Frank Schwarz Comparison of naturally occurring and

Monika Herten
Martin Sager
ligature-induced peri-implantitis bone
Katrin Bieling defects in humans and dogs
Anton Sculean
Jürgen Becker

Authors’ affiliations: Key words: animal study, dental implant, ligature-induced, naturally occurring, peri-
Frank Schwarz, Monika Herten, Katrin Bieling,
implantitis
Jürgen Becker, Department of Oral Surgery,
Heinrich Heine University, Düsseldorf, Germany
Martin Sager, Animal Research Institute, Heinrich Abstract
Heine University, Düsseldorf, Germany
Anton Sculean, Department of Periodontology, Objectives: The aim of the present study was to evaluate and compare naturally occuring
Radboud University Medical Center, Nijmegen, and ligature-induced peri-implantitis bone defects in humans and dogs.
The Netherlands
Material and Methods: Twenty-four partially and fully edentulous patients undergoing
Correspondence to: peri-implant bone augmentation procedures due to advanced peri-implant infections were
Priv. Doz. Dr Frank Schwarz included in this study (n ¼ 40 implants). Furthermore, peri-implantitis was induced by
Department of Oral Surgery
Heinrich Heine University ligature placement and plaque accumulation in five beagle dogs for three months
Westdeutsche Kieferklinik Moorenstr. 5 40225 following implant insertion (n ¼ 15 implants). The ligatures were removed when about 30%
Düsseldorf, Germany
Tel.: ( þ ) 49 211 8118149
of the initial bone was lost. During open flap surgery, configuration and defect
Fax: ( þ ) 49 211 1713542 characteristics of the peri-implant bone loss were recorded in both humans and dogs.
e-mail: info@frank-schwarz.de Results: Open flap surgery generally revealed two different classes of peri-implant bone
defects. While Class I defects featured well-defined intrabony components, Class II defects
were characterized by consistent horizontal bone loss. The allocation of intrabony
components of Class I defects regarding the implant body allowed a subdivision of five
different configurations (Classes Ia–e). In particular, human defects were most frequently
Class Ie (55.3%), followed by Ib (15.8%), Ic (13.3%), Id (10.2%), and Ia (5.4%). Similarly, bone
defects in dogs were also most frequently Class Ie (86.6%), while merely two out of 15
defects were Classes Ia and Ic (6.7%, respectively).
Conclusions: Within the limits of the present study, it might be concluded that
configurations and sizes of ligature-induced peri-implantitis bone defects in dogs seemed
to resemble naturally occurring lesions in humans.

Nowadays, there is considerable evidence fined as an inflammatory process that

Date:
Accepted 20 April 2006
To cite this article:
Schwarz F, Herten M, Sager M, Bieling K, Sculean A,
Becker J. Comparison of naturally occurring and ligature-
induced peri-implantitis bone defects in humans and
dogs.
Clin. Oral Impl. Res., 18, 2007; 161–170
doi: 10.1111/j.1600-0501.2006.01320.x
Copyright r Blackwell Munksgaard 2006
supporting the view that microbial coloni-
zation plays a major role in the etiology of
peri-implant infections (Mombelli et al.
1988; Becker et al. 1990; Alcoforado et al.
1991). The host response to biofilm forma-
tion on implant surfaces includes a series of
inflammatory reactions that initially occur
in the soft tissue (Hultin et al. 2002).
Subsequently, peri-implant mucositis is a
term used to describe reversible inflamma-
tory reactions in the mucosa adjacent to an
implant, whereas peri-implantitis is de-
affects the tissues around an osseointe-
grated implant in function, resulting in a
loss of supporting alveolar bone (Albrekts-
son & Isidor 1994). The prevalence of peri-
implantitis is difficult to estimate but may
vary between 2% and 10% of all implants
inserted (Esposito et al. 1998; Mombelli &
Lang 1998). In recent years, an experimen-
tal peri-implantitis model was developed
and used in both dogs and monkeys in
order to study the pathogenesis of peri-
implantitis. In this model, peri-implantitis

