Tord Berglundh Morphogenesis of the peri-implant

Ingemar Abrahamsson
Maria Welander
mucosa: an experimental study in dogs
Niklaus P. Lang
Jan Lindhe

Authors’ affiliations: Key words: biologic width, dental implants, histology, morphometry, soft tissue, titanium
Tord Berglundh, Ingemar Abrahamsson, Maria
Welander, Jan Lindhe, Department of
Periodontology, The Sahlgrenska Academy at Abstract
Göteborg University, Göteborg, Sweden Purpose: The objective of the present experiment was to study the morphogenesis of the
Niklaus P. Lang, University of Berne, Berne,
Switzerland mucosal attachment to implants made of c.p. titanium.
Material and methods: All mandibular premolars were extracted in 20 Labrador dogs. After
Correspondence to: s
a healing period of 3 months, four implants (ITI Dental Implant System) were placed in the
Tord Berglundh
Department of Periodontology right and left sides of the mandible. A non-submerged implant installation technique was
The Sahlgrenska Academy at Göteborg University used and the mucosal tissues were secured to the conical marginal portion of the implants
Box 450
S-405 30 Göteborg with interrupted sutures. The sutures were removed after 2 weeks and a plaque control
Sweden program including daily cleaning of the remaining teeth and the implants was initiated.
e-mail: [email protected]
The animals were sacrificed and biopsies were obtained at various intervals to provide
healing periods extending from Day 0 (2 h) to 12 weeks. The mandibles were removed and
placed in the fixative. The implant sites were dissected using a diamond saw and processed
for histological analysis.
Results: Large numbers of neutrophils infiltrated and degraded the coagulum that
occupied the compartment between the mucosa and the implant during the initial phase of
healing. At 2 weeks after surgery, fibroblasts were the dominating cell population in the
connective tissue interface but at 4 weeks the density of fibroblasts had decreased.
Furthermore, the first signs of epithelial proliferation were observed in specimens
representing 1–2 weeks of healing and a mature barrier epithelium occurred after 6–8
weeks of healing. The collagen fibers of the mucosa were organized after 4–6 weeks of
healing.
Conclusion: It is suggested that the soft-tissue attachment to implants placed using a non-
submerged installation procedure is properly established after several weeks following
surgery.

Implant placement – submerged as well as osseointegration, from the oral cavity

non-submerged – requires an incision of (Berglundh et al. 1991).
the mucosa at the recipient site. Following Experiments in the dog (Berglundh et al.
Date: the installation of the titanium rod, the 1991; Buser et al. 1992; Cochran et al.
Accepted 10 July 2006 severed mucosa is placed in close contact 1997; Hermann et al. 2001) have docu-
To cite this article: with the implant surface. During healing of mented that the mucosal attachment to the
Berglundh T, Abrahamsson I, Welander M, Lang NP,
Lindhe J. Morphogenesis of the peri-implant mucosa: an
the soft tissue wound, an attachment is implant following 3–12 months of healing
experimental study in dogs. formed between the mucosa and the tita- was similar to that characterizing gingival
Clin. Oral Impl. Res. 18, 2007; 1–8
doi: 10.1111/j.1600-0501.2006.01380.x nium dioxide layer of the implant. Once tissue (at teeth) and was comprised of two
properly matured, this attachment effec- portions: one epithelial and one connective
tively separates the bone tissue, the tissue portion. In the studies referred to,

c 2007 The Authors. Journal compilation

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Berglundh et al . Morphogenesis of the peri-implant mucosa

Table 1. Schedule for implant installation and biopsy

Day 0 Day 4 Week 1 Week 2 Week 4 Week 6 Week 8 Week 12
Group I Installation
Left Biopsy Day 0
Group I Installation
Right Biopsy Day 4
Group II Installation
Left Biopsy 1 week
Group II Installation
Right Biopsy 2 weeks
Group III Installation
Left Biopsy 4 weeks
Group III Installation
Right Biopsy 6 weeks
Group IV Installation
Left Biopsy 8 weeks
Group IV Installation
Right Biopsy 12 weeks

Each group (I–IV) included five animals.

