List of bacterial species associated to dental implant biofilm.
Abstract
Osseointegration is a biological process in which histological, surgical, infectious factors, biomechanical load, and the choice of biomaterials all play important roles. In the case of dental implants, the success of this process is also influenced by the design, composition, and properties of the implant surface, which may stimulate cell bioactivity and promote osteoblast adhesion. Currently, the raw materials most frequently used in the manufacture of dental implants are titanium, its alloys, and certain ceramic materials such as zirconia. Multiple macroscopic designs incorporating various diameters, lengths, shapes, and types of screw offer different options for specific clinical situations. The characteristics of implant surfaces have aroused great interest, due to their importance in osseointegration. The different methods used to modify surface properties are classified as additive (i.e., impregnation and coating) or subtractive (i.e., physical, mechanical and chemical methods). The surface characteristics of dental implants also have a significant influence on peri-implant microbiota.
Keywords
- Dental implant
- Titanium
- Osseointegration
- Surface roughness
- Coating
- Peri-implantitis
1. Introduction
Over many years, dental implants have been developed and modified in order to achieve an optimal interaction between the body and the implanted material and thus to improve osseointegration and reduce the complications due to colonization of bacterial plaque [1].
Proper integration of the surface of a dental implant with the surrounding bone is essential to ensure the longevity and function of the prosthesis supported by the implant [2]. The cell adhesion between the bone interface and the implant surface is considered the most biologically important stage in the process. This structural and functional integration is influenced by the activity of adjacent cells and by the properties of the implant surface itself.
Some implant surfaces may influence the differentiation and proliferation of osteoblasts and may affect the regulation of the transcription factors responsible for the expression of the genes associated with the formation of the bone matrix. Their use may even shorten the implant integration period [3].
The treatment of a surface can be classified according to mechanical, chemical, and physical processes. In dental implants, the modifications of the outer surface are designed to modify the topography and surface energy. This improves wettability and increases cell growth and proliferation, which eventually accelerates the process of osseointegration [4–7].
The biocompatibility and roughness of the materials are the key features in the interaction between the tissue and osseointegration [8]. In addition, the surface of dental implants can be significantly increased using suitable modification procedures such as additive or subtractive techniques [9, 10].
2. Biomaterials for dental implants
Currently, the main materials used in the composition of dental implants are commercially pure titanium (cp Ti), Ti alloys, and ceramic compounds.
2.1. Alloys
2.2. Ceramic compounds
Zirconia implants, as a substitute for metals, are indicated in the restoration of anterior teeth with aesthetic aims. However, more prospective studies of their survival and long-term stability are required; indeed, some authors still recommend caution with regard to considering zirconia implants [19].
Implants with HA coating have demonstrated a faster reduction in early mobility and other potential advantages such as its short-term osseoconductive capacity. However, the rate of long-term survival of these implants is still controversial [21–25].
3. Macro-design of dental implants
The macro-design of dental implants determines their stability and their capacity to withstand the functional loads. The length, diameter, shape, and design of the screw are influential factors in the bone–implant interface. In the long term, these features may even determine the implant’s survival.
3.1. Implant length
Implant length is the distance from the prosthetic platform to the apex of the implant. Some authors have reported a lower survival rate for short implants, especially those <7 mm long [26, 27]. Eckert et al. [28], however, noted that the relation between implant length and survival was limited and was only noticeable when implants were <13 mm in length.
The type of bone and the cortical bone anchoring are probably more important factors than the implant length. Nonetheless, the indications of implants with extra short lengths (5–6 mm) should be carefully studied and considered, especially in areas with poor bone quality. Manufacturers are making great efforts to improve these implant surfaces so as to increase the area in contact with the bone and thus improve their prognosis [29, 30].
3.2. Implant diameter
The implant diameter is the distance from the outermost point of the screw to the opposite side. It measures the external dimension of the implant screw and should not be confused with the size of the implant platform.
Implant diameters usually range from 3 to 7 mm to make them compatible with the most sizes of alveolar processes. The choice of diameter depends on both surgical and prosthetic factors. In order to achieve maximum primary stability, the implant should be lodged between the vestibular-lingual/palatal cortical bones. From a biomechanical point of view, wider implants are able to join a larger amount of bone to the implant surface and obtain a higher bicortical anchorage, thus achieving a better distribution of stress in the surrounding bone. Another advantage of large diameter implants is that they can be inserted immediately in failure sites [31–33]. Some authors have found that increasing implant diameter by 1 mm increases the surface of bone–implant contact by 35% [34]. However, another parameter to consider is the crestal bone around the implant. According to Misch [35], this bone has a strong influence on the occlusal load; this author hypothesizes that it may be even more important than the length and diameter of the implant itself.
The primary stability of dental implants at the time of surgery has been considered an important factor for integration [36]. Langer et al. recommended large diameter implants to improve primary stability in low-density bones. The authors argue that increasing the diameter increases the bone–implant contact, thereby reducing initial implant mobility [37].
