Bone Mineral Apposition Rates at Early

Implantation Times Around Differently Prepared

Titanium Surfaces: A Study in Beagle Dogs
Paulo G. Coelho, DDS, PhD1/Jose N. Freire, DDS, PhD2/Rodrigo Granato, DDS, PhD3/
Charles Marin, DDS, PhD4/Estevam A. Bonfante, DDS, PhD1/Jose N Gil, DDS, PhD3/
Sung-Kiang Chuang, DDS, DMSc5/Marcelo Suzuki, DDS6

Purpose: This study evaluated the bone mineral apposition rate (MAR) at the bone-implant
interface region of alumina-blasted/acid-etched (AB/AE), plasma-sprayed hydroxyapatite (PSHA),
and nanometric-scale bioceramic-coated surfaces at early implantation times in a dog tibia model.
Materials and Methods: Implants (n = 12 per group) with three different surfacesAB/AE, PSHA,
and a bioceramic coating in the 300- to 500-nm thickness rangewere placed bilaterally along
the proximal tibiae of six male beagles. Implants remained for 3 and 5 weeks in vivo. Ten and
2 days prior to euthanization, calcein green and oxytetracycline were administered for bone
labeling. Following euthanization, the limbs were retrieved by sharp dissection and the implants
and bone were processed nondecalcified into ~30-m-thick sections along the implant long axis.
MAR was measured by the distance between bone labels over time at the interface region (to
0.5 mm from the implant surface) and at regions > 3 mm from the implant surface (remote site).
A generalized linear mixed-effects analysis of variance model was conducted with significance
levels set at .05. Results: Irrespective of implant surface, the MAR at the interface region was
significantly higher than the MAR at the remote site. Significant MAR differences in the interface
region were observed between the different surfaces (PSHA > AB/AE > nano). Conclusions: Bone
kinetics during early healing stages were influenced by implant surface modifications. Int J Oral
Maxillofac Implants 2011;26:6369

Key words: endosseous implant, in vivo, mineral apposition rate, surface properties

1 Assistant

Professor, Department of Biomaterials and

Biomimetics, New York University, New York, New York.
2Private Practice, Florianopolis, Brazil.
3Instructor, Department of Dentistry, Universidade Federal de
Santa Catarina, Florianopolis, Brazil.
4Research Associate, School of Dentistry, Department of Oral
and Maxillofacial Surgery, Pontifcia Univesidade Catlica do
Rio Grande do Sul, Porto Alegre, Brazil.
5Assistant Professor, Department of Oral and Maxillofacial
Surgery, Harvard School of Dental Medicine and
Massachusetts General Hospital, Boston, Massachusetts.
6Clinical Assistant Professor, Department of Prosthodontics,
Tufts University School of Dental Medicine, Boston,
Massachusetts.
Correspondence to: Dr Paulo Coelho, Department of Biomaterials
and Biomimetics, New York University, 345 24th Street, Room
806, New York, NY 10010. Email: pgcoelho@nyu.edu

he concept of osseointegration1,2 has changed

dental practice over the last two decades. This
treatment modality presents success rates exceeding
95%,3 especially when implants are placed in regions
with relatively high cortical/trabecular ratios (ie, the
anterior mandible).4 However, lower success rates,
often associated with poorer biomechanical fixation, have been reported for regions of lower cortical/trabecular ratios (ie, the posterior maxilla). 5 This
decreased success rate has led clinicians to allow longer osseointegration periods (time allowed for bone
healing after surgical placement of implants) in an
attempt to increase the biomechanical fixation prior
to loading, resulting in increased treatment times for
implant therapy.6
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In an attempt to improve on this circumstance, design