Fig. 2. Implants and surrounding mucosa at 4 weeks

Fig. 1. Implants in the right side of the mandible immediately after installation (a) and after suturing (b).
of healing.

the epithelial portion was about 1.5–2 mm et al. 2003; Abrahamsson et al. 2004). In implants with interrupted sutures (Fig. 1).
s
long while the cell-rich portion (Moon brief, solid screw implants (ITI Dental The sutures were removed after 2 weeks
et al. 1999) of the zone of connective tissue Implant System; Straumann AG, Basel, and a plaque control program including
attachment was about 1–1.5 mm high. Switzerland) with a diameter of 4.1 mm daily cleaning of the remaining teeth and
The soft tissue dimensions were unre- were used. The intra-osseous part of the the implants was initiated.
lated to whether the implants were initially implant was 10 mm long and was config- The animals were sacrificed and biopsies
submerged and subsequently abutment ured with a turned or sandblasted and acid- were obtained at various intervals to pro-
connected or non-submerged (Abrahams- etched -surface topography. The transmu- vide healing periods extending from Day 0
son et al. 1996, 1999). The mature epithe- cosal portion of the implant was 2.8 mm (2 h) to 12 weeks (Table 1). At each biopsy
lial and connective tissue dimensions of high and had a polished surface. interval, the animals were sacrificed with
s
the peri-implant mucosa seemed to be an overdose of Sodium-Pentothal (Abbott
dependent on biological demands (Ber- Experimental animals Scandinavia AB, Solna, Sweden) and per-
glundh & Lindhe 1996; Cochran et al. The regional Ethics Committee for Animal fused through the carotid arteries by a
1997; Hermann et al. 2000, 2001). Research, Göteborg, Sweden, approved the fixative (Karnovsky 1965). The mandibles
No data are currently available, however, study protocol. Twenty Labrador dogs were were removed and placed in the fixative.
that describe the time that is required to included in the experiment. All mandibu- The implant sites were dissected using
s
allow the epithelial and connective tissue lar premolars were extracted. After a heal- a diamond saw (Exakt , Apparatebau,
compartment of the soft tissue attachment ing period of 3 months, the implant Noderstedt, Germany) and processed for
to form and mature. installation procedure outlined in Table 1 histological analysis.
The objective of the present experiment was initiated. Thus, buccal and lingual
was therefore to study the morphogenesis muco-periosteal flaps were elevated and
Histological preparation and analysis
of the mucosal attachment to implants four implants were placed in the right and
made of c.p. titanium. left sides of the mandible of all 20 dogs (Fig. Decalcified sections
2) according to the technique previously Two of the implant sites in each quadrant
described (Berglundh et al. 2003) and the were prepared using a modification of the
Material and methods schedule outlined in Table 1. A non-sub- ‘fracture technique’ described by Berglundh
merged implant installation technique was et al. (1991, 1994). Before the tissue was
The experimental model used was pre- used and the mucosal tissues were secured fully decalcified, incisions were made par-
viously described in detail (Berglundh to the conical marginal portion of the allel with the long axis of the implants and

2 | Clin. Oral Impl. Res. 18, 2007 / 1–8 c 2007 The Authors. Journal compilation
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 Berglundh et al . Morphogenesis of the peri-implant mucosa

Fig. 3. (a) Implant with surrounding hard and soft tissues at 2 h after installation. Ground section, original magnification  16. (b) Detail of (a). Blood cloth separating
the mucosa from the implant and bone, original magnification  25. (c) Peri-implant hard and soft tissues 2 h after implant placement. Decalcified section, original
magnification  25. (d) Detail of (c). Connective tissue wound surface, original magnification  50.

lingual plane using a cutting–grinding unit

s
(Exakt , Apparatebau, Norderstedt, Ger-
many). From each implant site, two central
sections were obtained and further reduced
to a final thickness of about 20 mm by
micro-grinding and polishing using a mi-
s
cro-grinding unit (Exakt ). The remaining
mesial and distal portions were cut in a
perpendicular (mesial–distal) direction and
two central sections were prepared from
each unit. The sections were stained in
toluidine blue.

