Post on 20-Jul-2016
Surface-modified zirconia implants:tissue response in rabbits
Isabella RocchiettaFilippo FontanaAlessandro AddisPeter SchupbachMassimo Simion
Authors’ affiliations:Isabella Rocchietta, Department of Periodontology,School of Dentistry, University of Milan, Milan,ItalyFilippo Fontana, Department of Implant Dentistry,School of Dentistry, University of Milan, Milan,ItalyAlessandro Addis, CRABCC – Research Center onBiotechnological Applications, University of Milan,Milan, ItalyPeter Schupbach, Department of Periodontics,School of Dental Medicine, University ofPennsylvania, Philadelphia, PA, USAMassimo Simion, Department of Periodontology,School of Dentistry, University of Milan, Milan,ItalyIsabella Rocchietta, Filippo Fontana, MassimoSimion, Institute for Dental Research andEducation, Milan, Italy
Correspondence to:Isabella RocchiettaDepartment of PeriodontologySchool of DentistryUniversity of MilanMilanItalyTel.: þ 39 02 66988259Fax: þ 39 02 66711591e-mail: isabella.rocchietta@gmail.com
Key words: BIC, rabbit model, removal torque, tissue response, zirconia implants
Abstract
Aim: To evaluate the bone tissue response to zirconia implants with three different surface
modifications in comparison with the oxidized titanium surface with the goal to optimize
osseointegration in terms of strength and speed.
Materials and methods: A total of 18 rabbits with 143 implants were used. One hundred
and twenty-three were threaded zirconia ceramic implants with three different surface
topographies and 20 modified titanium oxide implants were controls. Each rabbit received
eight implants and sacrificed after 3 weeks. The removal torque test (RTQ) and histology
were performed.
Results: Sixteen out of 18 rabbits completed the study with a total of 110 implants. No
statistical significance was observed between the chemical modification implants compared
with the topographically modified zirconia implant in terms of interfacial shear strength
proven by the RTQ applied. No statistical significance was also observed in the bone-to-
implant contact between the zirconia implants and the control oxidized implants.
Conclusions: The findings suggest that additional specific chemical modifications of the
topographically modified zirconia implants do not seem to enhance the bone-to-implant
contact and appear not to increase the interfacial shear strength.
Many suggestions have been made to im-
prove and accelerate bone deposition at the
interface with dental implants. These may
concern the implant design, choice of ma-
terial, surface modification, stiffness and
strain induction.
The material of choice for dental im-
plants is commercially pure titanium (Bra-
nemark et al. 1977; Adell et al. 1981). This
biocompatible material has been used ex-
tensively, showing high success rates (Bra-
nemark et al. 1977; Adell et al. 1990).
Nevertheless, osseointegration has been
achieved with the use of other various
biomaterials such as titanium alloy (Parr
et al. 1985), poly and single crystal alumina
(Driskell & Heller 1977; Kawahara et al.
1980), bioactive glass (Gross et al. 1981),
hydroxyapatite (Denissen et al. 1983), tita-
nium-sprayed titanium (Schroeder et al.
1981) and ceramic-coated metals (Thomas
et al. 1987).
The family of ceramic materials includes
alumina (Al2O3) or zirconia (ZrO2), both
bioinert nonresorbable metal oxides. Zirco-
nia implants have excellent resistance to
corrosion and wear, good biocompatibility
and high bending strength and fracture
toughness. Moreover, zirconia possesses
high fracture resistance due to its energy-
absorption property during the martensitic
transformation of tetragonal particles into
monoclinic ones (Akagawa et al. 1993).
Zirconia ceramics have twice the bending
Date:Accepted 1 April 2009
To cite this article:Rocchietta I, Fontana F, Addis A, Schupbach P, SimionM. Surface-modified zirconia implants: tissue responsein rabbits.Clin. Oral Impl. Res. 20, 2009; 844–850.doi: 10.1111/j.1600-0501.2009.01727.x
844 c� 2009 John Wiley & Sons A/S
strength of alumina (Akagawa et al. 1993).
