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Early Bone Response to Dual Acid-Etched
and Machined Dental Implants Placed in
the Posterior Maxilla: A Histologic and
Histomorphometric Human Study
Francesco Guido Mangano, DDS,* Jefferson Trabach Pires, DDS,†Jamil Awad Shibli, DDS, MS, PhD,‡
Eitan Mijiritsky, DMD,§ Giovanna Iezzi, DDS, PhD,¶ Adriano Piattelli, DDS, MD,kand Carlo Mangano, DDS, MD#
Nowadays, dental implants repre-
sent a predictable and effective
solution for the rehabilitation of
partially and totally edentulous patients,
with satisfactory high survival and suc-
cess rates, as confirmed by several clin-
ical studies in the medium and long
term.
1–3
However, the survival and suc-
cess rates of implants placed in areas of
poor bone quality, such as the posterior
maxilla, are still lower than those of
implants placed in the anterior areas
of the maxilla, or in the mandible,
where the bone density is higher.
4,5
The demand for improved dental
implant survival at sites of lower bone
density, such as the posterior maxilla,
has stimulated researchers to introduce
implant design alterations and therefore
surface modifications, to increase the
early bone response and accelerate
osseointegration.
5,6
In fact, the implant surface is the
first part of the biomedical device to
interact with the host: body fluids and
cells interact with the implant surface,
and micrometer-scale features (such as
cavities, grooves, ridges, and wells)
play an important role in determining
molecular and cellular responses.
6,7
Accordingly, in the last years, a variety
of rough-surfaced implants have been
introduced in the market.
8–10
Acid-etching and sandblasting are
2 of the most commonly used methods
for the preparation of rough implant
surfaces.
11–13
In the acid-etching procedure, dental
implants are immersed in acidic solu-
tions; the result obtained, namely the
erosion of the surface with formation of
peaks and cavities of various dimensions,
depends on the concentration of the
acidic solutions, the immersion time,
and the temperature.
14
In general, acid-
etched surfaces are obtained by combined
*Researcher, Department of Surgical and Morphological
Science, Dental School, University of Varese, Varese, Italy.
†Researcher, Dental Research Division, Guarulhos University,
Sao Paulo, Brazil.
‡Professor, Head of Oral Implantology Clinic, Dental Research
Division, Guarulhos University, Sao Paulo, Brazil.
§Senior Lecturer, Department of Oral Rehabilitation, Maurice
and Gabriela Goldschleger School of Dental Medicine, University
of Tel Aviv, Tel Aviv, Israel.
¶Researcher, Department of Medical, Oral and Biotechnological
Sciences, University of Chieti-Pescara, Chieti, Italy.
kFull Professor, Department of Medical, Oral and
Biotechnological Sciences, University of Chieti-Pescara, Chieti,
Italy.
#Professor, Department of Dental Sciences, University Vita
Salute S. Raffaele, Milan, Italy.
Reprint requests and correspondence to: Francesco Guido
Mangano, DDS, Piazza Trento 4, 22015 Gra vedona (Como),
Italy, Phone: +39-0344-85524, Fax: +39-0344-530251,
E-mail: francescomangano1@mclink.net
ISSN 1056-6163/16/02601-001
Implant Dentistry
Volume 26 Number 1
Copyright © 2016 Wolters Kluwer Health, Inc. All rights
reserved.
DOI: 10.1097/ID.0000000000000511
Purpose: To compare the early
bone response to implants with dual
acid-etched (DAE) and machined
(MA) surface, when placed in the
posterior human maxilla.
Materials and Methods: Four-
teen patients received 2 implants in
the posterior maxilla: 1 DAE and
1 MA. After 2 months, the implants
were retrieved for histologic/
histomorphometric evaluation. The
bone-to-implant contact (BIC%), bone
density in the threaded area (BDTA
%), and the bone density (BD%) were
calculated. The Wilcoxon matched-
pairs signed rank test was used to
evaluate differences (BIC%, BDTA%,
and BD%) between the surfaces.