161

Schwarz et al . Peri-implantitis bone defects in humans and dogs
lesions were induced by terminating the
plaque control regimen, and placement of
cotton ligatures submarginally around im-
plants. This resulted in progressive inflam-
mation and a rapid breakdown of peri-
implant soft and hard tissues (Lindhe
et al. 1992; Lang et al. 1993; Schou et al.
1993; Marinello et al. 1995; Baron et al.
2000; Zitzmann et al. 2004). Based on
these observations, it has been assumed
that the removal of bacterial plaque bio-
films seems to be a prerequisite for the
therapy of peri-implant infections (Mom-
belli & Lang 1994). Accordingly, ligature-
induced animal models have also been used
in order to evaluate several treatment ap-
proaches such as access flap surgery, deb-
ridement and chemical conditioning of the
implant surface, topical or systemic anti-
biotic and/or antimicrobial therapy, and
bone regenerative procedures at both non-
submerged and submerged implants (Erics-
son et al. 1996; Persson et al. 1996;
Hürzeler et al. 1997; Schou et al. 2003a,
2003b, 2003c, 2004). Even though clini-
cally healthy peri-implant tissues were
obtained and maintained in most of these
studies, the amount of documented bone
regeneration and re-osseointegration varied
considerably. In most of these studies, the
re-establishment of osseointegration has
even been questioned (Schou et al. 2004).
Several factors have been discussed to ex-
plain the lack of re-osseointegration at fail-
ing implants. First of all, decontamination
of structured implant surfaces is difficult to
achieve, as conventional treatment ap-
proaches, including plastic curettes, so-
nic/ultrasonic scalers and air-powder
flow, have been proven to be insufficient
for obtaining a complete removal and elim-
ination of both plaque biofilms and bacteria
on roughened implant surfaces (Kreisler et
al. 2005; Schwarz et al. 2005a). Second,
the extent of an implant surface, which has
been previously exposed to bacterial plaque
biofilm formation, to serve as a sufficient
base to establish new bone-to-implant con-
tact following decontamination is still un-
known (Baier & Meyer 1988; Sennerby &
Lekholm 1993; Schwarz et al. 2005a).
Previous studies, however, have also
pointed out that defect morphology plays
a major role in the healing process follow-
ing guided tissue regeneration of intrabony
periodontal defects. In particular, it was
demonstrated that the deeper the defect,
162 | Clin. Oral Impl. Res. 18, 2007 / 161–170
the greater was the amount of clinical
improvement, while the wider the defect,
the lower were the attachment and bone
gains (Garrett et al. 1988; Tonetti et al.
1993, 1996). Furthermore, it has also been
shown that the number of residual bony
walls was related to the outcomes of var-
ious regenerative treatment approaches
(Goldman & Cohen 1958; Schallhorn et
al. 1970). As mentioned above, several
animal studies attempted to evaluate pro-
cedures used for surgical treatment of peri-
implantitis bone defects. Unfortunately,
the configuration and sizes of the bone
defects were not reported in these studies
(Ericsson et al. 1996; Persson et al. 1996;
Hürzeler et al. 1997; Schou et al. 2003a,
2003b, 2003c, 2004). Furthermore, the
extent to which ligature-induced peri-im-
plant bone defects may reflect on the con-
figuration of naturally occurring peri-
implantitis bone defects in humans still
remains unknown.
Therefore, the aim of the present study
was to evaluate and compare naturally
occuring and ligature-induced peri-implan-
titis bone defects in humans and dogs.
Materials and methods
Study population
Twenty-four partially and fully edentulous
patients with moderate to advanced peri-
implantitis attending the Department of
Oral Surgery, Heinrich Heine University,
Düsseldorf, Germany, for peri-implant
bone augmentation procedures were in-
cluded in this study. The patient popula-
tion consisted of eight men and 16 women
(mean age 54.2
13.4 years) exhibiting a
total of n ¼ 40 implants. All patients had
been previously treated by a single course
of nonsurgical instrumentation of respec-
tive titanium implants using plastic cur-
ettes (Straumann AG, Waldenburg,
Switzerland), followed by pocket irrigation
with a 0.2% chlorhexidine digluconate
s
solution (Corsodyl , GlaxoSmithKline
Consumer Healthcare, Bühl, Germany)
(CHX) and subgingival application of
s
CHX gel 0.2% (Corsodyl Gel, GlaxoS-
mithKline Consumer Healthcare) or an
s
Er:YAG laser (KEY 3 , KaVo, Biberach,
Germany) (Schwarz et al. 2005b). The
criteria needed for inclusion were as fol-
lows: (1) the presence of at least one screw-
16000501, 2007, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1600-0501.2006.01320.x by Readcube (Labtiva Inc.), Wiley Online Library on [28/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
type implant with a probing depth 46 mm,
(2) no implant mobility, (3) the presence of
keratinized peri-implant mucosa, (4) no
signs of acute periodontitis, (5) a good level
of oral hygiene (plaque index o1 (Löe
1967)), and (6) non-smoker. Hollow cylin-
der implants were excluded from the study.
Each patient was given a detailed descrip-
tion of the procedure and was required to
sign an informed consent before participa-
tion. The study was in accordance with the
Helsinki Declaration of 1975, as revised in
2000 and all participants signed informed
consent forms. The study protocol was
approved by the ethical committee of the
Heinrich Heine University. During open
flap surgery, configuration and defect char-
acteristics of the peri-implant bone loss
were recorded.
Animals
Five 6-year-old female beagle dogs (mean
weight 16.3 kg) were used in the study. All
animals exhibited a fully erupted perma-
nent dentition. During the experiment, the
dogs were fed once per day with soft-food
diet and water. Animal selection, manage-
ment, and surgery protocol were approved
by the Animal Care and Use Committee of
the Heinrich Heine University and the
Bezirksregierung Düsseldorf.
Ligature-induced peri-implantitis
The experimental segment of the study
started after an adaption period of 4 weeks.
The study was performed in three surgical
phases. In the first phase, extraction of the
mandibular 2nd, 3rd, 4th premolar, and 1st
molar (P2-M1) was performed bilaterally.
After 4 months of healing, surgical implan-
tation of screw-typed implants was per-
formed according to a one-stage healing
procedure during the second phase. Follow-
ing implant insertion, a plaque control
program was initiated. Tooth and implant
cleaning were maintained by the use of a
toothbrush once a day for 3 months. Radio-
graphs were obtained before and immedi-
ately after tooth extraction as well as
immediately after implant insertion. After
3 months of healing, cotton ligatures were
placed in a sub-marginal position around
each implant according to a method de-
scribed previously (Lindhe et al. 1992), and
the plaque control regimen was termi-
nated. In brief, ligatures were forced into
a position directly apical of the gingival

