Periodontology 2000, Vol. 0, 2017, 1–15 © 2017 John Wiley & Sons A/S.
iley & Sons A/S. Published by John Wiley & Sons Ltd
Printed in Singapore. All rights reserved
Comparison of peri-implant and
periodontal marginal soft tissues
in health and disease
SASO IVANOVSKI & RYAN LEE
The structures of the soft tissues, including the
epithelial and connective tissue elements, that
envelop a dental implant are in many ways analogous
to those that surround the natural dentition (57). As is
the case with teeth, dental implants also have an
intra-osseous component that is situated within alve-
olar bone and provides structural anchorage, and a
component that is transmucosal and facilitates
attachment of the dental restoration. Although the
periodontium and peri-implant supporting structures
share similar histologic and clinical features, there are
several fundamental differences between the anchor-
age and attachment of teeth and implants. A key dif-
ference is that there is no periodontal ligament or
cementum around dental implants, with the alveolar
bone coming into direct contact with the implant
surface.
As is the case with teeth, the transmucosal compo-
nent of implants needs to provide a physical and
physiological barrier between the external oral envi-
ronment and the underlying tissues. The implant–
mucosa interface also includes a sulcus resembling
that associated with teeth, as well as an attachment
apparatus. Indeed, the architecture of the supra-
alveolar transmucosal components, consisting of a
sulcus, junctional epithelium and connective tissue
attachment, is similar around implants and teeth
(Fig. 1). Although both the transmucosal component
of implants and the transgingival component of teeth
have a sulcus (in health)/pocket (in disease) and a
connective tissue attachment, important differences
exist, which have clinical implications for the mainte-
nance of peri-implant mucosal health, as well as for
the diagnosis and management of peri-implant dis-
ease. This review will compare and contrast the anat-
omy of the transmucosal (gingival) components of
PERIODONTOLOGY 2000
implants and teeth, and explore how the unique fea-
tures of the implant–mucosa interface impact on clin-
ical features of peri-implant tissues in health and
disease.
Gingival and peri-implant
epithelial attachment
Dental endo-osseous implants are placed into a surgi-
cally created osteotomy in alveolar bone. Generally,
the alveolar bone is accessed via a surgical incision in
the mucosa. The transmucosal attachment is formed
after adaptation of the mucosal wound edges to the
transmucosal part of the implant. Therefore, the soft-
tissue attachment around the implant develops fol-
lowing surgical intervention, unlike that of the tooth,
which develops simultaneously with the periodon-
tium and remains structurally continuous with the
surrounding tissues. Following implant surgery, the
epithelial cells at the wound edges are coded to prolif-
erate and cover the wound to ensure wound closure
and continuity (55). These cells have the ability to
adhere to the implant surface and to produce a basal
lamina and hemidesmosomes, creating an epithelial
seal that resembles the junctional epithelium around
teeth (55).
The gingival junctional epithelium is part of the
attachment apparatus between the tooth and gingiva.
The innermost cells of the junctional epithelium form
the epithelial attachment apparatus, which ensures a
tight seal against the tooth surface (20) (Fig. 2A,B,D).
This adherence to the tooth surface means that the
junctional epithelium plays a critical role in tissue
homeostasis and defence against microorganisms
and their constituents (20). Similarly, it is universally
1
Ivanovski & Lee
accepted that the integrity of the epithelial attach-
ment between the implant and the peri-implant
mucosa is critical for maintaining osseointegration
(44).
Consistent with the epithelial structure and
arrangement of the natural dentition, the peri-
implant mucosa consists of a well-keratinized oral
epithelium at the outer surface, which is continuous
with a sulcular epithelium lining the lateral aspect of
the gingival sulcus (57). This inner lining epithelial
attachment of the peri-implant mucosa resembles
the junctional epithelium of the teeth in its histologi-
cal characteristics. Berglundh et al. (16, 17) showed,
in an experimental animal study, that an epithelial
structure of a few cell layers in thickness extends
approximately 2 mm apically from the soft-tissue
margin. It is believed that the formation of this barrier
epithelium facing the implant is a natural result of
wound healing, with the epithelial cells proliferating
along the exposed implant surface until continuity of
2
Fig. 1. Cross-section of the buccal
dento-alveolar region (A) and of the
buccal and coronal part of the peri-
implant bone and mucosa (B). Simi-
lar anatomical components (i.e.
sulcular epithelium, junctional
epithelium and connective tissue)
are present in both periodontal and
peri-implant mucosa. Sections were
stained using periodic acid–Schiff
(PAS) and toluidine blue. Original
magnification 340. Adapted from
Berglundh et al. (16).
the epithelium is restored. The apical cells of the bar-
rier epithelium terminate approximately 1–1.5 mm
coronal to the bone crest, and are separated from the
bone by a noninflamed, collagen-rich, cell-poor con-
nective tissue zone (16). It has been shown that
epithelial proliferation is initiated at 1–2 weeks of
healing and that the mature barrier epithelium is
established after 6–8 weeks of healing (19).
Gingival and peri-implant
connective tissue
In an experimental animal study, Berglundh et al.