Small diameter implants have been introduced for narrow residual alveolar ridges and for edentulous spaces with small interdental distances. These implants do not include mini-implants, which are used to hold temporary dentures and have diameters <2.7 mm [38]. The main indications for narrow implants are the lower incisors, upper lateral incisors, and the restoration of teeth with residual spaces smaller than 5 mm without any possibility of space recovery or bone regeneration [39]. The main limitation of these implants is their reduced resistance to occlusal loads [40].
3.3. Implant shape
Shape has been one of the most thoroughly studied aspects of implant design. The most current implant systems are solid cylinders with thread; hollow implants are rare today. As for the design of the thread, attempts have been made to increase their self-threading capacity and to reduce heat generation during implantation. These design variations are most often applied in the crestal and apical areas. Some designs have attempted to imitate the natural root with a stepped cylindrical shape in the apical and crestal third of the implant. Some authors note that stepped cylindrical implants achieve better stress distribution and crestal bone load than conical and cylindrical implants [41].
Kan et al. [42] reported that threaded implants provide the best immediate retention. Other studies show that the use of a serrated thread can increase primary stability and that thread geometry plays an important role in the biomechanical properties of the implants [43, 44].
4. Dental implant surface treatments
Currently, the most manufacturers of dental implants are introducing changes in implant surfaces in order to improve the success and quality of osseointegration.
Some studies have noted that with greater surface roughness, the rate of osseointegration, and the biomechanical fixation of Ti implants both increase [45, 46]. The methods used to modify the surface properties can be divided into additive and subtractive. Before certain surface treatments, pretreatment such as grit blasting or polishing may sometimes be indicated to guarantee the absence of contaminations, scratches, and irregularities [47, 48].
4.1. Additive methods
Additive methods supply extra materials to the implant surface, either via coating or via impregnation. Coating involves the addition of a material of variable thickness to the surface of the core material. The techniques used are Ti plasma spraying (TPS), plasma-sprayed HA coating, alumina coating, and biomimetic calcium phosphate (CaP). For its part, impregnation requires the full integration of the chemical material or agent into the Ti core. This is the case of CaP crystals within the TiO2 oxide layer or the incorporation of fluoride ions to the surface [8].
4.2. Subtractive methods
Subtractive techniques are procedures that remove a layer of core material or deform the surface in order to increase its roughness [58]. These methods can be divided into mechanical, chemical, and physical. Removal of surface material using mechanical methods includes shaping/removing, grinding, machining, or grit blasting using physical force. Chemical treatment of Ti alloys using either alkaline or acid solutions is carried out not only to increase the roughness but also to modify the composition and improve the wettability and surface energy [59]. Complementary physical treatment of the coating surface, such as thermal spray and plasma spray, improves the aesthetic appearance of the materials and their performance [8].
Aparicio et al. [61] observed that the increase in the surface roughness of the material induced by blasting in cp Ti was not the only cause of the differences in the electrochemical behavior and corrosion resistance; they also mentioned the compressive residual surface stresses induced by shotblasting.
Commercially, pure Ti is a bioinert material which lacks the ability to establish chemical bonds with surrounding bone. Kokubo et al. [62] demonstrated that the treatment of this Ti with heat and alkali procedures rendered it bioactive. Aparicio et al. [63] observed that the surface of the implant achieved by grit blasting and thermo-chemical treatment improved adhesion and differentiation of human osteoblasts. Gil et al. [64] also observed positive results for this bioactive Ti, although improvements are necessary in order to prevent bacterial colonization. It is important to bear in mind that bacteria have a greater capacity to colonize rough surfaces [8] (Figure 2).
Some researchers have found that the apatite layers formed on grit-blasted surfaces have a higher adhesion strength to the substrate than plasma-sprayed apatite coatings. They note the potential clinical application of this type of surface treatment in dental implants [65].
The evolution of bioactive surfaces into osseoconductive biomimetic surfaces (Contact Ti) was described by Gil et al. In this process, a CaP layer is obtained on the implant surface by thermo-chemical treatments. This achieves a structure equal to the CaP formed by the mineral content of the bone (HA). This apatite should not be confused with an additive coating; in this case, there is an extremely strong chemical bond and so it is not dislodged by mechanical action. These bioactive implant surfaces significantly reduce the time of osseointegration. The most important mechanisms involved are the protein adsorption capacity, wettability, and an optimized zeta potential which reduces the electrostatic dispersion between particles. Finally, this procedure also aims to increase the kinetics of adhesion, proliferation, and differentiation of osteoblast cells compared to other current surface treatments in order to facilitate bone formation around the implants [66–68] (Figure 3).
4.3. Other techniques
Other procedures such as ion implantation, laser treatment, sputtering, and the combination of some of the techniques already mentioned have also been studied in order to improve the surface properties of dental implants [81–84].