In addition, this material is highly radio-
paque (Minamizato 1990), can be easily
cut for abutment preparation, making it
an attractive endosseous dental implant
material. Its ivory color, similar to the
color of the natural tooth, renders it extre-
mely useful in esthetically critical areas
especially when the soft tissue of the pa-
tient is not optimal (Ahmad 1998). Also,
zirconia can transmit light, which makes it
an ideal candidate for use in esthetic re-
storations (Ahmad 1998).
Although a review of the literature in-
dicates that sensitivity to titanium is rare,
two reports showed possible hypersensitive
reactions to titanium; hence, the zirconia
implants provide the possibility of a metal-
free treatment option to patients who re-
quest this (Peters et al. 1984; Lalor et al.
1991).
Studies in animals have demonstrated
that zirconia implants possess good bio-
compatibility and direct bone apposition.
The bone-to-implant contact reported in a
study on monkeys ranged between 66%
and 81% with different loading designs
(Akagawa et al. 1998). Similar results
were reported in a comparative study of
loaded and unloaded zirconia implants,
where no fibrous tissue was detected at
the implant–bone interface (Akagawa et al.
1993). Newly formed bone was observed in
close contact with zirconia ceramic sur-
faces in a rabbit study that reported a
bone-to-implant contact of 68.4% (Scarano
et al. 2003).
The available documentation, hence, in-
dicates that zirconia ceramics are suitable
materials for use as dental implants. How-
ever, continued research has been focusing
its attention on increasing the bone-to-
implant contact as well as the speed of
bone formation through surface modifica-
tions, to reach optimal standards. Sennerby
et al. (2005) investigated two different
topographic zirconia surface alterations, re-
porting a strong bone tissue response after 6
weeks of healing in the rabbit bone. The
modified zirconia implants showed up to a
four- to fivefold increase in the resistance
to torque forces compared with machined
zirconia implants, hence suggesting that
surface zirconia modifications might in-
crease stability in bone.
The aim of the present study was to
evaluate whether the implant overall
success can be achieved by an additional
chemical modification of the topographi-
cally altered zirconia surface. In particular,
it was of interest as to whether, by chemi-
cal modification, the bioinert zirconia
surface may become osteoconductive, al-
lowing for contact osteogenesis. The bone-
to-implant contact values of two different,
structurally and chemically modified sur-
faces and of only one structurally modified
surface were compared with an oxidized
implant surface. The latter has shown
osteoconductive properties allowing fast
bone formation (Zechner et al. 2003;
Schupbach et al. 2005). In addition, the
removal torque test (RTQ) was performed
on the two chemically modified zirconia
surfaces and the topographically modified
zirconia surface.
Materials and methods
Eighteen adult New Zealand White rabbits
(48 months old) weighing approximately
3–4 kg were included in the study. A total
of 143 implants were used in this study,
123 of which were represented by threaded
zirconia ceramic implants with three dif-
ferent surfaces (41 for each surface modifi-
cation). Twenty oxidized titanium
implants (Ti-Unitet, Nobel Biocare AB,
Goteborg, Sweden) were used as controls.
All animals were treated in accordance
with both policies and principles of labora-
tory animal care and with the European
Union guidelines (86/609/EEC) approved
by the Italian Ministry of Health (Law
116/92). The surface modifications were
divided as follows: topographically modi-
fied zirconia (Zi-Unite), topographically
and chemically modified zirconia A (Pro-
mimic) and topographically and chemically
modified zirconia B (CoAT sputtered).
Each implant was 7 mm in length by
3.75 mm in diameter (MKIII design), lack-
ing an apical self-tapping bone chamber,
not to influence the results of the RTQs.
The three different zirconia implants pre-
sented with a 3 mm high squared head for
insertion and the RTQ.
Surface characteristics
The preparation of the topographically
modified zirconia implants (Zi-Unite), its
structural properties and roughness values
are given in detail elsewhere (Sennerby
et al. 2005). In brief, cold zirconium pow-
der (TZ-3YSB-E, Tosoh Corporation, To-
kyo, Japan) was isostatically pressed to
rods. The rods were presintered and pressed
to rods. A porous surface was achieved by
coating the implants with a slurry contain-
ing zirconia powder and a pore former
(patent application SE0302539-2) (Adil-
stam & Iverhed 2003). Subsequently, the
implants were sintered. By this process, the
pore former was burned off, which yielded
in a porous surface. The roughness value
for the porous zirconia surface was Sa
1.24 mm, which was to that of oxidized
titanium implants (Sa 1.3mm).
