This study evaluated 3 implant surfaces in a dog model: (1) resorbable-blasting media + acid-etched (RBMa), alumina-blasting + acid-etching (AB/AE), and AB/AE + RBMa (hybrid). All of the surfaces were minimally rough, and Ca and P were present for the RBMa and hybrid surfaces. Following 2 weeks in vivo, no significant differences were observed for torque, bone-to-implant contact, and bone-area fraction occupied measurements. Newly formed woven bone was observed in proximity with all surfaces.

Introduction

The contact between bone and endosseous implants is usually well established and maintained after implant placement, resulting in a success rate often exceeding 90% over 10 years.1,2  Past investigations have shown that surface modification methods have been successful in increasing the host response to the implants, resulting in better long-term bone morphology as well as the initial interaction between the host and the implant.3  As a result, surface modifications in texture and chemistry such as increasing the roughness and the addition of calcium- and phosphorus-based bioceramic coatings are among the most investigated aspects of the implant studies.36 

In previous studies, surface texture modification has proven to be effective in increasing the host response in in vivo, in vitro, and ex vivo studies.7  More bone-to-implant interaction has been shown in surfaces with increased roughness as compared with as-machined or smooth surfaces (Sa < 0.5 μm). The best osseointegration measurable by bone-to-implant contact (BIC) has been shown in the moderately rough surfaces (Sa between 1 and 2 μm).36  Surface roughness can be achieved in a variety of ways, including acid etching, anodization, and grit blasting with nonresorbable media such as alumina, silica, or titanium oxides or with resorbable-blasting media (RBM) such as hydroxyapatite, tricalcium phosphates, or a combination of Ca-P phases followed by acid etching or passivation treatment that leaves little to absent amount of Ca and P on the final product.3 

Increasing the surface roughness has resulted in improved early host-to-implant response, but a surface chemistry alteration involving bioceramic coating of implants using the thick plasma-sprayed hydroxyapatite (PSHA) has shown to result in higher degrees of fixation at earlier implantation times compared with moderately rough uncoated implants.810  However, PSHA-coated implants rely on mechanical interlocking between the grit-blasted or etched metallic surfaces and the ceramic-like PSHA coating, and this physical interaction among the bulk metallic, metallic oxide, and bioceramic surface has been considered a weak link based on frequent adhesive failures that have reportedly occurred on different implant configurations.810 

In an attempt to take advantage of increased osseoconductivity of the Ca-P while avoiding the mechanical drawbacks of PSHA coatings, integration of Ca-P particles at a reduced amount through various techniques such as ion beam–assisted deposition,1113  sputtering,14,15  discrete crystalline deposition,1619  and RBM20,21  processes have shown promising results as compared with uncoated, roughened implants. Specific to RBM processing, various factors such as blasting media composition, blasting particle size, processing parameters such as blasting pressure and distance, and subsequent acid etching are shown to have effect on early host-to-implant surfaces.3  However, the amount and the form of Ca-P that demonstrate optimal host-bone interaction have not been determined conclusively. Consequently, the aim of this investigation was to evaluate the biomechanical fixation and to histomorphologically and histomorphometrically characterize 3 different implant surfaces: (1) RBM + acid etching (RBMa), (2) alumina blasting + acid-etching (AB/AE), and (3) AB/AE + RBMa surface (hybrid).

Materials and Methods

The endosseous Ti-6Al-4V implants used in this study were 3.75 mm in diameter by 10 mm in length. Three surface modifications were investigated: RBMa, AB/AE, and the hybrid.

The AB/AE surface was achieved by blasting the surface with large particles of Al2O3 with a size of ∼300 to 400 μm followed by acid etching with hydrochloric/sulfuric acid. The RBMa surface was achieved by blasting with HA/TCP (20%/80% ratio) particles with a size of ∼200 to 400 μm followed by cleaning with HNO3 at room temperature for 10 minutes. The hybrid surface (AB/AE + RBMa) was obtained by first applying the AB/AE treatment and subsequently applying the RBMa surface treatment. All implant surfaces were sterilized under gamma radiation.