Histological analysis
The histological examination was per-
s
formed in a Leitz DM-RBE microscope
(Leica, Heidelberg, Germany) equipped
s
with an image system (Q-500 MC ; Leica).
In the sections, the implant margin (I), the
marginal portion of the peri-implant mu-
cosa (PM), the marginal level of bone-to-
implant contact (B) and the apical exten-
Fig. 4. (a) Soft and hard tissues at 4 days of healing. Decalcified section, original magnification  25.
sion of the barrier epithelium (aJE) were
(b) Detail of (a),original magnification  100. identified and used for the linear measure-
ments. The vertical distances between the
at the mesial and distal aspects of the were produced from each tissue unit with landmarks were determined in a direction
biopsies. Buccal and lingual portions of the the microtome set at 3 mm. The sections parallel to the long axis of the implant.
peri-implant tissues were dissected and one were stained in PAS and toluidine blue The composition of an 80 mm wide area
mesio-buccal, one mesio-lingual, one disto- (Schroeder 1969). From each tissue unit, of the connective tissue facing the trans-
buccal and one disto-lingual unit were pre- six selected sections representing the entire mucosal portion of the implant was as-
pared. Decalcification was completed in circumference of the implant were exposed sessed using a point-counting procedure
ethylenediamine tetra aceticacid, and dehy- to histological examination. (Schroeder & Münzel-Pedrazzoli 1973;
dration was performed in serial steps of Berglundh et al. 1991; Abrahamsson et al.
ethanol concentrations. Secondary fixation Non-decalcified sections 1999). The measurements were confined
s
in OsO4 of the tissue samples was carried In the remaining four sites of each animal, to the EPON -embedded sections and in-
out and the units were finally embedded in ground sections were prepared according to cluded three zones of the peri-implant
s s
EPON (EPON Fluka chemie, Buchs, the methods described by Donath & Breu- mucosa (zone 1, coronal; zone 2, middle;
Switzerland) (Schroeder 1969). Sections ner (1982). The blocks were cut in a bucco- and zone 3, apical). A lattice comprising

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Berglundh et al . Morphogenesis of the peri-implant mucosa

100 light-points was superimposed over A coagulum occupied the compartments marginal portion of the tissue, proliferation
the tissue at a magnification of  1000 between the mucosa and the implant and of epithelium had occurred and the first
and the relative proportions of the connec- between the mucosa and the alveolar pro- signs of a barrier (junctional) epithelium
tive tissue occupied by collagen (Co), cess immediately after surgery (Fig. 3). At 4 were observed. Bone remodeling was in-
fibroblasts (Fi), vascular structures (V), days of healing, the blood cloth was infil- tense at this phase of healing and the
mononuclear leukocytes (M), polymorpho- trated by numerous neutrophil granulo- marginal level of bone to implant contact
nuclear leukocytes (PMN) and residual tis- cytes and an initial mucosal seal was was located at a more apical position than
sue (R), e.g., nerves, matrix components and established at this early phase of healing at 1 week of healing.
unidentified structures, were determined. by the clustering of leukocytes in a dense The structure and composition of the
Mean values and standard deviations were fibrin network (Fig. 4). This provisional peri-implant mucosa at 4 weeks of healing
calculated for each implant and animal. seal persisted at 1 week of healing. The were different from that of earlier phases
area occupied by the leukocyte-infiltrated (Fig. 7). A barrier epithelium had formed
fibrin tissue, however, was considerably and occupied about 40% of the mucosal
Results smaller than at 4 days and was confined interface to titanium. The connective tis-
to the marginal portion of the soft tissue sue was well organized and contained large
Healing was uneventful following implant interface. The tissue in the apical part of portions of collagen and fibroblasts. Bone
installation in all 160 implant sites. The the mucosal interface at 1 week was domi- remodeling had resulted in a distinct crestal
peri-implant mucosa exhibited minor signs nated by collagen and fibroblasts (Fig. 5). bone portion at a position of about 3.2 mm
of inflammation during the first 2 weeks At 2 weeks after surgery, the peri-im- apical of the soft tissue margin.
of healing. From 4 weeks, the mucosa plant mucosa adhered to the implant sur- Tissue maturation and collagen fiber
was stable and well attached to the bone face by a connective tissue that was rich in organization was evident from 6 to 12
(Fig. 2). cells and vascular structures (Fig. 6). In the weeks of healing, and the formation of
barrier epithelium was completed between
6 and 8 weeks (Figs 8–10). A dense layer of
elongated fibroblasts formed the connec-
tive tissue interface to titanium. In con-
nective tissue compartments lateral to the
implant interface, few vascular structures
were found. Fibroblasts were interposed
between thin collagen fibers, the direction
of which was mainly parallel to the im-
plant surface.