Ion implantation causes atomic rearrangement. It permits the injection of any element on a nearby surface with a beam of high-energy ions (10 KeV) which impacts on the surface of the metal in a vacuum chamber. On colliding with the ions of the substrate material, the incident ions lose energy and settle on the surface of the nearby metal. This technique is considered an ultra clean process because the concentration and depth of the impurities are easy to control, allowing the creation of a layer of high purity. Furthermore, the adhesion between the implanted surface and the substrate is excellent; the process does not alter the properties of the core and is highly reproducible and controllable [85]. However, some authors warn that the possible modification of the nanoscale features and the creation of stress on the Ti surface should be taken into consideration [86, 87].
Ultraviolet (UV) photo-functionalization is one of the recent advances in the chemical modification of implant surfaces which does not alter the bioactive properties.
Laser technology is an extremely clean, fast, and accurate method which allows nanostructural micromachining at the implant surface [88]. Laser peening involves striking the metal with high-intensity pulses of a laser light beam which produces a deep, regular honeycomb pattern with small pores [2].
The slow rate sputter deposition method achieves a thin layer of Ti oxide (300 pm–6.3 nm). This technique increases the oxygen components without altering the surface topography. These biological activities are correlated with the thickness of the TiO2 coating and the oxygen saturation of the surface. This means that the biological response of Ti can be improved even with picometer super thin coatings [69].
5. Peri-implantitis related to dental implant surfaces
Peri-implantitis is an infectious disease of an already integrated dental implant that causes inflammation of the surrounding hard and soft tissue, leading to the loss of supporting bone (Figure 4 and 5). The sequence of microbial colonization on dental implants and biofilm formation is similar to that of teeth. The bacteria that colonize dental implants include the same species as those present in healthy gums and in locations with gingivitis [89–91]. Several
The surface characteristics of dental implants—roughness, wettability, surface free energy, and composition—play a crucial role in bacterial adhesion and colonization. The highest adhesion capacity is observed on rough Ti surfaces. Some authors have observed that mean roughness values below 0.088 microns significantly inhibit plaque adhesion and maturation [92]. Furthermore, decreasing the wettability of dental implants favors bacterial colonization. Some authors suggest that autoclave-sterilized Ti presents a higher rate of bacterial colonization, given the loss of surface wettability (Figure 5).
Surface free energy is the sum of the forces of cohesion and adhesion that determine whether or not there is impregnation (the dispersion of the liquid over a surface). Decreasing surface free energy inhibits bacterial adhesion and biofilm formation on the surface of dental implants and abutments [93]. Thus, bacterial adherence is correlated with the presence of surface components with nonpolar or hydrophobic characteristics [93–95]. Finally, the type of metal and its composition also has an effect on bacterial adhesion and biofilm formation on its surface. Pure metals, especially Ti, nickel, iron, and vanadium, have some bacteriostatic capacity [96].
Some authors have concluded that ZnO and TiO2 reduce the adhesion of staphylococcal bacteria and increase the adhesion of osteoblasts [97]. The addition of silver compounds to increase antimicrobial action has also been studied [98]. Other authors have analyzed the behavior of Ti surfaces modified with vancomycin attached via covalent bonds and have reported a stable surface with a greater inhibition of bacterial adhesion than with Ti alone [99].
6. Conclusion
In this chapter, we have highlighted the important role of the macro- and micro-design of implants and their composition in the process of osseointegration. We have also stressed the significant influence of the surface characteristics of implants on the peri-implant microbiota. All in all, peri-implantitis is an important area for future research. It is extremely difficult to control the progress of an infection once it is established around an implant. The rough surfaces facilitate osseointegration, but also favor the adhesion of oral biofilm. Because of the multifactorial nature of infectious peri-implant complications, studies should also take into account the influence of the permucosal seal. This biological seal aims to integration the neck of the implant or the abutment with the gingival tissue and thus prevent peri-implant infections. Currently, the challenge in the treatment of implant surfaces is to demonstrate the potential of certain coatings for releasing local antimicrobial agents. Given the clear increase in inflammatory peri-implant diseases, we believe that future research should aim to devise new strategies for obtaining antibacterial biomaterials that can help in the prevention or treatment of peri-implantitis.
References
- 1.
Ananth H, Kundapur V, Mohammed HS, Anand M, Amarnath GS, Mankar S. A review on biomaterials in dental implantology. Int J Biomed Sci. 2015; 11(3): 113–120. - 2.
Ogle OE. Implant surface material, design, and osseointegration. Dent Clin N Am. 2015; 59(2): 505–20. doi:10.1016/j.cden.2014.12.003 - 3.
Cochran DL, Buser D, ten Bruggenkate CM, et al . The use of reduced healing times on ITI implants with a sandblasted and acid-etched (SLA) surface: early results from clinical trials on ITI SLA implants. Clin Oral Implants Res. 2002; 13(2): 144–153. doi:10.1034/j.1600-0501.2002.130204.x - 4.