(16) histologically demonstrated a complex connec-
tive tissue arrangement around teeth, consisting of a
fan-shaped pattern of supra-alveolar principal con-
nective tissue fibers projecting from the root cemen-
tum into the soft and hard tissues of the marginal
periodontium in lateral, coronal and apical directions

Fig. 2. Histological sections of the peri-implant mucosa fol-
lowing 8 weeks of healing. The image in the center shows a
section stained by hematoxylin and eosin. Environmental
scanning electron microcopy visualization (5003 magnifica-
tion) was performed of different areas along the surface facing
(Fig. 1A). In a later review, Schroeder et al. (83)
schematically described the gingival fibers according
to their preferential orientation. This schema identi-
fied dento-gingival, dento-periosteal, alveolo-gingival
and periosteo-gingival fiber groups that attach the
gingiva to teeth and bone; interpapillary fibers that
connect the vestibular and oral interdental papillae to
one another; and circular or semicircular transgingi-
val and transeptal fiber bundles that connect adjacent
teeth to one another.
Peri-implant mucosal connective tissue attachment
has somewhat similar clinical and histological fea-
tures to that of teeth. However, the main difference is
observed in the cellular composition and fiber orien-
tation. The connective tissue surrounding the dental
implant is in direct contact with the titanium dioxide
surface and it contains a dense network of collagen
fibers which, in major bundles, originate from the
Comparison of periodontal and peri-implant soft tissues
the abutment (indicated by red arrows): sulcular epithelium
(A); barrier epithelium (B); and connective tissue (C). Histo-
logical sections (hematoxylin and eosin staining) of the
epithelial layer (4003) (D) and the connective tissue (2003)
(E) are also shown. Adapted from Tomasi et al. (90).
periosteum of the alveolar bone crest, extending to
the mucosal margin (16). These fibers are orientated
in a direction parallel to the implant/abutment sur-
face (16, 31) (Figs 1B and 2C,E). This is in contrast to
the attachment of connective tissue to teeth, whereby
collagen fibers insert into the root cementum in a
perpendicular direction (16). It is important to note
that the difference in the orientation of collagen
fibers, under the strict plaque-control regime of the
study, was shown not to be of clinical significance as
the implant sites were devoid of inflammatory cell
infiltrates and the cuff-like barrier provided adequate
protection against the biofilm. From a morphogenetic
perspective, Berglundh et al. (19) reported, in a
canine model, that the connective tissue of the peri-
implant mucosa was organized after 4–6 weeks of
healing and that the maturation of the tissue took
place between 6 and 12 weeks of healing.
3
Ivanovski & Lee
Subsequently, Tomasi et al. (90) reported the corre-
sponding histological findings in a human study,
demonstrating that the peri-implant mucosal seal
developed completely within 8 weeks of healing.
In another animal study, it was reported that a
large number of fibroblasts were found in the peri-
implant mucosal attachment tissue close to the
implant surface (65). The fibroblasts in this histologi-
cal compartment were orientated with their long axis
parallel to the adjacent collagen fibers and to the
implant surface. These histological findings were not
consistent in more lateral compartments of the peri-
implant mucosal attachment, where greater vascular-
ity and denser collagen fiber structures were observed
but fewer fibroblasts were present. The authors con-
cluded that the fibroblast-rich barrier tissue, which
lies immediately next to the implant surface, plays an
important role in maintaining an adequate seal
against the external environment.
Factors influencing the
peri-implant mucosal barrier
A similar mucosal barrier formation has been
observed among different implant systems, including
both nonsubmerged and submerged types. Abra-
hamsson et al. (1) investigated and compared the
marginal peri-implant mucosal tissues between one-
stage and two-stage implant systems in an animal
model. The histological features described in the
study were in agreement with previous reports (22,
57), with the mucosal barrier surrounding the
implants in one-stage (nonsubmerged) and two-stage
(submerged) systems being similar to each other in
terms of both dimension and composition.
An in vitro study showed that attachment and pro-
liferation of human fibroblasts, epithelial cells and
connective tissue cells are affected by the surface
topography of titanium implants (23). Based on these
findings, it was suggested that different surface tex-
tures could be used to guide mucosal cell attachment
to the dental implant. However, an in vivo study
demonstrated that the surface characteristics (i.e.
roughness) of the healing abutment surface did not
influence the dimension and composition of the peri-
implant mucosal attachment (6).
In an animal study, Buser et al. (22) investigated
the soft-tissue reactions to nonsubmerged unloaded
implants with different surface characteristics at the
crestal area (i.e. rough sandblasted, fine sandblasted
and polished). The authors reported no significant
differences in soft tissue between the three implant
4
surfaces. Histomorphometric analysis demonstrated
that the length of direct connective tissue contact was
similar between the implants, but there appeared to
be less bone loss around roughened surface implants
compared with the other surfaces. Therefore, the
authors concluded that although the different surface
characteristics did not influence the healing pattern
of the peri-implant mucosal tissues, they did have an
impact on the final location of the most coronal
bone–implant contact (22). The findings were further
confirmed by subsequent studies (25, 58).
In contrast to the previous studies, recent preclin-
ical trials and human case reports by Nevins et al.