Dimensional changes
The mucosal height, including epithelial
and connective tissue dimensions assessed
during healing from 1 week, is illustrated
Fig. 5. (a) Peri-implant mucosa at 4 days of healing. Decalcified section, original magnification  50. (b) in Fig. 11. The overall height of the mu-
Detail of (a), original magnification  100. (c) Detail of (b). Leukocyte-infiltrated fibrin tissue in the interface cosa, assessed from the margin of the soft
to titanium, original magnification  400. tissue to the most coronal position of bone

Fig. 6. (a) Ground section of implant and surrounding hard and soft tissues representing 2 weeks of healing, original magnification  16. (b) Detail of (a), original
magnification  50. (c) Peri-implant tissues at 2 weeks. Formation of barrier epithelium in the marginal portion of the mucosa. Decalcified section, original
magnification  50. (d) Detail of (c). Marginal portion of the soft tissue interface to titanium, original magnification  100. (e) Detail of (c). Apical portion of the soft
tissue interface to titanium, original magnification  100.

4 | Clin. Oral Impl. Res. 18, 2007 / 1–8 c 2007 The Authors. Journal compilation
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 Berglundh et al . Morphogenesis of the peri-implant mucosa

Fig. 7. (a) Ground section of implant and peri-implant hard and soft tissues representing 4 weeks of healing, original magnification  16. (b) Detail of (a), original
magnification  50. (c) Peri-implant tissues at 4 weeks. Barrier epithelium occupying about 40% of the mucosal interface to titanium. Decalcified section, original
magnification  50. (d) Detail of (c), original magnification  100. (e) Detail of (d), original magnification  200.

to implant contact, increased from 1 to 2

weeks and varied between 3.1 and 3.5 mm
between 2 and 12 weeks of healing. A
barrier epithelium had started to form at 2
weeks. At 1 and 2 weeks, the barrier
epithelium extended to a position about
0.5 mm apical of the mucosal margin,
while at 4 weeks the distance amounted
to 1.42 mm. At 6 weeks, the dimension of
the barrier epithelium was established and
varied between 1.7 and 2.1 mm between 6
and 12 weeks.

Connective tissue composition

The composition of the connective tissue
assessed within the coronal (zone 1), mid-
dle (zone 2) and apical (zone 3) interface
Fig. 8. (a) Peri-implant tissues at 6 weeks. Decalcified section, original magnification  50. (b) Detail of (a). portion to the implant is presented in
Connective tissue portion immediately apical of the barrier epithelium, original magnification  100. (c)
Fig. 12. The tissue in zone 1 was available
Detail of (a). Apical part of the barrier epithelium, original magnification  200.
for analysis at days 0, 4, 1 week and
2 weeks, while at later healing intervals
the interface portion at this level was occu-
pied by a barrier epithelium. In the sections
representing day 0, the apical portion of the
interface (zone 3) was dominated by ery-
throcytes in a blood cloth, while in mar-
ginal portions (zones 1 and 2) the
assessment of the tissue composition in-
cluded the tissue lateral to the wound sur-
face of the mucosa secured by the sutures.
At day 4, the interface tissue was mainly
comprised of a matrix including fibrin and
degraded products of the coagulum. Neu-
trophil granulocytes (PMN) occurred in
large numbers while the volume of vessels
was small. The tissue composition in the
Fig. 9. (a) Decalcified section of peri-implant tissues representing 8 weeks of healing. Formation of barrier
epithelium completed, original magnification  50. (b) Detail of (a). Apical part of the barrier epithelium,
three zones was different at 1 and 2 weeks
original magnification  200. (c) Detail of (a). Connective tissue interface to titanium, original magnification of healing. While the marginal portion of
 200. the interface (zone 1) was dominated by the

