Ken Nakahara Single-staged vs.

two-staged implant
Maiko Haga-Tsujimura
Kosaku Sawada
placement in vertically deficient alveo-
Eizaburo Kobayashi lar ridges using bone ring technique –
Benoit Schaller
Nikola Saulacic
Part 2: implant osseointegration

Authors’ affiliations: Key words: animal experiments, bone implant interactions, bone regeneration, guided tissue
Ken Nakahara, Kosaku Sawada, Advanced regeneration, morphometric analysis, surgical techniques
Research Center, The Nippon Dental University
School of Life Dentistry at Niigata, Niigata, Japan
Maiko Haga-Tsujimura, Department of Histology, Abstract
The Nippon Dental University School of Life
Dentistry at Niigata, Niigata, Japan
Objectives: The aim of this study was to evaluate the osseointegration of implants placed in a
Eizaburo Kobayashi, Department of Oral and single-staged compared to two-staged procedure using bone ring technique.
Maxillofacial Surgery, The Nippon Dental Material and Methods: In this study were used standardized, vertical alveolar bone defects in
University School of Life Dentistry at Niigata,
Niigata, Japan dogs. In the test group, dental implants (Straumann BLâ, Basel, Switzerland) were inserted
Benoit Schaller, Nikola Saulacic, Department of simultaneously with bone ring technique. As control group served implants inserted 6 months
Cranio-Maxillofacial Surgery, Inselspital, Bern following grafting. Implants of both groups were left for an osseointegration period of 3 and
University Hospital and University of Bern, Bern,
Switzerland 6 months. The peri-implant bone loss and bone-to-implant contact within the bone ring and native
bone were analyzed morphometrically. An explorative statistical analysis was performed.
Corresponding author: Results: The peri-implant bone level remained relatively stable within groups and between groups
Nikola Saulacic, DDS, PhD
Department of Cranio-Maxillofacial Surgery, per given time period. Most of bone apposite on the implant surface in two groups was composed
Inselspital, of newly formed bone. A nonparametric analysis of variance (ANOVA) revealed no significant
Bern University Hospital and University of Bern
advantage for two-staged implant placement for new and total bone, except for residual bone
CH-3010 Bern, Switzerland
Tel.: +41 31 632 35 63 (P = .0084). Furthermore, two groups of implants performed similarly in bone ring and in native
Fax: +41 382 02 79 bone throughout the observation period.
e-mail: nikola.saulacic@insel.ch
Conclusions: In terms of osseointegration, both techniques are likely equally efficient in the
present defect model. The single-staged implant placement with cortical bone grafts warrants
further documentation in clinical studies.

Block bone grafts are considered the “gold This surgical modality, however, requires at
standard” for the vertical bone augmentation, least two-tooth span and high patient compli-
due to the osteogenic capacity, osteoconduc- ance. In majority of cases for the augmenta-
tivity and osteoinductivity (Miron et al. tion of the vertically deficient alveolar ridges,
2011). The apparent drawbacks of autogenous autogenous block bone grafting remains the
bone grafting are additional surgery and pos- treatment of choice (Rocchietta et al. 2008).
sible donor-site morbidity (Zouhary 2010). The dynamics of bone remodeling may be
The assessment of alternative treatment crucial for the process of osseointegration.
modalities was thus encouraged to avoid Cortical bone is considered stable enough to
these disadvantages. Vertical guided bone withstand the load-bearing forces in the oral
regeneration (GBR) with simultaneous cavity (McAllister & Haghighat 2007), but is
implant placement enables the formation of characterized by the absence of viable bone
considerable amounts of new bone with and reduced rate of revascularization (Ennek-
stable peri-implant bone level (Simion et al. ing et al. 1980; Hammack & Enneking 1960).
2001). Still, the risk of wound dehiscence and Prior to implant placement, the non-vital
Date:
site infection remains the concern when bone should be completely replaced by the
Accepted 20 March 2016
using this technique (Fontana et al. 2011). vital bone able to adapt to functional loading
To cite this article:
Nakahara K, Haga-Tsujimura M, Sawada K, Kobayashi E, The need for bone harvesting may be avoided (Goldberg & Stevenson 1987). Interestingly,
Schaller B, Saulacic N .Single-staged vs. two-staged implant using the principle of distraction osteogene- single-staged implants placed in the onlay
placement in vertically deficient alveolar ridges using bone
ring technique – Part 2: implant osseointegration. sis, as the bone regeneration occurs within cortical bone grafts showed no difference in
Clin. Oral Impl. Res. 28, 2017, e31–e38. the region of osteotomy (Saulacic et al. 2008). bone-to-implant contact (BIC) compared to
doi: 10.1111/clr.12851

© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd e31
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Nakahara et al
Osseointegration of implants placed using bone ring technique

implant placement after two (Rasmusson

et al. 1999; Dasmah et al. 2013) or 3 months
of graft healing (Rothamel et al. 2009). The
two-staged implant placement following
block bone grafting was though preferred
(Proussaefs & Lozada 2005; Cordaro et al.
2010; Roccuzzo et al. 2007) to evade an ini-
tial bone resorption and possible implant loss
(Boronat et al. 2010). A recent review of clini-
(a) (b) (c)
cal studies comparing success of single-staged
(61.5%–100%) and two-staged implant place- Fig. 1. Intraoperative view of the treated area. a: Standardized bone defects of 8 9 5 mm were created on the
ment (75%–98.3%) suggested the later tech- alveolar ridge. An implant was inserted through the several bone rings harvested from the mandible (b) or one bone
nique as more predictable (Clementini et al. ring harvested from the calvaria (c).

2013). The analyzed studies, however, fluctu-

ated considering the defined criteria of sur-
vival and success of implants and technique
itself.
Simultaneous implant placement with cor-
tical block bone graft was occasionally per-
formed using a bone ring technique to
support fixed prosthesis in edentulous jaw
(Penarrocha-Diago et al. 2005), short edentu-
lous space (Stevens et al. 2010) or single-
tooth gap (Fukuda et al. 2000; Tekin et al.
2011). This method advantages a shorter
overall treatment period of the vertically defi-
cient ridges, but lacks sufficient scientific
evidence to demonstrate its efficacy. In a dog
model, we recently compared the remodeling
of bone ring by single-staged and two-staged (b)
implants placed after 6 months of healing
(Nakahara et al. 2015). Whereas both groups
demonstrated approximately same total bone
volume, bone rings with simultaneously
placed implants showed more residual bone
and with delayed implant placement more
new bone at both 3 and 6 months of osseoin-
tegration. It is thus questionable how these
differences affect the bone apposition onto
the implant surface.
The second part of this study aimed to
compare the osseointegration and peri-
implant bone level of implants placed in a
single-staged versus two-staged procedure
using bone ring technique in the standardized
alveolar bone defects of dogs.

(a)
Material and Methods
Fig. 2. Illustration of histomorphometric measurements. a: The border between R1 (white line) and R2 (pink line)
is set 5 mm apically from the top of the surrounding bone. The measurements in R1 were performed from the first
Nine male, 1-year-old Beagle dogs were used point of BIC (fBIC, yellow point) and in R2 down to the lowest point of BIC (red point). b: The linear distances are
in the experiment. The study was approved measured from the implant shoulder (IS) to the fBIC (yellow point) and to the top of the surrounding bone (TSB).
by the Animal Experiment Ethics Committee
of The Nippon Dental University, School of
Life Dentistry at Niigata, Japan (No. 2013–144). the second surgery, two vertical ridge defects group, bone rings were fixed with 1-mm sub-
The surgeries and the implant placement of 8 mm (mesio-distal) to 5 mm (apico-coro- crestally inserted dental implant (Bone Level
were performed as previously described nal) were created on each side of the mand- Implant SLActiveâ, Ø 3.3 mm, length
(Nakahara et al. 2015). Four premolars were ible (Fig. 1a). The cortical bone grafts were 10 mm; Straumann AG, Basel, Switzerland).
extracted from both sides of the mandible harvested from the mandibular ramus in two In all sites, two or three layers of bone ring
and left for a healing period of 3 months. At dogs using the trephine drill. In the test were used because of the insufficient bone

e32 | Clin. Oral Impl. Res. 28, 2017 / e31–e38 © 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
 16000501, 2017, 7, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/clr.12851 by Université de Reims Champagne-Ardenne, Wiley Online Library on [09/03/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Nakahara et al
Osseointegration of implants placed using bone ring technique

Mitsubishi Tanabe Pharma Corporation,

Osaka, Japan).

