7
The mucosal barrier at implant abutments of different materials Maria Welander Ingemar Abrahamsson Tord Berglundh Authors’ affiliation: Maria Welander, Ingemar Abrahamsson, Tord Berglundh, Department of Periodontology, The Sahlgrenska Academy at Go ¨ teborg University, Go ¨ teborg, Sweden Correspondence to: Maria Welander, Department of Periodontology The Sahlgrenska Academy at Go ¨ teborg University Box 450 405 30 Go ¨ teborg Sweden Tel.: þ 4631 786 3780 Fax: þ 4631 786 3791 e-mail: [email protected] Key words: biomaterials, dental implants, gold alloy, histology, peri-implant mucosa, soft tissue, titanium, zirconia Abstract Objective: The aim of the present study was to analyze the soft tissue barrier formed to implant abutments made of different materials. Material and methods: Six Labrador dogs, about 1 year old, were used. All mandibular premolars and the first, second and third maxillary premolars were extracted. Three months later four implants (OsseoSpeedt, 4.5 9 mm, Astra Tech Dental, Mo ¨ lndal, Sweden) were placed in the edentulous premolar region on one side of the mandible and healing abutments were connected. One month later, the healing abutments were disconnected and four new abutments were placed in a randomized order. Two of the abutments were made of titanium (Ti), while the remaining abutments were made of ZrO 2 or AuPt-alloy. A 5-months plaque control program was initiated. Three months after implant surgery, the implant installation procedure and the subsequent abutment shift were repeated in the contra-lateral mandibular region. Two months later, the dogs were euthanized and biopsies containing the implant and the surrounding soft and hard peri-implant tissues were collected and prepared for histological analysis. Results: It was demonstrated that the soft tissue dimensions at Ti- and ZrO 2 abutments remained stable between 2 and 5 months of healing. At Au/Pt-alloy abutment sites, however, an apical shift of the barrier epithelium and the marginal bone occurred between 2 and 5 months of healing. In addition, the 80-mm-wide connective tissue zone lateral to the Au/Pt-alloy abutments contained lower amounts of collagen and fibroblasts and larger fractions of leukocytes than the corresponding connective tissue zone of abutments made of Ti and ZrO 2 . Conclusion: It is suggested that the soft tissue healing to abutments made of titanium and ZrO 2 is different to that at abutments made of AuPt-alloy. The soft tissue barrier around dental im- plants serves as a protective seal between the oral environment and the underlying peri-implant bone. The interface between the peri-implant mucosa and dental implants made of c.p. titanium is com- prised of one epithelial and one connective tissue component and the structure and function of this barrier tissue were de- scribed previously (Berglundh et al. 1991, 2007; Buser et al. 1992; Berglundh & Lindhe 1996; Abrahamsson et al. 1997, 1999, 2002, 2003; Cochran et al. 1997). The clinical situation in implant therapy may for technical or esthetic reasons re- quire alternative materials to titanium in the transmucosal part of the implant. The choice of the material, however, must be Date: Accepted 5 November 2007 To cite this article: Welander M, Abrahamsson I, Berglundh T. The mucosal barrier at implant abutments of different materials. Clin. Oral Impl. Res. 19, 2008; 635–641. doi: 10.1111/j.1600-0501.2008.01543.x c 2008 The Authors. Journal compilation c 2008 Blackwell Munksgaard 635

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The mucosal barrier at implantabutments of different materials

Maria WelanderIngemar AbrahamssonTord Berglundh

Authors’ affiliation:Maria Welander, Ingemar Abrahamsson, TordBerglundh, Department of Periodontology, TheSahlgrenska Academy at Goteborg University,Goteborg, Sweden

Correspondence to:Maria Welander, Department of PeriodontologyThe Sahlgrenska Academy at Goteborg UniversityBox 450405 30 GoteborgSwedenTel.: þ 4631 786 3780Fax: þ 4631 786 3791e-mail: [email protected]

Key words: biomaterials, dental implants, gold alloy, histology, peri-implant mucosa, soft

tissue, titanium, zirconia

Abstract

Objective: The aim of the present study was to analyze the soft tissue barrier formed to

implant abutments made of different materials.