margin. Subsequently, a ‘pocket’ was cre-
ated that enabled the establishment of a
subgingival microflora. The ligatures were
exchanged once every 3 weeks and re-
moved when approximately 30% of the
initial bone support was lost based on
evaluation using standardized radiomicro-
graphs (approximately 3 months) (distance
between the implant shoulder and the
marginal bone level). Four weeks after
ligature removal, the defects were ran-
domly instrumented either (a) non-surgi-
cally or (b) surgically (n ¼ 15 implants
each) using different treatment approaches
according to a split-mouth design. The
clinical, radiographic, and histologic results
after 3 months of healing will be reported
elsewhere. During open flap surgery and
following removal of granulation tissue in
group b (n ¼ 15 defects), configuration and
defect characteristics of the ligature-in-
duced peri-implant bone loss were re-
corded.
Surgical procedure – dogs
After sedation with acepromazine
(0.17 mg/kg body weight), the dogs were
anesthetized with 21.5 mg/kg thiopental-
sodium. For all surgical procedures, inhala-
tion anesthesia was administered using
s(a-v/o)
i(v/o)
s(b-v/o)
d s(c-v/o)
i(v/o)
s(c-m)
i(m)
i(d)
i(v/o)
s(c-v/o)
Fig. 1. Illustrations of Class I defects. (a) Class Ia – vestibular/oral view; (b) Class Ia – occlusal view; (c) Class Ib – occlusal view; (d) Class Ic – occlusal view; (e) Class Id –
occlusal view; (f) Class Ie – occlusal view. Arrows, s – component; circles, i – components.
Schwarz et al . Peri-implantitis bone defects in humans and dogs
oxygen and nitrous oxide and isoflurane.
To maintain hydration, all animals re-
ceived a constant-rate infusion of lactated
Ringer’s solution while anesthetized. In
the first surgery, P2-M1 were carefully
removed after reflection of full-thickness
mucoperiosteal flaps and tooth separation.
After wound closure by means of matress
sutures, the sites were allowed to heal for
4 months. Prophylactic administration of
clindamycine (11 mg/kg body weight,
s
Cleorobe , Pharmacia Tiergesundheit, Er-
langen, Germany) was performed intra-
and postoperatively for 10 days. In the
second surgery, bilateral vestibular inci-
sions were made and full-thickness muco-
periosteal flaps were elevated to expose the
respective sites for implant placement in
the mandible. Three surgical implant sites
were prepared bilaterally, at a distance of
10 mm apart, using a low-trauma surgical
technique under copious irrigation with
sterile 0.9% physiological saline. Three
sand-blasted and acid-etched (SLA) tita-
nium implants were placed in each side of
the mandible (narrow neck, + 3.3 mm,
s
length 10 mm, ITI Dental Implant Sys-
tem, Straumann AG) (n ¼ 6 implants per
dog) according to a one-stage procedure and
covered with healing abutments (height:
s(c-v/o)
b i(v/o)
e s(c-v)
i(v)
s(c-d) s(c-m) s(c-d)
i(m)
i(d)
i(o)
s(c-o)
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s
2 mm, ITI Dental Implant System, Strau-
mann AG). The implants were inserted in
a way so that the borderline between the
bony and transmucosal part (BTB) of the
implant coincided with the bone crest.
Following irrigation, mucoperiosteal flaps
were repositioned and primary wound clo-
sure was achieved with consecutive resorb-
able 5 polyglygolic acid sutures (Resorba,
Nürnberg, Germany). The surgical proce-
dure of phase three will be reported else-
where. In brief, bilateral vestibular
incisions were made and full-thickness
mucoperiosteal flaps were reflected to
expose the respective peri-implant bone
defects.
Configuration assessment of peri-implant
bone defects
During open flap surgery in both humans
and dogs, the following measurements
were carried out by one previously cali-
brated examiner using a periodontal probe
(PCP 12, Hu-Friedy Co., Chicago, Illinois,
USA) (Figs 1 and 2):
s(a-v/o): vertical dehiscence-type
component of the defect, measured as
the linear mid-vestibular/-oral (v/o)
distance from BTB to the alveolar
s(c-v/o)
c i(v/o)
i(m)
i(d)
s(c-m) s(c-d)
f s(c-v)
i(v)
s(c-m) s(c-d)
i(m)
i(d)
i(o)
s(c-o)
163 | Clin. Oral Impl. Res. 18, 2007 / 161–170
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Schwarz et al . Peri-implantitis bone defects in humans and dogs

