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Bone Graft and Substitutes Associated With Titanium Dome For Vertical Bone Formation in Osseointegrated Implants
Bone Graft and Substitutes Associated With Titanium Dome For Vertical Bone Formation in Osseointegrated Implants
Purpose: This animal study investigated vertical bone formation (VBF) around implants and used
histomorphometric analysis to compare different bone-filling materials associated with a massive titanium
dome as a tissue barrier. Materials and Methods: Seven dogs were submitted to surgical procedures
with extraoral access to the lower edge of the mandible, and four implants were semi-inserted in each
animal. Each implant received one treatment: autogenous bone with clot (AB), control clot (C), synthetic
graft (Biogran [BG]), or xenograft (Bio-Oss [BO]). Massive titanium domes were stabilized over the implants.
Histologic analysis was performed after 3 months, and quantitative aspects were evaluated in extraosseous
and intraosseous threads on Image Pro-Plus software. Results: VBF around implants exhibited significant
values in AB compared with other groups. BG and BO presented statistical equivalency to AB and C in the
apposition and filling of extraosseous threads. There was no difference between groups for parameters
evaluated in intraosseous threads. Conclusion: The experimental model was valid for evaluation of VBF
around implants placed in atrophic mandibles. Considering the limitations of this study, histomorphometric
analysis evidenced better outcomes for group AB. Even though groups BG and BO presented worse
outcomes than AB, they were slightly better compared with the control group. Int J Oral Maxillofac Implants
2018;33:311–318. doi: 10.11607/jomi.5762
Keywords: animal experiments, biomaterials, bone-implant interactions, bone regeneration, guided tissue
regeneration
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Zendron et al
b c
membranes were combined with different grafting (mandible dimension) and characteristics of bone re-
materials in mandibles of dogs, demonstrating con- generation similar to humans.17 After approval by the
tact between the newly formed bone tissue and the University of São Paulo - USP - Animal Ethics Commit-
implant.11 Another study12 using titanium domes com- tee (USP-026/2016), the animals were kept in standard
pared with e-PTFE membranes associated or not with individual cages and fed ad libitum. Twenty-four hours
autogenous bone fragments in dogs demonstrated prior to surgery, the chosen dog was then maintained
greater mean bone gain when the domes were used. on a restricted soft diet to prevent any gastrointestinal
Concerning the performance of xenogeneic or allo- intercurrence during the surgical procedure. One day
plastic grafts associated with VBF in implants, animal before surgery, shaving of the lower mandibular area
studies revealed that the association of Bio-Oss and and intraoral disinfection were performed under seda-
collagen membrane in immediate implant placement tion by intramuscular injection of dihidrotiazine chlo-
promoted bone regeneration, similar to the utilization ride (1.5 mL/10 kg). The main surgical procedures were
of autogenous bone.13 Due to its three-dimensional then conducted under intravenous general anesthesia
microparticulate porous configuration, the synthetic with sodium thiopental (1 mL/kg). The anesthesia was
material Biogran allows diffusion of nutrients, blood applied through open vein access maintained by the
vessels, and cell proliferation, with potential of new injection of saline throughout surgery, aiming hydra-
bone formation in animal studies.14 Another study tion at subsequent administration of complementary
analyzing bioactive glass around implants placed in anesthetic doses.
rat tibiae and femurs demonstrated better stability of The animal was placed in supine position, and
implants in the newly formed tissue compared with local disinfection was performed by application of
the hydroxyapatite group.15 However, other studies chlorhexidine digluconate (0.2%); a medial incision
observed that, after 1 year, the biomaterials (Bio-Oss was performed, extending from the symphysis to
and Biogran) associated with hollow and massive Tef- the level of the mandibular angle. Bilateral periosteal
lon capsules delayed bone healing in the mandibu- incisions were performed on the mandibular lower
lar ramus of rats in simulations of periodontal and extension at both the right and left sides.9 The bone
peri-implant defects. Fibrous connective tissue was ob- surface at the mandibular body was exposed by a
served between particles, while the control group with total-thickness flap. These surfaces were manually
hollow capsules exhibited significant bone filling.16 planed using bone files (Hu-Friedy) under constant
The critical factors for the success or failure of VBF irrigation to achieve an even surface with at least 6
associated with implants, as well as the performance mm height and 45 mm extension measured with a
and analysis of biomaterials in these borderline con- periodontal probe, to represent the atrophic ridge.
