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1.  Osseointegration of zirconia implants: an SEM observation of the bone-implant interface 
Head & Face Medicine  2008;4:25.
The successful use of zirconia ceramics in orthopedic surgery led to a demand for dental zirconium-based implant systems. Because of its excellent biomechanical characteristics, biocompatibility, and bright tooth-like color, zirconia (zirconium dioxide, ZrO2) has the potential to become a substitute for titanium as dental implant material. The present study aimed at investigating the osseointegration of zirconia implants with modified ablative surface at an ultrastructural level.
A total of 24 zirconia implants with modified ablative surfaces and 24 titanium implants all of similar shape and surface structure were inserted into the tibia of 12 Göttinger minipigs. Block biopsies were harvested 1 week, 4 weeks or 12 weeks (four animals each) after surgery. Scanning electron microscopy (SEM) analysis was performed at the bone implant interface.
Remarkable bone attachment was already seen after 1 week which increased further to intimate bone contact after 4 weeks, observed on both zirconia and titanium implant surfaces. After 12 weeks, osseointegration without interposition of an interfacial layer was detected. At the ultrastructural level, there was no obvious difference between the osseointegration of zirconia implants with modified ablative surfaces and titanium implants with a similar surface topography.
The results of this study indicate similar osseointegration of zirconia and titanium implants at the ultrastructural level.
PMCID: PMC2583968  PMID: 18990214
2.  Behavior of osteoblastic cells cultured on titanium and structured zirconia surfaces 
Head & Face Medicine  2008;4:29.
Osseointegration is crucial for the long-term success of dental implants and depends on the tissue reaction at the tissue-implant interface. Mechanical properties and biocompatibility make zirconia a suitable material for dental implants, although surface processings are still problematic. The aim of the present study was to compare osteoblast behavior on structured zirconia and titanium surfaces under standardized conditions.
The surface characteristics were determined by scanning electron microscopy (SEM). In primary bovine osteoblasts attachment kinetics, proliferation rate and synthesis of bone-associated proteins were tested on different surfaces.
The results demonstrated that the proliferation rate of cells was significantly higher on zirconia surfaces than on titanium surfaces (p < 0.05; Student's t-test). In contrast, attachment and adhesion strength of the primary cells was significant higher on titanium surfaces (p < 0.05; U test). No significant differences were found in the synthesis of bone-specific proteins. Ultrastructural analysis revealed phenotypic features of osteoblast-like cells on both zirconia and titanium surfaces.
The study demonstrates distinct effects of the surface composition on osteoblasts in culture. Zirconia improves cell proliferation significantly during the first days of culture, but it does not improve attachment and adhesion strength. Both materials do not differ with respect to protein synthesis or ultrastructural appearance of osteoblasts. Zirconium oxide may therefore be a suitable material for dental implants.
PMCID: PMC2614982  PMID: 19063728
3.  Comparisons of maximum deformation and failure forces at the implant–abutment interface of titanium implants between titanium-alloy and zirconia abutments with two levels of marginal bone loss 
Zirconia materials are known for their optimal aesthetics, but they are brittle, and concerns remain about whether their mechanical properties are sufficient for withstanding the forces exerted in the oral cavity. Therefore, this study compared the maximum deformation and failure forces of titanium implants between titanium-alloy and zirconia abutments under oblique compressive forces in the presence of two levels of marginal bone loss.
Twenty implants were divided into Groups A and B, with simulated bone losses of 3.0 and 1.5 mm, respectively. Groups A and B were also each divided into two subgroups with five implants each: (1) titanium implants connected to titanium-alloy abutments and (2) titanium implants connected to zirconia abutments. The maximum deformation and failure forces of each sample was determined using a universal testing machine. The data were analyzed using the nonparametric Mann–Whitney test.
The mean maximum deformation and failure forces obtained the subgroups were as follows: A1 (simulated bone loss of 3.0 mm, titanium-alloy abutment) = 540.6 N and 656.9 N, respectively; A2 (simulated bone loss of 3.0 mm, zirconia abutment) = 531.8 N and 852.7 N; B1 (simulated bone loss of 1.5 mm, titanium-alloy abutment) = 1070.9 N and 1260.2 N; and B2 (simulated bone loss of 1.5 mm, zirconia abutment) = 907.3 N and 1182.8 N. The maximum deformation force differed significantly between Groups B1 and B2 but not between Groups A1 and A2. The failure force did not differ between Groups A1 and A2 or between Groups B1 and B2. The maximum deformation and failure forces differed significantly between Groups A1 and B1 and between Groups A2 and B2.
Based on this experimental study, the maximum deformation and failure forces are lower for implants with a marginal bone loss of 3.0 mm than of 1.5 mm. Zirconia abutments can withstand physiological occlusal forces applied in the anterior region.
PMCID: PMC3667051  PMID: 23688204
Abutment; Dental implant; Failure force; Maximum deformation force; Titanium alloy; Zirconia
4.  Surface Modifications of Dental Ceramic Implants with Different Glass Solder Matrices: In Vitro Analyses with Human Primary Osteoblasts and Epithelial Cells 
BioMed Research International  2014;2014:742180.