changes to improve the host biologic/biomechanical response to implants have been researched extensively.79
These design changes primarily include macrogeometry9 and surface modifications.7,9,10 Among the different surface modifications applied to dental implants,
incorporation of bioceramics such as hydroxyapatite
(HA) have been investigated most frequently.11 This
interest is partly a result of the similar chemical composition of HA versus natural bone and also the fact
that HA can be applied to implant surfaces by various
industrial processing methods.12,13
Most commercially available bioceramic coatings
are processed as a 20- to 50-m-thick plasma-sprayed
HA (PSHA) coating.8,1216 While high bone-to-bio
ceramic bonding17 and bone-to-implant contact
percentages have been observed at early implantation times for PSHA-treated implants,8,1216,18 studies
have shown that coatings may be partially dissolved/
resorbed after some time in vivo.8,14,15,18,19 This partial
dissolution arises from difficulties in controlling coating composition during manufacturing,20 where the
final coating structure typically presents various calcium- and phosphorus-based crystalline and amorphous phases in different amounts.12,13,20 Also, PSHA
coatings normally rely on mechanical interlocking
between a grit-blasted or etched metallic substrate
and the ceramiclike PSHA material for physical integrity during implant placement and function.12 This
interface region between the metallic substrate, oxide layer, and ceramic coating has been regarded as
a weak link at which failures have been reported after
long periods in vivo.12,13,16
In an attempt to benefit from the osseoconductive properties observed in calcium- and phosphorus-based coatings while decreasing the long-term
dependence on mechanical interlocking between
coatings and implantable devices, bioceramic coatings in reduced scales have been developed for
implant surfaces through various processing techniques.14,15,21,22 Previous research in different animal
models concerning thin coatings in the micrometer14,21 and nanometer (from 30 to 50 nm to 300 to
500 nm)2325 ranges have shown static histomorphometric and biomechanical results after short26 and
long14,21 implantation times that were better than
those of uncoated implants and somewhat comparable to those of thick PSHA-coated implants.9,14,18,19
However, while promising in vivo results have
been achieved through reduced-scale coatings in
endosseous implants, comparative analyses regarding their effect on bone healing kinetics with respect
to uncoated and PSHA coatings during the early
stages of healing have not been performed to date.
The objective of this study was to evaluate the bone

mineral apposition rate (MAR) at the bone-implant

interface region of alumina-blasted/acid-etched (AB/
AE), PSHA-coated, and nanometer-thickness bio
ceramic-coated surfaces at early implantation times
in a dog tibia model.

Materials and Methods

Materials

For this study, three different implant surfaces were

used: AB/AE, PSHA-coated, and nanothickness ion
beamassisted deposition bioceramic (Nano). All surfaces were fabricated on cylindric titanium-aluminumvanadium implants (4 mm in diameter by 10 mm in
length, no threads). Previous detailed physicochemical characterizations23,24 have shown that the PSHA
coatings were about 20 to 30 m thick and presented
with about 40% crystalline HA content, and the thin
bioceramic coating was 300 to 500 nm for the Nano
implants. The Nano coating was calcium- and phosphorous-based with amorphous atomic structures.23,24
Surface roughness assessment has also shown that,
despite the nanothick bioceramic deposition, the initial AB/AE roughness parameters were maintained.23,24
The PSHA surface roughness was greater than that of
the other surfaces.23,24

Methods

Following approval by the Bioethics Committee for

Animal Experimentation at Universidade Federal de
Santa Catarina, six male beagle dogs, each approximately 18 months of age, were acquired and kept in
an animal care facility for a period of 12 weeks prior to
surgery. All surgical procedures were performed under general anesthesia. The preanesthetic procedure
comprised intramuscular administration of atropine
sulfate (0.044 mg/kg) and xylazine chlorate (8 mg/
kg). General anesthesia was then obtained following an intramuscular injection of ketamine chlorate
(15 mg/kg). Following hair shaving, skin exposure,
and antiseptic cleaning with iodine solution in the
surgical and surrounding areas, a 5-cm incision at
the skin level was performed. A flap was reflected
and the proximal tibia was exposed. Three implants
were sequentially placed distally beginning at 2 cm
below the synovial capsule 1 cm from each other in
each tibia (six implants in each animal). The implant
placement technique was performed according to
the manufacturers recommendation. The procedures comprised an initial cortical plate perforation
with a 2-mm-diameter pilot drill under saline irrigation and subsequent drilling with burs of increasing diameters (up to 4 mm in 1-mm increments) at
50 rpm without saline irrigation. The implants were