Results: In the MA implants,
a mean (6SD) BIC%, BDTA%, and
BD% of 21.76 (612.79), 28.58
(616.91), and 21.54 (611.67),
respectively, was reported. In the
DAEimplants,amean(6SD) BIC
%, BDTA%, and BD% of 37.49
(629.51), 30.59 (621.78), and
31.60 (618.06), respectively, was
reported. Although the mean BIC%
of DAE implants value was almost
double than that of MA implants, no
significant differences were found
between the 2 groups with regard
to BIC% (P¼0.198) and with re-
gardtoBDTA%(P¼0.778) and
BD% (P¼0.124).
Conclusions: The DAE surface
increased the periimplant endosseous
healing properties in the native bone
of the posterior maxilla. (Implant
Dent 2016;26:1–6)
Key Words: bone healing, histology,
histomorphometry, humans
MANGANO ET AL IMPLANT DENTISTRY /VOLUME 26, NUMBER 1 2016 1
Copyright Ó2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
treatment with strong acids, such as hy-
drochloric acid (HCl) and sulfuric acid
(H
2
SO
4
), or with hydrofluoric acid (HF)
and nitric acid (HNO
3
).
15
Dual acid-etched (DAE) surface
implants are a good example of the
application of these treatments, and the
clinical application of these implants
has been extensively documented, with
high survival and success rates.
16–18
DAE surfaces promote the organization
of fibrin clot and the adhesion of plate-
lets in the early healing phases.
19
In sev-
eral animal studies, DAE implants have
shown improved histologic and histo-
morphometric bone response, when
compared with machined (MA) dental
implants,
20–22
and higher removal tor-
que values.
23,24
Until now, however, only a few
histologic and histomorphometric
studies have investigated the early
bone response to DAE implants placed
in humans.
25–28
Most of these studies
werebasedonfewsamples,
26,28
retrieved from different subjects,
26
and only in a few of them the implants
were inserted and retrieved from the
posterior maxilla.
25,27
Hence, the aim of the present
controlled histologic and histomorpho-
metric study was to compare the early
periimplant endosseous healing prop-
erties of DAE and MA implants, when
placed in native mature bone of the
posterior maxilla.
MATERIALS AND METHODS
Study Design
The present controlled histologic and
histomorphometric study evaluated the
early bone response to DAE surface
implants and MA implants, inserted
in the posterior human maxilla. Each
patient received 2 transitional implants
(n ¼1 DAE implant: test;andn¼1MA
implant: control). These implants were
left submerged for an undisturbed healing
period of 2 months and finally retrieved
for the histologic and histomorphometric
evaluation. Bone-to-implant contact (BIC
%, defined as the amount of mineralized
bone in direct contact with the implant
surface), bone density in the threaded area
(BDTA%, defined as the fraction
of mineralized bone tissue within the
threaded area), and bone density (BD%,
defined as bone density in a 500-mm-wide
zone lateral to the implant surface) were
the histomorphometric parameters evalu-
ated in this study.
Patient Selection
A total of 14 subjects (6 men, 8
women; aged between 45 and 74 years,
mean age 59.0 68.5 years) who were
referred to the Oral Implantology
Clinic, Dental Research Division,
Guarulhos University, SP, Brazil, for
oral rehabilitation with dental implants,
were included in the present study.
Inclusion criteria were good systemic
and oral health and sufficient native
bone to place implants of 3.25 mm
diameter and 10 mm length. Exclusion
criteria were pregnancy, nursing, smok-
ing, and any systemic condition that
could affect bone healing. All partici-
pants received detailed explanations
about the nature of the study and signed
a written informed consent form. The
Institutional Clinical Research Ethics
Committee of Guarulhos University
approved the protocol of the present
study (CEP UnG #203/2013), which
was conducted according to the princi-
ples outlined in the World Medical As-
sociation’s Declaration of Helsinki on
experimentation involving human sub-
jects, as revised in 2008.
Implant Design and Surface Treatment
The transitional implants used in
the present study (BT Konic; Biotec-
BTK, Dueville, Vicenza, Italy) were
made of titanium grade 4 (ASTM
F67dISO 5832-2). All these implants
(test and control) were macroscopi-
cally identical, with a tapered design,
3.25 mm in diameter, and 10 mm in
length. The test implants had the sur-
face treated with a DAE procedure. A
mix of strong inorganic acids (H
2
SO
4
,
H
3
PO
4
, HCl, and HF) was used, in 2
different acid baths. After each acid
bath, implants were rinsed and washed
with distilled water, to neutralize and
remove acid residuals. Finally, im-
plants were taken to a cleaning room
ISO 7 class to be decontaminated
through a plasma spray decontamina-
tion process, in argon atmosphere. The
DAE implant surface was studied with
scanning electron microscopy (SEM)
(Fig. 1). The following standard
roughness parameters were measured:
Ra (the arithmetic mean of the absolute
height of all points), Rq (the square
root of the sum of the squared mean
difference of all points), and Rt (the
difference between the highest and
the lowest points). The SEM evalua-
tion of DAE surface implants revealed
ameanRaof1.12(60.41) mm, a mean
Rq of 1.34 (60.69) mm, and a mean Rt
of 3.86 (61.40) mm, respectively. The
control implants had a MA surface.