Ceramic materials show excellent esthetic behavior, along with an absence of hypersensitivity, making them a possible alternative implant material in dental surgery. However, their surface properties enable only limited osseointegration compared to titanium implants. Within this study, a novel surface coating technique for enhanced osseointegration was investigated biologically and mechanically. Specimens of tetragonal zirconia polycrystal (TZP) and aluminum toughened zirconia (ATZ) were modified with glass solder matrices in two configurations which mainly consisted of SiO2, Al2O3, K2O, and Na2O. The influence on human osteoblastic and epithelial cell viability was examined by means of a WST-1 assay as well as live/dead staining. A C1CP-ELISA was carried out to verify procollagen type I production. Uncoated/sandblasted ceramic specimens and sandblasted titanium surfaces were investigated as a reference. Furthermore, mechanical investigations of bilaterally coated pellets were conducted with respect to surface roughness and adhesive strength of the different coatings. These tests could demonstrate a mechanically stable implant coating with glass solder matrices. The coated ceramic specimens show enhanced osteoblastic and partly epithelial viability and matrix production compared to the titanium control. Hence, the new glass solder matrix coating could improve bone cell growth as a prerequisite for enhanced osseointegration of ceramic implants.
PMCID: PMC4177732  PMID: 25295270
5.  Response of osteoblast-like cells cultured on zirconia to bone morphogenetic protein-2 
The aim of this study was to compare osteoblast behavior on zirconia and titanium under conditions cultured with bone morphogenetic protein-2.
MC3T3-E1 cells were cultured on sandblasted zirconia and sandblasted/etched titanium discs. At 24 hours after seeding MC3T3-E1, the demineralized bone matrix (DBM) gel alone and the DBM gel with bone morphogenetic protein-2 (BMP-2) were added to the culture medium. The surface topography was examined by confocal laser scanning microscopy. Cellular proliferation was measured at 1, 4, and 7 days after gel loading. Alkaline phosphatase activity was measured at 7 days after gel loading. The mRNA expression of ALPase, bone sialoprotein, type I collagen, runt-related transcription factor 2 (Runx-2), osteocalcin, and osterix were evaluated by real-time polymerase chain reaction at 4 days and 7 days.
At 1, 4, and 7 days after loading the DBM gel alone and the DBM gel with BMP-2, cellular proliferation on the zirconia and titanium discs was similar and that of the groups cultured with the DBM gel alone and the DBM gel with BMP-2 was not significantly different, except for titanium with BMP-2 gel. ALPase activity was higher in the cells cultured with BMP-2 than in the other groups, but there was no difference between the zirconia and titanium. In ALPase, bone sialoprotein, osteocalcin, Runx-2 and osterix gene expression, that of cells on zirconia or titanium with BMP-2 gel was much more highly increased than titanium without gel at day 7. The gene expression level of cells cultured on zirconia with BMP-2 was higher than that on titanium with BMP-2 at day 7.
The data in this study demonstrate that the osteoblastic cell attachment and proliferation of zirconia were comparable to those of titanium. With the stimulation of BMP-2, zirconia has a more pronounced effect on the proliferation and differentiation of the osteoblastic cells compared with titanium.
PMCID: PMC3213233  PMID: 22087413
Bone morphogenetic protein-2; Cell differentiation; Cell proliferation; Zirconium oxide
6.  Heat and Radiofrequency Plasma Glow Discharge Pretreatment of a Titanium Alloy Promote Bone Formation and Osseointegration 
Journal of cellular biochemistry  2013;114(10):10.1002/jcb.24585.
Orthopedic and dental implants manifest increased failure rates when inserted into low density bone. We determined whether chemical pretreatments of a titanium alloy implant material stimulated new bone formation to increase osseointegration in vivo in trabecular bone using a rat model. Titanium alloy rods were untreated or pretreated with heat (600°C) or radiofrequency plasma glow discharge (RFGD). The rods were then coated with the extracellular matrix protein fibronectin (1 nM) or left uncoated and surgically implanted into the rat femoral medullary cavity. Animals were euthanized 3 or 6 weeks later, and femurs were removed for analysis. The number of trabeculae in contact with the implant surface, surface contact between trabeculae and the implant, and the length and area of bone attached to the implant were measured by histomorphometry. Implant shear strength was measured by a pull-out test. Both pretreatments and fibronectin enhanced the number of trabeculae bonding with the implant and trabeculae-to-implant surface contact, with greater effects of fibronectin observed with pretreated compared to untreated implants. RFGD pretreatment modestly increased implant shear strength, which was highly correlated (r2 = 0.87 – 0.99) with measures of trabecular bonding for untreated and RFGD-pretreated implants. In contrast, heat pretreatment increased shear strength 3 to 5-fold for both uncoated and fibronectin-coated implants at 3 and 6 weeks, suggesting a more rapid increase in implant-femur bonding compared to the other groups. In summary, our findings suggest that the heat and RFGD pretreatments can promote the osseointegration of a titanium alloy implant material.