(66–68) suggested that it may be possible to pro-
mote the formation of perpendicularly attached
connective tissue fibers to the implant surface with
the use of laser-microgrooved abutments. These
assertions are based on a series of studies (66–68)
investigating whether precisely defined microchan-
nels on the implant abutment surface would pro-
mote connective tissue attachment rather than
adaptation, which in turn may limit apical migration
of the junctional epithelium, ultimately preventing
crestal bone loss. The microchannels were gener-
ated by a computer-controlled laser ablation tech-
nique that created a microgrooved topography.
Although it was reported that the composition of
the peri-implant mucosal attachment was similar to
that in previous studies (18, 36–38), polarized light
microscopy of the mucosa–implant interface
revealed functionally oriented collagen fibers aligned
perpendicularly to the implant abutment surface
(67, 68). The presence of perpendicularly attached
collagen fibers was also confirmed by scanning elec-
tron microscopy (67). Remodeling of the bone in a
coronal direction was also observed, which was
attributed to inhibition of the epithelial attachment
and to promotion of connective tissue attachment
to the abutment surface.
It has also been suggested that a perpendicular
orientation of the subepithelial connective tissue
attachment at the transmucosal part of the
implant can be achieved by altering the chemical
characteristics of the implant surface, rather than its
topography per se (84). It was observed that the
peri-implant connective tissue at chemically
modified hydrophilic implant abutment surfaces
appeared to promote the formation of a mixture of
collagen fibers with both parallel and perpendicular
orientation (see Fig. 3). In contrast, the hydrophobic
implant surfaces were associated with a dense con-
nective tissue with parallel-running collagen fibers
and low vascularity (84).

A B
Although the connective tissue attachment out-
comes with laser microgrooved topography and
hydrophilic surfaces are promising, further investiga-
tion is warranted to investigate the effects of topo-
graphical and chemical modification of the implant
surface on the establishment of peri-implant mucosal
attachment.
Biological width
The term ‘biologic width’ refers to the entire dimen-
sion extending from the connective tissue attachment
to the apical extent of the junctional epithelium. The
dimensions of the biologic width of the natural denti-
tion were studied by Gargiulo et al. (29) and Vacek
et al. (91) in humans. The authors of the earlier study
reported that it consisted of a gingival sulcus, an
epithelial attachment and a connective tissue attach-
ment, and their average values were 0.69 mm,
0.97 mm and 1.07 mm, respectively (29). The latter
study confirmed the results of the earlier study,
reporting average values of 1.14 mm for epithelial
attachment and 0.77 mm for connective tissue
attachment (91). The authors of both studies con-
cluded that the most consistent value between indi-
viduals was the dimension of the connective tissue
attachment (69).
In the case of the peri-implant mucosa, compara-
ble histomorphometric findings were reported with
respect to the attachment dimensions in numerous
preclinical studies. Berglundh et al. (16, 18) described
2 mm of epithelial attachment and 1–1.5 mm of con-
nective tissue attachment separating the epithelium
from the bone crest. As is the case with the biologic
Comparison of periodontal and peri-implant soft tissues
Fig. 3. Histological views of connec-
tive tissue reactions adjacent to the
transmucosal part of hydrophilic (A)
and hydrophobic surfaces (B). Colla-
gen fibers are partially extended and
attached perpendicularly to hydro-
philic implant surfaces, whereas
newly formed dense connective tis-
sues run parallel to hydrophobic
implant surfaces. Masson–Goldner
trichrome Stain (original magnifica-
tion 3500). Adapted from Schwarz
et al. (84).
width of the natural dentition, the peri-implant
mucosal attachment dimensions are also regarded as
being relatively consistent in most cases. In a canine
model, Cochran et al. (24) examined the dimensions
and relationships of peri-implant mucosal attach-
ment in nonsubmerged one-part implants under
unloaded and loaded circumstances. The results
illustrated that the biological width was consistent
and similar in both loaded and unloaded situations.
However, it is important to note that there are sev-
eral factors which may influence the dimension of
the biologic width around peri-implant tissues,
namely the different designs and surface characteris-
tics of different commercially available implant sys-
tems and various placement protocols. These
variables are often related to the quality of the muco-
sal seal and determine the amount of crestal bone
loss that occurs during the establishment of the bio-
logical width. The effect of these variables is explored
in the following sections and is summarized in
Table 1.
Surface characteristics
Cochran et al. (24) reported that there were no differ-
ences in the dimensions of the newly formed biologic
width between implants with a titanium plasma-
sprayed or a sandblasted acid-etched surface. These
findings were consistent with the results of subse-
quent preclinical studies, which reported similar bio-
logic width dimensions around implants with rough
(acid-etched) and smooth (turned) surfaces, with a
tendency for the biologic width to be greater on the
rough surface, but this was not statistically significant
(5, 6). Subsequently, Watzak et al. (93) demonstrated
5
Ivanovski & Lee

Table 1. Summary of factors that may determine the biologic width dimensions by influencing physiological bone
remodeling and/or peri-implant mucosal integrity

Factors that may influence Positive influence Negative influence No influence

soft-tissue integrity and/or
physiological crestal bone
remodeling
 Hydrophilic vs hydrophobic
Surface characteristics
sand blasted and acid
etched (84)
 Hydrophilic acid-etched
vs. hydrophobic machined
(85)
Abutment materials
Implant–abutment
interface
 Platform switching
Implant design
(12, 51, 60)
 Internal connection
compared with external
connection (30)
 gold alloy, Porcelain (3, 94)
 Peri-implant mucosa
thickness (≤ 2 mm) (18)
 Repeated abutment removal
(2)
 Subcrestal placement of
tissue-level implant (22, 32)
 Two-stage (piece) implants:
Biologic width re-establish-
ment 2 mm apical to the
microgap (36–38, 73)
 Titanium plasma sprayed vs.