Surgical Protocol
Twenty-eight transitional implants
(n ¼14 test implants and n ¼14 control
implants) were inserted in this study.
All implants were placed under aseptic
conditions. After local anesthesia,
a crestal incision connected with 2
releasing vertical incisions was made.
Mucoperiosteal flaps were raised and
conventional implants were inserted,
in accordance with the surgical and
prosthetic plan prepared for each
patient. Then, 2 transitional implants
(n ¼1 test implant and n ¼1 control
implant) were inserted in each patient.
The transitional implants were placed in
the posterior maxilla (in the areas of
second premolars/first molars), distally
to the most posterior conventional
implant. The assignment of test and
control implants (right posterior max-
illa or left posterior maxilla) was ran-
dom, as determined by a coin toss.
The implant sites were prepared accord-
ing to the manufacturer’s recommenda-
tions, under profuse irrigation with
sterile saline. The stability of all im-
plants was checked using a dedicated
instrument (Osstell Mentor; Osstell,
Fig. 1. SEM evaluation of the DAE implant
surface. The surface presented micron-sized
shallow cavities uniformly covered by sub-
microscopic pittings limited by razor-sharp
cusps and edges.
2EARLY BONE RESPONSE TO DAE AND MA IMPLANTS MANGANO ET AL
Copyright Ó2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Goteborg, Sweden): if an implant
showed insufficient primary stability
(,35), a backup surgical site had to
be prepared. The flaps were then
sutured. Clindamycin 300 mg (Clinda-
min C; Teuto, Anapolis, Goias, Brazil)
was administered 3 times a day for
a week, to avoid postsurgical infection.
Postoperative pain was controlled with
600 mg of ibuprofen (Actron; Bayer
Scherig Pharma, Berlin, Germany)
every 12 hours for 2 days. To enable
subjects to control postoperative dental
biofilm, 0.12% chlorhexidine rinses
(Chlorhexidine; OralB, Boston, MA)
were prescribed, twice a day for 14
days. The sutures were removed after
10 days. All transitional implants were
left submerged for an undisturbed
healing period of 2 months. After this,
during the 2-stage surgery to uncover
the conventional implants, the 2 tran-
sitional implants (test and control) and
the surrounding tissues were retrieved
from each patient, using a 4.5-mm-
wide trephine bur.
Histologic and
Histomorphometric Evaluation
The biopsies were fixedbyimme-
diate immersion in 10% buffered for-
malin and processed (Precise 1
Automated System; Assing, Rome,
Italy) to obtain thin ground sections,
as previously described.
26,27
The
specimens were dehydrated in an
ascending series of alcohol rinses and
embedded in glycol-methacrylate resin
(Technovit 7200 VLC; Kulzer, Wehr-
heim, Germany). After polymeriza-
tion, the specimens were sectioned
lengthwise along the larger axis of the
implants with a high-precision dia-
mond disk at about 150 mm, and
ground down to about 30 mm. Two to
3 slides were obtained from each
implant, stained with basic fuchsin
and toluidine blue. The specimens
were analyzed under a transmitted
light microscope (Laborlux S; Leitz,
Wetzlar, Germany) that was connected
to a high-resolution video camera
(3CCD-JVC KY-F55B; JVC, Yokoha-
ma, Japan) and interfaced to a monitor
and a personal computer PC (Intel Pen-
tium III 1200 MMX; Intel, Santa Clara,
CA). This optical system was associ-
ated with a digitizing pad (D-Pad;
Matrix Vision GmbH, Oppenweiler,
Germany) and a histometry software
package with image-capture function-
alities (Image-Pro Plus 4.5; Media
Cybernetics, Immagini & Computer
Snc, Milan, Italy). For the histomor-
phometric evaluation, the BIC%,
defined as the amount of mineralized
bone in direct contact with the implant
surface, was measured around all
implant surfaces. The BDTA%,
defined as the fraction of mineralized
bone tissue within the threaded area,
andtheBD%ina500-mm-wide zone
lateral to the implant surface were
measured bilaterally, as previously
reported.
