Massimiliano ReaSara RicciPaolo GhensiNiklaus P. LangDaniele BotticelliClaudio Soldini

Marginal healing usingPolyetheretherketone as healingabutments: an experimental studyin dogs

Authors’ affiliations:Massimiliano Rea, Daniele Botticelli, Faculty ofDentistry, University of Medical Science, LaHabana, CubaSara Ricci, Paolo Ghensi, University of Padoa,Padova, ItalyPaolo Ghensi, Centre for Integrative Biology(CIBIO), Universit�a degli Studi di Trento, Trento,ItalyNiklaus Peter Lang, Center for Dental Medicine,University of Zurich, Zurich, Switzerland;University of Bern, Bern, SwitzerlandDaniele Botticelli, ARDEC Academy, AriminumOdontologica, Rimini, ItalyDaniele Botticelli, POI – Programa Odontol�ogicoInternacional, Cartagena de Indias, ColombiaClaudio Soldini, CLC Scientific, Vicenza, Italy

Corresponding author:Daniele Botticelli, PhDPOI- Programa Odontol�ogico InternacionalCentro Hist�orico, Av. VenezuelaEdificio City Bank, Piso 5, Oficina 5GCartagena de Indias, ColombiaTel./Fax: +0057 5 6468359e-mail: daniele.botticelli@ardec.it

Key words: animal study, bone, dental implants, healing, healing abutment, histology

implant dentistry, polyetheretherketone, soft tissue

Abstract

Objective: To evaluate the marginal soft and hard tissue healing at titanium and

Polyetheretherketone (PEEK) healing implant abutments over a 4-month period.

Material and Methods: In six Labrador dogs, all mandibular premolars and first molars were

extracted. After 4 months of healing, flaps were elevated, and two implants were installed at each

side of the mandible, one in the premolar and the other in the molar regions. Four different types

of healing abutments were positioned on the top of each implant: (i) titanium (Ti); (ii) PEEK

material bonded to a base made of titanium (Ti-P), randomly positioned in the premolar region;

(iii) PEEK, pristine (P); and (iv) PEEK, roughened (P-R), randomly positioned in the molar region.

The flaps were sutured to allow a non-submerged healing, and after 4 months, the animals were

sacrificed and ground sections obtained for histological evaluation.

Results: A higher resorption of the buccal bone crest was observed at the PEEK bonded to a base

made of titanium abutments (1.0 � 0.3 mm) compared to those made of titanium (0.3 � 0.4 mm).

However, similar dimensions of the peri-implant mucosa and similar locations of the soft tissues in

relation to the implant shoulder were observed. No statistically significant differences were seen in

the outcomes when the pristine PEEK was compared with the roughened PEEK abutments. The

mean apical extension of the junctional epithelium did not exceed the implant shoulder at any of

the abutment types used.

Conclusions: The coronal level of the hard and soft tissues allows the conclusion that the use of

PEEK as healing abutments may be indicated.

The wound healing process, follows implant

surgery, includes a series of sequential bio-

logical events that, at the hard tissue level,

include the formation of coagulum, granula-

tion tissue, and the deposition of a provi-

sional matrix and woven bone. These

processes will result in the integration of

the implants into pristine bone (Berglundh

et al. 2003; Abrahamsson et al. 2004; Rossi

et al. 2014). Moreover, the peri-implant soft

tissue also undergoes a sequential matura-

tion process, again starting with the forma-

tion of a coagulum followed by that of

granulation tissue. This will result in the

establishment of a barrier epithelium and a

connective tissue compartment attaching to

the implant surface (Berglundh et al. 2007;

Welander et al. 2008). Hence, the peri-

implant soft tissue functions as a protective

seal for homeostasis.