Surface characterization

Nine implants (n = 3 each group) were used for surface topography assessment by scanning electron microscopy (SEM) and atomic force microscopy (AFM). SEM (Philips XL 30, Eindhoven, the Netherlands) was performed at various magnifications under an acceleration voltage of 15 kV. Surface 3-dimensional (3D) imaging was collected by AFM (Nanoscope IIIa Multimode system, Digital Instruments, Santa Barbara, Calif) in contact mode. A scanner with a maximum 125-μm horizontal and 5-μm vertical range and a 200-μm Si3N4 cantilever tip using a constant force of 0.12 N/m was used. The region analyzed was the flat part of the implant cutting edges, and 35- × 35-μm scan areas were used.22,23 Three scans per implant were performed, and Sa (arithmetic mean of the absolute value of the height within the sampling area) and Sq (root mean square value of the surface departures within the sampling area) parameters determined. Statistical analysis at the 95% level of significance was performed by one-way analysis of variance.

Surface-specific chemical assessment was performed by x-ray photoelectron spectroscopy (XPS). The implants were inserted in a vacuum transfer chamber and degassed to 10−7 torr. The samples were then transferred under vacuum to a Kratos Axis 165 multitechnique XPS spectrometer (Kratos Analytical Inc, Chestnut Ridge, NY). Survey and high-resolution spectra were obtained using a 165-mm mean radius concentric hemispherical analyzer operated at constant pass energy of 160 eV for survey and 80 eV for high-resolution scans. The take-off angle was 90°, and a spot size of 150 μm × 150 μm was used. The implant surfaces were evaluated at various locations.

In vivo laboratory model

For the animal model, 16 implants of each of the 3 surfaces were used. The study was composed of 8 adult male beagle dogs ∼1.5 years of age. The protocol received the approval of the Ethics Committee for Animal Research at Pontifica Universidade Católica do Rio Grande do Sul, Brazil.

Prior to general anesthesia, intramuscular atropine sulfate (0.044 mg/kg) and xilazine chlorate (8 mg/kg) were administered. A 15-mg/kg ketamine chlorate dose was then used to achieve general anesthesia.

The proximal medial tibia on the right side was initially shaved with a razor blade and followed by the application of antiseptic iodine solution. An incision through the skin of ∼5 cm in length was used for access to the periosteum, which was elevated for bone exposure.

Standardized osteotomies were made with sequential drills (pilot drill, followed by 2 mm, 2.5 mm, 3.0 mm, 3.5 mm) at 1200 rpm under abundant saline irrigation. The first implant was inserted 2 cm below the joint capsule line at the central anteromedial position of the proximal tibiae (procedures were performed bilaterally). The other two devices were placed along the distal direction at distances of 1 cm from each other along the central region of the bone. The implants were screwed into the drilled sites with a torque wrench and remained for 2 weeks. It should be noted that because of the dimensional interplay between drilling and implant design (implant threads' 3.25-mm inner diameter and the osteotomy's 3.5-mm diameter), intimate contact was achieved between bone and the implant microthreads in the cervical region, and healing chambers were created at regions where larger threads were present. The order in which the implants with different surfaces were placed was alternated along the tibia, with the starting implant being interchanged in every tibia. Balanced surgical procedures were used to allow the comparison of the torque and histology of same number of implant surfaces, surgical site (1 through 3), and animal at 2 weeks.

To avoid any damage to the implant-bone interface due to removal of a callus overgrowth after limb retrieval, a cover screw was installed in each implant. Standard layered suture techniques were used for wound closure (4-0 vicryl, internal layers; 4-0 nylon, the skin). Postsurgical medication included antibiotics (penicillin, 20 000 UI/kg) and analgesics (ketoprophen, 1 mL/5 kg) for a period of 48 hours postoperatively. The euthanasia was performed by anesthesia overdose 2 weeks after placement.