29
Statistical Analysis
All collected data were inserted in
a sheet for statistical analysis (Excel
2003; Microsoft, Redmond, WA).
Mean, SDs, median, and 95% confi-
dence intervals of histomorphometric
values (BIC%, DBTA%, and BD%)
were calculated for each implant and
then for each group of implants (test vs
control implants). The Wilcoxon
matched-pairs signed rank test was
used to evaluate differences (BIC%,
BDTA%, and BD%) between the
implant surfaces. The level of signifi-
cance was set at 0.05. All computations
were carried out with a statistical anal-
ysis software (SPSS 17.0; SPSS Inc.,
Chicago, IL).
Fig. 2. Test implant (DAE surface). Newly
formed trabecular bone with small marrow
spaces was found along the implant
perimeter, lacking only in the apical portion,
maybe due to procedure of surgical
removal. Low-density (D3-D4) preexisting
bone, typical of the posterior maxilla, was
also evident (histological staining: acid
fuchsin-toluidine blue, 318).
Fig. 3. Test implant (DAE surface). Newly
formed bone could be observed inside the
concavities of the implant threads, where
active osteoblasts secerning osteoid matrix
were present. In some areas, this matrix was
undergoing mineralization. Preexisting bone
with a low affinity for fuchsin and not in
contact with the implant surface could also
be seen (histological staining: acid fuchsin-
toluidine blue, 340).
Fig. 4. Control implant (MA surface), preex-
isting bone was in contact with the implant
surface mainly in the coronal portion. Tra-
beculae of newly formed bone going toward
the implant surface were observed in the
middle and apical portions (histological
staining: acid fuchsin-toluidine blue, 318).
Fig. 5. Control implant (MA surface), only in
few fields newly formed trabecular bone in
contact with the implant surface was present
(histological staining: acid fuchsin-toluidine
blue, 340).
MANGANO ET AL IMPLANT DENTISTRY /VOLUME 26, NUMBER 1 2016 3
Copyright Ó2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
RESULTS
Clinical Observations
After 2 months of healing, a total of
28 transitional implants (n ¼14 test im-
plants and n ¼14 control implants) were
retrieved and evaluated. Three implants
(one test implant and 2 control implants)
were not clinically stable and showed no
osseointegration, although they did not
show any sign of infection. The remain-
ing 25 implants were clinically stable at
the time of retrieval.
Histologic and
Histomorphometric Results
The bone surrounding both implant
groups was healthy. Woven bone with
several osteocyte lacunae and preexist-
ing bone were present; the woven newly
formed bone was separated from the
preexisting bone by cement lines. Some
bone remodeling was observed, at early
stages, even in the coronal portions of
the specimens.
In the test group (DAE surface),
newly formed trabecular bone with
small marrow spaces was found
throughout the implant body, with the
exception of the apical portion; this is
because of the surgical removal.
Newly formed bone was found also in
the coronal part of the implant. Preex-
isting bone is also evident, with a qual-
ity comprised between D3 and D4
(Fig. 2). Inside of the implant threads,
the concavities were colonized by new
bone formation, with the presence of
active osteoblasts secerning osteoid
matrix; in some areas, this matrix was
undergoing mineralization. Preexist-
ing bone, not in contact with the
implant surface, showed low quality
and low affinity for fuchsin (Fig. 3).
In the control group (MA surface),
the implant was in contact with the bone
tissue mainly in the coronal portion,
where preexisting bone could be de-
tected. In the middle and apical por-
tions, newly formed trabeculae coming
from the old bone and going toward the
implant surface could be observed
(Fig. 4). Inside of the concavities, only
in few fields newly formed trabecular
bone in contact with the implant surface
was found (Fig. 5).