Material and methods: Six Labrador dogs, about 1 year old, were used. All mandibular

premolars and the first, second and third maxillary premolars were extracted. Three months

later four implants (OsseoSpeedt, 4.5 � 9 mm, Astra Tech Dental, Molndal, Sweden) were

placed in the edentulous premolar region on one side of the mandible and healing

abutments were connected. One month later, the healing abutments were disconnected

and four new abutments were placed in a randomized order. Two of the abutments were

made of titanium (Ti), while the remaining abutments were made of ZrO2 or AuPt-alloy. A

5-months plaque control program was initiated. Three months after implant surgery, the

implant installation procedure and the subsequent abutment shift were repeated in the

contra-lateral mandibular region. Two months later, the dogs were euthanized and biopsies

containing the implant and the surrounding soft and hard peri-implant tissues were

collected and prepared for histological analysis.

Results: It was demonstrated that the soft tissue dimensions at Ti- and ZrO2 abutments

remained stable between 2 and 5 months of healing. At Au/Pt-alloy abutment sites,

however, an apical shift of the barrier epithelium and the marginal bone occurred between

2 and 5 months of healing. In addition, the 80-mm-wide connective tissue zone lateral to the

Au/Pt-alloy abutments contained lower amounts of collagen and fibroblasts and larger

fractions of leukocytes than the corresponding connective tissue zone of abutments made

of Ti and ZrO2.

Conclusion: It is suggested that the soft tissue healing to abutments made of titanium and

ZrO2 is different to that at abutments made of AuPt-alloy.

The soft tissue barrier around dental im-

plants serves as a protective seal between

the oral environment and the underlying

peri-implant bone. The interface between

the peri-implant mucosa and dental

implants made of c.p. titanium is com-

prised of one epithelial and one connective

tissue component and the structure and

function of this barrier tissue were de-

scribed previously (Berglundh et al. 1991,

2007; Buser et al. 1992; Berglundh &

Lindhe 1996; Abrahamsson et al. 1997,

1999, 2002, 2003; Cochran et al. 1997).

The clinical situation in implant therapy

may for technical or esthetic reasons re-

quire alternative materials to titanium in

the transmucosal part of the implant. The

choice of the material, however, must be

Date:Accepted 5 November 2007

To cite this article:Welander M, Abrahamsson I, Berglundh T. The mucosalbarrier at implant abutments of different materials.Clin. Oral Impl. Res. 19, 2008; 635–641.doi: 10.1111/j.1600-0501.2008.01543.x

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 635

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based on its ability to promote integration

to the connective tissue of the peri-implant

mucosa during healing.

The healing around implants made of

gold-alloys or ceramic materials were ana-

lyzed in experimental studies in animals.

The majority of studies described integra-

tion between bone and the biomaterial and

it was reported that osseointegration to

titanium was superior to that at gold-alloys

(Albrektsson et al. 1982; Thomsen et al.

1997; Abrahamsson & Cardaropoli 2007).

Healing around ceramic implants made of

zirconium, on the other hand, resulted in

bone formation in contact with the bio-

material, which was similar to that at

implants made of titanium (Albrektsson

et al. 1985; Thomsen et al. 1997; Sennerby

et al. 2005).

The integration of oral mucosa to im-

plant components of different materials

was examined in few studies. Abrahams-

son et al. (1998), in an experimental study

in dogs, reported that the implant material

was of decisive importance for the quality

of the attachment that formed between the

mucosa and the implant abutment. While

abutments made of aluminum-based cera-

mic provided conditions for a mucosal

attachment that was similar to that of

titanium, gold-alloy abutments did not

promote healing that resulted in integra-

tion of connective tissue to the implant

component and, in such sites, the mucosal

attachment was established apical to the

abutment/fixture junction. Conflicting

data were reported in an experimental

study on dogs by Abrahamsson &

Cardaropoli (2007). In this experiment,

the soft tissue dimensions were similar

at implants made of gold-alloy and tita-

nium. Furthermore, Vigolo et al. (2006)

in a study on 20 subjects reported that

no clinical differences in soft tissue

conditions were detected between im-

plants with either titanium or gold-alloy

abutments.