At necropsy, the limbs were retrieved by sharp dissection, the soft tissue was removed by surgical blades, and initial clinical evaluation was performed to determine implant stability. Half of the implants (specimens from the right limb) were then referred to biomechanical testing, and the other half (specimens from the left limb) were processed for histology.

For the torque testing, the tibia was adapted to an electronic torque machine equipped with a 200-Ncm torque load cell (Test Resources, Minneapolis, Minn). Custom machined tooling was adapted to each implant's internal connection, and the bone block was carefully positioned to avoid specimen misalignment during testing. The implants were torqued in the counterclockwise direction at a rate of ∼0.196 radians/min, and a torque vs displacement curve was recorded for each specimen.

For histology processing, the bone blocks were kept in 10% buffered formalin solution for 24 hours, washed in running water for 24 hours, and gradually dehydrated in a series of alcohol solutions ranging from 70% to 100% ethanol. Following dehydration, the samples were embedded in a methacrylate-based resin (Technovit 9100, Heraeus Kulzer GmbH, Wehrheim, Germany) according to the manufacturer's instructions. The blocks were then cut into slices (∼300 μm thickness), aiming the center of the implant along its long axis with a precision diamond saw (Isomet 2000, Buehler Ltd, Lake Bluff, Ill), and glued to acrylic plates with an acrylate-based cement, and a 24-hour setting time was allowed prior to grinding and polishing. The sections were then reduced to a final thickness of ∼30 μm by means of a series of SiC abrasive papers (400, 600, 800, 1200, and 2400; Buehler Ltd) in a grinding/polishing machine (Metaserv 3000, Buehler Ltd) under water irrigation.24  The sections were then stained with toluidine blue and referred to optical microscopy evaluation.

The BIC was determined at ×50 to ×200 magnification (Leica DM2500M, Leica Microsystems GmbH, Wetzlar, Germany) by means of computer software (Leica Application Suite, Leica Microsystems GmbH). The regions of BIC along the implant perimeter were subtracted from the total implant perimeter, and calculations were performed to determine the BIC. The bone area fraction occupied (BAFO) between threads in trabecular bone regions was determined at ×100 magnification (Leica DM2500M, Leica Microsystems GmbH) by means of computer software (Leica Application Suite, Leica Microsystems GmbH). The areas occupied by bone were subtracted from the total area between threads, and calculations were performed to determine the BAFO (reported in percentage values of BAFO).25 

Friedman's test at the 95% level of significance and Dunn's post hoc test were used for multiple comparisons between groups for torque, BIC, and BAFO.

Results

The implant surfaces' electron micrographs and 3D atomic force microscopies are presented in Figures 1 and 2, respectively. The AB/AE presented a minimally rough surface without the presence of embedded alumina particles (Figure 1a), while the RBMa surface electron micrographs showed that the acid-etching procedure was partially effective at removing embedded blasting media particles (Figure 1b). The hybrid surface presented a morphology similar to the RBMa surface (Figure 1c). The AFM assessment showed that the AB/AE surface presented significantly higher mean Sa (P < .03) and Sq (P < .04) values compared with the RBMa (Figure 3). The hybrid surface roughness presented intermediate values (Figure 3).

Figure 1.

Implant surfaces' electron micrographs of (a) alumina-blasting + acid-etching surface depicting a surface without the presence of embedded alumina particles. (b) The resorbable-blasting media + acid-etched (RBMa) micrograph shows a surface with evidence that the acid-etching procedure was partially effective at removing embedded blasting media particles. (c) The hybrid surface presenting a similar morphology to the RBMa surface.

Figure 1.

