Surface-modified zirconia implants: tissue response in rabbits

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: [email protected]

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

mailto:[email protected]

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.


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.



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.



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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Surface-modified zirconia implants: tissue response in rabbits

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