In the MA implants, the histomor-
phometric evaluation revealed mean
(6SD) BIC%, BDTA%, and BD% of
21.76 (612.79), 28.58 (616.91), and
21.54 (611.67), respectively. In the
DAE implants, the histomorphometric
analysis revealed mean (6SD) BIC%,
BDTA%, and BD% of 37.49 (629.51),
30.59 (621.78), and 31.60 (618.06),
respectively (Table 1). For the MA
implants, the BIC% ranged from 0 to
44.21; for the DAE implants, the BIC%
ranged from 0 to 78.08. Although the
mean BIC% of DAE implants value was
almost double than that of MA implants,
the Wilcoxon matched-pairs signed rank
testfoundnosignificant differences
between the 2 groups of implants, with
regard to BIC% (P¼0.198). The
BDTA%wassimilarinthe2groups,as
it ranged from 0 to 54.51 for the MA im-
plants, and from 0 to 60.5 for the DAE
implants. Again, the Wilcoxon matched-
pairs signed rank test failed to find a sig-
nificant difference between the 2 groups
of implants, with regard to BDTA% (P¼
0.778). Finally, for the MA implants, the
BD% ranged from 0 to 38; for the DAE
implants, the BD% ranged from 0 to 55.9.
Although BD% was higher in the test
group than in the control group, this dif-
ference was not statistically significant
(P¼0.124).
DISCUSSION
At present, the relationship between
surface topography and osseointegration
is well recognized.
8–10
In fact, the nature
of the implant surface is known to influ-
ence the rate of osteoblast proliferation,
matrix synthesis, and local autocrine fac-
tor production, which all, ultimately,
influence the rate of osseointegra-
tion.
8–10
Rough surfaces have demon-
strated better adsorption of biomolecules
from biological fluids, which has the
potential to alter the cascade of events that
leads to bone healing and intimate appo-
sition with the device.
7,9,12
In vitro reports
indicate that rough surfaces improve the
initial cellular response, including cyto-
skeletal organization and cellular differ-
entiation with matrix deposition.
6,7,9,12,19
Histologically, it has been demonstrated
that rough surfaces can effectively pro-
mote better and faster osseointegration
when compared with MA surfaces.
20–
22,25–29
From a clinical point of view,
several studies have reported excellent
long-term survival/success rates for
rough surface implants.
2,16–18
In challenging implant cases, such
as immediate loading, immediate
implant placement in postextraction
sockets, and placement of implants in
“poor”quality bone, the acceleration of
early periimplant bone healing might be
very useful;
4,5
however, the precise
nature of surface characteristics needed
for optimal osseointegration remains to
be elucidated.
6,8,12,19
Among different
surface treatments, acid etching seems
to be one of the most popular, and DAE
implants have been used for several
years, with satisfactory high survival
and success rates.
16–18
At present, histologic and histo-
morphometric assessments are the
most accurate methods to investigate
the bone healing processes and the
morphological characteristics of the
bone-implant interface.
30
Unfortu-
nately, only a few studies in the present
literature have dealt with histologic
Table 1. Mean, SD, Range, and Confidence Interval of BIC%, BDTA, and BD% of DAE and MA Implants Placed in the Posterior
Maxilla (n ¼14 Subjects)
%
DAE Surface (Test Implants) MA Surface (Control Implants)
PMean (SD) Range CI 95% Mean (SD) Range CI 95%
BIC 37.49 (29.51) 0–78.08 22.04–52.94 21.76 (12.79) 0–44.21 15.07–28.45 0.198
BDTA 30.59 (21.78) 0–60.5 19.19–41.99 28.58 (16.91) 0–56.78 19.73–37.43 0.778
BD 31.60 (18.06) 0–55.9 22.14–41.06 21.54 (11.67) 0–38 15.43–27.65 0.124
Wilcoxon matched-pairs signed rank test (level of significance set at 0.05).
CI indicates confidence interval.
4EARLY BONE RESPONSE TO DAE AND MA IMPLANTS MANGANO ET AL
Copyright Ó2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
and histomorphometric evaluation of
human-retrieved DAE implants: this
is because of ethical issues re-
lated to implant retrieval from human
subjects.
25–29
Lazzara et al
25
conducted a human
histologic/histomorphometric study to
compare the percentage of BIC% at
6 months for DAE and MA titanium
implant surfaces. Eleven patients were
selected for installation of 1 DAE and
1 MA mini-implants (2 mm diameter 3
5 mm length), in the posterior maxilla
(type III and type IV bone), during con-
ventional dental implant surgery.