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Coelho et al

gently tapped into the drilling sites and a polyethylene healing screw was adapted to the implant top to
prevent callus overgrowth and facilitate later implant
location. Standard layered suturing procedures were
performed for soft tissue closure. Postsurgical medication included antibiotics (penicillin, 20,000 IU/kg)
and analgesics (ketoprofen, 1 mL/5 kg) for a period of
48 hours postoperatively. Euthanasia was performed
by an overdose of anesthetic.
Each dog provided a 3-week and 5-week (one evaluation time per limb) sample of the control (AB/AE),
Nano, and PSHA implant surfaces per three-implant
locations through sequenced surgical procedures
(implant surfaces were interpolated from sites 1 to
3 from proximal to distal). The overall distribution of
implants per animal ensured placement of an equal
number (n = 6) of AB/AE, Nano, and PSHA implants for
each in vivo evaluation time.
Calcein green and oxytetracycline (10 mg/kg) were
administered sequentially at 10 and 2 days prior to
euthanization for bone fluorescent labeling. At necropsy, the proximal tibia was exposed by sharp dissection, and the limbs were removed and contact
radiography performed to confirm implant location
and orientation. The proximal tibia was reduced into
smaller sections containing one implant per block.
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) according to the manufacturers instructions. The blocks were then cut into slices (each about
~300 m thick) at the center of the implant along its
long axis with a precision diamond saw (Isomet 2000,
Buehler) and glued to acrylic glass plates with an
acrylate-based cement. A 24-hour setting time was
allowed prior to grinding and polishing. The sections
were then reduced to a final thickness of ~30 m by
means of a series of silicon carbide abrasive papers
(400, 600, 800, 1,200, and 2,400 grit; Buehler) in a
grinding/polishing machine (Metaserv 3000, Buehler)
under abundant water irrigation.27
For fluorescent microscopy, the nondecalcified
sections were placed under an optical microscope
(Olympus) equipped with an ultraviolet light source
including barrier filters. For assessment of MAR, two
different regions of interest were evaluated (Fig 1). The
first region of interest comprised the bone area along
both sides of the implant to a distance of 0.5 mm from
the implant surface (interface region). The second region of interest was set in the region > 3 mm away
from the implant surface (control MAR site, which is
a remote site for assessment of bone MAR that is not

Fig 1The implants in nondecalcified sections were divided

into regions of interest for assessment of MAR. The first region comprised the bone-implant interface MAR (from 0 to 0.5
mm from the implant surface; areas outlined in red), and the
second region of interest comprised regions > 3 mm from the
implant surface (remote site MAR; area outlined in yellow).

influenced by implant surgery/placement23). A digital

camera was used to capture sequential (by area, including the whole bone-implant region perimeter)
images of the regions of interest at both sides of
the implant (magnification 80), and the measurements were performed using a customized computer
software template (Bioquant NOVA, Bioquant Image
Analysis). The MAR for the different regions of interest
was determined by the distance in micrometers between calcein green and oxytetracycline fluorescent
labels, divided by the number of days between the
administration of each fluorescent label.28,29 At least
20 measurements per specimen were performed per
region of interest. For qualitative analysis of the boneimplant interfaces, transmitted light microscopy
(Olympus) in polarized mode was utilized.