100

90

80

s(a) 70

Frequency [%]
60 Humans - upper jaw
Humans - lower jaw
50
Humans - total
40 Humans - lower jaw

30

20

10

0
1a 1b 1c 1d 1e 1l
Defect classes
Fig. 2. Illustration of Class II defect – vestibular/oral Fig. 3. Frequency distribution of different defect classes in humans and dogs.
view.
8.0

7.0
bone crest;
s(b-v/o): horizontal dehiscence-type
6.0
component of the defect, measured as
the maximum linear distance of vestib-
ular/oral (v/o) bone walls; 5.0
Humans - upper jaw
s(c-v/o): circumferential component of
mm

Humans - lower jaw

the defect, measured as the linear mid- 4.0
Humans - total
vestibular/-oral (v/o) distance from the Humans - lower jaw
implant surface to the inner surface of 3.0
the alveolar bone. In case of a dehis-
cence component, the outer surface of
2.0
the alveolar bone served as a landmark
(negative values ¼ implant body ex-
ceeded outer surface of the alveolar 1.0
bone);
s(c-m): circumferential component of 0.0
s( s( s( s s s s
the defect, measured as the linear dis- a- b- a- s(b- (c- (c- (c- (c- i(v) i(m i(d) i(o) Cla
v) v) o) o) v) m d) o) ) ss
) II
tance from the mesial (m) bone wall of -s
(a
the defect to the implant surface; )
Components
s(c-d): circumferential component of
the defect, measured as the linear dis- Fig. 4. Configuration assessment of peri-implantitis bone defects: mean values (
SD in mm) of different
tance from the distal (d) bone wall of components as measured intra-operatively in humans and dogs.
the defect to the implant surface;
i(v/o, m, d): intrabony component of Statistical analysis s(c-d), i(v/o, m, d), and s(a) values within
the defect, measured as the linear dis- The statistical analysis was performed groups. The a error was set at 0.05.
tance from the alveolar bone crest to using a commercially available software
s
the bottom of the defect (v/o, m, d); program (SPSS 14, SPSS Inc. Chicago,
and IL, USA). The mean values of all para- Results
s(a): supraalveolar component of the meters were calculated. Normal distribu-
Configuration assessment of peri-implant
defect, measured as the maximum lin- tion was looked for by the Kolmogorov– bone defects
ear mesial or distal (m, d) distance from Smirnow test. The paired t-test was used to Individual scores of s(a-v/o), s(b-v/o), s(c-v/
BTB to the alveolar bone crest. compare s(a-v), s(b-v), s(c-v), s(c-o), s(c-m), o), s(c-m), s(c-d), i(v/o, m, d), and s(a) in

164 | Clin. Oral Impl. Res. 18, 2007 / 161–170

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Schwarz et al . Peri-implantitis bone defects in humans and dogs