PMCID: PMC3786157  PMID: 23649564
Dental implant; fibronectin; osteoblast; cell differentiation; bone mineralization; osseointegration
7.  Bacterial adhesion and colonization differences between zirconia and titanium implant abutments: an in vivo human study 
Several parameters have been described for determining the success or failure of dental implants. The surface properties of transgingival implant components have had a great impact on the long-term success of dental implants. The purpose of this study was to compare the tendency of two periodontal pathogens to adhere to and colonize zirconia abutments and titanium alloys both in hard surfaces and soft tissues.
Twelve patients participated in this study. Three months after implant placement, the abutments were connected. Five weeks following the abutment connections, the abutments were removed, probing depth measurements were recorded, and gingival biopsies were performed. The abutments and gingival biopsies taken from the buccal gingiva were analyzed using real-time polymerase chain reaction to compare the DNA copy numbers of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, and total bacteria. The surface free energy of the abutments was calculated using the sessile water drop method before replacement. Data analyses used the Mann Whitney U-test, and P-values below 0.05 find statistical significance.
The present study showed no statistically significant differences between the DNA copy numbers of A. actinomycetemcomitans, P. gingivalis, and total bacteria for both the titanium and zirconia abutments and the biopsies taken from their buccal gingiva. The differences between the free surface energy of the abutments had no influence on the microbiological findings.
Zirconia surfaces have comparable properties to titanium alloy surfaces and may be suitable and safe materials for the long-term success of dental implants.
PMCID: PMC3543937  PMID: 23346465
Bacterial adhesion; Dental abutments
8.  Initial bacterial adhesion on resin, titanium and zirconia in vitro 
The aim of this in vitro study was to investigate the adhesion of initial colonizer, Streptococcus sanguis, on resin, titanium and zirconia under the same surface polishing condition.
Specimens were prepared from Z-250, cp-Ti and 3Y-TZP and polished with 1 µm diamond paste. After coating with saliva, each specimen was incubated with Streptococcus sanguis. Scanning electron microscope, crystal violet staining and measurement of fluorescence intensity resulting from resazurin reduction were performed for quantifying the bacterial adhesion.
Surface of resin composite was significantly rougher than that of titanium and zirconia, although all tested specimens are classified as smooth. The resin specimens showed lower value of contact angle compared with titanium and zirconia specimens, and had hydrophilic surfaces. The result of scanning electron microscopy demonstrated that bound bacteria were more abundant on resin in comparison with titanium and zirconia. When total biofilm mass determined by crystal violet, absorbance value of resin was significantly higher than that of titanium or zirconia. The result of relative fluorescence intensities also demonstrated that the highest fluorescence intensity was found on the surface of resin. Absorbance value and fluorescence intensity on titanium was not significantly different from those on zirconia.
Resin specimens showed the roughest surface and have a significantly higher susceptibility to adhere Streptococcus sanguis than titanium and zirconia when surfaces of each specimen were polished under same condition. There was no significant difference in bacteria adhesion between titanium and zirconia in vitro.
PMCID: PMC3141123  PMID: 21814616
Biofilm; Resin; Titanium; Zirconia
9.  Techniques for dental implant nanosurface modifications 
Dental implant has gained clinical success over last decade with the major drawback related to osseointegration as properties of metal (Titanium) are different from human bone. Currently implant procedures include endosseous type of dental implants with nanoscale surface characteristics. The objective of this review article is to summarize the role of nanotopography on titanium dental implant surfaces in order to improve osseointegration and various techniques that can generate nanoscale topographic features to titanium implants.
A systematic electronic search of English language peer reviewed dental literature was performed for articles published between December 1987 to January 2012. Search was conducted in Medline, PubMed and Google scholar supplemented by hand searching of selected journals. 101 articles were assigned to full text analysis. Articles were selected according to inclusion and exclusion criterion. All articles were screened according to inclusion standard. 39 articles were included in the analysis.
Out of 39 studies, seven studies demonstrated that bone implant contact increases with increase in surface roughness. Five studies showed comparative evaluation of techniques producing microtopography and nanotopography. Eight studies concluded that osteoblasts preferably adhere to nano structure as compared to smooth surface. Six studies illustrated that nanotopography modify implant surface and their properties. Thirteen studies described techniques to produce nano roughness.
Modification of dental osseous implants at nanoscale level produced by various techniques can alter biological responses that may improve osseointegration and dental implant procedures.
PMCID: PMC4279049  PMID: 25558347
Intelligent surfaces; Sputtering; Superhydrophillic; Chemical vapor deposition; Osseointegration; Engineered surface
10.  Strain driven fast osseointegration of implants 
Although the bone's capability of dental implant osseointegration has clinically been utilised as early as in the Gallo-Roman population, the specific mechanisms for the emergence and maintenance of peri-implant bone under functional load have not been identified. Here we show that under immediate loading of specially designed dental implants with masticatory loads, osseointegration is rapidly achieved.
We examined the bone reaction around non- and immediately loaded dental implants inserted in the mandible of mature minipigs during the presently assumed time for osseointegration. We used threaded conical titanium implants containing a titanium2+ oxide surface, allowing direct bone contact after insertion. The external geometry was designed according to finite element analysis: the calculation showed that physiological amplitudes of strain (500–3,000 ustrain) generated through mastication were homogenously distributed in peri-implant bone. The strain-energy density (SED) rate under assessment of a 1 Hz loading cycle was 150 Jm-3 s-1, peak dislocations were lower then nm.