Statistical Procedures

The primary predictor variable was implant surface,

ie, AE/AB versus Nano versus PSHA. Secondary predictor variables were implant surgical site (first, second, or third site, from proximal to distal) and time in
vivo (3 or 5 weeks). For statistical analysis, the groups
were used and defined as references. To assess the adjusted relationship between various groups and the
major outcome (MAR), the investigators constructed
a generalized linear mixed-effects analysis of variance
model. The level of statistical significance in the multivariate model was set at a P value (an level) of .05.
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Coelho et al

HA

100 m

Fig 2 Polarized light microscopy of the bone-implant interfaces of (a) AB/AE, (b) Nano, and (c) PSHA-treated implant surfaces. The
PSHA coating between the bone and the implant substrate was observed in most specimens at both implantation times.
Fig 3Fluorescence microscopy showing calcein green and
oxytetracycline bone labeling in close proximity and (inset) away
from the bonePSHA implant-treated surface. Arrows denote
the remaining thickness of HA along the implant surface. The
interlabel distance was determined by a customized computer
software template.

Implant

Bone

50 m

HA

200 m

All P values were two-sided. Database preparation

and management and statistical analyses were carried out using SAS version 9.1 (20022003) statistical
software (SAS Institute Inc) using the SAS procedure
code proc mixed.

Results
No complications regarding procedural conditions,
postoperative infections, or other clinical concerns, were
observed during the course of the animal experiment.
Overall observation of the nondecalcified histologic sections showed that, in all specimens, the implant
was in contact with cortical and trabecular bone. Evaluation at a higher magnification under polarized light

showed the presence of intimate contact between

all implant surfaces and cortical and trabecular bone
along the implant perimeter. Unlike the PSHA-treated
implants, where interfaces between bone and coating and coating and implant substrate were observed
(Fig 2), no evidence of a bone-bioceramic interface
was observed for the Nano implants (Fig 2).
All bone in the samples showed calcein green and
oxytetracycline labeling within cortical and trabecular bone in sites along the bone-implant interface
and > 3 mm away from the implant surface. This allowed measurements of the interlabel distance and
MAR calculation (Fig 3). The MAR at the interface region of interest was significantly higher than that at
the remote site (> 3 mm from the implant surface),
and significant differences were observed between

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Coelho et al

Table 1 Generalized Linear Mixed-Effects Analysis of Variance Summary Statistics

Variable

Mean MAR SD

Coefficient

Standard error

t statistic

Time
5 wk

2.88 0.66

0.09593

0.02910

3.30

.0011

3 wk

2.98 0.65

0.000 (reference)

Reference

Reference

Reference

2.75 0.72

0.01675

0.1106

0.15

.8892

Site
Site 3
Site 2

2.77 0.60

0.01868

0.1106

0.17

.8766

Site 1

2.59 0.65

0.0000 (reference)

Reference

Reference

Reference

AB/AE

2.72 0.49

0.3940

0.08231

4.79

< .0001

Implant surface
Nano

2.56 0.68

0.2394

0.08231

2.91

.0038

PSHA

2.80 0.78

0.4711

0.08231

5.72

< .0001

Control MAR

2.33 0.58

0.0000 (reference)

Reference

Reference

Reference

The control MAR was collected at a remote bone site at regions > 3mm from the bone-implant interface.

surfaces (PSHA > AB/AE > Nano) (Table 1). No differences in MAR were detected between surgical sites,
and a slight variation was observed in MAR for the different periods (3 and 5 weeks) (Table 1).

Discussion
The search for more biocompatible and osseoconductive endosseous implant systems has led researchers
to test extensive modifications of surface texture and
chemistry.10,11 Studies have shown that histologic
and biomechanical parameters were improved by
increasing the as-machined surface roughness by
various methods.10,11 However, whether surface texturing yields improved in vivo performance versus
the incorporation of bioactive ceramics on implant
surfaces remains controversial.
While it has been shown that thick PSHA bio
ceramic coatings are highly biocompatible and osseoconductive,8,1216,18 they have fallen out of
favor in clinical practice because of their potential
process-inherent limitations such as mechanical failure (fracture between coating and metallic substrate
after integration) and chemical instability (uneven
dissolution properties). As an alternative, thin bioceramic coatings with controlled composition and
thickness plus enhanced adhesion to the metallic
substrate have been introduced.8,12,14,15,21,22