Histological preparation and analysis

Following harvesting, the bone samples were
fixed in 10% neutral formalin and then pro-
cessed into undecalcified ground sections.
The embedded tissue blocks were cut
mesiodistally along the implant axis using a
slow-speed diamond saw (VC-50; Leco, MI,
USA) into approximately 800-lm-thick
(a) (b) ground sections. The sections were then
grounded and polished to a final thickness of
approximately 300 lm (Knuth-Rotor-3;
Struers, Rodovre/Copenhagen, Denmark).
The labeled bone was observed and pho-
tographed under a confocal laser scanning
microscope (LSM710; Carl Zeiss, Oberko-
chen, Germany). The sections were stained
with toluidine blue combined with fuchsin
(Schenk et al. 1984) and photographed under
a light microscope equipped with a digital
imaging system (AxioCam; Carl Zeiss, Ober-
kochen, Germany).
(c) (d)
Histomorphometric analysis was per-
Fig. 3. Histological sections illustrating the peri-implant bone level and the surrounding bone in four groups. a: In formed using three different morphometric
the 3-month test group, the top of the bone around the implant is higher than the implant shoulder. b: The control parameters: (i) percentage of BIC, deter-
group at 3 months of osseointegration period demonstrates peri-implant bone level sloping down away from the
mined for bone deposited along the implant
implant shoulder. c: The peak of the surrounding bone locates much higher than the implant shoulder at 6 months
of osseointegration period of the test group. d: The bone attached to the implant is the highest, and the surrounding
surface from the first to last point of con-
bone is comparatively flat in the 6-month control group. tact (Fig. 2a); (ii) linear distance from the
implant shoulder to the first BIC (fBIC);
and (iii) linear distance from the implant
shoulder to the top of the surrounding bone
Table 1. The distance between implant shoulder to the first BIC (fBIC) and the top of the
surrounding bone (TSB) for both groups (TSB; Fig. 2b). We calculated the percentage
of the implant surface covered by residual
Time point Group FBIC TSB
bone (graft bone and old host bone), newly
3 Months Test 0.85 ( 1.89, 0.13) 0.37 (0.20, 1.54)
formed bone (osteoid, woven bone and new
Control 0.07 ( 1.41, 0.04) 0.09 ( 0.79, 0.22)
6 Months Test 0.26 ( 0.89, 0.21) 1.04 ( 0.57, 1.68) lamellar bone), total bone (residual bone
Control 0.02 ( 0.68, 0.17) 0.27 ( 0.11, 0.41) and newly formed bone) and soft tissue.
Measures are expressed in %: median (minimum, maximum). Two regions of interest were selected con-
sidering the bottom of the grafted bone
ring, coronally to the fBIC (R1) and apically
to the lowest BIC (R2). The measurements
thickness (Fig. 1b). One bone ring from the Sigma-Aldrich, St. Louis, MO, USA) at were performed on the mesial and distal
calvaria region was thus used per bone defect 3 weeks before euthanasia and with calcein side of each implant and the means in each
in all other sites of seven dogs (Fig. 1c). Bone (3 mg/kg b.w, once daily for 2 days; Wako group calculated.
rings in the control group were initially stabi- Pure Chemicals, Osaka, Japan) at 1 week
lized with osteosynthesis mini-screws before euthanasia. Statistical analysis
(Modus ∅ 1.5 mm, length 10 mm; Medartis The linear measurements (fBIC and TSB)
AG, Basel, Switzerland). Thereafter, all sites Sample preparation were characterized using descriptive statis-
were covered with collagen membranes (Bio- One dog in the test group with bone ring tics (median, minimum and maximum).
Gideâ; Geistlich Pharma, Wolhusen, Switzer- harvested from the mandibular ramus died The percentage of BIC was reported as
land). In the control group, dental implants during the surgery. Two dogs of each group means and standard deviations. Normal dis-
were placed after 6 months of healing. The were killed after an osseointegration period tribution was not assumed due to the small
flaps were sutured to allow a submerged heal- of 3 (3M) and 6 months (6M). Two samples sample size. A nonparametric analysis of
ing of all implants. were randomly selected from each dog for variance (ANOVA) for longitudinal data was
For the dynamic labeling of bone formation the analysis, giving a sample size of four applied using a Brunner–Langer model to
and bone remodeling, animals were intra- per group and healing period (n = 4). The assess the impact of implant placement on
muscularly injected with alizarin red S animals were euthanized by an intravenous the amount of hard and soft tissues cover-
(20 mg/kg b.w, once daily for 2 days; overdose of thiopental sodium (Ravonalâ; ing implant surface in the bone ring and in