As described in a series of experimental

studies (Berglundh et al. 1991; Abrahamsson

et al. 1996; Cochran et al. 1997; Abra-

hamsson & Soldini 2006), the peri-implant

mucosa consists of a long barrier epithelium

of about 2 mm and a 1–1.5 mm connective

tissue compartment characterized by a large

proportion of collagen (Berglundh et al. 1991;

Berglundh & Lindhe 1996). The establish-

ment of an adequate biological width is con-

sidered a prerequisite for achieving a long-

term stable implant homeostasis (Abra-

hamsson et al. 1996).

Biocompatibility of implant materials used

in the transmucosal portion may be a prereq-

uisite for positive treatment outcomes (Abra-

hamsson et al. 1998). Owing to its very high

resistance to corrosion and biocompatibility

(Steinemann 1998), commercially pure (c.p.)

titanium is usually recognized as the

Date:Accepted 20 March 2016

To cite this article:Rea M, Ricci S, Ghensi P, Lang NP, Botticelli D, Soldini C.Marginal healing using Polyetheretherketone (PEEK) ashealing abutments: an experimental study in dogs.Clin. Oral Impl. Res. 00, 2016, 1–5doi: 10.1111/clr.12854

© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 1

standard not only for implant manufacturing,

but also for the abutment portion of the

implants.

However, for esthetic or technical reasons,

materials different from titanium may be

chosen in the transmucosal portion of the

implant–abutment complex during healing.

In an animal experiment (Abrahamsson

et al. 1998), the importance of the abutment

material for the quality of the attachment

between the mucosa and the implant was

studied. Abutments made of titanium or of

highly sintered alumina-based ceramics

established similar conditions for mucosal

healing to the abutment surface. On the

opposite, at sites were abutments were made

of gold alloys or dental porcelain, a recession

of the soft tissue margin and concomitant

bone resorption were observed.

Since the 1990s, polyetheretherketone

(PEEK) has been used in orthopedic surgery

with considerable clinical success (Brantigan

et al. 2004; Toth et al. 2006). As an alterna-

tive to titanium abutments, PEEK tempo-

rary abutments have been recently

introduced for implant-supported provisional

single crowns. These abutments appeared to

be easily modeled at the chairside and yield

whitish rather than a silver color that may

improve esthetic outcomes (Koutouzis et al.

2011).

To date, limited information is available

on the effect of PEEK on the peri-implant soft

tissue interface. Hence, the aim of the pre-

sent animal study was to evaluate the mar-

ginal soft and hard tissue healing at titanium

and PEEK healing implant abutments over a

4-month period.

Material and methods

The research protocol was submitted to and

approved by the Ethical Committee of the

People’s Liberation Army General Hospital,

Laboratory Animal Welfare of Beijing, PR of

China.

Six Labrador dogs (4 years of age and 25–

26 kg in weight) were used for the experi-

ment. At all surgical sessions, the dogs

were anesthetized with 3% pentobarbital

sodium 30 mg/kg i.v. Local anesthesia was

injected at the experimental sites. The ani-

mals were kept in intravenous infusion of

physiologic saline. Penicillin i.m. was

injected during (320 i.u.) and after the oper-

ation (160 i.u.) for 3 days, concomitantly

with an analgesic.

All mandibular premolars and first molars

were extracted bilaterally, and after 4 months

of healing, full-thickness flaps were elevated

in the edentulous alveolar ridges in the right

and left sides of the mandible. Two implant

sites were prepared, one in the premolar and

one in the molar regions. Implants, 10 mm

long and 4 mm in diameter (CLC Conic;

CLC Scientific, Vicenza, Italy), were installed

with the shoulder placed at the level of the

buccal alveolar bony crest (Fig. 1a). Four dif-

ferent types of healing abutments were posi-

tioned on the top of each implant, three of

which were made of PEEK. They were

divided into two groups, the first including (i)

titanium (Ti; Fig. 1b) and (ii) PEEK bonded to

a base of titanium (Ti-P; Fig. 2a), randomly

positioned in the premolar region. The sec-

ond group included (iii) pure PEEK (P; Fig. 2b)

and (iv) PEEK roughened with a burr (P-R;

Fig. 1c), randomly positioned in the molar

region. Finally, the flaps were sutured to

allow a non-submerged healing (Fig 1d).