sandblasted and acid etched
(24)
 Dual thermal acid-etched
(Osseotiteâ) vs. turned
surface abutment (5, 6)
 Commercially pure titanium
vs. titanium plasma sprayed
vs. sandblasted and acid-
etched (93)
 Rough sandblast vs. fine
sandblast vs. polished (22)
 Commercially pure titanium,
aluminium oxide (3),
zirconium dioxide (94),
gold alloy (8, 92)
 One-stage implant vs.
two-stage implant (4, 27)

that the biologic width was not influenced by modifi-

cation of the implant surface after 18 months of
loading.
In contrast, Schwarz et al. (84) investigated the
effects of implant surface chemistry (i.e. hydrophilic-
ity) and microtopography on both soft- and hard-
tissue integration around implants, demonstrating
that hydrophilic surfaces resulted in a more intimate
soft-tissue attachment. The authors concluded that
soft-tissue integration was influenced by hydrophilic-
ity rather than by topography. Furthermore, in a
subsequent human clinical trial, three healing abut-
ments with different surface characteristics, namely
hydrophobic machined, modified hydrophilic
micro-rough pure titanium and modified hydrophilic
micro-rough titanium-zirconium alloy, were used to
evaluate the effects of hydrophilicity on peri-implant
soft-tissue integration. It was demonstrated that the
dimension of the junctional epithelium was consis-
tent, regardless of the healing abutment surface
characteristics, while the quality of epithelial and
subepithelial connective tissue contact with the heal-
ing abutment was improved by hydrophilicity (85).
Abutment materials
Commercially pure titanium has been the material of
choice for dental implant abutments because of its
well-documented biocompatibility, as well as its
physical and mechanical features (9). In an attempt
to improve esthetic outcomes, there has been a trend
towards the development and use of abutments made
of other materials, such as tooth-colored materials.
Abrahamsson et al. (3) demonstrated that the type of
abutment material influenced the mucosal attach-
ment. In this animal study, four types of materials
were assessed: commercially pure titanium; highly
sintered aluminium-based ceramic (aluminium
oxide); gold alloy; and dental porcelain fused to gold.
Commercially pure titanium and aluminium-based
ceramic established similar conditions for mucosal
healing and allowed routine formation of epithelial
and connective tissue attachment to the abutment
(3). Abutments made of gold alloy or dental porcelain,
however, appeared to have a negative influence on
wound healing and connective tissue attachment,
resulting in the margin of the mucosa receding and

6

bone resorption occurring, with the epithelium–con-
nective tissue attachment being established apical to
the abutment–fixture junction (3). Moreover, in
another preclinical study, Welander et al. (94) ana-
lyzed the soft-tissue healing associated with abut-
ments made of titanium, zirconium and gold alloy,
demonstrating that the mucosal healing to abutments
made of gold alloy was inferior to that of zirconium
and titanium abutments. The junctional epithelium
and the marginal bone levels were found to extend to
a more apical position at the gold alloy compared
with the titanium and zirconia abutments at
5 months of healing. It was found that the connective
tissue in contact with the gold-alloy abutments con-
tained fewer collagen fibers and fibroblasts, but
increased numbers of inflammatory cells, compared
with the corresponding tissue at the titanium and zir-
conium abutments. Therefore, it was suggested that
the composition of connective tissue at the gold-alloy
abutments may be representative of compromised
mucosal tissue adaption, resulting in apical extension
of the epithelium and hence the position of the mar-
ginal bone (94).
In contrast, a subsequent preclinical study by Abra-
hamsson et al. (8) found that the peri-implant soft-
tissue dimensions were not influenced by the use of
either commercially pure titanium or gold-alloy abut-
ments. Similarly, in a clinical study comparing tita-
nium and gold-alloy abutments, Vigolo et al. (92)
reported no clinical difference in peri-implant mar-
ginal bone levels and of peri-implant soft-tissue heal-
ing between the two materials. The contrasting
findings between these studies may be attributed to
methodological differences, including the type of
implant systems used in the studies.