Bone was in direct contact to the implant surface (bone/implant contact rate 90%) from day one of implant insertion, as quantified by undecalcified histological sections. This effect was substantiated by ultrastructural analysis of intimate osteoblast attachment and mature collagen mineralisation at the titanium surface. We detected no loss in the intimate bone/implant bond during the experimental period of either control or experimental animals, indicating that immediate load had no adverse effect on bone structure in peri-implant bone.
In terms of clinical relevance, the load related bone reaction at the implant interface may in combination with substrate effects be responsible for an immediate osseointegration state.
PMCID: PMC1277014  PMID: 16270927
11.  Ag-plasma modification enhances bone apposition around titanium dental implants: an animal study in Labrador dogs 
Dental implants with proper antibacterial ability as well as ideal osseointegration are being actively pursued. The antimicrobial ability of titanium implants can be significantly enhanced via modification with silver nanoparticles (Ag NPs). However, the high mobility of Ag NPs results in their potential cytotoxicity. The silver plasma immersion ion-implantation (Ag-PIII) technique may remedy the defect. Accordingly, Ag-PIII technique was employed in this study in an attempt to reduce the mobility of Ag NPs and enhance osseointegration of sandblasted and acid-etched (SLA) dental implants. Briefly, 48 dental implants, divided equally into one control and three test groups (further treated by Ag-PIII technique with three different implantation parameters), were inserted in the mandibles of six Labrador dogs. Scanning electron microscopy, X-ray photoelectron spectroscopy, and inductively coupled plasma optical emission spectrometry were used to investigate the surface topography, chemical states, and silver release of SLA- and Ag-PIII-treated titanium dental implants. The implant stability quotient examination, Microcomputed tomography evaluation, histological observations, and histomorphometric analysis were performed to assess the osseointegration effect in vivo. The results demonstrated that normal soft tissue healing around dental implants was observed in all the groups, whereas the implant stability quotient values in Ag-PIII groups were higher than that in the SLA group. In addition, all the Ag-PIII groups, compared to the SLA-group, exhibited enhanced new bone formation, bone mineral density, and trabecular pattern. With regard to osteogenic indicators, the implants treated with Ag-PIII for 30 minutes and 60 minutes, with the diameter of the Ag NPs ranging from 5–25 nm, were better than those treated with Ag-PIII for 90 minutes, with the Ag NPs diameter out of that range. These results suggest that Ag-PIII technique can reduce the mobility of Ag NPs and enhance the osseointegration of SLA surfaces and have the potential for future use.
PMCID: PMC4298332  PMID: 25609967
surface modification; micro/nanostructure; silver; ion implantation; osseointegration
12.  Biomechanical evaluation of dental implants with different surfaces: Removal torque and resonance frequency analysis in rabbits 
Macroscopic and especially microscopic properties of implant surfaces play a major role in the osseous healing of dental implants. Dental implants with modified surfaces have shown stronger osseointegration than implants which are only turned (machined). Advanced surface modification techniques such as anodic oxidation and Ca-P application have been developed to achieve faster and stronger bonding between the host bone and the implant.
The purpose of this study was to investigate the effect of surface treatment of titanium dental implant on implant stability after insertion using the rabbit tibia model.
Three test groups were prepared: sandblasted, large-grit and acid-etched (SLA) implants, anodic oxidized implants, and anodized implants with Ca-P immersion. The turned implants served as control. Twenty rabbits received 80 implants in the tibia. Resonance frequencies were measured at the time of implant insertion, 2 weeks and 4 weeks of healing. Removal torque values (RTV) were measured 2 and 4 weeks after insertion.
The implant stability quotient (ISQ) values of implants for resonance frequency analysis (RFA) increased significantly (P < .05) during 2 weeks of healing period although there were no significant differences among the test and control groups (P > .05). The test and control implants also showed significantly higher ISQ values during 4 weeks of healing period (P < .05). No significant differences, however, were found among all the groups. All the groups showed no significant differences in ISQ values between 2 and 4 weeks after implant insertion (P > .05). The SLA, anodized and Ca-P immersed implants showed higher RTVs at 2 and 4 weeks of healing than the machined one (P < .05). However, there was no significant difference among the experimental groups.
The surface-modified implants appear to provide superior implant stability to the turned one. Under the limitation of this study, however, we suggest that neither anodic oxidation nor Ca-P immersion techniques have any advantage over the conventional SLA technique with respect to implant stability.
PMCID: PMC2994679  PMID: 21165264
surface treatment; bone to implant contact; removal torque; dental implant
13.  Investigation of anodized titanium implants coated with triterpenoids extracted from black cohosh: an animal study 
The purpose of this study was to evaluate bone response to anodized titanium implants coated with the extract of black cohosh, Asarum Sieboldii, and pharbitis semen.
Forty anodized titanium implants were prepared as follows: group 1 was for control; group 2 were implants soaked in a solution containing triterpenoids extracted from black cohosh for 24 hours; group 3 were implants soaked in a solution containing extracts of black cohosh and Asarum Sieboldii for 24 hours; group 4 were implants soaked in a solution containing extracts of pharbitis semen for 24 hours. The implants from these groups were randomly and surgically implanted into the tibiae of ten rabbits. After 1, 2, and 4 weeks of healing, the nondecalcified ground sections were subjected to histological observation, and the percentage of bone-to-implant contact (BIC%) was calculated.