Implant surfaces' electron micrographs of (a) alumina-blasting + acid-etching surface depicting a surface without the presence of embedded alumina particles. (b) The resorbable-blasting media + acid-etched (RBMa) micrograph shows a surface with evidence that the acid-etching procedure was partially effective at removing embedded blasting media particles. (c) The hybrid surface presenting a similar morphology to the RBMa surface.

Figure 2.

Three-dimensional atomic force microscopies of (a) alumina-blasting + acid-etching, (b) resorbable-blasting media + acid-etched, and (c) hybrid surface.

Figure 2.

Three-dimensional atomic force microscopies of (a) alumina-blasting + acid-etching, (b) resorbable-blasting media + acid-etched, and (c) hybrid surface.

Figures 3–4.

Figure 3. Atomic force microscopy assessment of measurable roughness parameters showed that the alumina-blasting + acid-etching surface presented significantly higher mean Sa (P < .03) and Sq (P < .04) values compared with resorbable-blasting media + acid-etched. The hybrid surface roughness presented intermediate values. All surfaces were in the minimally rough range (Sa 0.5–1 μm). The number of asterisks denotes statistically homogeneous groups. Figure 4. Removal torque statistics summary (mean ± 95% confidence interval) for the different surfaces at 3 weeks.

Figures 3–4.

Figure 3. Atomic force microscopy assessment of measurable roughness parameters showed that the alumina-blasting + acid-etching surface presented significantly higher mean Sa (P < .03) and Sq (P < .04) values compared with resorbable-blasting media + acid-etched. The hybrid surface roughness presented intermediate values. All surfaces were in the minimally rough range (Sa 0.5–1 μm). The number of asterisks denotes statistically homogeneous groups. Figure 4. Removal torque statistics summary (mean ± 95% confidence interval) for the different surfaces at 3 weeks.

The AB/AE XPS survey analysis showed peaks of Ti, Al, V, C, and O (Table), while the RBMa and hybrid surfaces presented Ti, Al, Ca, C, P, and N (Table). High-resolution spectrum evaluation showed that for all surfaces, titanium was found primarily as TiO2 with a very low level of metallic Ti, and carbon was observed primarily as hydrocarbon (C-C, C-H) with lower levels of oxidized carbon forms. For both the RBMa and hybrid groups, calcium and phosphate were detected in varied atomic concentrations. For the RBMa and hybrid groups, calcium and phosphate atomic concentrations ranged from ∼1 to 3.5 and ∼1 to ∼2.5 atomic percentage, respectively.

Table

Average chemical composition for the 3 different surfaces (atomic percentage)*

Average chemical composition for the 3 different surfaces (atomic percentage)*
Average chemical composition for the 3 different surfaces (atomic percentage)*

The animal surgical procedures and follow-up demonstrated no complications regarding procedural conditions, postoperative infection, or other clinical concerns. The biomechanical testing results showed that implant surface did not have a significant effect on torque to interface fracture (P = .51; Figure 4).

Qualitative evaluation of the toluidine blue–stained thin sections showed intimate contact between cortical and trabecular bone (Figure 5) for all implant surfaces, showing that all 3 surfaces are biocompatible and osseoconductive. At 2 weeks, newly formed woven bone was observed in close proximity to all implant surfaces (Figure 6). The histomorphometric results demonstrated that the implant surface also did not have a significant effect on BIC and BAFO (P = .46 and P = .64; Figures 7a and 7b, respectively).

Figure 5.

Representative optical microscopy montage depicting close contact between implant surfaces and cortical and trabecular bone regions (toluidine blue staining; original magnification ×25).

Figure 5.

Representative optical microscopy montage depicting close contact between implant surfaces and cortical and trabecular bone regions (toluidine blue staining; original magnification ×25).

Figure 6.

Representative histologic section at 3 weeks for (a) alumina-blasting + acid-etching, (b) resorbable-blasting media + acid-etched, and (c) hybrid surfaces. Note the close proximity of newly formed woven bone with all implant surfaces.

Figure 6.