There is limited information on soft

tissue integration to implants made of

zirconium. Results presented in clinical

reports indicated that favorable soft tissue

results were obtained around abutments

made of zirconium (Brodbeck 2003; Kohal

& Klaus 2004a; Tan & Dunne 2004).

Glauser et al. (2004) in a 4-year follow-up

on 18 subjects reported that healthy mu-

cosal conditions and stable marginal bone

levels were observed at implants with zir-

conium abutments.

The aim of the present study was to

further analyze the soft tissue barrier

formed to implant abutments made of

different materials.

Material and methods

Six Labrador dogs, about 1 year old, were

used. The regional Ethics Committee for

Animal research, Goteborg, Sweden, ap-

proved the study protocol. All surgical

procedures were performed using general

anesthesia induced with propofol (10 mg/

ml, 0.6 ml/kg) intravenously and sustained

with N2O : O2 (1 : 1, 5–2) and isoflurane

employing endotracheal intubation.

At the start of the experiment, all man-

dibular premolars and the first, second and

third maxillary premolars were extracted.

Three months later, buccal and lingual

mucoperiostal flaps were elevated and

four implants (OsseoSpeedt, 4.5 ST �9 mm, Astra Tech Dental, Molndal,

Sweden) were placed in the edentulous

premolar region in one side of the mand-

ible. Healing abutments (Zebrat 6 mm,

Astra Tech Dental, Molndal, Sweden)

were connected to the implants and the

flaps were adjusted and sutured.

One month after implant placement, the

healing abutments were disconnected and

four new abutments were placed in a

randomized order (Fig. 1). Two of the

abutments were made of titanium (Ti),

while the remaining abutments were

made of ZrO2 (ceramic) or AuPt-alloy

(cast-to). All abutments had similar dimen-

sions and geometry. A 5-month plaque

control program was initiated. The pro-

gram included cleaning of implants and

teeth with a toothbrush and dentifrice

once a day, 5 days a week.

Three months after implant surgery, the

implant installation procedure and the sub-

sequent abutment shift were repeated in

the contra-lateral mandibular region.

Two months later, i.e. 5 months after

the first abutment connection procedure,

the dogs were euthanized by an overdose of

Sodium-Pentothals

(Abbott Scandinavia

AB, Solna, Sweden) and perfused through

the carotid arteries by a fixative (Karnovsky

1965). The mandibles were removed and

placed in the fixative. The implant sites

were dissected using a diamond saw (Exakt

Apparatebau, Norderstedt, Germany). The

tissue blocks that included the implant and

the surrounding soft and hard peri-implant

tissues, were processed using a modifica-

tion of the fracture technique (Thomsen &

Ericson 1985) as described by Berglundh et

al. (1991, 1994). The tissue samples were

placed in ethylenediaminetetraacetic acid

(EDTA). Before the hard tissue was fully

decalcified incisions, parallel with the long

axis of the implant, were made through the

peri-implant tissues. Four different units,

mesio-buccal, disto-buccal, mesio-lingual

and disto-lingual were hereby obtained and

carefully separated from the implants. Dec-

alcification was completed in EDTA and

dehydration was performed in serial steps

of ethanol concentrations. A secondary

fixation in OsO4 was performed and the

specimens were embedded in epoxy resin

(EPONs

Fluka Chemie GmbH, Buchs,

Switzerland) (Schroeder 1969). Sections

were produced with the microtome set at

3 mm and stained in PAS and toluidine blue

(Schroeder 1969).

The histological examination was per-

formed in a Leica DM-RBEs

microscope

(Leica, Heidelberg, Germany) equipped

with an image system Q-500 MCs

(Leica).

Fig. 1. The four abutments (from left: Ti, ZrO2, Ti, Au/Pt-alloy) in place 1 month after implant placement.

Welander et al . The mucosal barrier at implant abutments of different materials

636 | Clin. Oral Impl. Res. 19, 2008 / 635–641 c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard

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Histological measurements

In each section, the following landmarks

were identified and used for the linear

measurements (Fig. 2): PM, the margin of

the peri-implant mucosa; aJE, the apical

termination of the barrier epithelium; B,

the marginal level of bone to implant con-

tact; A/F, the abutment/fixture borderline.

The vertical distances between the land-

marks were determined in a direction that

was parallel to the long axis of the implant.