All groups exhibited good bone healing with the bone tissue in direct contact with the surface of the implant. Group 2 (52.44 ± 10.98, 25.54 ± 5.56) showed a significantly greater BIC% compared to that of group 3 (45.34 ± 5.00, 22.24 ± 2.20) with respect to the four consecutive threads and total length, respectively. The BIC% of group 1 (25.22 ± 6.00) was significantly greater than that of group 3 (22.24 ± 2.20) only for total length.
This study did not show any remarkable effects of the extract of black coshosh and the other natural products on osseointegration of anodized titanium implants as coating agents. Further studies about the application method of the natural products on to the surface of implants are required.
PMCID: PMC3942522  PMID: 24605201
Titanium implant; Triterpenoid; Black cohosh; Pharbitis semen; Asarum Sieboldii; Bone-implant contact
14.  Osseointegration and biocompatibility of different metal implants - a comparative experimental investigation in sheep 
In the present study, 4 different metallic implant materials, either partly coated or polished, were tested for their osseointegration and biocompatibility in a pelvic implantation model in sheep.
Materials to be evaluated were: Cobalt-Chrome (CC), Cobalt-Chrome/Titanium coating (CCTC), Cobalt-Chrome/Zirconium/Titanium coating (CCZTC), Pure Titanium Standard (PTST), Steel, TAN Standard (TANST) and TAN new finish (TANNEW). Surgery was performed on 7 sheep, with 18 implants per sheep, for a total of 63 implants. After 8 weeks, the specimens were harvested and evaluated macroscopically, radiologically, biomechanically (removal torque), histomorphometrically and histologically.
Cobalt-Chrome screws showed significantly (p = 0.031) lower removal torque values than pure titanium screws and also a tendency towards lower values compared to the other materials, except for steel. Steel screws showed no significant differences, in comparison to cobalt-chrome and TANST, however also a trend towards lower torque values than the remaining materials. The results of the fluorescence sections agreed with those of the biomechanical test. Histomorphometrically, there were no significant differences of bone area between the groups. The BIC (bone-to-implant-contact), used for the assessment of the osseointegration, was significantly lower for cobalt-chrome, compared to steel (p = 0.001). Steel again showed a lower ratio (p = 0.0001) compared to the other materials.
This study demonstrated that cobalt-chrome and steel show less osseointegration than the other metals and metal-alloys. However, osseointegration of cobalt-chrome was improved by zirconium and/or titanium based coatings (CCTC, TANST, TAN, TANNEW) being similar as pure titanium in their osseointegrative behavior.
PMCID: PMC3315746  PMID: 22400715
15.  Biomechanical and Histological Evaluation of Roughened Surface Titanium Screws Fabricated by Electron Beam Melting 
PLoS ONE  2014;9(4):e96179.
Various fabrication methods are used to improve the stability and osseointegration of screws within the host bone. The aim of this study was to investigate whether roughened surface titanium screws fabricated by electron beam melting can provide better stability and osseointegration as compared with smooth titanium screws in sheep cervical vertebrae.
Roughened surface titanium screws, fabricated by electron beam melting, and conventional smooth surface titanium screws were implanted into sheep for 6 or 12 weeks (groups A and B, respectively). Bone ingrowth and implant stability were assessed with three-dimensional imaging and reconstruction, as well as histological and biomechanical tests.
No screws in either group showed signs of loosening. Fibrous tissue formation could be seen around the screws at 6 weeks, which was replaced with bone at 12 weeks. Bone volume/total volume, bone surface area/bone volume, and the trabecular number were significantly higher for a define region of interest surrounding the roughened screws than that surrounding the smooth screws at 12 weeks. Indeed, for roughened screws, trabecular number was significantly higher at 12 weeks than at 6 weeks. On mechanical testing, the maximum pullout strength was significantly higher at 12 weeks than at 6 weeks, as expected; however, no significant differences were found between smooth and roughened screws at either time point. The maximum torque to extract the roughened screws was higher than that required for the smooth screws.
Electron beam melting is a simple and effective method for producing a roughened surface on titanium screws. After 12 weeks, roughened titanium screws demonstrated a high degree of osseointegration and increased torsional resistance to extraction over smooth titanium screws.