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Nakahara et al
Osseointegration of implants placed using bone ring technique

cal sign of infection in all sites, except

for the sample with advanced bone resorp-
tion.

Peri-implant bone
In some samples of the 3M test group, the
peak of the cortical bone was located coro-
nally to the implant shoulder (Fig. 3a). Out-
side the peri-implant area, the surrounding
bone became relatively flat. The level of the
surrounding bone in the 3M control group
(b) was flat without a peak (Fig. 3b). Median val-
ues of fBIC and TSB in the test group ( 0.85
and 0.37 mm, respectively) were higher than
in the control group ( 0.07 and 0.09 mm,
respectively; Table 1). The height of the sur-
rounding bone in the 6M test group varied;
the bony peak in three samples was higher
than the implant shoulder (Fig. 3c), while in
one sample without healing cap was observed
a delimited area of marginal bone resorption
without a bony peak. Surrounding bone in
the 6M control group was more compact and
flat corresponding to the 3M control group,
(c) decreasing further away from the implant
shoulder (Fig. 3d). Median fBIC values
decreased, while TSB values increased from 3
to 6 months of osseointegration period in
both groups, being always higher in the test
group ( 0.26 and 1.04 mm, respectively) than
in the control group ( 0.02 and 0.27 mm,
respectively).

Three-month osseointegration period

Intensive bone remodeling was characteris-
(a) (d) tic for the implants of the 3M test group.
Active remodeling was frequently observed
Fig. 4. Histological observation in the 3-month test group. a: New bone (NB) is observed around the implant and around the residual bone graft and around
around grafted bone (GB). The upper and lower boxed areas in (a) are shown in (c) and in (d), respectively. Figure (b)
implant, but not within the graft bone
shows the image of fluorescent bone labeling in the same area as (c). b: New bone is labeled around the blood
vessels. c: The newly formed bone with canals including vessels surrounds the implant and grafted bone. d: The (Fig. 4a). New bone around the implant sur-
trabecular bone is connected directly to the implant in the lower area with rich bone marrow (BM). face was found by light and fluorescent
microscope, penetrated by many blood ves-
sels (Fig. 4b, c). The size of vessels within
residual bone seemed to be smaller than
native bone. Repeated measurements were quently found around exposed implants and within new bone. In the cortical bone area
designed, as the two time points were con- implants with loosed healing caps. One and in the trabecular bone in the R2, the
sidered dependent. A significance level of exposed implant site from the 3M test implant surface made contact mainly with
0.05 was chosen. The statistical analysis group showed advanced resorption. A rela- newly formed bone (Fig. 4d).
was performed using a licensed software tively thick layer of soft tissue was Signs of advanced osseointegration were
package (R Foundation for Statistical Com- observed between layers of graft bone, found in the 3M control group (Fig. 5a).
puting, version 3.2.2, Vienna, Austria). dental implant and the host bone in this The newly formed bone was facing the
sample. However, new bone was formed implant surface, with little residual bone
Results near the soft tissue. All implants with remained. The vessels perforated compara-
loosed healing caps were covered with the tively uniform layer of compact bone, sprin-
General observations healed soft tissue. Direct contact between kling over the surrounding bone. The new
All eight animals healed uneventfully, with- the implant and the bone was observed in bone formation around the implant was
out clinical signs of infection or implant all samples, without remarkable difference demonstrated by bone labeling (Fig. 5b) and
loss throughout the observation period. in histological findings between the test the distribution of osteoblasts with woven
Signs of marginal bone resorption were fre- and control group. There was no histologi- bone (Fig. 5c). The apical part of implants