Position of implant–abutment interface
In a preclinical study, Berglundh & Lindhe (18) inves-
tigated the effects of the location and dimensions of
the transmucosal attachment during wound healing
following implant placement. The authors demon-
strated that at sites which had the peri-implant
mucosa thinned (to a width ≤ 2 mm) before wound
closure and abutment connection, angular osseous
defects developed at the implant marginal border and
the original soft-tissue dimensions became re-estab-
lished (18). Consequently, it can be concluded that a
certain width of peri-implant mucosa is genetically
predetermined and the dimensions of this soft-tissue
are preserved through bone resorption. Moreover, in
a clinical study, Hammerle et al. (32) investigated the
effect of subcrestal placement of the polished surface
Comparison of periodontal and peri-implant soft tissues
of nonsubmerged implants on marginal soft- and
hard-tissue healing. The authors observed that after
one year of function subcrestal placement of one-
stage implants resulted in osseointegration to the
rough-smooth surface interface, and hence more api-
cal establishment of the biological width at the
expense of the crestal bone.
Abutment removal and reconnection
The effect of repeated abutment removal and subse-
quent reconnection on the marginal peri-implant tis-
sue was investigated in a canine model (2). The
frequency of the reconnection used in the study was
once every month for 6 months, and one-piece
implants with an external hex abutment connection
were used. The results showed that disturbances in
the soft-tissue interface caused by the process of
repeated abutment removal resulted in a more apical
repositioning of the connective tissue zone. The
authors suggested that the normal sequence of
wound healing following abutment removal and
replacement caused epithelial cells to proliferate and
protect the exposed breach in connective tissue. Con-
nective tissue and marginal bone remodeling then
occurred to ensure re-formation of the biologic width
dimensions, resulting in the characteristic finding of
crestal bone resorption around dental implants
placed at the level of the bone crest. Although the fre-
quency of abutment removal in this study did not
simulate routine clinical scenarios, it did illustrate the
importance of soft-tissue integrity for the mainte-
nance of the marginal bone levels around an implant.
Implant design
It has been demonstrated that the soft-tissue dimen-
sions of both one- and two-part implant designs are
almost identical (1). Clinical evaluation of one- and
two-stage surgical protocols has also shown similar
outcomes in terms of soft tissue integration, with no
effect on the resultant biologic width (4, 27). This was,
however, in contrast to the findings of Hermann et al.
(38), who found that the soft-tissue dimension of
one-piece implants was relatively smaller than that of
two-piece implants. The biologic width of the one-
piece implant more closely resembled that of the nat-
ural dentition (38).
A series of studies conducted by Hermann et al.
(36–38) demonstrated that in two-part implant
systems, bone remodeling occurred in an apical
location of 2 mm from the microgap (i.e. the
implant–abutment interface), regardless of the
7
Ivanovski & Lee
positioning of the implant relative to the bone crest
(i.e. depth of placement). The authors speculated that
the greater apical extension of epithelial attachment
in submerged two-part implants could be attributed
to microbial contamination (or leakage) from the
microgap after the abutment connection. Conse-
quently, as the implant is placed deeper subcrestally,
this leads to more apical extension of the junctional
epithelium and hence deeper pocketing. More
recently, Pontes et al. (73) conducted a similar pre-
clinical study to evaluate the histomorphometric out-
comes around implants inserted at different levels in
relation to the crestal bone and under different load-
ing conditions (73). The results were consistent with
those of Hermann et al. (38).
The issue of crestal bone loss resulting from the re-
establishment of biologic width apical to the implant–
abutment interface has more recently been addressed
by changes in implant design referred to as ‘platform
switching’, which results in a horizontal mismatch
between the diameter of the implant and the abut-
ment. The rationale for this approach is that the
internal repositioning of the implant–abutment inter-
face would shift the inflammatory cell infiltrate,
formed at this interface, away from the crestal bone,
resulting in biologic width re-establishment in a pre-
dominantly horizontal, rather than vertical, dimen-
sion (51). In turn, this minimizes the vertical bone
resorption that occurs as a result of physiological
remodeling associated with biologic width formation.
It has also been proposed that platform shifted
implants have a biomechanical advantage by moving
stress concentration from the outer edges of the
implant (60). A recent systematic review and meta-
analysis of nine clinical trials concluded that platform
switching was indeed a desirable design feature that
minimizes vertical crestal bone loss (12), although its
effectiveness is variable and dependent on the fea-
tures of individual systems.
Probing periodontal and peri-
implant pockets
Probing of the gingival sulcus aims to assess a num-
ber of periodontal parameters, a major one being the
measurement of the pocket depth, which is the dis-
tance from the most apically penetrated portion of
the junctional epithelium to the gingival sulcus mar-
gin. Numerous studies have demonstrated that the
periodontal attachment apparatus provides an ade-
quate physical barrier (or seal) against probe penetra-
tion in the absence of inflammation, with the
8
maximum penetration of the probe tip remaining
within the junctional epithelium (14, 61). However, in
the presence of an inflammatory lesion, the epithelial
attachment loses its barrier function, allowing the
periodontal probe to penetrate beyond the apical
extension of the junctional epithelium and into the
connective tissue (14, 72). The extent of probe pene-
tration is influenced by factors such as probing force,
angulation, probe-tip diameter, root surface anat-
omy, inflammatory state of the periodontium and
firmness of the marginal tissues (79). Despite the limi-
tations associated with the use of a periodontal
probe, it is still considered to be one of the most
important diagnostic tools for the assessment of peri-
odontal status and for the evaluation of the outcomes
of periodontal therapy. Likewise, probing around the
peri-implant mucosal tissue plays a crucial role in the
assessment of peri-implant mucosal health. However,
in addition to the established limitations associated
with probing around periodontal pockets, the unique
features of the peri-implant mucosal structures can
further influence the pocket-depth measurements at
peri-implant sites.