Rosales-Leal JI, Rodríguez-Valverde MA, Mazzaglia G, et al . Effect of roughness, wettability and morphology of engineered titanium surfaces on osteoblast-like cell adhesion. Colloids Surf A Physicochem Eng Asp. 2010; 365(1–3): 222–229. doi:10.1016/j.colsurfa.2009.12.017 - 5.
Nakae H, Yoshida M, Yokota M. Effects of roughness pitch of surfaces on their wettability. J Mater Sci. 2005; 40(9–10): 2287–2293. - 6.
Ponsonnet L, Reybier K, Jaffrezic N, et al . Relationship between surface properties (roughness, wettability) of titanium and titanium alloys and cell behaviour. Mater Sci Eng C. 2003; 23(4): 551–560. doi:10.1016/S0928-4931(03)00033-X - 7.
Sollazo V, Pezzetti F, Scarano A, et al . Zirconium oxide coating improves implant osseointegration in vivo. Dent Mater. 2008; 24(3): 357–361. doi:10.1016/j.dental.2007.06.003 - 8.
Jemat A, Ghizali MJ, Razali M, Otsuka Y. Surface modifications and their effects on titanium dental implants. Biomed Res Int. 2015; 2015: 791725. doi:10.1155/2015/791725 - 9.
Lacefield WR. Materials characteristics of uncoated/ceramic coated implant materials. Adv Dent Res. 1999; 13: 21–26. doi:10.1177/08959374990130011001 - 10.
Ozcan M, Hammerle C. Titanium as a reconstruction and implant material in dentistry: advantages and pitfalls. Materials. 2012; 5(9): 1528–1545. doi:10.3390/ma5091528 - 11.
Jacobs JJ, Gilbert JL, Urban RM. Current concepts review: corrosion of metal orthopaedic implants. J Bone Jt Surg Am. 1998; 80A: 268–282. - 12.
Neoh KG, Hu X, Zheng D, et al . Balancing osteoblast functions and bacterial adhesion on functionalized titanium surfaces. Biomaterials. 2012; 33: 2813–2822. doi:10.1016/j.biomaterials.2012.01.018 - 13.
Steinemann S. Titanium—the material of choice? Periodontology. 2000, 1998; 17(1): 7–21. doi:10.1111/j.1600-0757.1998.tb00119.x - 14.
ASM Material Data Sheet. Available at: http://asm.matweb.com/search/SpecificMaterial.asp?bassnum5MTP642. Accessed December 2015. - 15.
Delgado-Ruiz RA, Calvo-Guirado JL, Abboud M, et al . Histologic and histomorphometric behavior of microgrooved zirconia dental implants with immediate loading. Clin Implant Dent Relat Res. 2013; 16(6): 856–872. doi:10.1111/cid.12069 - 16.
Koch FP, Weng D, Krämer S, et al . Osseointegration of one-piece zirconia implants compared with a titanium implant of identical design: a histomorphometric study in the dog. Clin Oral Implants Res. 2010; 21(3): 350–356. doi:10.1111/j.1600-0501.2009.01832.x - 17.
Moller B, Terheyden H, Acil Y, et al . A comparison of biocompatibility and osseointegration of ceramic and titanium implants: an in vivo and in vitro study. Int J Oral Maxillofac Surg. 2012; 41(5): 638–645. doi:10.1016/j.ijom.2012.02.004 - 18.
Assal PA. The osseointegration of zirconia dental implants. Schweiz Monatsschr. Zahnmed. 2013; 123(7–8): 644–654. - 19.
Wennerberg A, Albrektsson T. On implant surfaces: a review of the current knowledge and opinions. Int J Oral Maxillofac Implants. 2010; 25(1): 63–74. - 20.
Strnad Z, Strnad J, Povysil C, et al . Effect of plasma-sprayed hydroxyapatite coating on the osteoconductivity of commercially pure titanium implants. Int J Oral Maxillofac Implants. 2000; 15(4): 483–490. - 21.
Geurs NC, Jeffcoat RL, McGlumphy EA, Reddy MS, Jeffcoat MK. Influence of implant geometry and surface characteristics on progressive osseointegration. Int J Oral Maxillofac Implants. 2002; 17(6): 811–815. - 22.
Faeda RS, Tavares HS, Sartori R, Guastaldi AC, Marcantonio EJR. Biological performance of chemical hydroxyapatite coating associated with implant surface modification by laser beam: biomechanical study in rabbit tibias. J Oral Maxillofac Surg. 2009; 67: 1706–1715. doi:10.1016/j.joms.2009.03.046 - 23.
Gottlander M, Johansson CB, Albrektsson T. Short and long-term animal studies with a plasma-sprayed calcium phosphate-coated implant. Clin Oral Implants Res. 1997; 8(5): 345–351. - 24.