Wounds were checked three times per

weeks. Abutment cleaning was performed

throughout the entire duration of the

experiment, three times per week as well.

After 4 months of healing, the dogs were

sacrificed with an overdose of 3% pentobarbi-

tal sodium, and potassium chloride was sub-

sequently administered.

Histological preparation

The mandibles were removed and then main-

tained in a solution of 4% formaldehyde.

Block sections, each containing one implant,

were prepared and dehydrated in a series of

graded ethanols and subsequently embedded

in resin (Technovit� 7200 VLC; Kulzer,

Friedrichsdorf, Germany). Each block was cut

in a bucco-lingual plane using a diamond

band saw fitted in a precision slicing

machine (Apparatebau; Exakt�, Norderstedt,

Germany). One central section was selected

and reduced to a thickness of about 50 lm

using a cutting–grinding device (Apparate-

bau). The histological slides were stained

with toluidine blue and examined under a

(a) (b)

(c) (d)

Fig. 1. (a) The implants were installed with the shoulder placed at the level of the buccal alveolar bony crest. (b)

Abutment in titanium placed on the implant. (c) Abutment in polyetheretherketone (PEEK) roughened with a burr

placed on the implant. (d) Flaps sutured around an abutment in pure PEEK.

2 | Clin. Oral Impl. Res. 0, 2016 / 1–5 © 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Rea et al �PEEK as abutment material

standard light microscope for histometric

analysis.

Histological evaluation

In an Eclipse Ci microscope (Nikon Corpora-

tion, Tokyo, Japan) equipped with a digital

video camera (Nikon mod. DS-Fi1; Nikon

Corporation) connected to a computer, the

following landmarks were identified at the

buccal and lingual aspects (Fig. 3): (PM) top

of the peri-implant mucosa at the buccal and

lingual aspects; (JE) end of junctional epithe-

lium; (C) top of the adjacent bony crest; (B)

coronal extension of osseointegration; (IS)

shoulder of the implant. The following mea-

surements were performed: the distances

between IS and C (IS-C), IS and B (IS-B), PM

and IS (PM-IS), and PM-JE. Moreover, the

residual bone defect and the distances PM-B

and JE-B were calculated.

Data analysis

Mean values and standard deviations (SD) as

well as 25th, 50th (median), and 75th per-

centiles were calculated for each outcome

variable.

The statistical evaluations were performed

separately between Ti and Ti-P, to test the

influence of the use of bonded PEEK on mar-

ginal healing, as well as between P and P-R,

to test the influence on marginal healing of a

roughened prepared PEEK surface.

The Wilcoxon test for paired observations

was applied for statistical analysis using the

IBM SPSS Statistics V.19 (IBM Inc. Chicago,

IL, USA). The level of significance was set at

a = 0.05.

Results

Histological evaluation

All implants were integrated so that an n = 6

was obtained for all evaluations.

Table 1 reports the data on hard tissue and

Table 2 the data on soft tissues, both buc-

cally and lingually. Only mean values �SD

at the buccal aspects are reported in the text.

Examples of healing are reported in the histo-

logical slides in Fig. 4.

Titanium (Ti) vs. PEEK material bonded to abase made of titanium (Ti-P)

At the buccal aspect, IS-C and IS-B were

0.3 � 0.4 mm and 1.0 � 1.0 mm at Ti and

1.0 � 0.3 mm and 1.1 � 0.5 mm at Ti-P

sites, respectively. The difference was statis-

tically significant only for IS-C.

PM-IS and PM-B were 3.2 � 0.7 and

4.2 � 0.4 mm at Ti and 3.1 � 0.5 and

4.2 � 0.7 mm at Ti-P, respectively.