both humans and dogs are presented in

Tables 1 and 2. Open flap surgery generally
revealed two different classes of peri-im-
plant bone defects (Figs 1–6). While Class I
defects featured well-defined intrabony
components, Class II defects were charac-
terized by consistent horizontal bone loss,
identifiable as a supra-alveolar exposition
of structured implant surface areas (Figs 1
and 2). The allocation of intrabony compo-
nents of Class I defects regarding the im-
plant body allowed a subdivision of five
different configurations (Fig. 1a–f). In par-
ticular, Class Ia defects featured a com-
bined horizontal and vertical loss of the
adjacent vestibular alveolar bone, leading to
dehiscence-type defect configurations (Fig.
5a and b). In three cases (patients nos. 19
and 21), the implant body exceeded the
outer surface of the alveolar bone, leading
to negative s(c-v) values (Table 1a). Open
flap surgery merely revealed Class Ia de-
fects exhibiting the dehiscence-type com-
ponent at the vestibular aspect of the
alveolar crest (Fig. 1a and b). Class Ib
defects generally exhibited higher s(b-v)
values than Class Ia defects. Additionally,
Class Ib defects were characterized by
clearly identifiable s(c-m) and s(c-d) com-
Fig. 5. Clinical and radiological view of ligature-induced peri-implantitis bone defects in dogs. (a, b) Class Ia defect ponents (Figs 1c, 6a and b). Measurement
(No. 2-034); (c, d) combined Class Ic þ II defect (No. 1-036); (e, f) combined Class Ie þ II defect (No. 5-046).

Fig. 6. Clinical and radiological view of naturally occurring peri-implantitis bone defects in humans. (a, b) Class Ib defect (No. 9-022); (c, d) combined Class Ie þ II defect
(No. 2-023); (e, f): Combined Class Ie þ II defect (No. 15-047); (g, h) combined Class Ie þ II defect (No. 12-024); (i, j) Class Ie defect (No. 20-021)

165 | Clin. Oral Impl. Res. 18, 2007 / 161–170

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Schwarz et al . Peri-implantitis bone defects in humans and dogs

of both s(c-m) and s(c-d) generally exhib-
ited comparable values (P40.05, respec-
tively) (Tables 1a and b). In contrast,
Class Ic defects revealed additional s(c-o)
components, which seemed to be within
the range of respective s(c-v) values
(P40.05, respectively). However, the cir-
cumferential bony defect did not result in a
dehiscence-type defect at the oral aspects of
the alveolar crest (Figs 1d, 5c and d). Con-
sequently, Class Id defects exhibited higher
s(c-o) values than Class Ic defects, result-
ing in a dehiscence-type defect at the oral
aspect of the alveolar bone (Po0.01, re-
spectively) (Fig. 1e). In these cases, s(a-o)
and s(b-o) values seemed to be within the
range of respective s(a-v) and s(b-v) values
(P40.05, respectively). However, s(c-o)
values were generally higher than respec-
tive s(c-v) values (Po0.01, respectively)
(Tables 1a and b). In contrast, Class Ie
defects exhibited clearly identifiable s(c-v),
s(c-o), s(c-m), and s(c-d) components
but without dehiscence-type defects at
both the oral and lingual aspects of the
alveolar crest (Figs 1f, 5e and f, 6c–h).
Even though Class Ie defects predomi-
nantly exhibited comparable s(c-v) and
s(c-o) as well as s(c-m) and s(c-d) values,
one implant revealed isolated s(c-d) and