Jones JD, Saigusa M, Van Sickels JE, Tiner BD, Gardner WA. Clinical evaluation of hydroxyapatite-coated titanium plasma-sprayed and titanium plasma-sprayed cylinder dental implants: a preliminary report. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol. 1997; 84(2): 137–141. doi:10.1016/S1079-2104(97)90058-5 - 25.
Zhou W, Liu Z, Xu S, Hao P, Xu F, Sun A. Long-term survivability of hydroxyapatite-coated implants: a meta-analysis. Oral Surg. 2011; 4(1): 2–7. doi:10.1111/j.1752-248X.2010.01112.x - 26.
Winkler S, Morris HF, Ochi S. Implant survival to 36 months as related to length and diameter. Ann Periodontol. 2000; 5(1): 22–31. - 27.
Wyatt CC, Zarb GA. Treatment outcomes of patients with implant supported fixed partial prostheses. Int J Oral Maxillofac Implants. 1998; 13(2): 204–211. - 28.
Eckert SE, Koka S, Wolfinger G, Choi YG. Survey of implant experience by prosthodontists in the United States. J Prosthodont. 2002; 11(3): 194–201. doi:10.1053/jopr.2002.127768 - 29.
Geng JP, Tan KB, Liu GR. Application of finite element analysis in implant dentistry: a review of the literature. J Prosthet Dent. 2001; 85(6): 585–598. doi:10.1067/mpr.2001.115251 - 30.
Nedir R, Bischof M, Briaux JM, Beyer S, Szmukler-Moncler S, Bernard JP. A 7-year life table analysis from a prospective study on ITI implants with special emphasis on the use of short implants. Results from a private practice. Clin Oral Implants Res. 2004; 15(2): 150–157. doi:10.1111/j.1600-0501.2004.00978.x - 31.
Ivanoff CJ, Sennerby L, Johansson C, Rangert B, Lekholm U. Influence of implant diameters on the integration of screw implants. An experimental study in rabbits. Int J Oral Maxillofac Surg. 1997; 26(2): 141–148. doi:10.1016/S0901-5027(05)80837-9 - 32.
Mahon JM, Norling BK, Phoenix RD. Effect of varying fixture width on stress and strain distribution associated with an implant stack system. Implant Dent. 2000; 9(4): 310–320. - 33.
Ettinger RL, Spivey JD, Han DH, Koorbusch GF. Measurement of the interface between bone and immediate endosseous implants: a pilot study in dogs. Int J Oral Maxillofac Implants. 1993; 8(4): 420–427. - 34.
Misch CE. Contemporary implant dentistry. St. Louis: Elsevier. 3rd ed. 1999. ISBN:978-0-323-04373-1. - 35.
Misch CE. Implant design considerations for the posterior regions of the mouth. Implant Dent. 1999; 8(4): 376–386. - 36.
Kohn DH. Overview of factors important in implant design. J Oral Implantol. 1992; 18(3): 204–219. - 37.
Langer B, Langer L, Herrmann I, Jorneus L. The wide fixture: a solution for special bone situations and a rescue for the compromised implant. Part 1. Int J Oral Maxillofac Implants. 1993; 8(4): 400–408. - 38.
Kanie T, Nagata M, Ban S. Comparison of the mechanical properties of 2 prosthetic mini-implants. Implant Dent. 2004; 13(3): 251–256. - 39.
Vigolo P, Givani A. Clinical evaluation of single-tooth mini-implant restoration: a five-year retrospective study. J Prosthet Dent. 2000; 84: 50–54. doi:10.1067/mpr.2000.107674 - 40.
Himmlova L, Dostalova T, Kacovsky A, Konvickova S. Influence of implant length and diameter on stress distribution: a finite element analysis. J Prosthet Dent. 2004; 91(1): 20–25. doi:10.1016/j.prosdent.2003.08.008 - 41.
Holmgren EP, Seckinger RJ, Kilgren LM, Mante F. Evaluating parameters of osseointegrated dental implants using finite element analysis—a two dimensional comparative study examining the effects of implant diameter, implant shape, and load direction. J Oral Implantol. 1998; 24(2): 80–88. - 42.
Kan JY, Rungcharassaeng K, Kim J, Lozada JL, Goodacre CJ. Factors affecting the survival of implants placed in grafted maxillary sinuses: a clinical report. J Prosthet Dent. 2002; 87(5): 485–489. doi:10.1067/mpr.2002.124202 - 43.
Hansson S, Werke M. The implant thread as a retention element in cortical bone: the effect of thread size and thread profile: a finite element study. J Biomech. 2003; 36(2): 1247–1258. doi:10.1016/S0021-9290(03)00164-7 - 44.
Lin S, Shi S, LeGeros RZ, LeGeros JP. Three-dimensional finite element analyses of four designs of a high-strength silicon nitride implant. Implant Dent. 2000; 9(1): 53–60. - 45.
Cochran DL, Schenk RK, Lussi A, Higginbottom FL, Buser D. Bone response to unloaded and loaded titanium implants with a sandblasted and acid-etched surface: a histometric study in the canine mandible. J Biomed Mater Res. 1998; 40(1): 1–11. - 46.