ditions, have not yet been fully elucidated in the lit- In each mandibular body, two areas 25 mm apart
erature. Considering the limitations of experiments were selected, resulting in four sites per dog. Four
with animal models, this study aimed to evaluate VBF custom-fabricated implants (3.3 × 6.0 mm) (Conexão
around implants and compared, by histomorphomet- Sistemas de Prótese Ltda) were partially inserted af-
ric analysis, different bone filling materials associated ter conventional instrumentation in densely cortical
with a titanium device as a tissue barrier. areas, totaling 28 implants. Thus, three threads per
implant remained exposed and protruding in relation
to the original bone level, and three threads remained
MATERIALS AND METHODS below the bone level (Fig 1a). Four perforations were
performed using a 1.0-mm bur on the cortical bone
This study was performed on seven male healthy mon- around the implants to expose the medullar spaces
grel dogs with a mean age of 26 months and with a of the bone tissue (Fig 1b). These perforations aimed
mean body weight of 21 kg. The selection of this animal to increase the availability of regenerative cells in the
model was based on the requirement of a larger animal experimental wound area.
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Zendron et al
Each animal received four implants, and each pro- Table 1 Standardized Exposure of
truding aspect of the implants received one particular Extraosseous Threads Between
treatment, each one containing 1 mL of peripheral ve- Groups (Mean [mm] and SD)
nous blood filling the internal space of the tissue barri-
ers. The groups were divided as follows: AB (n = 12) C (n = 12) BG (n = 12) BO (n = 12)
Mean 2.64a 2.64a 2.57a 2.56a
• C (control group): filled with blood clot SD 0.3 0.14 0.16 0.12
• AB (autogenous bone): cortical bone chips SD = standard deviation; n = number of observations; AB =
harvested during planing of bone surfaces in the autogenous bone; C = control; BG = Biogran; BO = Bio-Oss.
Different lowercase letters represent statistically significant
mandibular body differences.
• BG (Biogran, Biomet 3i): synthetic graft
(Granule size: 300 to 355 µm) Histomorphometric Measurements
• BO (Bio-Oss, Geistlich Pharma AG, Division All parameters were analyzed by a single calibrated
biomaterials): bovine graft (Granule size: 0.25 to examiner (intraclass correlation coefficient = 0.98), as
1.00 mm) follows:
The protruding aspects of the implants were then • VBF: height of new bone formation, considering
covered with custom-fabricated commercially pure the initially exposed implant threads, taking
titanium dome-shaped tissue barriers, measuring as a reference point the original cortical bone
4.8 × 5.0 mm of internal space (Conexão Sistemas and the implant shoulder. For each slide, the
de Prótese Ltda) (Fig 1c). Each of the four structures mesial and distal portions of the implant/barrier
was filled with material of one experimental group, assembly were individually considered (n = 12). For
randomly assigned by drawing lots. The material was standardization, all exposed implant surfaces were
easily maintained inside the dome due to its massive measured per experimental group (Table 1). The
structure and with the use of venous peripheral blood percentages of VBF were then calculated in relation
associated or not with filling materials, establishing a to the measurement of exposed threads.
blood clot. Also, the bleeding perforations made in the
bone around the implants further preserved a viable The other parameters were analyzed by slide
clot. The barriers were fixated to the cortical bone by (n = 24) and included the following:
means of 1.2 mm commercially pure titanium minis-
crews (Intermedic Technology). • Filling of extraosseous threads: percentage of
Sutures were performed in layers using resorbable filling of each thread positioned above the original
sutures (Vicryl 5-0 Ethicon, Johnson & Johnson) for cortical bone level
periosteum and muscular tissue, and nylon sutures • Bone-to-implant contact in extraosseous threads:
for the skin (Mononylon 2-0 Ethicon, Johnson & John- percentage of contact between the bone tissue
son). After the surgical procedures, dogs received in- and implant in each exposed thread
tramuscular injections of 30,000 U/kg of antibiotics • Filling of intraosseous threads: percentage of
(Pentabiótico, Fort Dodge Saúde Animal) for 9 days. filling of each thread positioned below the original
Externally, a topical antibiotic solution containing cortical bone level
rifampicin sodium chloride was applied for 7 days • Bone-to-implant contact in intraosseous threads:
(Rifocina Hoechst-Marion Roussel S/A). An Elizabethan percentage of contact between the bone tissue
collar (Agrosolo, LTDA) was maintained in place for and implant in each thread positioned below the
30 days to protect the surgical area from inadvertent original cortical bone level
movements of the animal.