Table 1a. Distribution, configuration, and sizes (mm) of naturally occuring peri-implantitis bone defects in humans: upper jaw (n ¼ 31
defects)
No. Regio Type Age PR Class I s(a-v) s(b-v) s(a-o) s(b-o) s(c-v) s(c-m) s(c-d) s(c-o) i(v) i(m) i(d) i(o) Class II s(a)
2 013 BRA 4 O-TC e 2 2 2 2 6 6 6 6 þ 4
2 015 BRA 4 O-TC e 2 3 3 2 6 7 7 6 þ 3
2 023 BRA 4 O-TC e 1 2 2 2 1 3 3 1 þ 4
2 025 BRA 4 O-TC e 2 2 2 2 5 6 7 6 þ 3
3 021 BRA 6 S-C d 8 6 6 6 2 3 3 3 1 2 2 1 
9 022 REP 8 S-C b 3 5 1 2 2 2 2 2 
10 014 MTX 4 O-BA e 1 2 2 0 1 3 3 0 þ 1
10 015 MTX 4 O-BA e 1 2 2 0 1 3 1 0 þ 1
10 016 MTX 4 O-BA e 0 2 2 0 1 3 3 0 þ 1
11 024 MTX 3 O-BA e 0 2 2 0 0 2 2 0 þ 1
11 025 MTX 3 O-BA e 0 2 2 0 0 2 2 0 þ 1
11 026 MTX 3 O-BA e 1 2 2 0 1 2 2 0 þ 1
12 024 ITI 1 NP e 2 3 2 2 3 4 3 2 þ 2
13 025 ITI 2 NP e 0 2 0 0 0 1 0 0 
14 024 ITI 6 B-C e 1 0 0 0 2 0 0 0 þ 1
14 025 ITI 6 B-C e 2 0 0 0 3 0 0 0 þ 1
14 026 ITI 6 B-C e 1 0 0 0 2 0 0 0 þ 1
14 027 ITI 6 B-C e 1 0 0 0 2 0 0 0 þ 1
15 016 KSI 5 S-C b 2 6 1 2 1 3 3 2 
16 024 ITI 4 S-C d 3 6 3 5 2 3 2 3 4 4 4 4 þ 2
16 025 ITI 4 S-C d 3 6 3 4 1 3 2 3 3 4 4 3 þ 2
16 026 ITI 4 S-C d 2 6 3 4 1 3 2 4 3 4 4 3 þ 2
17 023 MTX 5 S-C c 6 6 1 2 2 1 1 2 2 2 þ 2
18 014 ITI 3 S-C b 4 4 1 2 2 0 2 2 þ 1
18 015 ITI 3 S-C b 3 4 1 2 2 0 2 2 þ 1
19 015 ITI 5 S-C c 4 5 1 2 3 1 0 3 3 2 þ 1
19 022 ITI 5 S-C c 5 5 1 2 2 2 1 2 2 2 þ 2
19 025 ITI 5 S-C c 4 5 1 2 2 1 1 3 3 2 þ 2
20 021 FRI 3 S-C e 0 0 3 2 0 0 4 4 þ 1
21 011 FRI 4 S-C a 8 2 1 0 þ 1
21 012 FRI 4 S-C a 6 2 1 0 þ 1
s s s
BRA, Brånemark System , Nobel Biocare, Göteborg, Sweden; MTX, Spline Twist (MTX) , Zimmer Dental, Freiburg, Germany; ITI, ITI (SLA, TPS) , Straumann,
s s
Waldenburg, Switzerland; KSI, KSI Bauer Schraube , KSI Bauer Schraube GmbH, Bad Nauheim, Germany; FRI, Frialit , Dentsply Friadent, Mannheim,
s
Germany; REP, Replace , Nobel Biocare, Göteborg, Sweden.

Table 1b. Distribution, configuration, and sizes (mm) of naturally occuring peri-implantitis bone defects in humans: lower jaw (n ¼ 9
defects)
No. Regio Type Age PR Class I s(a-v) s(b-v) s(a-o) s(b-o) s(c-v) s(c-m) s(c-d) s(c-o) i(v) i(m) i(d) i(o) Class II s(a)
1 044 ITI 6 S-C c 3 6 1 2 2 2 1 2 2 2 þ 4
4 044 TSV 1 O-BA e 1 2 0 0 1 4 0 0 
5 044 MTX 3 O-BA e 2 2 2 2 1 1 1 1 þ 6
6 036 TGO 3 S-C e 1 1 1 1 1 1 1 1 þ 4
7 044 FRI 3 S-C b 5 8 1 2 2 1 2 2 
8 034 CAM 5 S-C e 1 2 0 0 1 2 0 0 
15 047 BRA 5 S-C b 3 6 1 2 1 3 5 4 
22 047 CAM 3 S-C e 1 2 2 1 2 2 2 2 þ 1
23 036 CAM 2 S-C e 1 2 2 1 1 3 3 1 þ 2
s s s s
BRA, Brånemark System ; CAM, Camlog Screw Line , Camlog, Wimsheim, Germany; FRI, Frialit , Dentsply Friadent; IMZ, IMZ (Twin Plus) , Dentsply Friadent,
s s s s
Mannheim, Germany; ITI, ITI (SLA, TPS) ; KSI, KSI Bauer Schraube , KSI Bauer Schraube GmbH; MTX, Spline Twist (MTX) ; REP, Replace ; TSV, Tapered Screw
s s s
Vent , Zimmer Dental, Freiburg, Germany; TGO, Osseotite (TG) , 3i, Karlsruhe, Germany; ZLD, ZL-Duraplant (Ticer) , ZL Microdent, Breckerfeld, Germany; PR,
Prosthetic Reconstruction; S, single-tooth restoration; B, bridgework; O, overdenture; C, crown; TC, tapered crown; BA, bar attachment; NP, non-provided.