Promimic surface (chemically modified surface A)
A hydroxyapatite coating was obtained by
dipping the zirconia implants into a stable
solution, which contained surfactants,
water, organic solvent and crystalline na-
noparticles of hydroxyapatite with a CaP
ratio of 1.67. The diameter of the hydro-
xyapatite particles was approximately
10 nm. After the dipping procedure, the
implants were dried for half an hour in
open air, allowing the solvent to evaporate.
This was followed by a heat treatment at
7001C for 5 min in an oxygen atmosphere
to remove all dispersing agents.
CoAT-sputtered surface (chemically modifiedsurface B)
A hydoxyapatite coating was obtained by
sputtering a thin layer of hydroxapatite on
the zirconia surface. The treatment re-
sulted in a o150-nm-thick hydroxyapatite
coat on the titanium surface.
An implant of each type was photo-
graphed in a Zeiss Supra VP scanning
electron microscope (Zeiss, Oberkochen,
Germany) (Fig. 1). Zi-Unite implants
were characterized by a porous surface
with pore openings in the lower micro-
meter range (Fig. 1A) and a smooth surface
of the single zirconia particles. (Fig. 1B).
With Promimic implants, the smooth sur-
face of the single zirconia particles was
covered by a single layer of irregularly
shaped Ca/P crystals (Fig. 1C and D),
whereas with CoAT-Sputtered implants,
the particles were covered by a continuous,
thin layer of Ca/P (Fig. 1E and F). The
oxidized implant surface was characterized
by pore openings in the lower micrometer
range and volcano-like elevations (Fig. 1G
and H).
Rocchietta et al . Surface-modified zirconia implants
c� 2009 John Wiley & Sons A/S 845 | Clin. Oral Impl. Res. 20, 2009 / 844–850
Surgical technique
New Zealand SPF rabbits weighing be-
tween 3.2 and 3.5 kg were housed in
individual cages in an animal room main-
tained at 22� 21C and 55� 10% relative
humidity with ventilation 18–20 times/h
and a 12-h light–dark cycle. The rabbits
were allowed free access to diet and water,
and they underwent an adaptation and
observation period for 1 week before sur-
gery.
The animals were operated under a gen-
eral anaesthetic by intramuscular injec-
tions of a combination of a dose of 35 mg/
kg ketamine (Inoketam 1000s
; Virbac
S.r.l., Milan, Italy) and a dose of 5 mg/kg
xylazine (Rompuns
; Bayer S.p.A., Milan,
Italy).
The legs were shaved, washed and de-
contaminated with betadine before surgical
draping. The distal femoral condyles and
proximal tibial metaphysis on both sides
were surgically exposed via a skin incision
and the muscles were dissected to allow
elevation of the periosteum using sterile
surgical techniques. The implant site was
prepared following the Branemarks
proto-
col using drills with increasing diameter
under profuse irrigation with sterile saline
and the implants were placed after thread-
ing with a screw tap. No countersink pre-
paration was needed. Each rabbit received
eight implants, two in each tibiae and two
in each femur. The implants were placed
approximately 10 mm apart and the zirco-
nia implants were positioned with one
visible thread above the cortex, whereas
the oxidized titnaium implants were in-
serted with the head on top of the cortex.
Fascia and skin were sutured in separate
layers with resorbable sutures (Figs 2–5).
Randomization
Every rabbit received two implants in each
tibiae and femur, resulting in a total of
eight implants per animal, irrespective of
whether the animals were subject to the
histologic analysis or the removal torque
analysis. A total of 143 implants instead of
144 (18 � 8) were inserted to maintain an
equal balance between the number of im-
plants inserted per group i.e. each surface
modification group (test) comprised 41
implants each (41 � 3) and 20 implants
were allocated to the TiUnitet group (con-
trol). This resulted in a total of 143 im-
plants inserted and one free site where no
implant was inserted.