PM-JE and JE-B were 2.9 � 0.6 and

1.2 � 0.9 mm at Ti abutment and 2.5 � 0.4

and 1.7 � 0.6 mm at Ti-P abutment, respec-

tively. None of these differences was statisti-

cally significant.

PEEK (P) vs. PEEK roughened (P-R)

At the buccal aspect, IS-C and IS-B were

1.0 � 1.0 and 1.6 � 1.7 mm at P abutment

and 0.6 � 0.6 and 1.3 � 0.8 mm at P-R abut-

ment, respectively. None of the differences

was statistically significant.

PM-IS was 3.0 � 1.2 and 4.6 � 1.3 mm at

P abutment and 2.4 � 0.7 and 3.7 � 1.2 mm

at P-R abutment, respectively. None of the

differences was statistically significant.

PM-JE and JE-B were 3.0 � 0.3 and

1.7 � 1.2 mm at P abutment and 2.1 � 0.3

and 1.6 � 0.9 mm at P-R abutment, respec-

tively. None of the differences was statisti-

cally significant.

Discussion

In the present animal study, soft and hard tis-

sue integration of titanium and PEEK

(polyetheretherketone) healing implant abut-

ments, pure or roughened as well, was

assessed after 4 months.

A higher resorption of the bony crest was

observed at the PEEK bonded to a base made

of titanium abutments compared to those of

commercially pure titanium. However, similar

dimensions of the peri-implant mucosa width

and similar locations of the soft tissues in rela-

tion to the implant shoulder were observed.

No statistically significant differences were

seen in the outcomes when the pure PEEK

was compared with the roughened PEEK abut-

ments. The mean apical extension of the junc-

tional epithelium did not exceed the implant

margin at any of the abutment types used.

The peri-implant soft tissue represents a

protective seal guaranteeing homeostasis of

the implant/tissue interface. To examine

tissue integration to four different types of

abutment materials, namely titanium,

aluminum-based ceramics, gold alloy, and

dental porcelain, an experimental study

was performed in dogs (Abrahamsson et al.

1998). It was demonstrated that the quality

of the attachment between the mucosa and

the implant abutments was influenced by the

quality of the abutment materials. The

(a) (b)

Fig. 2. (a) Abutment in polyetheretherketone (PEEK) bonded to a base of titanium; (b) Abutment in pure PEEK.

Fig. 3. Diagram illustrating the landmarks for the histo-

logical evaluation. PM, top of the peri-implant mucosa;

(C) top of the adjacent bony crest; (IS) shoulder of the

implant; (B) coronal extension of osseointegration.

© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 3 | Clin. Oral Impl. Res. 0, 2016 / 1–5

Rea et al �PEEK as abutment material

barrier epithelium and the marginal bone

level were found to extend to a more apical

position at cast-to (gold alloy and dental

porcelain) than at c.p. Ti- and aluminum-

based ceramic abutments at 6 months of

healing. These results indicate that the heal-

ing at cast-to abutments was inadequate and

that the apical shift of barrier epithelium

established a mucosal seal that extended api-

cal to the abutment/fixture border, that is in

contact with the titanium surface of the

implant. In the present experiment, on the

contrary, the junctional epithelium did not

extend apically the implant margin, being

the mean distance PM-IS higher than that of

PM-JE at all types of abutment used.

In another animal study (Welander et al.

2008), the healing to abutments made of gold

alloy was different compared to that to tita-

nium and ceramic (ZrO2) abutments. While

the soft tissue dimensions at Ti- and ZrO2

abutments remained stable between 2 and

5 months of healing, at gold alloy abutment

sites, an apical shift of the barrier epithelium

and the marginal bone was observed. These

studies showed that abutments made from

titanium, aluminum-based ceramics, and zir-

conium do not interfere with an optimal soft

tissue integration and establishing proper tis-

sue dimensions.