The composition of the connective tis-

sue compartment of the peri-implant mu-

cosa that was in contact with the different

abutments and interposed between aJE and

A/F was assessed using a stereological

technique as described previously (Schroe-

der & Munzel-Pedrazzoli 1973; Berglundh

et al. 1991; Abrahamsson et al. 1999). The

analysis was confined to an 80-mm-wide

tissue zone lateral to the abutment inter-

face. A lattice comprising 100 light points

was superimposed over the tissue at a

magnification of � 1000 and the relative

proportions of the connective tissue occu-

pied by collagen (Co), fibroblasts (Fi), vas-

cular structures (V), leukocytes (Leu) and

residual tissue (R) (e.g., nerves, matrix

components and unidentified structures)

were determined. The relative volume of

infiltrating leukocytes within the barrier

epithelium was assessed according to

methods described by Schroeder (1973)

and Berglundh et al. (1992a, 1992b). A

lattice comprising 400 points was super-

imposed over the epithelium at a magnifi-

cation of � 1000 and the percentage of

infiltrating leukocytes in relation to the

volume of the barrier epithelium was

determined.

Data analysis

Mean values from the different assess-

ments were calculated for each abutment

type and animal (n¼6). Differences were

analyzed using the two-way analysis of

variance (ANOVA) and the Student–

Newman–Keuls test. The null hypothesis

was rejected at Po0.05.

Results

One implant in one dog was lost during the

healing after implant surgery. Healing at

the 47 remaining implant sites was

uneventful.

Histological observations

The soft tissue interface to the different

implant abutments comprised an epithelial

and connective tissue portion that followed

the geometry of the devices made of tita-

nium (Ti), ZrO2 (ceramic) and AuPt-alloy

(cast-to). In sections from Ti- and ceramic-

abutment sites, the dimensions of epithe-

lial and connective tissue components

remained stable between 2 and 5 months

of healing. At cast-to sites, however, an

apical shift of the barrier epithelium and

the level of marginal bone occurred in most

sites between 2 and 5 months of healing.

The results from the linear measurements

are presented in Table 1. Thus, the barrier

epithelium at Ti- and ceramic abutments

at 2 months of healing extended to a dis-

tance apical of PM that was 1.80 and

1.60 mm, while at 5 months the corre-

sponding dimensions were 1.83 and

1.75 mm, respectively. In sections repre-

senting cast-to abutments; however, the

mean PM to aJE distance increased from

1.56 to 2.07 mm between 2 and 5 months

of healing. Similar observations were made

regarding the position of marginal bone

level at the different abutments. Thus, at

Ti- and ceramic-abutment sites the dis-

tance between A/F and B was 1.17 and

1.07 mm at 2 months, and 1.02 and

0.95 mm at 5 months, respectively. The

corresponding distances at cast-to abut-

ment sites representing 2 and 5 months

of healing were 1.05 and 1.71 mm, respec-

tively.

The results from the assessments of the

composition of the connective tissue com-

partment in contact with the different

abutments are presented in Tables 2 and

3. The barrier epithelium extended to a

position that was apical of the A/F border-

line in four out of six cast-to abutment sites

at 5 months of healing and, hence, im-

peded connective tissue analysis. In sites

representing 2 months of healing, the

volume fractions occupied by collagen and

fibroblasts were significantly smaller at

cast-to sites than at Ti and ceramic sites.

Conversely, the proportions of leukocytes

and residual tissue were significantly larger

Fig. 2. Buccal-lingual section showing the land-

marks used for the histometric measurements.

PM, the marginal portion of the peri-implant mu-

cosa; aJE, the apical extension of the barrier epithe-

lium; A/F, the abutment/fixture borderline; B, the

marginal level of bone to implant contact.

Table 1. Dimensions of the peri-implant mucosa at 2 and 5 months of healing

Landmarks Ti Ceramic Cast-to

2 m 5 m 2 m 5 m 2 m 5 m

PM–B 3.13 (0.33) 2.85 (0.37) 3.08 (0.39) 2.82 (0.38) 3.04 (0.34) 3.54 (1.05)PM–aJE 1.80 (0.29) 1.83 (0.22) 1.60 (0.31) 1.75 (0.27) 1.56 (0.40) 2.07 (0.51)A/F–B 1.17 (0.26) 1.02 (0.34) 1.07 (0.27) 0.95 (0.27) 1.05 (0.41) 1.71 (1.30)

Mean values and standard deviations.