PMCID: PMC4005762  PMID: 24788866
16.  In vivo assessment of the effect of controlled high- and low-frequency mechanical loading on peri-implant bone healing 
The aim of this study was to investigate the effect of controlled high- (HF) and low-frequency (LF) mechanical loading on peri-implant bone healing. Custom-made titanium implants were inserted in both tibiae of 69 adult Wistar rats. For every animal, one implant was loaded by compression through the axis of tibia (test), whereas the other one was unloaded (control). The test implants were randomly distributed among four groups receiving different loading regimes, which were determined by ex vivo calibration. Within the HF (40 Hz) or LF (2 Hz) loading category, the magnitudes were chosen as low- (LM) and high-magnitude (HM), respectively, leading to constant strain rate amplitudes for the two frequency groups. This resulted in the four loading regimes: (i) HF-LM (40 Hz–0.5 N); (ii) HF-HM (40 Hz–1 N); (iii) LF-LM (2 Hz–10 N); and (iv) LF-HM (2 Hz–20 N) loading. Loading was performed five times per week and lasted for one or four weeks. Tissue samples were processed for histology and histomorphometry (bone-to-implant contact, BIC; and peri-implant bone fraction, BF) at the cortical and medullar level. Data were analysed statistically with ANOVA and paired t-tests with the significance level set at 0.05. For the one-week experiments, an increased BF adjacent to the implant surface at the cortical level was exclusively induced by the LF-HM loading regime (2 Hz–20 N). Four weeks of loading resulted in a significant effect on BIC (and not on BF) in case of HF-LM loading (40 Hz–0.5 N) and LF-HM loading (2 Hz–20 N): BIC at the cortical level significantly increased under both loading regimes, whereas BIC at the medullar level was positively influenced only in case of HF-LM loading. Mechanical loading at both HF and LF affects osseointegration and peri-implant BF. Higher loading magnitudes (and accompanying elevated tissue strains) are required under LF loading to provoke a positive peri-implant bone response, compared with HF loading. A sustained period of loading at HF is needed to result in an overall enhanced osseointegration.
PMCID: PMC3367822  PMID: 22279157
implant; mechanobiology; animal; osseointegration; loading frequency
17.  Surface Contaminants Inhibit Osseointegration in a Novel Murine Model 
Bone  2011;49(5):923-930.
Surface contaminants, such as bacterial debris and manufacturing residues, may remain on orthopaedic implants after sterilization procedures and affect osseointegration. The goals of this study were to develop a murine model of osseointegration in order to determine whether removing surface contaminants enhances osseointegration. To develop the murine model, titanium alloy implants were implanted into a unicortical pilot hole in the mid-diaphysis of the femur and osseointegration was measured over a five week time course. Histology, backscatter scanning electron microscopy and x-ray energy dispersive spectroscopy showed areas of bone in intimate physical contact with the implant, confirming osseointegration. Histomorphometric quantification of bone-to-implant contact and peri-implant bone and biomechanical pullout quantification of ultimate force, stiffness and work to failure increased significantly over time, also demonstrating successful osseointegration. We also found that a rigorous cleaning procedure significantly enhances bone-to-implant contact and biomechanical pullout measures by two-fold compared with implants that were autoclaved, as recommended by the manufacturer. The most likely interpretation of these results is that surface contaminants inhibit osseointegration. The results of this study justify the need for the development of better detection and removal techniques for contaminants on orthopaedic implants and other medical devices.
PMCID: PMC3200470  PMID: 21801863
contaminants; osseointegration; murine; histomorphometry; biomechanical testing
18.  Biological Functionalization of Dental Implants with Fibronectin: A Scanning Electron Microscopic Study 
Early stages of peri-implant bone formation play an essential role in the osseointegration and long-term success of dental implants. Biological implant surface coatings are an emerging technology to enhance the attachment of the implant to the surrounding bone and stimulate bone regeneration. The purpose of this study was to determine the effect of coating the implant surface with fibronectin on osseointegration.
Material and methods
The experiment was conducted on a total of twelve New Zealand white mature male rabbits, weight between 2.5–4 kg. Twenty four pure titanium implants were used in this study. Each rabbits received two implants, one implant in each tibia; the implant in the right limb was coated with fibronectin (experimental group), whilst on the contralateral side the implants were placed without coating (control group). Six rabbits were sacrificed for Scanning Electron Microscopic evaluation after 4 and 8 week healing periods.
The results of the present study demonstrating the mean gap distance between the bone and implant was greater in the control group compared to fibronection group at both observation periods however, the difference between these two groups was not statistically significant.
Thus, it could be suggested that the biological functionalization of dental implants with fibronectin, may influence the integration or biocompatibility and bonding of the implant to the surrounding bone.
PMCID: PMC4039585  PMID: 24899880
Dental implant; Osseointegration; Biofunctionalization; Extracellular matrix; Fibronectin
19.  Biomolecular surface coating to enhance orthopaedic tissue healing and integration 
Biomaterials  2007;28(21):3228-3235.
Implant osseointegration is a prerequisite for clinical success in orthopaedic and dental applications, many of which are restricted by loosening. Biomaterial surface modification approaches, including calcium-phosphate ceramic coatings and macro/microporosity, have had limited success in promoting integration. To improve osseointegration, titanium surfaces were coated with the GFOGER collagen-mimetic peptide, selectively promoting α2β1 integrin binding, a crucial event for osteoblastic differentiation. Titanium surfaces presenting GFOGER triggered osteoblastic differentiation and mineral deposition in bone marrow stromal cells, leading to enhanced osteoblastic function compared to unmodified titanium. Furthermore, this integrin-targeted coating significantly improved in vivo peri-implant bone regeneration and osseointegration, as characterized by bone-implant contact and mechanical fixation, compared to untreated titanium in a rat cortical bone-implant model. GFOGER-modified implants also significantly enhanced osseointegration compared to surfaces modified with full-length type I collagen, highlighting the importance of presenting specific biofunctional domains within the native ligand. In addition, this biomimetic implant coating is generated using a simple, single-step procedure that readily translates to a clinical environment with minimal processing and cytotoxicity concerns. Therefore, this study establishes a biologically active and clinically relevant implant coating strategy that enhances bone repair and orthopaedic implant integration.