Ericsson & Lindhe (26) investigated the probing
depths around natural teeth and dental implants in a
canine model. The resistance offered by the gingiva at
teeth and the peri-implant mucosa at osseointegrated
titanium implants was assessed in response to a stan-
dardized probing force of 0.5N. The results revealed
that probing of the dento–gingival interface caused a
slight compression of the gingival tissue, whereas, at
the implant sites, it resulted in both compression and
a lateral dislocation of the peri-implant mucosa.
Moreover, the average probing depth at the implant
sites was deeper than at the tooth sites. At tooth sites
with healthy gingiva, the tip of the probe terminated
close, but consistently coronal, to the apical cells of
the junctional epithelium, whilst at implant sites, the
probe tip penetrated apical of a laterally displaced
junctional epithelium and ended close to the crest of
the alveolar bone. However, the results reported in
this study were not in full agreement with data
reported in subsequent experimental studies. The
deeper penetration of the probe tip at the healthy
peri-implant sites reported in this study may be
attributed to the high probing force employed (0.5N).
In a subsequent study, the extent of penetration of
the peri-implant probe in health and disease (mu-
cositis and peri-implantitis) was investigated in a dog
experimental model (49). A smaller standardized
probing force, of 0.2N, was applied in this study. It
was reported that the average probing depths at
healthy sites and at sites with mucositis were about
 Comparison of periodontal and peri-implant soft tissues

1.8 mm and 1.6 mm, respectively. However, at sites A B

with peri-implantitis, the probe penetrated close to
the alveolar bone, exceeding the connective tissue
level by a mean of 0.52 mm, and the average probing
depth was significantly deeper (3.8 mm) than that at
healthy sites. Hence, the authors concluded that
probe penetration was affected by the density of the
peri-implant connective tissues and demonstrated
that periodontal probing with a light force was a reli-
able diagnostic tool for distinguishing healthy peri-
implant tissues from diseased ones. Furthermore,
Etter et al. (28) evaluated peri-implant mucosal heal-
ing using standardized probing with a force of 0.25N
in an experimental model, reporting complete re-
establishment of the mucosal integrity/seal within
5 days without eliciting an adverse inflammatory
response. C D
Probing depths at teeth and implants were further
evaluated in both healthy and inflamed sites in pri-
mates (82). It was demonstrated that the probe tip was
located at a similar distance from the bone in healthy
tooth sites and implant sites, whereas in the presence
of inflammation (i.e. mucositis and peri-implantitis),
the probe tip at the implant sites was consistently
located at a more apical position than at inflamed
tooth sites (Fig. 4). The authors concluded that in the
presence of inflammation, probing depth measure-
ments at implants are not fully comparable with those
at teeth, and the inflammatory status of the soft tis-
sues had a more profound effect on the probing depth
measurements in peri-implant tissue compared with
gingival tissue. Moreover, in a subsequent preclinical
Fig. 4. Histological views of peri-implant and periodontal
study, Abrahamsson & Soldini (7) demonstrated that a
tissue probing in health (A, B) and disease (C, D). Adapted
light probing force (0.2N) resulted in penetration of from Schou et al. (82).
the probe to similar depths at healthy tooth and
implant sites. The distance from the probe tip to the
alveolar bone crest was approximately 1 mm at both the vascular plexus of the periodontal ligament. The
teeth and implants. From these studies, it can be con- vascular network of the junctional epithelium collar,
cluded that probing with a light force (0.2–0.25N) in known as the gingival plexus, is different from that of
noninflamed tissue results in penetration to similar the gingival epithelium. Anatomically it extends from
depths, in relation to the bone crest, at implant and the coronal to the apical terminal ends of the junc-
tooth sites. However, in the presence of inflammation, tional epithelium, both vestibularly and orally, as well
the probe tip penetrates more deeply into the peri- as interdentally. This vascular network of mainly
implant connective tissues, reaching closer to the post-capillary venules is rich in anastomoses and
alveolar bone crest compared with tooth sites. resembles a thin vascular basket. The capillary loops
have been shown to have the ability to increase in
size and number in response to inflammation. During
Vascular structure of gingiva and inflammation, in response to lymphokines or other
peri-implant mucosa inflammatory mediators, the capillaries resemble
high endothelial venules and facilitate migration of
The human gingival tissue is a highly vascularized neutrophilic granulocytes. The fact that the venules
complex. The main sources of the gingival vascula- of the gingival plexus develop into high endothelial
ture are the large supraperiosteal blood vessels and venules that proliferate under challenge suggests that

9
Ivanovski & Lee
they play a role in selective homing and entry of lym-
phocytes (83).