Table 2. The composition of the connectivetissue zone between aJE and A/F at 2months of healing

% Ti Ceramic Cast-to

Co 41.4 (10.7) 43.5 (7.7) 18.6 (6.9)n

V 7.3 (5.1) 6.6 (3.1) 3.9 (3.6)Fi 29.2 (9.1) 35.0 (9.0) 15.9 (6.9)n

Leu 7.5 (4.0) 6.5 (3.9) 25.3 (6.4)n

R 14.6 (9.3) 8.5 (7.2) 36.5 (17.0)n

Mean values and standard deviations.nPo0.05 between cast-to and Ti and between

cast-to and ceramic.

Welander et al . The mucosal barrier at implant abutments of different materials

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 637 | Clin. Oral Impl. Res. 19, 2008 / 635–641

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at cast-to abutment sites than at tissue

units obtained from Ti- and ceramic-abut-

ment sites. The tissue composition in

sections prepared from the 5-month speci-

mens from cast-to abutment sites was

similar to that assessed in the 2-month

samples. At Ti- and ceramic-abutment

sites, however, the densities of collagen

increased and leukocytes decreased be-

tween 2 and 5 months of healing

(Figs 3a–c and 4a–c). The large differences

in tissue composition at 2 months between

sites representing cast-to abutments on

the one hand and Ti- and ceramic abut-

ments on the other, persisted at 5 months

of healing. Thus, in cast-to sites available

for connective tissue analysis the densities

of collagen and fibroblasts remained

smaller, while the proportions of leuko-

cytes and residual tissue were found to be

larger than in Ti- and ceramic-abutment

sites (Fig. 5a–c).

The results from the assessments of

leukocytes residing in the barrier epithe-

lium of the peri-implant mucosa are

reported in Table 4. At 2 months, the

relative volume of infiltrating leukocytes

within the epithelium was 6.7–6.8% at Ti

and cast-to abutments and 5.2% at ceramic-

abutment sites. This difference was statis-

tically significant. At 5 months of healing,

the densities of leukocytes had decreased

and varied between 3.5% and 4.5%.

Discussion

In the present study, soft tissue healing to

implant abutments made of titanium,

ZrO2 and AuPt-alloy was analyzed. It

was demonstrated that the soft tissue

dimensions at Ti and ZrO2 abutments

remained stable between 2 and 5 months

of healing. At Au/Pt-alloy abutment sites,

however, an apical shift of the barrier

epithelium and the marginal bone occurred

between 2 and 5 months of healing. In

addition, the connective tissue interface at

Au/Pt-alloy abutments contained lower

amounts of collagen and fibroblasts and

larger fractions of leukocytes than the con-

nective tissue interface of abutments made

of Ti and ZrO2. It is suggested that the soft

tissue healing to abutments made of tita-

nium and ZrO2 is different to that at

abutments made of AuPt-alloy.

Soft tissue healing to implant abutments

of different materials was examined pre-

viously. Thus, Abrahamsson et al. (1998)

placed six Branemark implants in the man-

dibular premolar regions of five dogs. Abut-

ments made of c.p. titanium, ceramic

(highly sintered Al2O3), gold-alloy and

dental porcelain were connected in a sec-

ond stage surgery 3 months later. Biopsies

were obtained after 6 months of plaque

control. It was reported that healing at

ceramic and titanium abutments allowed

the formation of a mucosal attachment

that included an epithelial and a connective

tissue portion that were about 2 mm and

1–1.5 mm high, respectively. Abrahams-

son et al. (1998) also reported that no

proper mucosal attachment was formed to

Table 3. The composition of the connectivetissue zone between aJE and A/F at 5months of healing

% Ti Ceramic Cast-tonn

Co 50.1 (5.3) 48.5 (6.1) 18.1 (25.6)V 6.5 (1.2) 8.0 (7.6) 4.9 (6.9)Fi 36.8 (6.9) 34.2 (9.5) 16.8 (22.3)Leu 1.6 (2.0) 2.6 (2.0) 29.8 (23.5)R 5.1 (1.8) 6.8 (7.4) 31.4 (31.3)

Mean values and standard deviations.nnData obtained from two animals.