166 | Clin. Oral Impl. Res. 18, 2007 / 161–170

 16000501, 2007, 2, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1600-0501.2006.01320.x by Readcube (Labtiva Inc.), Wiley Online Library on [28/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Schwarz et al . Peri-implantitis bone defects in humans and dogs

s(c-o) components (Fig. 6i and j). Gener-
ally, s(c-v), s(c-o), s(c-m), and s(c-d) were
associated with varying intrabony defect
components. Furthermore, Class I defects
were predominantly associated with a
Class II defect component. This seemed
to be particularly true for Class Ic–e con-
figurations (Tables 1 and 2). Statistical
analysis revealed no significant differences
of mean s(a-v), s(b-v), s(c-v), s(c-o), s(c-m),
s(c-d), i(v/o, m, d), and s(a) values between
dogs (P40.05, respectively).
Comparison of peri-implant bone defects
in humans and dogs
The mean age of implants in humans was
4.1
1.4 years (Tables 1a and b). As
described above, the mean age of implants
in dogs at surgical defect examination was
6 months. Frequency distributions of Class
Ia–e and Class II defects in both humans
and dogs are summarized in Fig. 3. In
particular, naturally occuring peri-implan-
titis bone defects in humans were most
frequently Class Ie (55.3%), followed by
Class Ib (15.8%), Class Ic (13.3%), Class
Id (10.2%), and Class Ia (5.4%). Similarly,
ligature-induced peri-implantitis bone de-
fects in dogs were also most frequently of
Class Ie (86.6%). However, merely two
out of 15 defects were Classes Ia and Ic
(6.7%, respectively), while Classes Ib and
Id were not observed (Figs 5 and 6). The
mean scores of s(a-v), s(b-v), s(c-v), s(c-o),
s(c-m), s(c-d), i(v/o, m, d), and s(a) seemed
to be comparable in both humans and dogs
(Fig. 4).
Discussion
The results of the present study have in-
dicated that configurations and sizes of
ligature-induced peri-implantitis bone de-
fects in dogs seemed to resemble naturally
occurring lesions in humans. In particular,
circumferential bone loss without dehis-
cence of the adjacent alveolar crest was
the most frequently observed type of defect
configuration in both humans (55.3%) and
dogs (86.6%). In these cases, circumferen-
tial bone loss was generally associated with
a horizontal loss of the supporting alveolar
bone. As described above, the ligature-in-
duced peri-implantitis model has been
widely applied in studying the initiation,
pathogenesis, and treatment of peri-im-
plant infections (Lindhe et al. 1992;
Lang et al. 1993; Schou et al. 1993;
Marinello et al. 1995; Baron et al. 2000;
Zitzmann et al. 2004). In this context, it
must be emphasized that peri-implantitis
has been classified as a disease process
associated with microorganisms known
from chronic periodontitis (for a review,
see Mombelli 2002). Furthermore, in
many respects the bacterial profile of su-
pra- and subgingival plaque associated with
periodontitis in beagle dogs has been ob-
served to resemble that reported in human
periodontal disease (Syed et al. 1981). The
previous observation that placement of
cotton ligatures submarginally around
implants resulted in enhanced bacterial
plaque accumulation and subsequently
progressive inflammation and a rapid
breakdown of peri-implant soft and hard
tissues is in agreement with the present
results, as approximately 30% of the initial
bone support was lost within 3 months
after the first ligature placement. In this
context, it must also be emphasized that
there was a consistency in defect config-
uration and size between dogs, as evi-
denced by statistically nonsignificant
mean s(a-v), s(b-v), s(c-v), s(c-o), s(c-m),
s(c-d), i(v/o, m, d), and s(a) values. All
these data, in addition to the results of
the present study, seem to indicate, at least
in part, that the beagle dog may represent
an appropriate bacteriological model for
investigating peri-implant infections.
However, unfortunately, there are cur-
rently no data evaluating configurations
and sizes of ligature-induced peri-implant
bone defects in dogs and naturally occur-
ring lesions in humans. In particular, pre-
vious animal studies using beagle and
labrador dogs merely reported that ligatures
were removed when radiographic observa-
tion revealed an initial bone loss of approxi-
mately 30–50% (Grunder et al. 1993;
Jovanovic et al. 1993; Ericsson et al.
1996; Persson et al. 1996; Hürzeler
et al. 1997; Machado et al. 1999; Persson
et al. 1999; Wetzel et al. 1999; Machado
et al. 2000; Deppe et al. 2001; Nociti et al.
2001a, 2001b; Persson et al. 2001a, 2001b,
2004). However, a limited number of these
studies provided some clinical figures illus-
trating the defect configuration of ligature-
induced peri-implant bone loss in some
implants. Based on the limited information
attainable from these figures, it seemed
that the defects were most likely Class Ie
associated with Class II. In this context,
however, it must be queried whether these