Wennerberg A, Hallgren C, Johansson C, Danelli S. A histomorphometric evaluation of screw-shaped implants each prepared with two surface roughnesses. Clin Oral Implants Res. 1998; 9(1): 11–19. doi:10.1034/j.1600-0501.1998.090102.x - 47.
Gu YW, Khor KA, Pan D, Cheang P. Activity of plasma sprayed yttria stabilized zirconia reinforced hydroxyapatite/Ti6–Al–4V composite coatings in simulated body fluid. Biomaterials. 2004; 25(16): 3177–3185. doi:10.1016/j.biomaterials.2003.09.101 - 48.
Ferraris S, Spriano S, Pan G, et al . Surface modification of Ti–6Al–4V alloy for biomineralization and specific biological response: part I, inorganic modification. J Mater Sci Mater Med. 2001; 22(3): 533–545. doi:10.1007/s10856-011-4246-2 - 49.
Simmons CA, Valiquette N, Pilliar RM. Osseointegration of sintered porous-surfaced and plasma spray-coated implants: an animalmodel study of early postimplantation healing response and mechanical stability. J Biomed Mater Res. 1999; 47(2): 127–138. - 50.
Ong JL, Chan DCN. Hydroxyapatite and their use as coatings in dental implants: a review. Crit Rev Biomed Eng. 2000; 28(5–6): 667–707. doi:10.1615/CritRevBiomedEng.v28.i56.10 - 51.
Knabe C, Klar F, Fitzner R, Radlanski RJ, Gross U. In vitro investigation of titanium and hydroxyapatite dental implant surfaces using a rat bone marrow stromal cell culture system. Biomaterials. 2002; 23(15): 3235–3245. doi:10.1016/S0142-9612(02)00078-9 - 52.
Hung KY, Lo SC, Shih CS, Yang YC, Feng HP, Lin YC. Titanium surface modified by hydroxyapatite coating for dental implants. Surf Coat Technol. 2013; 231: 337–345. doi:10.1016/j.surfcoat.2012.03.037 - 53.
Eom TG, Jeon GR, Jeongetal CM. Experimental study of bone response to hydroxyapatite coating implants: bone implant contact and removal torque test. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012; 114(4): 411–418. doi:10.1016/j.oooo.2011.10.036 - 54.
Ochsenbein A, Chai F, Winter S, Traisnel M, Breme M, Hildebrand HF. Osteoblast responses to different oxide coatings produced by the sol–gel process on titanium substrates. Acta Biomater. 2008; 4(5): 1506–1517. doi:10.1016/j.actbio.2008.03.012 - 55.
Braceras I, Alava JI, Oñate JI, et al . Improved osseointegration in ion implantation-treated dental implants. Surf Coat Technol. 2002; 158–159: 28–32. doi:10.1016/S0257-8972(02)00203-7 - 56.
Fouda MFA, Nemat A, Gawish A, Baiuomy AR. Does the coating of titanium implants by hydroxyapatite affect the elaboration of free radicals. An experimental study. Aust J Basic Appl Sci. 2009; 3: 1122–1129. - 57.
Xie Y, Liu X, Zheng X, Ding C, Chu PK. Improved stability of plasma-sprayed dicalcium silicate/zirconia composite coating. Thin Solid Films. 2006; 515(3): 1214–1218. doi:10.1016/j.tsf.2006.07.124 - 58.
Le Guéhennec L, Soueidan A, Layrolle P, Amouriq Y. Surface treatments of titanium dental implants for rapid osseointegration. Dent Mater. 2007; 23(7): 844–854. doi:10.1016/j.dental.2006.06.025 - 59.
Liu X, Chu PK, Ding C. Surface modification of titanium, titanium alloys, and related materials for biomedical applications. Mater Sci Eng R Rep. 2004; 47(3–4): 49–121. doi:10.1016/j.mser.2004.11.001 - 60.
Jones FH. Teeth and bones: applications of surface science to dental materials and related biomaterials. Surf Sci Rep. 2001; 42(3–5): 75–205. doi:10.1016/S0167-5729(00)00011-X - 61.
Aparicio C, Gil FJ, Fonseca C, Barbosa M, Planell JA. Corrosion behaviour of commercially pure titanium shot blasted with different materials and sizes of shot particles for dental implant applications. Biomaterials. 2003; 24(2): 263–273. doi:10.1016/S0142-9612(02)00314-9 - 62.
Kokubo T, Miyaji F, Kim HM, Nakamura T. Spontaneous formation of bonelike apatite layer on chemically treated titanium metals. J Am Ceram Soc. 1996; 79(4): 1127–1129. doi:10.1111/j.1151-2916.1996.tb08561.x - 63.
Aparicio C, Gil FJ, Planell JA. Human-osteoblast proliferation and differentiation on grit-blasted and bioactive titanium for dental applications. J Mater Sci Mater Med. 2002; 13(12): 1105–1111. - 64.