Fig. 3. (a) Buccal-lingual section of the peri-implant tissues at a titanium abutment at 5 months of healing.

Original magnification � 25. (b) Detail given in (a) showing the barrier epithelium with a few infiltrating

leukocytes and the underlying connective tissue. Original magnification � 400. (c) Detail given in (a)

showing the collagen rich connective tissue with fibroblasts and few vessels in the abutment/connective tissue

interface area. Original magnification � 400.

Fig. 4. (a) Buccal-lingual section of the peri-implant tissues at a ceramic abutment at 5 months of healing.

Original magnification � 25. (b) Detail given in (a) showing the barrier epithelium with a few infiltrating

leukocytes and the underlying connective tissue. Original magnification � 400. (c) Detail given in (a)

showing the collagen rich connective tissue with fibroblasts and few vessels in the abutment/connective tissue

interface area. Original magnification � 400.

Welander et al . The mucosal barrier at implant abutments of different materials

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abutments made of gold-alloy and dental

porcelain and at such sites, recession of the

mucosal margin and bone resorption

occurred. The finding in the study by

Abrahamsson et al. (1998) that healing to

abutments made of gold-alloy was different

than that at ceramic and titanium abut-

ments is supported by observations made

in the current experiment. Thus, the bar-

rier epithelium and the marginal bone level

were found to extend to a more apical

position at cast-to (Au/Pt-alloy) than at

Ti and ceramic abutments at 5 months of

healing. This finding indicates that healing

at 2 months at cast-to abutments was

incomplete and that the apical shift of

epithelium and marginal bone that was

observed at 5 months in the present study

represents a stage of tissue reaction to

establish a mucosal seal that extended

apical to the A/F border, i.e., in contact

with the titanium surface of the implant.

In the present study, it was also demon-

strated that the connective tissue portion of

the mucosa that was in contact with cast-

to abutments contained smaller amounts

of collagen and fibroblasts and larger pro-

portions of inflammatory cells and residual

tissue than the corresponding tissue unit at

ceramic and Ti abutments. The connective

tissue composition at the cast-to abut-

ments revealed in the current study may

thus resemble an insufficient mucosal

adaptation resulting in epithelial prolifera-

tion and bone loss.

The finding presented in the present

experiment and in the study by Abrahams-

son et al. (1998) that soft tissue healing to

implant components made of gold-alloy

was insufficient, is not in agreement with

data reported in a recent study by Abra-

hamsson & Cardaropoli (2007). They eval-

uated soft and hard tissue healing to

implants made of titanium or gold-alloy.

Implants were placed in the mandibular

premolar regions of four dogs and biopsies

were collected after 6 months. The histo-

logical analysis of the ground sections

revealed that the dimension of the barrier

epithelium and the position of the marginal

bone were similar at sites representing

titanium and gold-alloy implants. The

absence of differences in soft tissue dimen-

sions between the two implant types in the

study by Abrahamsson & Cardaropoli

(2007) is partly consistent with observa-

tions made in sites from 2 months of

healing in the present study. Thus, the

values describing the apical extension of

the barrier epithelium and the position of

the marginal bone at cast-to (Au/Pt) abut-

ments were comparable to those at Ti and

ceramic sites. The evaluation of the com-

position of the connective tissue portion in

contact with the abutment material, how-

ever, revealed large differences between

cast-to sites on the one hand and Ti and

ceramic sites on the other. No qualitative

assessments of the soft tissue portion in

contact with the implants were made in

the study by Abrahamsson & Cardaropoli

(2007).

In the study by Abrahamsson et al.

(1998) referred to above, it was demon-

strated that soft tissue healing to a ceramic

abutment made of Al2O3 was similar to

that of c.p. titanium. This finding is inter-

esting in relation to observations made in

the present experiment. It should be

pointed out, however, that the ceramic

abutments used by Abrahamsson et al.

