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68:1667-1675, 2010
Purpose: This study tested the null hypothesis that differences in surgical instrumentation, macroge-
ometry, and surface treatment imposed by different implant systems do not affect early biomechanical
fixation in a canine mandible model.
Materials and Methods: The lower premolars of 6 beagle dogs were extracted and the ridges allowed
to heal for 8 weeks. Thirty-six (n ⫽ 12 each group) implants were bilaterally placed, remaining for 1 and
3 weeks in vivo. The implant groups were as follows: group 1, Ti-6Al-4V with a dual acid-etched surface
with nanometer scale discrete crystalline deposition (Nanotite; Certain Biomet-3i, West Palm Springs,
FL); group 2, Ti-6Al-4V with a titanium oxide-blasted fluoride-modified surface chemistry (Osseospeed 4.0
S; Astra Tech, Mölndal, Sweden); group 3: Ti-6Al-4V with a bioceramic microblasted surface (Ossean;
Intra-Lock International, Boca Raton, FL). Following euthanasia, implants were torqued to interface
failure and histologically evaluated. General linear modeling (ANOVA) at 95% level of significance was
performed.
Results: Histology showed that interfacial bone remodeling and initial woven bone formation were
observed around all implant groups at 1 and 3 weeks. Torque values were significantly affected by time in
vivo, implant group, and their interaction (P ⫽ .016, P ⬍ .001, and P ⫽ .001, respectively). Regarding torque
values, group 3, group 2, and group 1 ranked highest, intermediate, and lowest, respectively.
Conclusion: Early biomechanical fixation at 1 and 3 weeks was affected by surgical instrumentation,
macrogeometry, and surface treatment present for one of the implant systems tested. The null hypothesis
was rejected.
© 2010 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 68:1667-1675, 2010
Osseointegration is a phenomenon in which intimate plantology, implant therapy success ratios often ex-
contact between bone and biomaterials occurs at the ceed 90%.2,3 However, despite the high success rates
optical microscopy level, enabling dental implants to reported, basic scientists and clinicians have at-
replace load-bearing tooth organs and restore their tempted to decrease treatment time frames by reduc-
form and intraoral function.1 Specific to dental im- ing the healing period for establishment of osseointe-
*Assistant Professor, Department of Biomaterials and Biomimet- eral de Santa Catarina, Florianopolis, Brazil.
ics, New York University, New York, NY. **Assistant Professor, Department of Prosthodontics, Tufts Uni-
†Instructor, Department of Dentistry, Universidade Federal de versity School of Dental Medicine, Boston, MA.
Santa Catarina, Florianopolis, Brazil. Address correspondence and reprint requests to Dr Coelho:
‡Instructor, Department of Dentistry, Universidade Federal de 345 East 24th Street, Room 314a, Department of Biomaterials and
Santa Catarina, Florianopolis, Brazil. Biomimetics, New York University, New York, NY 10010; e-mail:
§Private Practice, Bauru, SP, Brazil. pgcoelho@nyu.edu
㛳Private Practice, Florianópolis, SC, Brazil. © 2010 American Association of Oral and Maxillofacial Surgeons
¶Senior Research Scientist, Department of Epidemiology and 0278-2391/10/6807-0033$36.00/0
Health Promotion, New York University, New York, NY.
doi:10.1016/j.joms.2010.02.050
#Associate Professor, Department of Dentistry, Universidade Fed-
1667
1668 BIOMECHANICAL EVALUATION OF ENDOSSEOUS IMPLANTS
gration.4 For that purpose, the most common tion prevents implant micromotion, a stability de-
approach is through modification of different implant crease will take place at early times after implanta-
design parameters.4,5 tion.22
Implant design alterations have included changes in Although substantial work has been published regarding
its structural material,6,7 its macrogeometry and/or the effects of macrogeometry and implant surface on early
surgical instrumentation,5,8,9 and surface modifica- bone-implant interaction,5,8,13,14,17,18,23,24 comparative
tions.10-12 Although it is not well defined whether studies regarding the effect of implant surgical ins-
biocompatible materials other than titanium and its trumentation/macrogeometry/surface on stability at
alloys improve the host-to-implant response, alter- early implantation times are sparse in the literature.