The animals were euthanized by an anesthetic over- Histomorphometric analyses, under the previ-
dose with sodium thiopental (4 mL/kg) 3 months af- ously exposed limits of threads of each implant (three
ter placement of implants and barriers. The mandibles threads per implant), were performed on the mesial
were dissected, and the blocks containing the experi- and distal sides, using a microscope connected to a
mental specimens (implant/barrier) were retrieved video camera and computer software (Image Pro-Plus,
and immersed in 4% neutral formalin for fixation. Media Cybernetics). Software tools to calculate linear
The decalcified sections (70 to 85 µm) were prepared and area measures were used to establish the exten-
from the center of the implant/barrier assembly, corre- sion of the regenerative process, filling with new bone
sponding to the longitudinal section (anteroposterior) formation, implant-bone contact fraction, and all the
of the mandibular base, as previously described.18 The measurements related to bone formation inside the ti-
sections were stained with 1% toluidine blue.18 tanium dome and the original cortical bone. Data were
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Zendron et al
A B
A B
A
A
B
Fig 2 Distinction between the Fig 3 Lamellar bone forma- Fig 4 Connective tissue fibers Fig 5 Fibrous connective tis-
newly formed bone (A: darker tion (arrows) near the surface of (arrows) oriented parallel to the sue (arrows) around the par-
blue) and the original cortical the implant (1% toluidine blue) implant surface (1% toluidine ticles of bioactive glass (A) (1%
bone (B: lighter blue) (1% tolu- (100×). blue) (100×). toluidine blue) (100×).
idine blue) (100×).
statistically analyzed by analysis of variance (ANOVA) osteons, surrounded by connective tissue and blood
for comparison of means of each parameter analyzed, vessels. These structures were always found above the
and by the Bonferroni t test for individual comparisons recently formed bone and distant from the flat cortical
(P < .01) between the different groups, to reveal the bone, suggesting an ongoing process of bone matrix
significant differences for each proposed treatment. deposition and mineralization, which was incomplete
at the 90-day healing period.
Nevertheless, some aspects were specifically ob-
RESULTS served in each group:
The histomorphometric analysis demonstrated that, • C: Bone formation was minimal in the majority of
among seven specimens, one presented infection and analyzed slides. Furthermore, the slides revealed
abscess formation and was excluded. The 24 slides mi- the presence of a dense connective tissue oriented
croscopically analyzed demonstrated direct bone ap- parallel to the implant surfaces inside the domes
position to titanium surfaces. (Fig 4).
• AB: Some specimens presented vertical bone
Qualitative Analysis formation that surpassed the reference mark used
Some general aspects were common to all investigat- for morphometry. Autogenous bone particles were
ed groups regarding the pattern of bone formation. incorporated to the mineralized matrix of newly
Besides the variable extent of bone formation among formed bone.
groups, no experimental treatment used to fill the re- • BG: Minimum vertical bone formation and contact
generative space changed the quality of newly formed between the newly formed bone and material
bone. The staining technique (1% toluidine blue) al- particles were observed. The histologic processing
lowed distinction between the newly formed bone of specimens by abrasion showed that the particles
(darker blue) and the original cortical bone (lighter had a central core of fibrous tissue and several
blue) (Fig 2). In all groups exhibiting new bone forma- fractures. The entire regenerative space was
tion, a highly stained woven bone type was observed, dominated by the presence of fibrous connective
covered by a thin layer of lamellar bone less stained than tissue.
the previous one (Fig 3). Although the staining method • BO: subtle bone formation similar to group BG was
was not specific to soft connective tissue, condensa- observed. In the majority of specimens, a fibrous
tions observed above the newly formed bone were connective tissue layer surrounded the particles
suggestive of bone-forming cells. At the inner part of (Fig 5).
the new woven bone, connective tissue and blood ves-
sels were present. All the referred newly formed bone Quantitative Analysis
herein established a close relationship with the re- The mean VBF was calculated in percentage, standard
maining flat cortical bone surface. Some poorly stained deviation, and number of observations for each exper-
structures were also observed, adjacent to the titani- imental group, which are described in Table 2. The per-
um implant surfaces, resembling the arrangement of centage of bone formation in relation to the extension
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Zendron et al
of protruding screws was calculated (Table 2). AB percentage of bone-to-implant contact at the exposed
proved to be significantly better than all groups (Fig 6). threads demonstrated that AB presented a significant-
BG and BO groups were demonstrated to be equiva- ly superior outcome compared with C. BG and BO were
lent to the C group. equivalent to AB and C (Fig 7) (Table 4).
The percentage of bone apposition on exposed The analysis of bone apposition on submerged
threads positioned above the original cortical bone screws and the submerged bone-to-implant contact
level demonstrated a significantly better outcome portion revealed that none of the treatments modi-
for the AB group compared with the C group. BG and fied the rate of bone formation and osseointegration
BO were equivalent to AB and C (Fig 7) (Table 3). The around the implants (Table 5).
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Zendron et al
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