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Nakahara et al
Osseointegration of implants placed using bone ring technique

bone, whereas the contact to the residual

bone was only negligible (Fig. 7d).

Statistical analysis
Mean values of BIC for the test and control
group were similar per given time point
(Table 2). Total BIC was composed mainly
of new bone in both groups. A nonparamet-
ric analysis of longitudinal data according
to the Brunner–Langer model revealed that
timing of implant placement was significant
for residual bone (P < .01; Table 3). New
(b)
and total bone decreased, while soft tissue
increased from 3 to 6 months of osseointe-
gration period (P < .05). Nevertheless, none
of the interaction terms was significant.

Discussion

The present study aimed to compare the

integration of implants placed simultane-
(c) ously with cortical bone grafts to implants
placed in the two-staged technique using a
standardized, acute saddle-type bone defect
(Iglhaut et al. 2014; Hoshi et al. 2015).
Mean BIC in the present study corresponds
to the previous results observed for the
same implant surface (Alharbi et al. 2014;
Bayounis et al. 2011). Similar values of BIC
in the two groups confirm former findings
(Rothamel et al. 2009; Dasmah et al. 2013)
on the longer period of observation. Further-
more, BIC values were comparable in bone
ring and in native bone irrespective of the
timing of implant placement. In the present
(a) (d) type of bone defect, single-staged implant
placement using bone ring may be consid-
Fig. 5. Histological observation in the 3-month control group. a: The newly formed bone surrounding implant con- ered equally efficient as the two-staged
sists mainly of the compact bone (CB). The upper and lower boxed areas in (a) are shown in (c) and in (d), respec-
technique.
tively. Figure (b) shows the image of fluorescent bone labeling in the same area as (c). b: The labeled lines are seen
near the implant surface. c: New bone is formed around the implant (arrowheads) compared to the mature bone far Following placement, an establishment of
from the implant. Woven bone (WB) with the line of osteoblasts corresponds to the bone labeling. d: Osseointegration the biologic width dimensions around
is achieved in the apical side. implants is to be expected (Berglundh et al.
1991). The median fBIC in the 3M test
group resembles these events, reaching the
was osseointegrated within the area of bone deposited onto the implant surface increased, values of up to 2.91 mm per implant side
marrow (Fig. 5d). reaching the apical portion on the implant (data not shown). Higher peri-implant bone
(Fig. 6d). Nevertheless, the amount of trabec- loss in the 3M test group seemingly indi-
Six-month osseointegration period ular bone remained stable compared to the cates the benefit of two-staged implant
Dental implants of both groups demon- 3M test group. placement, corresponding to the previous
strated a complete osseointegration (Fig. 6a). Newly formed bone in the 6M control results (Tran et al. 2010). Nevertheless, the
Newly formed bone in the 6M test group group was predominantly made of mature variation in data on linear measurement
exhibited the histological features of com- bone (Fig. 7a). The volume of the residual was so large that no statistical test was per-
pact bone comparable to the 3M test group, bone further decreased compared to the 3M formed. The size of the healing caps used
whereas the immature bone including control group with the surrounding bone in the present study apparently caused their
osteoid and woven bone was still visible fac- composed mainly of newly formed lamellar exposure and frequent loosening in both
ing implant surface (Fig. 6b, c). The border bone. Even in this group, the new imma- groups with sings of marginal bone resorp-
between the residual graft and newly formed ture bone was in contact with the implant tion. Disruption of the established mucosal
bone was less visible compared to the 3M surface (Fig. 7b, c). In R2, the implant sur- seal may be associated with the inflamma-
test group. The extent of trabecular bone face made contact with the cancellous tory response, dimensional changes of the

© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd e35 | Clin. Oral Impl. Res. 28, 2017 / e31–e38
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Nakahara et al
Osseointegration of implants placed using bone ring technique

statistical significance for new and total bone

suggests that the single-staged implant place-
ment did not impede the regenerative capac-
ity of bone graft.
Corresponding to the bone ring area, evi-
dently more new bone on the implant sur-
face than in the peri-implant area was
present in the native bone of both groups
(Nakahara et al. 2015). As the design of the
present study allowed only an explorative
statistical analysis, the data have to be
interpreted with caution. Nevertheless, our
(b)
results corroborate the previous findings
using abrasive-blasted and acid-etched
(Rothamel et al. 2009) and TiO2-blasted and
fluoridated surfaces (Dasmah et al. 2013).
Increased wettability by chemical modifica-
tion may significantly enhance the osteo-
conductive properties of the SLAâ surface
(Lang et al. 2011; Saulacic et al. 2012). The
type of implant surface has apparently more
impact on BIC than the stage of cortical
bone remodeling.
In the later stages of healing, the new
immature bone was remodeled and became
(c)
more compact. These histological features
also characterized the peri-implant bone
that became more even in the control than
in the test group, as shown by the mor-
phometric analysis. Nevertheless, it was
not possible to clearly distinguish the
transitional bone in remodeling process.
As a consequence of bone remodeling,
large contact area of new bone at implant
surface in both groups diminished. Corre-
sponding to the peri-implant area of the
(a) (d)
native bone, mean values of new and total
Fig. 6. Histological observation in the 6-month test group. a: Newly formed bone (NB) exists around the implant bone significantly decreased at 6 months
surface and around the residual graft bone (GB). The upper and lower boxed areas in (a) are shown in (c) and in (d), of osseointegration period. The same ten-
respectively. Figure (b) shows the image of fluorescent bone labeling in the same area as (c). b: Labeled bone close to dency was previously demonstrated for
the implant surface shows bone remodeling near the implant even after 6 months. c: The new bone covers the
non-loaded implants (Blanco et al. 2013).
implant surface. d: The apical side of implant integrates with the trabecular bone with bone marrow (BM).
Future studies should demonstrate whether
loading of implants placed with bone ring
technique would affect the BIC correspond-
peri-implant mucosa and marginal bone loss integration of implants. According to the ingly to the implants placed in the native
(Becker et al. 2012). All sites with loosed indication, the usually applied osseointegra- bone.
healing caps, however, completely healed tion period of 3 months (Cordaro et al. 2010;
without remarkable signs of inflammation. Mertens et al. 2013) was extended to
In the present model, the single-stage man- 6 months to obtain an overall treatment per- Conclusions
agement revealed no obvious negative influ- iod of 1 year (Cordaro et al. 2002; Rasmusson
ence in terms of peri-implant bone level. et al. 2012). Remodeling of bone ring chrono- In terms of new bone deposition, single-
BIC is one of the parameters that represent logically progressed up to 9 months, with staged implant placement did not affect the
the regenerative capacity of bone graft. Initial substantially more new bone formed in the regenerative capacity of bone graft compared
studies using turned implant surface found control group compared to the test group to two-staged technique. All morphometric
looser connective tissue and lower values of (Nakahara et al. 2015). The differences in parameters behaved similarly in bone ring
BIC for the single-staged than for the two- bone remodeling were confirmed for residual and in native bone over time. Single-staged
staged approach (Rasmusson et al. 1999; bone in contact with implant surface. In con- implant placement using bone ring technique
Lundgren et al. 1999). An enhanced regenera- trast to the peri-implant area, total bone may be considered equally efficient as the
tive capacity of bone grafts at the later stages deposited in the implant surface was com- two-staged procedure in the present type of
of healing was thus expected to ensure better posed largely of new bone. The absence of bone defect.