ations in macrogeometry and/or surgical instrumenta- Thus, this investigation tested the null hypothesis that
tion and surface modifications have demonstrated sig- different implant systems presenting distinct surgical
nificant effects at the early stages of bone healing instrumentation, macrogeometry, and surface would
around endosseous implants.5,8-12 not present alterations in biomechanical fixation at
Several studies have demonstrated that depending early implantation times in a canine mandible model.
on the interplay between final bone drilling and im-
plant geometric dimensions, different bone healing
mechanisms and kinetics may be observed.5,13-15 If Materials and Methods
there is intimate surgical fit between bone and im-
plant surface, the interfacial bone undergoes remod- This study used 36 endosseous implants with vari-
eling and is gradually substituted by woven bone that ations in bulk geometry and surface treatment from
is gradually replaced by mature lamellar bone.13 How- three manufacturers (12 of each type).
ever, if healing chambers form in regions in which The implant groups were as follows: group 1, Ti-
bone and implant are not in intimate contact because 6Al-4V threaded implant with a dual acid-etched sur-
of the interplay between drilling and implant dimen- face with nanometer scale discrete crystalline depo-
sions, rapid woven bone filling occurs and long-term sition (Nanotite; Certain Biomet-3i, West Palm
implant stability is ensured by bone modeling and Springs, FL); group 2, Ti-6Al-4V threaded implant (pre-
remodeling processes.5,13,14 senting microthreads in the cervical third) with a
Among surface modifications, implant texture has titanium oxide-blasted fluoride-modified surface
evolved from the as-turned surfaces toward moder- chemistry (Osseospeed, 4.0 S; Astra Tech, Mölndal,
ately rough surfaces because several studies have Sweden); group 3, Ti-6Al-4V threaded implant (pre-
shown improved histologic and biomechanical host- senting microthreads in the cervical third) with a
to-implant response.10,12,16,17 More recently, several bioceramic microblasted surface (Ossean; Intra-Lock
studies have shown that chemistry alterations to mod- International, Boca Raton, FL). The group 1 and 3
erately rough surfaces, such as the addition of fluoride devices presented the same physical dimensions with
or calcium phosphate in small scales (nanometer or respect to diameter (4 mm) and length (10 mm).
minute scale), have resulted in further improvements Group 2 implants had a 4-mm diameter and 11-mm
in bone to implant response at early implantation implant length.
times in vivo.12,13,15,18-20 Although several experimen- Following approval of the bioethics committee for
tal studies have demonstrated the effectiveness of animal experimentation at the Universidade Federal
surface modifications at early implantation times regard- de Santa Catarina, Brazil, 6 beagle dogs with closed
less of implant macrogeometry and drilling technique, growth plates (between 18 and 24 months of age) in
further experimentation is desirable to determine what good health were acquired for the study and followed
macrogeometry/drilling dimension/surface modification a 2-week in-house period before surgery.
results in optimal bone-to-implant response at early im- All surgical procedures were performed under gen-
plantation times. eral anesthesia. The preanesthetic procedure com-
From a clinical perspective, it is general consensus prised intramuscular administration of atropine sul-
that implant stability immediately and early after fate (0.044 mg/kg) and xylasin chlorate (8 mg/kg).
placement is desirable, because relative motion be- General anesthesia was then obtained following an
tween implant and bone may risk osseointegra- intramuscular injection of ketamine chlorate (15 mg/
tion.4,16,21 Histologic studies have shown that implant kg).
primary stability is rendered during placement, and Bilateral extractions of all 4 premolars (P1, P2, P3,
because of remodeling and subsequent bone apposi- and P4) were performed. The procedure involved a
tion bridging old bone and implant surface, biological full thickness mucoperiosteal flap, teeth sectioning in
or secondary stability is achieved.8,13,14 This rationale the buccolingual direction so individual roots could
has led to the presumption that if osteoclastic activity be extracted by means of root elevators and forceps
undermines primary stability before new bone forma- without bone wall damage. The soft tissue was closed
COELHO ET AL 1669
tively evaluated at 50⫻ to 200⫻ magnification (Leica levels at 1 and 3 weeks were also observed for group
DM2500M; Leica Microsystems, Wetzlar, Germany). 3. However, groups 2 and 3 presented comparable
Statistical evaluation of torque measures employed values at 3 weeks, and these values were significantly
a mixed-model analysis of variance (ANOVA) with 1 higher than group 1 (Table 6).