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Berglundh et al . Morphogenesis of the peri-implant mucosa

similar long zones of junctional/barrier

epithelium and connective tissue. The con-
nective tissue compartment located imme-
diately lateral to the implant was
characterized by its high density of collagen
and low density of vessels. Similar findings
were reported from another study in dogs
by Buser et al. (1992). They analyzed the
peri-implant mucosa after 3 months of
healing following implant placement using
a non-submerged installation procedure.
Healing resulted in the formation of junc-
tional epithelium and a connective tissue
that was in direct contact with the implant
surface. Buser et al. (1992) stated that the
connective tissue portion that was domi-
nated by collagen fibers and was free from
vessels resembled an ‘inflammation-free
scar tissue.’ Abrahamsson et al. (1996,
1999), using similar experimental models,
reported that the dimension and composi-
Fig. 10. (a) Ground section of implant and surrounding hard and soft tissues from biopsy obtained at 12 weeks
of healing, original magnification  25. (b) Detail of (a). Collagen fibers in the supra-alveolar connective tion of the peri-implant mucosa were not
tissue. Polarized light, original magnification  100. influenced by the installation procedure
(submerged or non-submerged) used. The
findings referred to above are consistent
4 PM-aJE aJE-B
infiltrated and degraded the coagulum that with observations made in the present
3.5
occupied the compartment between the experiment. In specimens representing 6,
3
2.5 mucosa and the implant during the initial 8 and 12 weeks of healing, the length of the
phase of healing. At 2 weeks after surgery, barrier epithelium as well as the connective
mm

2
1.5 fibroblasts were the dominating cell popu- tissue that was in contact with the implant
1 lation in the connective tissue interface surface was about 2 and 1.5 mm, respec-
0.5 but at 4 weeks the density of fibroblasts tively. In addition, the connective tissue in
0 had decreased. Furthermore, the first signs the apical and mid-portions (zones 2 and 3
1w 2w 4w 6w 8w 12 w
of epithelial proliferation were observed in of the soft tissue interface) at these healing
Fig. 11. Histogram illustrating the mucosal height specimens representing 1–2 weeks of intervals was dominated by collagen and
from 1 to 12 weeks of healing. Epithelial (red) and healing and a mature barrier epithelium fibroblasts, while vascular structures occu-
connective tissue (blue) dimensions.
occurred after 6–8 weeks of healing. The pied only a minor fraction of the tissue
collagen fibers of the mucosa were volume. This observation indicates that
organized after 4–6 weeks of healing. It is the wound-healing process that takes place
fibrin matrix, the middle and, in particular, suggested that the soft tissue attachment following implant placement using a non-
the apical part (zones 2 and 3) exhibited to implants placed using a non-submerged submerged installation procedure requires
large volume fractions of collagen and fi- installation procedure is properly estab- about 6 weeks to establish a soft tissue
broblasts. From 4 weeks of healing, the lished after several weeks following sur- barrier with proper dimensions and tissue
densities of collagen and fibroblasts in- gery. organization.
creased and were the dominating tissue In most animal experiments describing Van Drie et al. (1988) evaluated early
components. In the apical compartment, the structure and composition of the peri- phases of soft tissue healing around im-
collagen occupied more than 50% of the implant mucosa, models were used that plants in an experimental study in dogs.
tissue volume, while the volume of fibro- included healing periods varying between 3 Implants were placed in the mandible of
blasts varied between 32% and 37%. and 6 months. Berglundh et al. (1991), in a four beagle dogs using a two-stage installa-
study in beagle dogs, compared mucosa at tion procedure and transmucosal abut-
implants and teeth. Implants were placed ments were connected to the implants at
Discussion using a two-stage procedure in one side of 1, 3, 7 and 15 weeks before biopsy. The
the mandible and biopsies from tooth and histological examination of the peri-im-
In the present experiment, different phases implant sites were obtained 4 months after plant tissues included the assessments of
of wound healing in the soft tissue around abutment connection. It was reported that the distance between the apical level of the
implants were analyzed. It was demon- the soft tissue attachment to teeth and barrier epithelium and the bone crest as
strated that large numbers of neutrophils implants was comprised of correspondingly well as the composition of the connective