For more than 20 years, PEEK biocompati-

bility has been demonstrated (for review see

Utzschneider et al. 2010) and several studies

have been documented the successful clinical

performance of PEEK in orthopedic surgery

(Brantigan et al. 2004; Toth et al. 2006). Due

to its low modulus of elasticity, excellent

chemical stability, resistance to radiation

used in sterilization procedures, and trans-

parency to radio waves, compatibility with

reinforcing agents PEEK as a semi-crystalline

polymer is considered the best alternative

Table 1. Histological measurements of hard tissue dimensions in millimeters. (n = 6)

IS-C IS-B Residual bone defect

b l b l b l

PremolarsTitanium Mean (SD) 0.3 (0.4) �0.4 (0.8) 1.0 (1.0) 0.9 (1.4) 0.7 (1.0) 1.3 (1.4)Ti Median (25th; 75th) 0.3* (0.1; 0.5) �0.2 (�0.4; 0.0) 0.9 (0.3; 1.1) 0.3 (0.1; 0.7) 0.2 (0.0; 1.3) 0.8 (0.2; 2.0)Titanium–PEEK Mean (SD) 1.0 (0.3) 0.4 (1.0) 1.1 (0.5) 0.6 (0.7) 0.1 (0.3) 0.1 (0.6)Ti-P Median (25th; 75th) 1.1* (0.9; 1.2) 0.5 (0.1; 0.9) 1.1 (0.9; 1.2) 0.4 (0.1; 0.6) 0.0 (0.0; 0.0) 0.0 (0.0; 0.0)

MolarsPEEK Mean (SD) 1.0 (1.0) 0.2 (1.0) 1.6 (1.7) 0.8 (1.0) 3.0 (1.2) 2.3 (1.2)P Median (25th; 75th) 1.0 (0.4; 1.2) �0.1* (�0.3; 0.7) 1.0 (0.3; 3.0) 0.3 (0.0; 1.6) 2.9 (2.7; 3.1) 2.5 (2.2; 3.0)PEEK roughened Mean (SD) 0.6 (0.6) 0.8 (0.9) 1.3 (0.8) 1.3 (0.5) 2.4 (0.7) 1.8 (0.9)P-R Median (25th; 75th) 0.6 (0.3; 0.8) 0.8* (0.1;1.6) 1.2 (0.6; 1.9) 1.4 (1.1; 1.7) 2.7 (1.9; 3.0) 1.9 (1.4; 2.3)

B, coronal end of osseointegration; C, top of the bony crest. IS, implant shoulder.Mean values (SD, standard deviations) and Medians (25th and 75th percentiles).The implant shoulder was placed at the level of the buccal bone crest so that positive values for IS-C indicate loss of bone.*p < 0.05.

Table 2. Histological measurements of soft tissue dimensions in millimeters. (n = 6)

PM-IS PM-B PM-JE JE-B

b l b l b l b l

PremolarsTitanium Mean (SD) 3.2 (0.7) 2.7 (0.8) 4.2 (0.4) 3.6 (1.4) 2.9 (0.6) 2.3 (0.3) 1.2 (0.9) 1.3 (1.3)Ti Median (25th; 75th) 3.2 (2.8; 3.7) 2.3 (2.3; 2.9) 4.1 (3.9; 4.3) 3.1 (2.7; 4.2) 2.9 (2.5; 3.3) 2.4 (2.2; 2.4) 1.0 (0.5;1.7) 0.7 (0.4; 1.8)Titanium–PEEK Mean (SD) 3.1 (0.5) 3.1 (1.0) 4.2 (0.7) 3.7 (1.1) 2.5 (0.4) 2.7 (0.8) 1.7 (0.6) 1.0 (0.7)Ti-P Median (25th; 75th) 3.1 (2.8; 3.2) 3.4 (2.5; 3.8) 4.2 (3.7; 4.8) 4.0 (2.9; 4.3) 2.6 (2.4; 2.7) 2.9 (2.5; 3.2) 1.8 (1.3; 2.1) 0.9 (0.8; 0.9)