PMCID: PMC2034748  PMID: 17448533
biomimetic material; cell adhesion; collagen; osseointegration; integrin
20.  Multiple teeth replacement with endosseous one-piece yttrium-stabilized zirconia dental implants 
Objectives: The purpose of this study is to clinically and radiographically evaluate survival and success rate of multiple zirconia dental implants positioned in each patient during a follow-up period of at least 12 months up to 48 months. Study Design: Eight patients were treated for multiple edentulism with 29 zirconia dental implants. All implants received immediate temporary restorations and 6 months after surgery were definitively restored. 6 months to 4 years after implant insertion, a clinical-radiographic evaluation was performed in order to estimate peri-implant tissues health and peri-implant marginal bone loss. Results: Survival rate within follow-up period was therefore 100%. The average marginal bone loss (MBL) from baseline to 6 months was +1.375±0.388 mm; from 6 months to 1 year was +0.22±0.598 mm; from 1 year to 2 years was -0.368±0.387 mm; from 2 years to 3 years was -0.0669±0.425 mm; from 3 years to 4 years +0.048±0.262 mm. The mean marginal bone loss at 4 years from the implants insertion was +1.208 mm. Conclusions: According to several studies, when using a radiographic criterion for implant success, marginal bone loss below 0.9-1.6 mm during the first year in function can be considered acceptable. In our work, radiographic measurements of MBL showed values not exceeding 1.6 mm during the first year of loading and also 1 year up to 4 years after surgery further marginal bone loss was minimal and not significant. This peri-implant bone preservation may be associated to the absence of micro-gap between fixture and abutment since zirconia dental implants are one-piece implant. Moreover, zirconia is characterized by high biocompatibility and it accumulates significantly fewer bacteria than titanium.
Key words:Zirconia dental implants, multiple implants, radiographic evaluation, marginal bone loss (MBL).
PMCID: PMC3505720  PMID: 22926479
21.  An In Vitro Evaluation of the Biological Effects of Carbon Nanotube-Coated Dental Zirconia 
ISRN Dentistry  2013;2013:296727.
The purpose of this study is to evaluate functionalized multiwalled carbon nanotubes (fMWCNTs) as a potential coating material for dental zirconia from a biological perspective: its effect on cell proliferation, viability, morphology, and the attachment of an osteoblast-like cell. Osteoblast-like (Saos-2) cells were seeded on uncoated and fMWCNT-coated zirconia discs and in culture dishes that served as controls. The seeding density was 104 cells/cm2, and the cells were cultured for 6 days. Cell viability, proliferation and attachment of the Saos-2 cells were studied. The results showed that Saos-2 cells were well attached to both the uncoated and the fMWCNT-coated zirconia discs. Cell viability and proliferation on the fMWCNT-coated zirconia discs were almost the same as for the control discs. Better cell attachment was seen on the fMWCNT-coated than on the uncoated zirconia discs. In conclusion, fMWCNTs seem to be a promising coating material for zirconia-based ceramic surfaces to increase the roughness and thereby enhance the osseointegration of zirconia implants.
PMCID: PMC3762083  PMID: 24027638
22.  Acid Etching and Plasma Sterilization Fail to Improve Osseointegration of Grit Blasted Titanium Implants 
Interaction between implant surface and surrounding bone influences implant fixation. We attempted to improve the bone-implant interaction by 1) adding surface micro scale topography by acid etching, and 2) removing surface-adherent pro-inflammatory agents by plasma cleaning. Implant fixation was evaluated by implant osseointegration and biomechanical fixation.
The study consisted of two paired animal sub-studies where 10 skeletally mature Labrador dogs were used. Grit blasted titanium alloy implants were inserted press fit in each proximal tibia. In the first study grit blasted implants were compared with acid etched grit blasted implants. In the second study grit blasted implants were compared with acid etched grit blasted implants that were further treated with plasma sterilization. Implant performance was evaluated by histomorphometrical investigation (tissue-to-implant contact, peri-implant tissue density) and mechanical push-out testing after four weeks observation time.
Neither acid etching nor plasma sterilization of the grit blasted implants enhanced osseointegration or mechanical fixation in this press-fit canine implant model in a statistically significant manner.
PMCID: PMC3434975  PMID: 22962567
Acid etching; biocompatibility; endotoxin; implant surgery; grit blasting; plasma sterilization; titanium.
23.  Systemic intermittent parathyroid hormone treatment improves osseointegration of press-fit inserted implants in cancellous bone 
Acta Orthopaedica  2012;83(4):411-419.
Background and purpose
Intermittent administration of parathyroid hormone (PTH) has an anabolic effect on bone, as confirmed in human osteoporosis studies, distraction osteogenesis, and fracture healing. PTH in rat models leads to improved fixation of implants in low-density bone or screw insertion transcortically.