The rabbits used for histological measure-
ments received experimental and control
Fig. 1. Implant surfaces photographed in a Zeiss Supra VP scanning electron microscope. (a) Zi-Unite surface
with pore openings in the lower micrometer range. (b) Zi-Unite surface. Enlargement of the smooth surface of
the single zirconia particle. (c, d) Promimic surface. The smooth surface of the single zirconia particles are
covered by a single layer of irregularly shaped Ca/P crystals. (e, f) CoAT-sputtered surface. The particles are
covered by a continuous, thin layer of Ca/P. (g, h) TiUnitet surface. The oxidized implant surface is
characterized by pore openings in the lower micrometer range and volcano-like elevations.
Fig. 2. Clinical view of the tibia with the insertion
of a test implant.
Rocchietta et al . Surface-modified zirconia implants
846 | Clin. Oral Impl. Res. 20, 2009 / 844–850 c� 2009 John Wiley & Sons A/S
implants. The rabbits used for removal tor-
que measurements received only the three
types of experimental implants. The proto-
col was purposely designed to avoid the
control implants in the RTQ rabbits because
of a different macroscopic design of the latter
compared with the test implants. This was
thought to have an inevitable influence on
the implant shear strength determined by
the RTQ analysis. In all rabbits (histologic
and RTQ), the placement of the different
implant types alternated between the left
and the right hind limbs according to a
predefined rotating placement scheme.
Specimen preparation and analysis
Postoperatively, a dose of 1 mg/Kg/12 h
of flunixin (Finadynes
, Shering-Plough
S.p.A., Milan, Italy) was administered in-
tramuscularly as an analgesic, while anti-
biotic care was provided subcutaneously
using 2 mg/kg marbofloxacine [Marbocyls
1%; A.T.I. S.r.l., Ozzano Emilia (BO),
Italy] daily for 5 days.
All animals were sacrificed after 3 weeks
with an intravenous overdose of potassium
chloride after they had been anesthetized as
described previously. Before this, a radio-
graphic evaluation was performed by con-
ventional X-rays.
Eight rabbits, in which threaded zirconia
ceramic implants with the three different
surface topographies were placed, were
subjected to RTQ tests (TSTN, Mark-
10s
, Italy). The specimen was embedded
in a resin block to achieve stability for the
RTQ machine, which involved an electric
motor with a strain gauge mounted on a
metal frame. The grip was connected to the
squared head of the ceramic implant. A
fixed rotation rate was applied until failure
of the bone-to-implant interface occurred.
The peak RTQ value was registered.
The remaining 10 animals were used for
histology. The implants with surrounding
bone tissue were removed en bloc and
fixated by immersion in 4% buffered for-
maldehyde. In the following, dehydration
of the specimens was accomplished by
increasing ethanol concentrations using a
dehydration system with agitation and va-
cuum. The blocks were embedded in Kul-
zer Technovit 7200 VLC-resin (Haraeus
Kulzer GmbH, Wehrheim, Germany) and
sliced longitudinally on an Exakt cutting
unit (Exakt, Norderstedt, Germany). The
slices were reduced by microgrinding and
polishing using an Exakt griding unit to an
even thickness of 30–40 mm. These were
stained with toluidine blue/pyronine G
and examined in a Leica 6000DRB light
microscope (Leica Microsystems GmbH,
Wetzlar, Germany). Bone-to-implant con-
tact was measured outgoing from the bor-
der between cortical bone and the bone
marrow chamber of both, the tibia and
the femur.
Statistical analysis
Differences in removal torque and bone-to-
implant contact between the different im-
plant surfaces were analyzed using the
Friedman test (Po0.05), followed by pair-
wise Bonferroni-corrected Wilcoxon’s
signed ranks post hoc tests (Po0.05/3).
Results
Clinical observations
The healing period was uneventful. Sixteen
out of 18 rabbits completed the study. Two
rabbits had to be sacrificed at the time of
surgery due to femur fractures while insert-
ing the implants; hence, 16 implants were
lost all together. In the femurs of these 16
rabbits, two oxidized, three CoAT-sput-
tered and two Promimic implants were
lost due to an initial fracture line while
performing the implant site preparation.
Two CoAT-sputtered implants broke dur-
ing the RTQ and six Zi-Unite implants
were surgically positioned in proximity to
the rabbits’ cortical wall, and thus could
not be used for an appropriate bone-to-
implant evaluation. These losses resulted
in a total of 110 implants analyzed out of
143 implants that were originally included
in the study (Table 1). Clinically and radio-
graphically, all implants appeared to be
osseointegrated (Fig. 6).