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 Berglundh et al . Morphogenesis of the peri-implant mucosa

a Zone 1 and occupied about 60% of the entire

100% soft tissue that established contact with
R
90% PMN titanium.
80% Er In the experiment by Van Drie et al.
Mæ (1988), the composition of the connective
70%
Fi tissue lateral to the implant was deter-
60% V mined and it was reported that the collagen
50% Co density of this tissue portion increased
40% from 1 week up to 15 weeks of healing.
30%
This observation is in agreement with the
findings presented in the present study.
20%
The volume fraction of the connective
10%
tissue of the peri-implant mucosa that
0% was occupied by collagen and fibroblasts
Day 0 Day 4 1w 2w increased from day 4 to 4 weeks of healing,
while from 4 to 12 weeks no major changes
b Zone 2
100% in the composition of the connective tissue
R occurred.
90% PMN
In the current experiment, the connec-
80% Er
tive tissue that made contact with the
70% Mæ
Fi titanium surface underwent marked
60%
V changes during the early phases of healing.
50% Co While inflammatory cells were numerous
40% in the soft tissue wound at 4 days, 1 week
30% and 2 weeks, fibroblasts outnumbered the
20% other cells in specimens obtained from 4
10% weeks of healing. In addition, the shift
from an early leukocyte-dominated matrix
0%
Day 0 Day 4 1w 2w 4w 6w 8w 12 w to a connective tissue comprised of mainly
collagen fibers and fibroblasts appeared to
c Zone 3 occur from the apical compartment and in
100% conjunction with apical proliferation of
R
90% barrier epithelium from the margin of the
PMN
80%
mucosa. In other words, the formation of a
Er
Mæ
soft tissue barrier at implants is the result
70%
Fi of a maturation process within the connec-
60%
V tive tissue and epithelial proliferation dur-
50% Co ing wound healing. In the sections
40% representing 6, 8 and 12 weeks of healing,
30% elongated fibroblasts were found to occupy
20% the interface between connective tissue
10%
and titanium. Similar findings were pre-
sented from previous animal experiments
0%
Day 0 Day 4 1w 2w 4w 6w 8w 12 w from our laboratory. Moon et al. (1999) and
Abrahamsson et al. (2002) analyzed the
Fig. 12. Histograms illustrating the composition of an 80 mm wide area of the connective tissue facing
connective tissue interface to titanium im-
transmucosal portion of the implant from day 0 to 12 weeks of healing. Zone 1 (a) coronal, zone 2 (b) middle
and zone 3 (c) apical portions of the tissue. plants using light and transmission elec-
tron microscopy. In these experiments,
fibroblasts were orientated both parallel
tissue present in this location. It was current biopsy material the epithelium was and perpendicular to the long axis of the
reported that the distance between the found to extend a distance of only 0.5 mm implant surface and it was suggested that
apical extension of the epithelium and the from the mucosal margin and, hence, at this fibroblast-rich barrier played an im-
marginal bone remained unchanged in the these intervals represented 15–20% of the portant role in the establishment and main-
interval between 1 and 15 weeks of heal- soft tissue interface to the implant. During tenance of the soft tissue seal.
ing. This finding is not consistent with the the continued process of healing, the bar- The finding in the present material that
observations made in the current experi- rier epithelium migrated to a position of fibroblasts will settle in the connective
ment. Thus, after 1 and 2 weeks in the about 1–1.5 mm from the marginal bone tissue interface to titanium during healing

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Berglundh et al . Morphogenesis of the peri-implant mucosa

is in agreement with the results presented Acknowledgement: This project was

by Thomsen et al. (1986). They analyzed supported by a Research Program
the soft tissue around implants that were Project grant (179/2000) from the ITI
placed in the abdominal wall of rats. At 3 Foundation for the Promotion of Oral
weeks of healing, fibroblasts were fre- Implantology, Basel, Switzerland.
quently found in direct contact with the
implant surface and at 6 and 9 weeks the
collagen content had increased and fibro-
blasts as well as fibers were aligned with
the contour of the implant.
In conclusion, the present study demon-
strated that the soft tissue barrier adjacent
to titanium implants placed using a non-
submerged installation procedure devel-
oped its final characteristics within 6
weeks postoperatively. Before this time
period, the establishment of the barrier
epithelium and the maturation of the con-
nective tissue may be incomplete.

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