Gil FJ, Padrós A, Manero JM, Aparicio C, Nilsson M, Planell JA. Growth of bioactive surfaces on titanium and its alloys for orthopaedic and dental implants. Mater Sci Eng C. 2002; 22(1): 53–60. doi:10.1016/S0928-4931(01)00389-7 - 65.
Aparicio C, Rodriguez D, Gil FJ. Variation of roughness and adhesion strength of deposited apatite layers on titanium dental implants. Mater Sci Eng C. 2011; 31(2): 320–324. doi:10.1016/j.msec.2010.09.018 - 66.
Gil FJ, Manzanares N, Badet A, Aparicio C. Biomimetic treatment on dental implants for short-term bone regeneration. Clin Oral Investig. 2014; 18(1): 59–66. doi:10.1007/s00784-013-0953-z - 67.
Gil FJ, Espinar E, Llamas JM, Sevilla P. Fatigue live of bioactive titanium dental implants treated by means of grit-blasting and thermo-chemical treatment. Clin Implant Dent Res. 2014; 16(2): 273–281. doi:10.1111/j.1708-8208.2012.00468.x - 68.
Albertini M, Fernández-Yague M, Lázaro P, Herrero-Climent, et al . Advances in surfaces and osseointegration in implantology. Biomimetic surfaces. Med Oral Patol Oral Cir Bucal. 2015; 20(3): 316–325. - 69.
Pachauri P, Bathala LR, Sangur R. Techniques for dental implant nanosurface modifications. J Adv Prosthodont. 2014; 6(6): 498–504. doi:10.4317/medoral.20353 - 70.
Park J, Bauer S, Schlegel KA, Neukam FW, von der Mark K, Schmuki P. TiO2 nanotube surfaces: 15 nm-an optimal length scale of surface topography for cell adhesion and differentiation. Small. 2009; 5: 666–671. doi:10.1002/smll.200801476 - 71.
Sjöström T, Dalby MJ, Hart A, Tare R, Oreffo RO, Su B. Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells. Acta Biomater. 2009; 5(5): 1433–1441. doi:10.1016/j.actbio.2009.01.007 - 72.
Cho SA, Park KT. The removal torque of titanium screw inserted in rabbit tibia treated by dual acid etching. Biomaterials. 2003; 24(20): 3611–3617. doi:10.1016/S0142-9612(03)00218-7 - 73.
Al-Radha ASD, Dymock D, Younes C, O’Sullivan D. Surface properties of titanium and zirconia dental implant materials and their effect on bacterial adhesion. J Dent. 2012; 40(2): 146–153. doi:10.1016/j.jdent.2011.12.006 - 74.
Novaes ABJr, Papalexiou V, Grisi MFM, Souza SSLS, Taba MJr, Kajiwara JK. Influence of implant microstructure on the osseointegration of immediate implants placed in periodontally infected sites. Clin Oral Implants Res. 2004; 15(1): 34–43. doi:10.1046/j.1600-0501.2003.00968.x - 75.
Suzuki K, Aoki K, Ohya K. Effects of surface roughness of titanium implants on bone remodeling activity of femur in rabbits. Bone. 1997; 21(6): 507–514. doi:10.1016/S8756-3282(97)00204-4 - 76.
Vanzillotta P, Soares GA, Bastos IN, Simao RA, Kuromoto NK. Potentialities of some surface characterization techniques for the development of titanium biomedical alloys. Mater Res. 2004; 7(3): 437–444. doi:10.1590/S1516-14392004000300011 - 77.
Takeuchi M, Abe Y, Yoshida Y, Nakayama Y, Okazaki M, Akagawa Y. Acid pretreatment of titanium implants. Biomaterials. 2003; 24(10): 1821–1827. doi:10.1016/S0142-9612(02)00576-8 - 78.
Ban S, Iwaya Y, Kono H, Sato H. Surface modification of titanium by etching in concentrated sulfuric acid. Dent Mater. 2006; 22(12): 1115–1120. doi:10.1016/j.dental.2005.09.007 - 79.
Vandrovcova M, Jirka I, Novotna K, Lisa V, Frank O, Kolska Z, Stary V, Bacakova L. Interaction of human osteoblast-like Saos-2 and MG-63 cells with thermally oxidized surfaces of a titanium-niobium alloy. Plos One 2014; 9: e100475. doi:10.1371/journal.pone.0100475 - 80.
Kim H, Choi SH, Ryu JJ, Koh SY, Park JH, Lee IS. The biocompatibility of SLA-treated titanium implants. Biomed Mater. 2008; 3(2): 025011. doi:10.1088/1748-6041/3/2/025011 - 81.
Aparicio C, Padrós A, Gil FJ. In vivo evaluation of micro-rough and bioactive titanium dental implants using histometry and pull-out tests. J Mech Behav Biomed Mater. 2011; 4(8): 1672–1682. doi:10.1016/j.jmbbm.2011.05.005 - 82.