RTQ test
The results are shown in Table 2. Both
implants with a topographic and a
Fig. 3. Clinical view of the tibia with the insertion
of a control implant (TiUnitet).
Fig. 4. The test and control implants positioned.
Fig. 5. Two test implants inserted in the tibia ap-
proximately 8 mm apart.
Table 1. Implant distribution included in the study
Description Quantity
Topographically modified Zr (Zi-Unite) 29 (13 for histology, 16 for RTQ)Topographically and chemically modified Zr A(Promimic)
33 (18 for histology, 15 for RTQ)
Topographically and chemically modified Zr B(CoAT sputtered)
30 (16 for histology, 14 for RTQ)
Oxidized 18 (18 for histology)Total 110
Fig. 6. X-rays of the inserted test and control im-
plants before sacrifice.
Rocchietta et al . Surface-modified zirconia implants
c� 2009 John Wiley & Sons A/S 847 | Clin. Oral Impl. Res. 20, 2009 / 844–850
chemical modification (Promimic and
CoAT Sputtered) showed slightly higher
RTQ values than the topographic-modified
implant in the tibia and femur. Two
CoAT-sputtered implants broke during
the RTQ. These implants were excluded
from the statistical analysis, thus resulting
in a total of 14 (n¼number of implants)
implants tested for this group.
No significant differences between the
groups were found either in the femur
(P¼ 0.738) or in the femurþ tibia
(P¼ 0.332). In tibia, the primary analysis
indicated differences between the groups
(P¼ 0.039). However, the post hoc analysis
failed to demonstrate any difference be-
tween the groups (P40.068).
Histological description
The overview images of longitudinal
ground sections are given in Figs 7–10.
The implants were osseointegrated with
the first two threads in cortical bone and
the residual portion of the implant body
was hanging free in the bone marrow
chamber. New bone formation was visible
along the threads positioned in cortical
bone and outgoing from the coronal cortical
bone to and along the contour of the im-
plant threads. This is more pronounced at
higher magnifications. A small band of
woven bone, outgoing from the existing
bone, was formed along the surface of the
implant and a visible seam of osteoblasts
and osteoid indicated the ongoing bone
formation (Fig. 11). In the remaining areas,
the bone marrow was in direct contact with
the implant surface. Backscattered electron
microscopic images confirmed the histol-
ogy results. A small band of mineralized
bone formed directly on and along the sur-
face of the implant (Fig. 12). Osteocyte
lacunae were clearly visible in the newly
formed bone (Fig. 12).
The mean bone-to-implant contact va-
lues are summarized in Table 3. Six im-
plants in the Zi-Unite group were excluded
from this analysis due to a close contact of
the implant threads with the cortical wall
of the rabbits’ limbs, hence jeopardizing the
overall results.
No significant differences between the
groups were found either in the femur
(P¼ 0.984), the tibia (P¼ 0.130) or the
femurþ tibia (P¼ 0.292).
Table 2. Removal torque test values (N cm)
Zi-Unite Promimic CoAT sputtered
Median 95% CI n Median 95% CI n Median 95% CI n
Femur 31.8 25.1–62 9 33.3 21.6–55.3 8 40.5 25.8–53.8 7Tibia 25.8 10.2–97.4 7 41 30.1–55 7 27.1 12.8–98.3 7Femurþ Tibia 28.9 25.1–33.6 16 35 30.1–49.4 15 36.8 24.3–45.7 14
Fig. 7. Longitudinal ground section of a Zi-Unite
surface implant.
Fig. 8. Longitudinal ground section of a Promimic
surface implant.
Fig. 9. Longitudinal ground section of a CoAT-sput-
tered surface implant.
Fig. 10. Longitudinal ground section of a TiUnitet
surface implant.
Fig. 12. Backscattered electron microscope image of
the same specimen (Promimic). A small band of
mineralized bone formed directly on and along the
surface of the implant. Osteocytes lacunae were
clearly visible in the newly formed bone.