between-subjects factor (3 levels of implants). Statis-
tical significance was indicated by P levels less than
5%, and post hoc testing employed the Fisher least Table 2. IMPLANT DISTRIBUTION PER ANIMAL,
SITE, TIME IN VIVO, AND THEIR RESPECTIVE
significant difference test. TORQUE VALUES
The nondecalcified sample processing after con- uous bone-implant structures (Figs 2B, 3C,D, and 4C,
trolled torque to interface failure testing showed sim- D). Bone cracking at the thread tips was seldom
ilar bone-to-implant response. Higher magnification of observed at 3 weeks as the bone in intimate contact
the bone-implant interface region showed that the with the implant thread tips underwent remodeling
nondecalcified sections obtained following biome- (Figs 2B, 3C,D, and 4C,D).
chanical testing presented minimal morphologic dis-
tortion due to mechanical testing bone disruption
and/or thin section processing (Figs 2-4). Intimate
bone-to-implant interaction was observed for all im- Discussion
plant groups (Figs 2-4). Over the past 40 years, surgical and prosthetic
At 1 week, initial woven bone formation was ob- protocols substantially deviating from the classical
served around all implant groups. Irrespective of the 2-stage protocol27 have been suggested, typically un-
presence of microthreads in implant geometry, der the rationale of implant design modifications that
throughout the whole bone-implant interface perim- would enable improved healing or biomechanical be-
eter, all groups presented a combination of regions of havior.10,11,17,18,28 Although a substantial amount of
initial woven bone formation and gap regions be- research has been devoted to increasing the host-to-
tween old bone and implant surface characteristic of implant response at early implantation times,10,11,17,18,28,29
interfacial bone modelling-remodeling stages (Figs 2A, little information has been published to date concern-
3A,B, and 4A,B). Bone cracking due to implant place- ing the host-to-implant response considering the in-
ment was also observed at regions of microthreads terplay between surgical protocols and implant bulk
(Figs 3A and 4A), and large pitch threaded regions design.5 This investigation tested the null hypothesis
(Figs 2A, 3B, and 4B). that different implant systems presenting distinct sur-
At 3 weeks, irrespective of experimental group, gical instrumentation, macrogeometry, and surface
newly formed woven bone bridging the old bone and would not present alterations in biomechanical fixa-
implant surface filled the interfacial modelling-remod-
eling regions observed at 1 week, resulting in contin-
Table 6. TORQUE (N-cm) STATISTICAL SUMMARY FOR THE IMPLANT GROUP—TIME IN VIVO INTERACTION
TORQUE IN WHICH SIGNIFICANT DIFFERENCES WERE OBSERVED (P ⴝ .001)
95% CI 95% CI
Implant Group Time In Vivo Mean SE df Lower Bound Upper Bound
FIGURE 3. A, Optical micrograph of a group 2 thin section bone–implant interface shows bone modeling/remodeling represented by areas
of woven bone formation and gaps in the space separating old bone and implant surface at 1 week. Bone cracking induced by implant
placement is observed at the microthreaded region (arrow) as well as (B) large pitch thread regions (arrow). C, At the microthreads and also
(D) at the large pitch thread regions, newly formed woven bone is shown at 3 weeks, filling the gaps present at 1 week, where intimate contact
between bone and implant surface is observed.