Representative histologic section at 3 weeks for (a) alumina-blasting + acid-etching, (b) resorbable-blasting media + acid-etched, and (c) hybrid surfaces. Note the close proximity of newly formed woven bone with all implant surfaces.

Figure 7.

(a) Bone-to-implant contact and (b) bone area fraction occupied statistics summary (mean ± 95% confidence interval) for the different surfaces. The number of asterisks denotes statistically homogeneous groups.

Figure 7.

(a) Bone-to-implant contact and (b) bone area fraction occupied statistics summary (mean ± 95% confidence interval) for the different surfaces. The number of asterisks denotes statistically homogeneous groups.

Discussion

As a result of years of implant dentistry research, the implant surface modification has evolved from as-machined, smooth surfaces to microscopically moderately roughened surfaces that have shown to enhance bone healing after the placement of implants.3,4,7,26,27  Subsequent surface chemistry modifications such as the incorporation of bioactive ceramics have long been the focus of investigations as a positive factor for improved early bone healing. However, considering that surface chemistry modifications typically involve changes in surface topography,28  it is still unclear whether resulting topography changes alone and/or the combination with chemical modifications leads to improved osseointegration.5 

The surface treatments investigated in this study composed an alumina-blasted/acid-etched control, an RBMa, and a hybrid surface that combined AB/AE followed by RBMa treatment. A previous study has shown that subsequent etching RBM (RBMa) substantially reduced Ca and P amounts on the surface yet with no differences in removal torque, BIC, and BAFO when compared with a rougher control AB/AE.21  Another investigation has observed improved torque at 2 times in vivo for an RBMa compared with an overall smoother dual acid-etched surface used as a control.20  Because the dual-acid etched surface in the latter study resulted in lower torque values compared with the RBMa,20  it was speculated that surface roughness, rather than chemistry, was likely the factor influencing improved bone response. The rationale for evaluating the different surfaces at 2 weeks in vivo in the beagle dog model was based on our previous investigations, which have shown that high degrees of biomechanical fixation occur as early as 3 weeks in the beagle dog long bones.21,2940  The bone-healing pattern and long-term remodeling dynamics have been shown to be remarkably similar between species.41  However, the literature is sparse concerning the quantification of healing kinetics around implants between species. Although osseointegration rates are known to be higher in animal models compared with humans, its quantification is yet to be experimentally determined.

The rationale of testing the hybrid surface was to bring the surface roughness of this group to an approximate scale to the AB/AE group combined with the presence of CaP achieved with subsequent RBMa treatment. Despite the not significantly different roughness between AB/AE and the hybrid surfaces, the expected synergistic effect of combined roughness and chemical bonding involving implants with CaP remnants from blasting,20  early fixation, BIC, and BAFO of all three surfaces could not be confirmed. Future studies incorporating higher amounts CaP on implant surfaces are warranted.

There have been studies showing promising results concerning reduced-length scale bioactive ceramic integration on implant surfaces.20,35,36,40  However, specific to RBM surfaces, various factors such as particle size, blasting media composition, blasting pressure, distance, and the subsequent acid etching have been shown to affect the early host response to the implant,3,20,21  and thus, the current design rationale for the surface incorporation of Ca-P still remains to be determined.5,42 

The general results from this study show that all 3 surfaces investigated are biocompatible and osseoconductive, resulting in a similar bone-healing pattern with the cortical and trabecular bone in close interaction with the implant surface.25,43  Woven bone formation was observed in all 3 surfaces after the 2 weeks allowed after the initial placement.

In agreement with the biomechanical testing results, no significant differences were found among the 3 surfaces with regard to BIC and BAFO measurements. Thus, within the limitations of the present study, we conclude that the availability of Ca and P on the surface did not hasten early integration of the investigated surfaces.