Table 3. Bone-to-implant contact test values (%)
Zi-Unite Promimic CoAT sputtered TiUnitet
Median 95% CI n Median 95% CI n Median 95% CI n Median 95% CI n
Femur 24.1 0–73.8 6 42.5 15–60.5 7 47.7 24.6–92.6 6 31.5 25–78.9 8Tibia 33.8 0–80 7 42.9 0–71.4 11 36.1 7.9–56.4 10 64.4 47.5–91.1 10Femurþ Tibia 27.5 0–59.2 13 42.5 30.5–56.1 18 36.1 26.1–62.2 16 58.3 29.7–73 18
Fig. 11. Higher magnification of the Promimic sur-
face. A small band of woven bone, outgoing from the
existing bone was formed along the surface of the
implant and a visible seam of osteoblasts and osteoid
indicate the ongoing bone formation.
Rocchietta et al . Surface-modified zirconia implants
848 | Clin. Oral Impl. Res. 20, 2009 / 844–850 c� 2009 John Wiley & Sons A/S
Discussion
The present study showed bone formation
outgoing from the existing cortical bone
along the implant threads, to various de-
grees, for all the different surfaces examined.
The prerequisite for immediate or early
loading of implants is the maintenance of
primary stability achieved by fast bone
formation. The implant surface modifica-
tion is the key to accelerate and enhance
new bone formation, which translates to
higher values of bone–contact ratios and
greater resistance to RTQ. The aim of this
study was to investigate the bone tissue
response to three zirconia surface modifi-
cations compared with the oxidized tita-
nium dental implant.
Other than quantitative differences, the
bone apposition can be detected following
different mechanisms (Davies 1998).
Implants with machined surfaces have
been described as integrated by ingrowth
from adjacent bone surfaces, whereas sur-
face-modified implants also show bone
formation directly on the surface. The
topography and chemistry of this surface
influence the mechanism of bone apposi-
tion. All zirconia implants evaluated in
this study showed signs of contact osteo-
genesis. The same mechanism was
observed on two surface topographic mod-
ifications of zirconia implants reported in a
previous study (Sennerby et al. 2005). Sen-
nerby and colleagues showed a four- to
fivefold increase to torque forces of the
two topographic-modified zirconia surfaces
compared with a machined zirconia im-
plant. In our study, the additional chemical
modification seemed not to improve the
final outcome in terms of the strength and
speed of osteoconductivity.
A recent study showed that surface char-
acteristics have an important influence on
bone integration of zirconia implants
(Gahlert et al. 2007). Machined and sand-
blasted zirconia implants were compared
biomechanically and histomorphometri-
cally with SLA titanium dental implants.
Results reported higher values of bone
stability for the titanium SLA implant,
followed by the rough zirconia and the
machined zirconia. Further improvements
were needed to obtain interfacial biome-
chanical properties comparable with tita-
nium SLA surface. The authors reported a
mean RTQ value of 40.5 N/cm for their
rough zirconia implant. This result is si-
milar to our mean values for the topo-
graphic and chemically modified implants
(Promimic and CoAT Sputtered).
The bone-to-implant contact in this
study was measured only along the first
four threads of the implant at the border
between the cortical bone and the marrow
to achieve reliable results. Because of
the anatomy of the rabbit femur and tibiae,
the first implant threads were in close
proximity if not adjacent to the cortical
bone. The direct bone contact with the
implant can bias the overall results for
BIC values and RTQ measurements.
Hence, the first threads were excluded
from the BIC results, whereas the RTQ
values must take this limitation into
consideration. The RTQ was measured
for the zirconia with the three surface
modification implants only. The control
implants (oxidized titanium) were only
evaluated histologically. This was due to
a small difference in the macro-topography
(design) of the implant body between the
oxidized implant and the zirconia implant,
resulting in otherwise altered and incom-
parable results.
In conclusion, the findings suggest
that modified zirconia implants can
achieve good stability in bone. Within the
limits of the present study and its sample
size, the histology results (bone-to-implant
contact) show no statistical significance
between the zirconia implants and the
oxidized implants. The addition of the
specific chemical modifications to a
topographic-modified zirconia surface
does not seem to enhance bone apposition
and therefore does not seem to have a
beneficial effect on the interfacial shear
strength.
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