In comparison with the blood supply of the peri-
odontium, the corresponding vascular structure of
the peri-implant mucosa originates ‘solely’ from the
terminal branches of the larger vessels of the supra-
periosteum from the outer (vestibular) border of the
alveolar ridge (17). The blood vessels lateral to the
junctional epithelium in peri-implant mucosa, as in
the gingival vascular arrangement, form a character-
istic ‘crevicular plexus’ and are continuous with the
supra-periosteal vessels. The ‘crevicular plexus’
found lateral to the junctional epithelium of gingiva
and peri-implant mucosa have matching location
and composition, suggesting that the source of
leukocyte migration and accumulation is equivalent
in the two tissues (17). However, the richly vascular-
ized connective tissue adjacent to the root cemen-
tum in teeth has been found to be almost completely
devoid of vascular supply in the corresponding peri-
implant tissue (17). It has been hypothesized that this
‘inflammation-free scar tissue’ impairs the defence
system of tissues surrounding dental implants and
may make the peri-implant mucosal tissues more
susceptible to bacterial challenge (17, 22).
Significance of bleeding on probing
Bleeding on probing occurs after the insertion of a
probe into the gingival sulcus with light pressure
(0.25N) and is indicative of the presence of an inflam-
matory lesion in the gingival tissue (42, 47). Absence
of bleeding on probing, on the other hand, represents
periodontal health, with a high negative predictive
value, of 98.5%, for disease progression (41, 46).
Bleeding on probing has also been employed to
assess peri-implant tissue health. It has been demon-
strated, in an experimental animal model, that bleed-
ing on probing is more evident in the presence of
inflammation and that its frequency increases with
the severity of the inflammation (mucositis vs. peri-
implantitis), whereas healthy peri-implant sites show
no bleeding on probing (49). These findings were
confirmed by a prospective clinical study (40), which
investigated the prognostic value of bleeding on
probing in patients with progressive peri-implantitis,
and demonstrated a high negative predictive value
for bleeding on probing. This suggests that the
absence of bleeding on probing is a reliable indicator
of peri-implant tissue stability. Furthermore, Luter-
bacher et al. (59) evaluated the diagnostic value of
assessing the prevalence of bleeding on probing,
10
alone or in combination with microbiological testing,
for monitoring periodontal and peri-implant soft-
tissue conditions during supportive periodontal ther-
apy. The authors reported that bleeding on probing
alone had higher diagnostic accuracy for disease pro-
gression at implant sites than at tooth sites. The diag-
nostic value of bleeding on probing was even greater
when combined with the presence of microbial
pathogens at the implant sites. The positive predictive
value for bleeding on probing frequencies of more
than 50% at implant sites was 100%. In other words,
any site bleeding at more than half of the recall visits
over a 2-year period had disease progression (33).
Therefore, it can be concluded that bleeding on prob-
ing is an important diagnostic tool in monitoring
peri-implant mucosal tissue conditions.
Periodontal and peri-implant
diseases
The term peri-implantitis is defined as an infectious
condition of the tissues around osseointegrated
implants with loss of supporting marginal bone
(≥ 2 mm) and clinical signs of inflammation, includ-
ing bleeding on probing and suppuration (35, 80, 96).
Peri-implant mucositis is defined as inflammation of
the peri-implant mucosa without marginal bone loss
(50, 76).
The existing literature points to similarities
between periodontal and peri-implant diseases in
terms of etiology, pathogenesis, risk factors and
clinical presentation (34). The initiation of the two
diseases is dependent on the presence of a dental pla-
que biofilm, and few qualitative differences have been
reported between the biofilm found at periodontal
and peri-implantitis lesions (34). In both disease enti-
ties, a similar composition of the microbiota (gram-
negative anaerobes) was found at affected sites (9, 13,
52, 62–64, 87), although several studies have reported
the presence of certain microbes, such as Staphylo-
coccus aureus and Candida albicans, which are not
normally associated with periodontitis, at peri-
implantitis sites (21, 45, 53, 78). This may indicate a
potential role of gram-positive facultative cocci and
other putative pathogens in the development of peri-
implantitis.
The host inflammatory response to the accumula-
tion of biofilm in peri-implant mucositis appears to
be identical to that found in gingivitis; however, per-
sistent accumulation of biofilm may elicit a more pro-
nounced inflammatory response in peri-implant
mucosal tissues than in the dentogingival unit (34). It

has been reported that the extent of the inflammatory
cell infiltrate appeared to be more pronounced in
peri-implantitis, where it may extend to the bone
marrow (34), compared with that described in peri-
odontitis where the lesions were well contained
within the connective tissue compartment (48, 54, 81,
86). This may be attributed to structural differences
between the periodontal and peri-implant mucosal
tissues.
Although plaque is recognized as an essential
pathogenic factor in the development of both
periodontitis and peri-implantitis, the etiology of
peri-implantitis is multifactorial, and changes in local
ecological conditions that favor the growth of bacte-
rial pathogens are critical in the establishment of
peri-implant disease (64). The subgingival location of
the implant–abutment connection is an important
consideration in this context. It is noteworthy that
this interface is the subject of great variation between
different manufacturers, and hence the choice of
implant design may be important, especially in sus-
ceptible patients. Indeed, it is widely accepted that
multiple features of implant design, and the ability of
practitioners to manage these appropriately, has a
significant impact on the development of peri-
implant disease (50, 74).