25
After 6 months of undisturbed healing,
the mini-implants and surrounding hard
tissue were removed.
25
Histomorpho-
metric analysis indicated that the mean
BIC% value for the DAE surfaces
(72.96 625.13) was significantly high-
er than the mean BIC% value for the
MA surfaces (33.98 631.04).
25
The
authors concluded that in poorer quality
bone (posterior maxilla), implants with
DAE surface can guarantee a faster
bone healing when compared with im-
plants with MA surface.
25
In a more
recent histological study, the authors
retrieved 2 DAE implants from the
mandible, to repair damage to the infe-
rior alveolar nerve.
26
After 6 months of
healing, both implants seemed to be
surrounded by newly formed bone.
26
No gaps or fibrous tissues were present
at the bone-implant interface.
26
The
mean BIC% (61.3 63.8) was high.
26
In another study, the authors docu-
mented the osseointegration of 2 DAE
implants after 2 months of healing, with
different loading conditions.
28
A com-
pletely edentulous patient received
a total of 11 DAE implants in the man-
dible.
28
Six implants were immediately
loaded to support a provisional fixed
partial denture and 5 were left sub-
merged. After 2 months, 2 submerged
and 1 immediately loaded implants
were retrieved for histologic/histo-
morphometric analysis.
28
The BIC%
was 38.9 for the submerged implants
and 64.2 for the immediately loaded
one. The authors concluded that os-
seointegration can be achieved after
2 months by DAE implants placed in
the mandible, either when immedi-
ately loaded or when submerged and
unloaded.
28
Finally, in a recent work,
DAE surface was compared with
bioceramic molecular-impregnated
surface.
29
Ten subjects received 2
transitional mini-implants implants
(1 of each surface) during conven-
tional implant surgery in the posterior
maxilla.
29
After an undisturbed heal-
ing period of 2 months, the implants
and the surrounding tissue were
removed by means of a trephine and
were nondecalcified processed for
ground sectioning and analysis of
BIC%, BDTA%, and osteocyte index
(Oi).
29
At the end, histometric evalu-
ation showed significantly higher BIC
% and Oi for bioceramic molecular-
impregnated implants (P,0.05),
whereas BA% was not significantly
different between groups. The authors
concluded that bioceramic molecular-
impregnated surface can positively
modulate bone healing at early
implantation times compared with
the DAE surface.
29
In our present study, we have
decided to evaluate DAE (test) and
MA implants (control) with an intra-
individual comparison to overcome
the possible anticipated variability
between individuals. This represents
a clear advantage of our present study,
as an intraindividual comparison
between different surface is a rarity
in the literature.
25,29,30
In our study, in the MA implants,
the histomorphometric evaluation re-
vealed mean (6SD) BIC%, BDTA%,
and BD% of 21.76 (612.79), 28.58
(616.91), and 21.54 (611.67), respec-
tively. In the DAE implants, the histo-
morphometric analysis revealed mean
(6SD) BIC%, BDTA%, and BD% of
37.49 (629.51), 30.59 (621.78) and
31.60 (618.06), respectively.
Although the mean BIC% of DAE im-
plants value was almost double than
that of MA implants, the statistical anal-
ysis found no significant differences
between the 2 groups, with regard to
BIC% (P¼0.198). These statistical re-
sults may be influenced by the fact that
also nonosseointegrated samples (3)
have been included in our analysis,
and most of all, the overall number of
samples (14 per type) was low; if the
sample had been larger, we would prob-
ably have expected a statistically signif-
icant difference between the 2 groups in
the BIC%. No significant differences
were found in our study between
DAEandMAimplantswithregardto
BDTA% (P¼0.778) and BD% (P¼
0.124). Anyhow, our results indicate
that DAE surface can potentiate heal-
ing process and new bone apposition,
compared with MA surface.
It should be noted that most of
the human histologic/histomorphomet-
ric studies that are currently available in
the literature have focused on hard and
soft tissue reactions around experimen-
tal implants with smaller dimensions
than those of regular dental im-
plants.
25,29,31
To date, only a few studies
have evaluated the histological response
around standard-diameter implants,
13,30
and most of these were based on im-
plants removed for fracture.
13,32
In our
present study, we have used transitional
implants of standard dimensions
(3.25 mm diameter 310 mm length).