Material and methods
We examined the effect of human PTH (1–34) on the cancellous osseointegration of unloaded implants inserted press-fit in intact bone of higher animal species. 20 dogs were randomized to treatment with human PTH (1–34), 5 μg/kg/day subcutaneously, or placebo for 4 weeks starting on the day after insertion of a cylindrical porous coated plasma-sprayed titanium alloy implant in the proximal metaphyseal cancellous bone of tibia. Osseointegration was evaluated by histomorphometry and fixation by push-out test to failure.
Surface fraction of woven bone at the implant interface was statistically significantly higher in the PTH group by 1.4 fold with (median (interquartile range) 15% (13–18)) in the PTH group and 11% (7–13) in control. The fraction of lamellar bone was unaltered. No significant difference in bone or fibrous tissue was observed in the circumferential regions of 0–500, 500–1,000, and 1,000–2,000 μm around the implant. Mechanically, the implants treated with PTH showed no significant differences in total energy absorption, maximum shear stiffness, or maximum shear strength.
Intermittent treatment with PTH (1–34) improved xhistological osseointegration of a prosthesis inserted press-fit at surgery in cancellous bone, with no additional improvement of the initial mechanical fixation at this time point.
PMCID: PMC3427634  PMID: 22880714
24.  Early loading of hydrophilic titanium implants inserted in low-mineralized (D3 and D4) bone: one year results of a prospective clinical trial 
Head & Face Medicine  2013;9:37.
Pure titanium is the material of choice for contemporary dental implants. However, superficial reaction of the moderately rough titanium surface with atmospheric components decreases its hydrophilicity. INICELL® represents a chemical alteration and hydrophilization of a moderately rough i. e. sand-blasted and acid-etched titanium surface. The hydrophilicity leads to a more homogenous adsorption of proteins on the implant surface in-vitro, supporting the activation of a higher number of platelets and the generation of a homogenous, complete fibrin matrix in the early phases of osseointegration. This in turn helps to reduce the healing time and enhances the predictability of osseointegration in compromised bony situations.
The objective of this case series trial was therefore to investigate if early loading (after 8 weeks) of hydrophilic INICELL implants is feasible in patients with reduced bone quality.
In 10 patients, 35 hydrophilic implants were placed in sites revealing bone quality class 3 and 4, and uncovered after 4 weeks. Eight weeks later implants were released for loading if the tactile resistance was ≥35 Ncm. Lower resistances resulted in 12 weeks initial healing period. Insertion torque, ISQ, tactile resistance and vertical bone level were evaluated at implant installation, after 4 weeks (uncovering), 8 or 12 weeks (loading), and 12 weeks and one year after loading.
Mean implant insertion torque was 21 Ncm. 31 (88.6%) showed a tactile resistance of >35 Ncm after eight weeks and were released for prosthetic loading. Eight weeks after insertion, one implant (2.9%) had to be removed following a soft tissue complication. One implant had to be removed after 4 weeks due to a technical complication (fractured Osstell-abutment), it was therefore excluded from the analysis.
33 of 34 implants (97%) were loaded to occlusion and were in situ/functional one year after implantation. ISQs increased from 43 at baseline to 63 at eight weeks, and 72 at three months after loading. Then, ISQ remained constant until one year after loading.
Within the limitations of this prospective case series, hydrophilic implants may allow for shortening of the initial healing period even in bone with compromised density.
PMCID: PMC3866303  PMID: 24321192
Titanium implants; Hydrophilic surface; Healing time; Bone quality; Weak bone
25.  Characteristics and osteogenic effect of zirconia porous scaffold coated with β-TCP/HA 
The purpose of this study was to evaluate the properties of a porous zirconia scaffold coated with bioactive materials and compare the in vitro cellular behavior of MC3T3-E1 preosteoblastic cells to titanium and zirconia disks and porous zirconia scaffolds.
Titanium and zirconia disks were prepared. A porous zirconia scaffold was fabricated with an open cell polyurethane disk foam template. The porous zirconia scaffolds were coated with β-TCP, HA and a compound of β-TCP and HA (BCP). The characteristics of the specimens were evaluated using scanning electron microscopy (SEM), energy dispersive x-ray spectrometer (EDX), and x-ray diffractometry (XRD). The dissolution tests were analyzed by an inductively coupled plasma spectrometer (ICP). The osteogenic effect of MC3T3-E1 cells was assessed via cell counting and reverse transcriptase-polymerase chain reaction (RT-PCR).
The EDX profiles showed the substrate of zirconia, which was surrounded by the Ca-P layer. In the dissolution test, dissolved Ca2+ ions were observed in the following decreasing order; β-TCP > BCP > HA (P<.05). In the cellular experiments, the cell proliferation on titanium disks appeared significantly lower in comparison to the other groups after 5 days (P<.05). The zirconia scaffolds had greater values than the zirconia disks (P<.05). The mRNA level of osteocalcin was highest on the non-coated zirconia scaffolds after 7 days.
Zirconia had greater osteoblast cell activity than titanium. The interconnecting pores of the zirconia scaffolds showed enhanced proliferation and cell differentiation. The activity of osteoblast was more affected by microstructure than by coating materials.
PMCID: PMC4146729  PMID: 25177472
Zirconia porous scaffold; Osteogenic effect; Cellular response; β-TCP; HA

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