Ban S, Iwaya Y, Kono H, Sato H. Surface modification of titanium by etching in concentrated sulfuric acid. Dent Mater. 2006; 22(12): 1115–1120. doi:10.1016/j.dental.2005.09.007 - 83.
Velasco-Ortega E, Jos A, Cameán AM, Pato-Mourelo J, Segura-Egea JJ. In vitro evaluation of cytotoxicity and genotoxicity of a commercial titanium alloy for dental implantology. Mutat Res Genet Toxicol Environ Mutagen. 2010; 702(1): 17–23. doi:10.1016/j.mrgentox.2010.06.013 - 84.
Braceras I, Alava JI, Oñateetal JI. Improved osseointegration in ion implantation-treated dental implants. Surf Coat Technol. 2002; 158–159: 28–32. doi:10.1016/S0257-8972(02)00203-7 - 85.
Rautray TR, Narayanan R, Kim KH. Ion implantation of titanium based biomaterials. Prog Mater Sci. 2011; 56(8): 1137–77. doi:10.1016/j.pmatsci.2011.03.002 - 86.
Hanawa T, Kamiura Y, Yamamoto S, Kohgo T, Amemiya A, Ukai H, Murakami K, Asaoka K. Early bone formation around calcium-ion-implanted titanium inserted into rat tibia. J Biomed Mater Res. 1997; 36(1): 131–136. doi:10.1002/(SICI)1097-4636(199707)36:1<131::AID-JBM16>3.0.CO;2-L - 87.
Rautray TR, Narayanan R, Kwon TY, Kim KH. Surface modification of titanium and titanium alloys by ion implantation. J Biomed Mater Res B Appl Biomater. 2010; 93B(2): 581–591. doi:10.1002/jbm.b.31596 - 88.
Fasasia AY, Mwenifumbob S, Rahbarb N, Chenb J, Lid M, Beyeb AC, Arnoldb CB, Soboyejob WO. Nano-second UV laser processed micro-grooves on Ti6Al4V for biomedical applications. Mater Sci Eng C. 2009; 29(1): 5–13. doi:10.1016/j.msec.2008.05.002 - 89.
Tanner A, Maiden MF, Lee K, Shulman LB, Weber HB. Dental implant infections. Clin Infect Dis. 1997; 25(Suppl. 2): S213–S217. - 90.
Mombelli A, Van Oosten MA, Schurch EJr, Lang NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol. 1987; 2(4): 145–151. doi:10.1111/j.1399-302X.1987.tb00298.x - 91.
Rams TE, Roberts TW, Feik D, Molzan AK, Slots J. Clinical and microbiological findings on newly inserted hydroxyapatite-coated and pure titanium human dental implants. Clin Oral Implant Res. 1991; 2: 121–127. doi:10.1034/j.1600-0501.1991.020304.x - 92.
Wu-Yuan CD, Eganhouse KJ, Keller JC, Walters KS. Oral bacterial attachment to titanium surfaces: a scanning electron microscopy study. J Oral Implantol. 1995; 21(3): 207–213. - 93.
Subramani K, Jung RE, Molenberg A. Hammerle CHF. Int J Oral Maxillofac Implants. 2009; 24: 616. - 94.
Mabboux F, Ponsonnet L, Morrier JJ, Jaffrezic N, Barsotti O. Surface free energy and bacterial retention to saliva-coated dental implant materials—an in vitro study. Colloid Surf B Biointerfaces. 2004; 39(4): 199–205. doi:10.1016/j.colsurfb.2004.08.002 - 95.
Sardin S, Morrier JJ, Benay G, Barsotti O. In vitro streptococcal adherence a prosthetic and implant materials. Interactions with physicochemical surface properties. J Oral Rehabil. 2004; 31(2): 140–148. doi:10.1046/j.0305-182X.2003.01136.x - 96.
Bundy KJ, Butler MF, Hochman RF. An investigation of the bacteriostatic properties of pure metals. J Biomed Mater Res. 1980; 14(5): 653–663. doi:10.1002/jbm.820140511 - 97.
Colon G, Ward BC, Webster TJ. Increased osteoblast and decreased Staphylococcus epidermidis functions on nanophase ZnO and TiO2. J Biomed Mater Res A. 2006; 78A(3): 595–604. doi:10.1002/jbm.a.30789 - 98.
Ewald A, Glückermann SK, Thull R, Gbureck U. Antimicrobial titanium/silver PVD coatings on titanium. Biomed Eng Online. 2006; 5: 22. doi:10.1186/1475-925X-5-22 - 99.
Lauson MC, Bowman CN, Anseth KS. Vancomycin derivative photopolymerized to titanium kills S. epidermidis . Clin Orthop Relat Res. 2007; 461: 96–105. doi:10.1097/BLO.0b013e3180986706