(1998) were aluminum based, while the

ceramic abutments in the current study

were made of ZrO2. Although the ceramic

material was different in the two studies,

soft tissue healing in terms of tissue dimen-

sions and composition in both studies was

similar to that at abutments made of tita-

nium. Corroborating data were presented

in an experimental study by Kohal et al.

(2004b). They analyzed soft and hard

tissues around implants made of either

titanium or zirconium in six monkeys.

Biopsies were obtained 9 months after im-

plant placement. It was reported that soft

tissue dimensions were similar at titanium

and zirconium implants.

In the present study, the relative volume

of infiltrating leukocytes in the barrier

epithelium was analyzed. The presence of

migrating polymorphonuclear leukocytes

and other inflammatory cells in the junc-

tional/barrier epithelium in the mucosa

surrounding implants or teeth is a result

from a microbial challenge in adjacent

sulcus areas. The assessment of leukocytes

in the barrier epithelium was applied in

previous experiments to evaluate differ-

ences in epithelial attachment to implant

abutments or tooth enamel (Berglundh

et al. 1989, 1992a, 1992b). Recently,

Welander et al. (2007) applied this techni-

que to compare epithelial attachment to

titanium implants with or without an

ultrathin collagen coating. It was reported

Fig. 5. (a) Buccal-lingual section of the peri-implant tissues at a cast-to abutment at 5 months of healing.

Original magnification � 25. (b) Detail given in (a) showing the barrier epithelium with a few infiltrating

leukocytes and the underlying connective tissue. Original magnification � 400. (c) Detail given in (a)

showing the connective tissue with large numbers of fibroblasts and leukocytes and few collagen fibers in the

abutment/connective tissue interface area. Original magnification � 400.

Table 4. Percentage of leukocytes residingin the barrier epithelium at 2 and 5 monthsof healing

2 months 5 months

Ti 6.7 (1.7) 4.5 (1.9)Ceramic 5.2 (1.4)n 3.5 (1.7)Cast-to 6.8 (2.4) 4.0 (1.4)

Mean values and standard deviations.nPo0.05 between ceramic and Ti and between

ceramic and cast-to at 2 months of healing.

Welander et al . The mucosal barrier at implant abutments of different materials

c� 2008 The Authors. Journal compilation c� 2008 Blackwell Munksgaard 639 | Clin. Oral Impl. Res. 19, 2008 / 635–641

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that the density of leukocytes in the barrier

epithelium varied between 5% and 7% at

coated and uncoated implants after 4 and 8

weeks of healing. This result is consistent

with data presented in the present study.

Thus, at 2 months (8 weeks) of healing the

volume fraction occupied by leukocytes in

the barrier epithelium varied between

5.2% and 6.8%. In the specimens repre-

senting 5 months of healing, however, the

density of leukocytes in the epithelium had

decreased at all abutment types. The pro-

portion of leukocytes in the barrier epithe-

lium at ceramic (ZrO2) abutments was

smaller than that at Ti and cast-to abut-

ments. This observation indicates that the

ZrO2 material provided appropriate condi-

tions for epithelial attachment in the estab-

lishment of a proper mucosal seal. Another

explanation may be related to differences in

bacterial colonization on the abutment sur-

faces. Such a hypothesis was proposed by

Rimondini et al. (2002) and Scarano et al.

(2004). Rimondini et al. (2002) evaluated

microbial colonization on titanium and

zirconium discs in vitro and in vivo. While

only small differences were detected in

bacterial adherence between the two sur-

faces in the in vitro test, the results from

the in vivo model revealed that signifi-

cantly larger amounts of bacteria were

found on titanium than on zirconium discs.

Similar findings were reported by Scarano

et al. (2004). They analyzed the percentage

surface covered by bacteria on titanium and

zirconium discs. The discs were mounted

to removable acrylic devices that were

adapted to the premolar–molar regions of

10 subjects. Scanning electron microscopy

analysis of the discs that was performed

after 24 h revealed that the surface area

covered by plaque was significantly smaller

at zirconium than at titanium discs.

In summary, the present study demon-

strated that abutments made of titanium

and ZrO2 promoted proper conditions for

soft tissue healing, whereas abutments

made of Au/Pt-alloy failed to establish

appropriate soft tissue integration.

Acknowledgements: The present

study was supported by grants from

Astra Tech AB, Molndal, Sweden.

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