Table 2. Distribution, configuration, and sizes (mm) of ligature-induced bone defects in dogs: lower jaw (n ¼ 15 defects)
No. Regio Type Class I s(a-v) s(b-v) s(a-o) s(b-o) s(c-v) s(c-m) s(c-d) s(c-o) i(v) i(m) i(d) i(o) Class II s(a)
1 034 ITI e 1 2 2 1 2 3 3 2 
1 035 ITI e 1 1 1 1 2 3 3 2 
1 036 ITI c 5 5 1 2 1 1 2 2 2 2 þ 5
2 034 ITI a 3 2 1 0 
2 035 ITI e 1 2 2 1 2 2 2 2 
2 036 ITI e 2 2 2 1 2 3 3 2 þ 4
3 044 ITI e 2 2 2 1 3 6 6 6 þ 3
3 045 ITI e 1 1 1 1 2 2 2 1 
3 046 ITI e 2 2 2 1 5 6 5 3 þ 2
4 044 ITI e 1 1 1 1 1 2 2 2 þ 1
4 045 ITI e 1 1 1 1 1 2 2 2 þ 1
4 046 ITI e 1 2 1 1 2 2 2 2 þ 1
5 044 ITI e 1 1 1 1 2 2 2 2 
5 045 ITI e 1 2 1 1 2 2 2 1 
5 046 ITI e 2 2 2 1 3 3 2 2 þ 2
s
ITI, ITI (SLA) .

167 | Clin. Oral Impl. Res. 18, 2007 / 161–170

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Schwarz et al . Peri-implantitis bone defects in humans and dogs

defects might be designated as representa-
tive samples. Similarly, previous human
studies evaluating regenerative or resective
treatment of peri-implantitis lesions did
not report specific defect configurations
(Behneke et al. 2000; Haas et al. 2000;
Khoury & Buchmann 2001; Romeo et al.
2005). However, Behneke et al. (2000)
merely included progressive crater-like or
saucer-shaped peri-implantitis bone de-
fects, which were equivalent to Class Ie
defects of the present study. Furthermore,
defect depth (distance from the implant top
surface to the fundus of the defect – DD),
bone level (distance from the implant’s top
surface to the most coronal point of the
alveolar crest – BL) as well as defect width
(distance between the most coronal point of
the alveolar crest and the implant surface –
DW) were measured intraoperatively.
According to these measurements, DD
seemed to be equivalent to i(v/o, m, d),
BL to s(a), and DW to s(c-v), s(c-o), s(c-m),
and s(c-d). Regarding the mean values, BL
(3.8 mm) and DW (1.9 mm) seemed to be
within the range of equivalent parameters
measured in the present study. However,
the mean DD (6.9 mm) tended to be higher
than i(v/o, m, d) (Behneke et al. 2000).
Similarly, Haas et al. (2000) merely in-
cluded crater-like defects exhibiting an in-
trabony pocket depth of more than 6 mm
and only narrow vertical bone loss. Unfor-
tunately, the authors did not report specific
defect configurations (Haas et al. 2000).
When interpreting the present results, it
has also been noted that naturally occur-
ring peri-implantitis bone defects in
humans also exhibited conspicuous percen-
tages of Class Ib (15.8%), Class Ic (13.3%),
Class Id (10.2%), and to a minor extent
Class Ia (5.4%) configurations. This slight
discrepancy with respect to configuration
of naturally occurring and ligature-induced and sizes of ligature-induced peri-implanti-
peri-implantitis bone defects may be re- tis bone defects in dogs seemed to resemble
lated to the individual prosthetic recon- naturally occurring lesions in humans.
structions noted in the study population
of the present study. Indeed, it is impossi- Acknowledgements: This study was
ble to estimate to what extent the prosthe- supported by a grant of the ‘DGI –
tic reconstructions might have influenced Deutsche Gesellschaft für
plaque accumulation and subsequently Implantologie im Zahn-, Mund- und
progression of peri-implant bone loss. Kieferbereich’.
Furthermore, in three human cases, it
was observed that in comparison with
Class Ie implants, respective s(c-v) values
of Class Ia–d implants seemed to be very
low or considered negative. This observa-
tion was also supported by the observation
that both ligature-induced Class Ia and
Class Ic bone defects in dogs revealed low
s(c-v) values. Accordingly, it might be
hypothesized that the development of
peri-implantitis lesions, in particular Class
Ia and subsequently Class Ib-d defects,
might be related to the anatomy of the
alveolar bone (i.e., thickness of the vestib-
ular alveolar bone adjacent to the implant
body). In this context, it must also be
queried to what extent the implant system
might influence the development of peri-
implantitis lesions. Unfortunately, a draw-
back of the present study was the lack of
different implant systems and subse-
quently the evaluation of their specific
impact on the progression of ligature-in-
duced peri-implantitis in dogs. Therefore,
further studies are needed in order to clarify
these issues. Additional points of interest
may also be the impact of bone augmenta-
tion procedures at buccal dehiscence de-
fects on the development of Class Ia–d
configurations as well as the influence of
different defect configurations on regenera-
tion of peri-implantitis bone defects.
Within the limits of the present study, it
might be concluded that configurations

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