This may represent an advantage of our
study because we have evaluated how
the healing processes take place in a sit-
uation closer to the real one. However,
the retrieval of our transitional implants
was carried out in such a way that the
resulting prepared canal in bone could
be used for dental implants with a larger
diameter.
30
CONCLUSIONS
At present, only a few histologic
and histomorphometric studies have
evaluated the bone healing around
dental implants in humans; however,
the histological data from the retrieved
human implants are absolutely neces-
sary to obtain useful information about
the bone healing processes around
dental implants, as well as the bone-
implant interface. Within its limits
(such as the small sample size), the
present study reports that the DAE
surface improved the periimplant early
healing processes in the native bone of
the maxilla when compared with the
MA surface. Further studies on a larger
sample of patients are needed to con-
firm these results.
DISCLOSURE
The authors claim to have no
financial interest, either directly or
MANGANO ET AL IMPLANT DENTISTRY /VOLUME 26, NUMBER 1 2016 5
Copyright Ó2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
indirectly, in the products or informa-
tion listed in the article.
APPROVAL
The present study was approved by
the Institutional Clinical Research
Ethics Committee of Guarulhos Uni-
versity (number of approval: CEP UnG
#203/2013).
REFERENCES
1. Imburgia M, Del Fabbro M. Long-
term retrospective clinical and radiographic
follow-up of 205 Brånemark System Mk III
TiUnite implants submitted to either imme-
diate or delayed loading. Implant Dent.
2015;24:533–540.
2. Mangano C, Iaculli F, Piattelli A,
et al. Fixed restorations supported by
Morse-taper connection implants: A retro-
spective clinical study with 10–20 years of
follow-up. Clin Oral Implants Res. 2015;
26:1229–1236.
3. Maló P, de Araújo Nobre M,
Lopes A, et al. Axial implants in
immediate function for partial
rehabilitation in the maxilla and mandible:
A retrospective clinical study evaluating the
long-term outcome (up to 10 years).
Implant Dent. 2015;24:557–564.
4. Stach RM, Kohles SS. A meta-
analysis examining the clinical survivability
of machined-surfaced and osseotite im-
plants in poor-quality bone. Implant Dent.
2003;12:87–96.
5. Goiato MC, dos Santos DM,
Santiago JF Jr, et al. Longevity of dental
implants in type IV bone: A systematic
review. Int J Oral Maxillofac Surg. 2014;
43:1108–1116.
6. Shalabi MM, Gortemaker A,
van’t Hof MA, et al. Implant surface
roughness and bone healing: A systematic
review. J Dent Res. 2006;85:496–500.
7. Gittens RA, Scheideler L, Rupp F,
et al. A review on the wettability of
dental implant surfaces II: biological
and clinical aspects. Acta Biomater.
2014;10:2907–2918.
8. 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.
9. Mangano F, Chambrone L,
van Noort R, et al. Direct metal laser
sintering titanium dental implants: A
review of the current literature. Int J
Biomater. 2014;2014:461534.
10. Aljateeli M, Wang HL. Implant
microdesigns and their impact on
osseointegration. Implant Dent. 2013;22:
127–132.
11. Roccuzzo M, Bonino L,
Dalmasso P, et al. Long-term results of
a three arms prospective cohort study
on implants in periodontally
compromised patients: 10-Year data
around sandblasted and acid-etched
(SLA) surface. Clin Oral Implants Res.
2014;25:1105–1112.
12. Yang G, Fang W, Liu T, et al. Gene
expression profiling of bone marrow-
derived stromal cells seeded onto a sand-
blasted, large-grit, acid-etched-treated
titanium implant surface: The role of the
Wnt pathway. Arch Oral Biol. 2016;61:
71–78.
13. Mangano C, Perrotti V, Raspanti M,
et al. Human dental implants with
a sandblasted, acid-etched surface
retrieved after 5 and 10 years: A light and
scanning electron microscopy evaluation of
two cases. Int J Oral Maxillofac Implants.
2013;28:917–920.
14. Fandridis J, Papadopoulos T.
Surface characterization of three titanium
dental implants. Implant Dent. 2008;17:
91–99.