Coelho et al. Biomechanical Evaluation of Endosseous Implants. J Oral Maxillofac Surg 2010.
onset and an intermediate period of woven bone times despite the 3 systems’ differing surgical drilling
deposition and interfacial remodeling in dog mandi- techniques, geometries, and surfaces.
bles.5,8,9 The intimate contact between newly formed bone
Our histologic observations are in direct agreement and the 3 groups’ different surfaces suggest that they
with previous studies5,8,9 in which, irrespective of are all highly biocompatible and osseoconductive.
experimental group, initial woven bone formation Such observation is in direct agreement with previ-
along with bone remodeling at the interfacial region ously published experimental animal studies.13,19,20
was detected at 1 week and extended to 3 weeks.5,8,9 Although our previous investigations15,23-25 have mea-
All groups evaluated presented higher amounts of sured bone-to-implant contact values from histologic
woven bone at the interfacial region at 3 weeks, samples that were biomechanically tested with the
which may be explained by subsequent interfacial same methods used in the current investigation, those
bone remodeling and woven bone formation be- studies15,23-25 used experimental implant designs that
tween 1 and 3 weeks. The observation of bone crack- allowed biomechanical testing on a plane (cylindrical
ing at the implant thread tip regions at 1 week for all shaped implants without threads, unlike threaded im-
specimens and its near inexistence at 3 weeks sug- plants that change in position along their long axis
gests the extent of the region of high bone activity during testing, potentially causing higher interfacial
(formation and remodeling) temporally changed over disruption).
time. Such observation reflects the dynamic nature of In contrast with our histologic findings in which all
the bone–implant interface at early implantation implant groups presented similar interaction with
1674 BIOMECHANICAL EVALUATION OF ENDOSSEOUS IMPLANTS
FIGURE 4. A, Optical micrograph of group 3 bone-implant interface shows woven bone formation in close proximity with implant surface
at 1 week at the microthread and (B) also at the large pitch threaded regions, where bone cracking is induced by implant placement (arrow).
C and D, At 3 weeks, both regions of microthreads (C) and also large pitch threads (D) present a continuous implant– bone structure bridged
by newly formed woven bone.
Coelho et al. Biomechanical Evaluation of Endosseous Implants. J Oral Maxillofac Surg 2010.
bone at 1 and 3 weeks in vivo, significant differences be detected over time for all groups, our results
were observed in biomechanical testing. The general showed that 2 groups maintained their torque values
linear modeling (ANOVA) test detected a significant at the period of onset of woven bone formation and
increase of torque values over implantation time interfacial bone remodeling and a period during
when all implant groups were included. Significantly which substantial bone activity takes place in the dog
higher torque values were also observed between mandible model, rejecting the null hypothesis. Our
groups, with group 3, group 2, and group 1 ranked results, however, strongly suggest that the interplay
highest, intermediate, and lowest, respectively. Al- between surgical instrumentation, implant geometry,
though these observations are informative because and surface directly influences implant systems’ sta-
the different implant systems were placed according bility at early implantation times. However, because
to their manufacturer’s instructions, it should be this investigation was limited to only 2 evaluation
noted that mainly because of the different geometric points in vivo, temporal stability decreases and in-
configuration between systems, any attempt to com- creases among systems may have been hindered.
pare the torque values obtained in this study to stan- Thus, experimental multivariable studies concerning
dard insertion torque values commonly observed for specific effects of implant design aspects over a larger
humans or to compare the torque values obtained number of evaluation times are warranted.
between experimental implant groups would be of
limited value. Acknowledgments
Directly related to the null hypothesis, which stated This study was supported in part by the Department of Dentistry
that no differences in biomechanical behavior would at Universidade Federal de Santa Catarina, Brazil. The implants used
COELHO ET AL 1675
were purchased from all manufacturers except Intra-Lock Interna- 14. Coelho PG, Suzuki M, Guimaraes MV, et al: Early bone healing
tional, which donated the implants. The authors acknowledge around different implant bulk designs and surgical techniques:
valuable discussions with Dr Robert J. Miller before and during the A study in dogs. Clin Implant Dent Relat Res, 2009
preparation of the article. 15. Granato R, Marin C, Suzuki M, et al: Biomechanical and histo-
morphometric evaluation of a thin ion beam bioceramic de-
position on plateau root form implants: An experimental study
in dogs. J Biomed Mater Res B Appl Biomater 90:396, 2009
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