Thin coatings with controlled composition and

thickness, achievable through a variety of methods,
have been shown to positively influence the early
host-to-implant response compared to textured uncoated surfaces.11,14,17,21,2325,30,31 A previous biomechanical investigation that considered AB/AE, Nano,
and PSHA surfaces at 3 and 5 weeks in vivo in the
same animal model showed that early biomechanical
fixation was favored by the presence of a calcium- and
phosphorus-based coating. However, even though
the Nano surface presented significantly higher biomechanical fixation compared to AB/AE, higher mechanical fixation values were observed for the PSHA
group.24 In contrast to the differences observed in
biomechanical testing, static histomorphometric
evaluations of percent bone-to-implant contact were
in agreement with the present results, and no significant differences were observed between groups.24
In an attempt to better understand previous biomechanical and histomorphometric findings,24 the
present study sought to evaluate MAR at two different time points in the same animal model within the
same implantation time frames. The rationale for MAR
assessment from 0 to 0.5 mm from the implant surface originated from preliminary studies that showed
that regions adjacent to the implant surface show
higher bioactivity/remodeling levels compared to
remote sites (such as the control MAR sites utilized
in the present study).23,32 These investigations have
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also shown that, compared to bone-implant interface regions, modeling/remodeling levels remain
unchanged at regions away from the implant surface
such as in the physiologic region of interest considered in the present investigation.23,32
The data collected for the 3- and 5-week groups
evaluated MAR over two distinct time frames. The
3-week group evaluated MAR during days 9 to 19 of
the 21 implantation days, and the 5-week group evaluated MAR during days 23 to 33 of the 35 implantation days. The significant difference observed in MAR
at 3 and 5 weeks may also be accounted for by surgical trauma and subsequent modeling/remodeling of
the bone. The implantation time effect on MAR was
relatively small compared to differences between
other independent variables such as implant surface,
and based on previous histomorphometric and biomechanical results (no implantation time effect on
bone-to-implant contact and biomechanical fixation)
in the same animal model and with the same implantation times, this observation is probably of little clinical significance.
The results showed that, regardless of implant surface, high MARs were observed compared to the remote sites during the initial stages of implant healing,
which can be accounted for by the stimulus generated by surgical trauma and implant placement. However, the present findings support the hypothesis that
the early stages of healing are significantly affected
by surface modifications, since significant MAR differences were observed between the different implant
surfaces (PSHA > AB/AE > Nano).
Together, the present results and those of a previous biomechanical study24 concerning AB/AE, Nano,
and PSHA implants with the same implantation times
and in the same animal model suggest that high MAR
during the initial stages of healing (especially as the
absolute differences in MAR between groups did not
vary substantially, despite the statistically significant
differences) may not necessarily translate into improved biomechanical fixation. Since biomechanical
fixation was favored on bioceramic-coated implants,
it can be speculated that the coatingbone complex
interaction at the interface level may account for the
significantly lower torque to interface fracture for the
AB/AE group (uncoated) compared to the Nano and
PSHA groups,24 especially with the potentially widely
varying dissolution rates between the Nano and PSHA
coatings because of their substantially different thickness and microstructural configuration.9,14,15,24,33,34
Surface modifications have been employed successfully to endosseous dental implants with the
primary purpose of decreasing osseointegration
time.10,11 The vast majority of implant surface studies
have used static histomorphometric analyses, such as

bone density and bone-implant contact, and/or biomechanical testing and have not used bone kinetic
assessment as a comparison tool.11 One exception
is the study conducted by Suzuki et al,28 who investigated several static histomorphometric parameters
along with bone kinetic indicators such as MAR and
reported a significant implant surface effect. While
the present results have also demonstrated implant
surface effects on MAR, direct comparison with the
sparse number of previous studies is not possible because of different animal models, surgical sites, and
implantation times. Thus, more investigations considering MAR are recommended.

Acknowledgment
This study was partially supported by the Experimental Research Laboratory and Department of Oral and Maxillofacial
Surgery at Universidade Federal de Santa Catarina, Florianopolis, Brazil.

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