valid information about how strongly an implant is anchored in the bone. The present study showed a significant improvement in the interfacial bond strength of the FRC/BAG implant with increasing healing time. In this study, statistical unit was an implant. Having an animal as a statistical unit would have required more experimental animals and the results of this study must be considered by bearing in mind that only three animals were used per time point. It is unlikely that the difference in bone bonding between the threaded FRC implants found in this study is related to differences in surface topographies and surface volume as the non-coated FRC implants were moderately roughened with grit-blasting. The better bonding strength of the BAG-coated FRC implant is rather related to the surface activity of BAG and ionic exchange at the implant–bone interface. The BAG is
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known to be osseoconductive and also to improve bone quality in the close vicinity of the coated implant (31). The differences in bonding strength between nonthreaded and threaded FRC/BAG implants are obviously related to implant design (32). Furthermore, the total bioactive surface area was larger in threaded FRC implants as a result of the larger implant surface, which could have further improved bone quality at the implant–bone interface. The push-out failure of threaded FRC/BAG and FRC implants occurred in the bone tissue, not in the interfacial region, indicating that the bonding strength between bone and the implant surface was stronger than the newly formed bone tissue itself. This provided further evidence of good fixation between the FRC surface and bone tissue. However, in non-threaded BAGcoated implants, failure occurred at the coating–bone interface, which can be related to poor initial stability and the fact that in the FRC/BAG implant, the interface is assumed to be able to resist compressive stress but not high shear stress. However, in the threaded FRC specimens, with or without BAG coating, the interface was partly compressed with respect to the FRC surface, thus providing a better environment for the establishment of bone–implant integration. It should be noted that all the experimental implants were inserted using the press-fit protocol. Thus, the implants had poor primary stability, and their push-out strength was derived from bone apposition at the bone–implant interface. It is noteworthy that, after 12 wk, nonthreaded FRC/BAG implants had achieved bond strength similar to that of non-coated threaded FRC implants after 4 wk. With longer healing time the non-threaded FRC/BAG implants can establish better bone-to-implant integration. There was no evidence of breakdown or change in thickness of the BAG coating. The good mechanical and biologic responses suggest that the BAG embedded in the composite resin enhances the biologic performance of FRC implants. The interesting finding that uncoated and grit-blasted FRC implants also showed good osseointegration corresponds to the results obtained in a previous cellculture study (19), which revealed good osteoblast proliferation and bone formation on both uncoated and BAG-coated FRC specimens. However, the data presented here are based on micro-CT and mechanical push-out strength analyses, in which implants were integrated on unloaded conditions. More information is needed under loaded conditions before any definitive statements can be made about the integration of the FRC oral implants into bone. In conclusion, the findings of this study suggest that the threaded design of FRC implants can withstand static loading until failure without fracture. The strong relationship of maximum force with BV/ TV of BAG-coated FRC implants demonstrates that increased bone formation around the BAG coating plays an important role in the osseointegration of FRC implants.
Acknowledgements – Study was carried out in BioCity Turku Biomaterials Reserach Program (www.biomaterials.utu.fi) and its support is greatly appreciated. Conflicts of interest – In particular to the subject matter authors do not have conflicts of interests. Author Vallittu is a Board Member of and owner of calvarial implant producing company Skulle Implants Corporation and consults Stick Tech Ltd - Member of the GC Group.
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