15. Schliephake H, Aref A,
Scharnweber D, et al. Effect of
modifications of dual acid etched
implant surfaces on peri-implant bone
formation. Part I: Organic coatings. Clin
Oral Implants Res. 2009;20:31–37.
16. Sesma N, Pannuti C, Cardaropoli G.
Retrospective clinical study of 988 dual acid-
etched implants placed in grafted and native
bone for single-tooth replacement. Int J Oral
Maxillofac Implants. 2012;27:1243–1248.
17. Browaeys H, Defrancq J,
Dierens MC, et al. A retrospective
analysis of early and immediately
loaded osseotite implants in cross-arch
rehabilitations in edentulous maxillas
and mandibles up to 7 years. Clin
Implant Dent Relat Res. 2013;15:380–
389.
18. Calvo-Guirado JL, Gómez-Moreno
G, Delgado-Ruiz RA, et al. Clinical and
radiographic evaluation of osseotite-
expanded platform implants related to crestal
bone loss: A 10-year study. Clin Oral Im-
plants Res. 2014;25:352–358.
19. Park JY, Gemmell CH, Davies JE.
Platelet interactions with titanium:
Modulation of platelet activity by surface
topography. Biomaterials. 2001;22:2671–
2682.
20. Vernino AR, Kohles SS, Holt RA Jr,
et al. Dual-etched implants loaded after 1-
and 2-month healing periods: A histologic
comparison in baboons. Int J Periodontics
Restorative Dent. 2002;22:399–407.
21. WengD,HoffmeyerM,HurzelerMB,
et al. The Osseotite vs machined surface in
poor bone quality. A study in dogs. Clin Oral
Implants Res. 2003;14:703–708.
22. Yoo D, Marin C, Freitas G, et al.
Surface characterization and in vivo
evaluation of dual acid-etched and grit-
blasted/acid-etched implants in sheep.
Implant Dent. 2015;24:256–262.
23. Cordioli G, Majzoub Z, Piattelli A,
et al. Removal torque and
histomorphometric investigation of 4
different titanium surfaces: An experimental
study in the rabbit tibia. Int J Oral Maxillofac
Implants. 2000;15:668–674.
24. Bonfante EA, Granato R, Marin C,
et al. Early bone healing and biomechanical
fixation of dual acid-etched and as-
machined implants with healing chambers:
An experimental study in dogs. Int J Oral
Maxillofac Implants. 2011;26:75–82.
25. Lazzara RJ, Testori T, Trisi P, et al. A
human histologic analysis of Osseotite and
machined surfaces using implants with 2
opposing surfaces. Int J Periodontics
Restorative Dent. 1999;19:117–129.
26. Degidi M, Petrone G, Iezzi G, et al.
Bone contact around acid etched implants:
A histological an histomorphometrical
evaluation of two human retrieved implants.
J Oral Implantol. 2003;29:13–18.
27. Romanos G, Testori T, Degidi M,
et al. Histologic and histomorphometric
findings from retrieved, immediately
occlusally loaded implants in humans.
JPeriodontol.2005;76:1823–1832.
28. Testori T, Szmukler-Moncler S,
Francetti L, et al. Healing of osseotite
implants under submerged and
immediate loading conditions in a single
patient: A case report and interface
analysis after 2 months. Int J
Periodontics Restorative Dent. 2002;22:
345–353.
29. Shibli JA, Grassi S, Piattelli A,
et al. Histomorphometric evaluation of
bioceramic molecular impregnated and
dual acid-etched implant surfaces in
the human posterior maxilla. Clin
Implant Dent Relat Res. 2010;12:
281–288.
30. Donati M, Botticelli D, La Scala V,
et al. Effect of immediate functional loading
on osseointegration of implants used for
single tooth replacement. A human
histological study. Clin Oral Implants Res.
2013;24:738–745.
31. Shibli JA, Mangano C, Mangano F,
et al. A. Bone-to-implant contact around
immediately loaded direct laser metal-
forming transitional implants in human
posterior maxilla. J Periodontol. 2013;84:
732–737.
32. Mangano C, Piattelli A, Mortellaro C,
et al. Evaluation of peri-implant bone
response in implants retrieved for frac-
ture after more than 20 Years of loading:
A case series. J Oral Implantol. 2015;41:
414–418.
6EARLY BONE RESPONSE TO DAE AND MA IMPLANTS MANGANO ET AL
Copyright Ó2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