Abbreviations

     
  • AB/AE

    alumina-blasting + acid-etching

  •  
  • AFM

    atomic force microscopy

  •  
  • BIC

    bone-to-implant contact

  •  
  • BAFO

    bone area fraction occupied

  •  
  • PSHA

    plasma-sprayed hydroxyapatite

  •  
  • RBM

    resorbable-blasting media

  •  
  • RBMa

    resorbable-blasting media + acid-etched

  •  
  • SEM

    scanning electron microscope

  •  
  • XPS

    x-ray photoelectron spectroscopy

References

References
1
Chuang
SK
,
Tian
L
,
Wei
LJ
,
Dodson
TB
.
Predicting dental implant survival by use of the marginal approach of the semi-parametric survival methods for clustered observations
.
J Dent Res
.
2002
;
81
:
851
855
.
2
Chuang
SK
,
Wei
LJ
,
Douglass
CW
,
Dodson
TB
.
Risk factors for dental implant failure: a strategy for the analysis of clustered failure-time observations
.
J Dent Res
.
2002
;
81
:
572
577
.
3
Coelho
PG
,
Granjeiro
JM
,
Romanos
GE
,
et al
.
Basic research methods and current trends of dental implant surfaces
.
J Biomed Mater Res B Appl Biomater
.
2009
;
88
:
579
596
.
4
Wennerberg
A
,
Albrektsson
T
.
Effects of titanium surface topography on bone integration: a systematic review
.
Clin Oral Implants Res
.
2009
;
20
(
suppl 4
):
172
184
.
5
Wennerberg
A
,
Albrektsson
T
.
Structural influence from calcium phosphate coatings and its possible effect on enhanced bone integration
.
Acta Odontol Scand
.
2009
;
67
:
1
8
.
6
Wennerberg
A
,
Albrektsson
T
.
On implant surfaces: a review of current knowledge and opinions
.
Int J Oral Maxillofac Implants
.
2010
;
25
:
63
74
.
7
Elias
CN
,
Meirelles
L
.
Improving osseointegration of dental implants
.
Expert Rev Med Devices
.
2010
;
7
:
241
256
.
8
Kay
J
.
Calcium phosphate coatings for dental implants
.
Dent Clin North Am
.
1992
;
36
:
1
18
.
9
Lacefield
WR
.
Hydroxyapatite coatings
.
Ann N Y Acad Sci
.
1988
;
523
:
72
80
.
10
Lacefield
WR
.
Current status of ceramic coatings for dental implants
.
Implant Dent
.
1998
;
7
:
315
322
.
11
Coelho
PG
,
Lemons
JE
.
IBAD Nanothick Bioceramic Incorporation on Metallic Implants for Bone Healing Enhancement. From Physico/Chemical Characterization to In-vivo Performance Evaluation
.
Anaheim, Calif
:
Nanotech;
2005
.
12
Park
YS
,
Yi
KY
,
Lee
IS
,
Han
CH
,
Jung
YC
.
The effects of ion beam-assisted deposition of hydroxyapatite on the grit-blasted surface of endosseous implants in rabbit tibiae
.
Int J Oral Maxillofac Implants
.
2005
;
20
:
31
38
.
13
Yang
Y
,
Kim
KH
,
Ong
JL
.
A review on calcium phosphate coatings produced using a sputtering process—an alternative to plasma spraying
.
Biomaterials
.
2005
;
26
:
327
337
.
14
Vercaigne
S
,
Wolke
JG
,
Naert
I
,
Jansen
JA
.
A mechanical evaluation of TiO2-gritblasted and Ca-P magnetron sputter coated implants placed into the trabecular bone of the goat: part 1
.
Clin Oral Implants Res
.
2000
;
11
:
305
313
.
15
Vercaigne
S
,
Wolke
JG
,
Naert
I
,
Jansen
JA
.
A histological evaluation of TiO2-gritblasted and Ca-P magnetron sputter coated implants placed into the trabecular bone of the goat: part 2