e36 | Clin. Oral Impl. Res. 28, 2017 / e31–e38 © 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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Osseointegration of implants placed using bone ring technique

Acknowledgements: The authors

wish to thank Dr. Matthias Mottini for his
assistance with manuscript preparation and
Mr. Gabriel Fischer for statistical advice.
This study was founded by the International
Team for Oral Implantology (ITI), Basel,
Switzerland (No. 896_2013). Dental implants
were generously provided by Straumann AG,
Basel, Switzerland.

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implants placed in fresh extraction sockets: an
(a) (d)
experimental study in the beagle dog. Journal of
Clinical Periodontology 40: 421–429.
Fig. 7. Histological observation in the 6-month control group. a: The peri-implant bone exhibits the histological Boronat, A., Carrillo, C., Penarrocha, M. & Penar-
feature of compact bone (CB). The upper and lower boxed areas in (a) are shown in (c) and in (d), respectively. Fig- rocha, M. (2010) Dental implants placed simulta-
ure (b) shows the image of fluorescent bone labeling in the same area as (c). b: The new bone labeled by calcein neously with bone grafts in horizontal defects: a
(green) and alizarin (red) is present near the implant. c: The new bone including woven bone (WB) and osteoid is clinical retrospective study with 37 patients.
observed around the implant, which is consistent with the observation of bone labeling in (b). d: Newly formed International Journal of Oral & Maxillofacial
bone (NB) makes contact with the implant surface in the cancellous bone region. Implants 25: 189–196.

Table 2. Percentage of new bone (osteoid and mineralized bone), residual bone (old bone and graft bone), total bone (new and residual bone) and
soft tissue in contact with implant surface over time. Data are shown as means  SD
Region Time point Group New bone Residual bone Total bone Soft tissue
R1 3 months Test 70.41 (13.48, 66.82) 2.86 (3.14, 2.50) 73.28 (12.22, 69.16) 26.71 (10.04, 30.83)
Control 68.39 (10.41, 72.10) 2.04 (3.12, .00) 70.44 (11.67, 73.47) 29.55 (11.67, 26.52)
6 months Test 57.96 (16.60, 55.47) 7.30 (7.08, 7.09) 65.27 (14.56, 64.77) 34.72 (14.56, 35.22)
Control 61.30 (11.79, 57.09) 0.99 (2.80, 0.00) 62.29 (11.25, 59.47) 37.70 (11.25, 40.53)
R2 3 months Test 72.97 (13.32, 76.36) 2.31 (6.54, .00) 75.29 (12.15, 78.89) 24.70 (12.15, 21.11)
Control 75.64 (24.28, 85.61) 0.00 (.00, .00) 75.64 (24.28, 85.61) 24.35 (24.28, 14.38)
6 months Test 53.47 (19.66, 52.44) 4.64 (3.41, 5.23) 58.11 (20.44, 55.47) 41.88 (20.44, 44.52)
Control 51.63 (34.67, 35.46) 0.00 (0.00, 0.00) 51.63 (34.67, 35.46) 48.36 (34.67, 64.53)

Measures are expressed in %: mean (SD; median).

Table 3. Effect of bone type, time, implant staging and osseointegration time and interaction effects on the amount of new bone, residual bone,
total bone (new and residual bone) and soft tissue deposited on the implant surfaces
New bone Residual bone Total bone Soft tissue

Effect Statistic P Statistic P Statistic P Statistic P

Timing of implant placement (simultaneous versus delayed) 0.3168 0.5734 6.9327 0.0084 0.0099 0.9205 0.0032 0.9543
Bone type (Bone ring versus native bone) 0.0026 0.9591 1.7886 0.1810 0.0223 0.8810 0.0000 1.0000
Osseointegration time (3 versus 6 months) 5.2424 0.0220 1.0130 0.3141 5.3496 0.0207 5.3228 0.0210

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Nakahara et al
Osseointegration of implants placed using bone ring technique

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