MolarsPEEK Mean (SD) 3.0 (1.2) 2.3 (1.2) 4.6 (1.3) 3.1 (0.9) 3.0 (0.3) 2.1 (0.6) 1.7 (1.2) 1.0 (0.6)P Median (25th; 75th) 2.9 (2.7; 3.1) 2.5 (2.2; 3.0) 4.5 (3.6; 5.2) 3.1 (2.3; 3.6) 2.9 (2.8; 3.1) 2.0 (1.8; 2.3) 1.3 (0.8; 2.0) 0.9 (0.6; 1.2)PEEK roughened Mean (SD) 2.4 (0.7) 1.8 (0.9) 3.7 (1.2) 3.1 (0.7) 2.1 (0.3) 2.2 (0.7) 1.6 (0.9) 0.9 (0.4)P-R Median (25th; 75th) 2.7 (1.9; 3.0) 1.9 (1.4; 2.3) 3.3 (2.8; 4.7) 3.2 (2.6; 3.7) 2.0 (1.9; 2.3) 2.4 (1.6; 2.7) 1.3 (0.8; 2.3) 0.9 (0.7; 1.2)

B, coronal end of osseointegration; IS, implant shoulder; PM, top of the peri-implant mucosa.Mean values (SD, standard deviations) and Medians (25th and 75th percentiles).P < 0.05. None of these differences was statistically significant.

(a) (b)

Fig. 4. Ground sections illustrating examples of healing at (a) titanium abutment; (b) pure polyetheretherketone

abutment. Images originally grabbed at 920. Toluidine blue stain.

4 | Clin. Oral Impl. Res. 0, 2016 / 1–5 © 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Rea et al �PEEK as abutment material

material to titanium for spinal fusion cage

implants (Sobieraj et al. 2010).

While an evaluation of oral mucosal inte-

gration at implant abutments made of PEEK

has not been performed in an animal model

previously, a clinical study on humans was

instead carried out. Sixteen patients were

included in a prospective trial, and soft and

hard tissue responses to titanium and poly-

mer abutments were evaluated over a 3-

month period (Koutouzis et al. 2011). At

implant installation, healing abutments,

made either of titanium or of PEEK, were

placed transmucosally. Clinical and radio-

graphic examinations were performed at

implant installation and after 3 months to

assess changes of marginal bone levels and

soft tissue dimensions. No adverse events

were experienced. Moreover, the outcomes

indicated that PEEK abutments did not

increase the risk for marginal bone loss and

soft tissue recession during the initial healing

period.

The present study has, indeed, confirmed

these positive healing outcomes and hence

renders the PEEK to be used for healing abut-

ments as c.p. titanium abutments.

In conclusion, the present animal experi-

ment showed that, even though a higher

resorption of the buccal bone crest was found

at the PEEK bonded to titanium compared to

the titanium abutment sites, similar dimen-

sions of the peri-implant mucosa and similar

locations of the soft tissues in relation to the

implant shoulder were observed. When the

outcomes between pure and roughened PEEK

were compared, no statistically significant

differences were found. The junctional

epithelium did not extend apically to the

implant margin at any of the abutment used.

Acknowledgements: This study has

been supported by a CLC Scientific, Vicenza,

Italy, by ARDEC, Ariminum Odontologica

SRL, Rimini, Italy and by the Clinical

Research Foundation (CRF) for the Promotion

of Oral Health, Brienz, Switzerland.

Conflicts of interests

Dr Claudio Soldini declares a conflict or inter-

est with the implant brand used in this study

as co-owner for the company CLC Scientific.

All the other authors declare no conflict of

interest.

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© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 5 | Clin. Oral Impl. Res. 0, 2016 / 1–5

Rea et al �PEEK as abutment material