.
Clin Oral Implants Res
.
2000
;
11
:
314
324
.
16
Davies
JE
.
Bone bonding at natural and biomaterial surfaces
.
Biomaterials
.
2007
;
28
:
5058
5067
.
17
Mendes
VC
,
Moineddin
R
,
Davies
JE
.
The effect of discrete calcium phosphate nanocrystals on bone-bonding to titanium surfaces
.
Biomaterials
.
2007
;
28
:
4748
4755
.
18
Mendes
VC
,
Moineddin
R
,
Davies
JE
.
Discrete calcium phosphate nanocrystalline deposition enhances osteoconduction on titanium-based implant surfaces
.
J Biomed Mater Res A
.
2009
;
90
:
577
585
.
19
Orsini
G
,
Piattelli
M
,
Scarano
A
,
et al
.
Randomized, controlled histologic and histomorphometric evaluation of implants with nanometer-scale calcium phosphate added to the dual acid-etched surface in the human posterior maxilla
.
J Periodontol
.
2007
;
78
:
209
218
.
20
Marin
C
,
Granato
R
,
Suzuki
M
,
Gil
JN
,
Piattelli
A
,
Coelho
PG
.
Removal torque and histomorphometric evaluation of bioceramic grit-blasted/acid-etched and dual acid-etched implant surfaces: an experimental study in dogs
.
J Periodontol
.
2008
;
79
:
1942
1949
.
21
Marin
C
,
Granato
R
,
Suzuki
M
,
et al
.
Biomechanical and histomorphometric analysis of etched and non-etched resorbable blasting media processed implant surfaces: an experimental study in dogs
.
J Mech Behav Biomed Mater
.
2010
;
3
:
382
391
.
22
Meirelles
L
,
Albrektsson
T
,
Kjellin
P
,
et al
.
Bone reaction to nano hydroxyapatite modified titanium implants placed in a gap-healing model
.
J Biomed Mater Res A
.
2008
;
87
:
624
631
.
23
Meirelles
L
,
Arvidsson
A
,
Andersson
M
,
Kjellin
P
,
Albrektsson
T
,
Wennerberg
A
.
Nano hydroxyapatite structures influence early bone formation
.
J Biomed Mater Res A
.
2008
;
87
:
299
307
.
24
Donath
K
,
Breuner
G
.
A method for the study of undecalcified bones and teeth with attached soft tissues: the Sage-Schliff (sawing and grinding) technique
.
J Oral Pathol
.
1982
;
11
:
318
326
.
25
Leonard
G
,
Coelho
P
,
Polyzois
I
,
Stassen
L
,
Claffey
N
.
A study of the bone healing kinetics of plateau versus screw root design titanium dental implants
.
Clin Oral Implants Res
.
2009
;
20
:
232
239
.
26
Albrektsson
T
,
Wennerberg
A
.
Oral implant surfaces: part 1—review focusing on topographic and chemical properties of different surfaces and in vivo responses to them
.
Int J Prosthodont
.
2004
;
17
:
536
543
.
27
Albrektsson
T
,
Wennerberg
A
.
Oral implant surfaces: part 2—review focusing on clinical knowledge of different surfaces
.
Int J Prosthodont
.
2004
;
17
:
544
564
.
28
Dohan Ehrenfest DM, Coelho PG, Kang BS, Sul YT, Albrektsson T
.
Classification of osseointegrated implant surfaces: materials, chemistry and topography
.
Trends Biotechnol
.
2010
;
28
:
198
206
.
29
Coelho
PG
,
Bonfante
EA
,
Pessoa
RS
,
et al
.
Characterization of 5 different implant surfaces and their effect on osseointegration: a study in dogs
.
J Periodontol
.
2011
;
82
:
742
750
.
30
Suzuki
M
,
Guimaraes
MV
,
Marin
C
,
et al
.
Histomorphologic and bone-to-implant contact evaluation of dual acid-etched and bioceramic grit-blasted implant surfaces: an experimental study in dogs
.
J Oral Maxillofac Surg
.
2010
;
68
:
1877
1883
.
31
Suzuki
M
,
Calasans-Maia
MD
,
Marin
C
,
et al
.
Effect of surface modifications on early bone healing around plateau root form implants: an experimental study in rabbits
.
J Oral Maxillofac Surg
.
2010
;
68
:
1631
1638
.
32
Coelho
PG
,
Granato
R
,
Marin
C
,
Bonfante
EA
,
Janal
MN
,
Suzuki
M
.
Biomechanical and bone histomorphologic evaluation of four surfaces on plateau root form implants: an experimental study in dogs
.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod
.
2010
;
109
:
e39
e45
.
33
Granato
R
,
Marin
C
,
Gil
JN
,
et al
.
Thin bioactive ceramic-coated alumina-blasted/acid-etched implant surface enhances biomechanical fixation of implants: an experimental study in dogs
.
Clin Implant Dent Relat Res
.
2011
;
13
:
87
94
.
34
Coelho
PG
,
Suzuki
M
,
Guimaraes
MV
,
et al
.
Early bone healing around different implant bulk designs and surgical techniques: a study in dogs
.
Clin Implant Dent Relat Res
.
2010
;
12
:
202
208
.
35
Suzuki
M
,
Guimaraes
MV
,
Marin
C
,
Granato
R
,
Gil
JN
,
Coelho
PG
.
Histomorphometric evaluation of alumina-blasted/acid-etched and thin ion beam-deposited bioceramic surfaces: an experimental study in dogs
.
J Oral Maxillofac Surg
.
2009
;
67
:
602
607
.
36
Granato
R
,
Marin
C
,
Suzuki
M
,
Gil
JN
,
Janal
MN
,
Coelho
PG
.
Biomechanical and histomorphometric evaluation of a thin ion beam bioceramic deposition on plateau root form implants: an experimental study in dogs
.
J Biomed Mater Res B Appl Biomater
.
2009
;
90
:
396
403
.
37
Marin
C
,
Granato
R
,
Suzuki
M
,
Gil
JN
,
Piattelli
A
,
Coelho
PG
.
Removal torque and histomorphometric evaluation of bioceramic grit-blasted/acid-etched and dual acid-etched implant surfaces: an experimental study in dogs
.
J Periodontol
.
2008
;
79
:
1942
1949
.
38
Coelho
PG
,
Cardaropoli
G
,
Suzuki
M
,
Lemons
JE
.
Histomorphometric evaluation of a nanothickness bioceramic deposition on endosseous implants: a study in dogs
.
Clin Implant Dent Relat Res
.
2009
;
11
:
292
302
.
39
Coelho
PG
,
Lemons
JE
.
Physico/chemical characterization and in vivo evaluation of nanothickness bioceramic depositions on alumina-blasted/acid-etched Ti-6Al-4V implant surfaces
.
J Biomed Mater Res A
.
2009
;
90
:
351
361
.
40
Coelho
PG
,
Cardaropoli
G
,
Suzuki
M
,
Lemons
JE
.
Early healing of nanothickness bioceramic coatings on dental implants: an experimental study in dogs
.
J Biomed Mater Res B Appl Biomater
.
2009
;
88
:
387
393
.
41
Garetto
LP
,
Chen
J
,
Parr
JA
,
Roberts
WE
.
Remodeling dynamics of bone supporting rigidly fixed titanium implants: a histomorphometric comparison in four species including humans
.
Implant Dent
.
1995
;
4
:
235
243
.
42
Lemons
JE
.
Biomaterials, biomechanics, tissue healing, and immediate-function dental implants
.
J Oral Implantol
.
2004
;
30
:
318
324
.
43
Berglundh
T
,
Abrahamsson
I
,
Lang
NP
,
Lindhe
J
.
De novo alveolar bone formation adjacent to endosseous implants
.
Clin Oral Implants Res
.
2003
;
14
:
251
262
.