Two characteristics of implants that can play a role
in the development and progression of peri-implant
disease are the implant–abutment/restoration con-
nection and the implant surface.
Implant–abutment connection and
peri-implant disease
It has been shown that bacteria can colonize the
microgap at the implant–abutment interface and
reside within the internal components of implants,
and this provides them with an environment shel-
tered from host defences (39, 70, 75). The design of
the implant–abutment interface determines the size
of the microgap and therefore will influence the
degree of microleakage (88), with biological conse-
quences being soft-tissue inflammation that can lead
to bone loss (38).
The stability of the implant–abutment interface is
important in minimizing biological complications. It
is reasonable to expect that loosening of the restora-
tion would have a negative impact on the health of
the peri-implant tissues, as the interface between the
implant and abutment is usually below the mucosal
margin. Indeed, in a clinical report, the incidence of
biological complications was linked to technical
Comparison of periodontal and peri-implant soft tissues
complications (43). The nature of the connection (ex-
ternal vs. internal) can have an impact on technical
complications, such as screw loosening, and in this
regard an internal connection appears to offer an
advantage (30). It should also be considered that the
nature of the implant–abutment connection (e.g.
platform switching) may also influence the diagnosis
of peri-implantitis as it may affect the ability to probe
around implants (50).
Another consideration in relation to the design of
the implant–abutment/restoration connection relates
to the potential for peri-implant tissue problems
caused by clinician error. Incorrect seating of implant
componentry, and in particular subgingival cement
retention, are factors which can create a local envi-
ronment that leads to the initiation of peri-implantitis,
especially in susceptible patients. In a case-series
report, it was shown that excess luting cement was
associated with peri-implant disease in 81% of 39
cases, and upon removal of the excess cement, the
clinical signs of disease resolved in 74% of these cases
(95). A recent study has shown a direct correlation
between the depth of the implant crown margin
below the mucosal margin and the amount of unde-
tected residual cement (56), underlying the impor-
tance of avoiding or limiting the submucosal extent of
the restorative margin in cement retained restora-
tions.
It is generally recognized that iatrogenic factors (e.g.
excess cement remnants, inadequate restoration–
abutment seating, over-contouring of restorations,
implant malpositioning and technical complications)
can predispose to peri-implant disease (50, 74). Clini-
cians should have appropriate clinical training and a
thorough understanding of the relevant implant sys-
tem in order to avoid these problems, which may
cause significant problems in susceptible patients.
Implant surface characteristics and
peri-implant disease
It has been suggested that the roughness of the
implant surface, as well as its chemical composition,
has a significant impact on the amount and quality of
plaque formed (89). Indeed, both hydroxyapatite-
coated and rough-surfaced implants have been asso-
ciated with increased incidence of biological compli-
cations (15, 71). However, these findings are of
limited relevance to contemporary practice as the
implant systems used in these studies are no longer
manufactured. Furthermore, the initiation of bone
loss around hydroxyapatite-coated implants was
11
Ivanovski & Lee
associated with the delamination of the coating, and
hence the biological mechanisms are different from
the conventional peri-implant mucositis–peri-implan-
titis pathogenesis. A recent systematic review based
on human clinical trials found no evidence of
increased susceptibility to peri-implantitis of cur-
rently available moderately rough surfaces, although
it was acknowledged that there is a scarcity of avail-
able data on this topic (77). Of particular interest is a
prospective, multicenter, randomized, controlled 5-
year clinical trial comparing a hybrid implant design
(the coronal component of the implant was
machined) with fully micro-rough implants, which
showed no difference in the incidence of peri-implan-
titis. However, it should also be noted that there is
experimental evidence from preclinical animal stud-
ies that some currently available moderately rough
surfaces may be more susceptible to peri-implant dis-
ease progression (10, 11), but these findings need to
be validated by clinical trials.
Conclusion
The integrity of the peri-implant soft-tissue seal is cru-
cial for maintaining peri-implant tissue health.
Although the transmucosal component of the restored
implant shares some common features with teeth,
namely the presence of a junctional epithelium and a
connective tissue component, there are some impor-
tant differences. A key difference is the nature of the
relationship between the connective tissue and the
implant surface, whereby there is ‘adaptation’ of col-
lagen fibers in a parallel orientation in relation to the
implant, but insertion of fiber attachment perpendic-
ularly into cementum in the case of teeth. This, com-
bined with reduced cellularity and vascularity in the
peri-implant connective tissue, may make them more
susceptible to disease initiation and progression.
In terms of disease etiology, dental plaque is the
primary factor in both peri-implantitis and periodon-
titis. However, the presence of a subgingival connec-
tion between the implant and the abutment/
restoration poses some specific challenges, and the
maintenance of the integrity of this connection is
important in maintaining peri-implant tissue health.
It should be noted that implant design features, such
as the nature of the connection between the implant
and the abutment, as well as the abutment and
implant surface characteristics, may influence the
maintenance of the soft-tissue integrity around
implants. Iatrogenic factors, such as incorrect seating
of the abutment and/or the restoration, and
12
subgingival cement retention, will lead to loss of soft-
tissue integrity and hence to peri-implant disease.
References
1. Abrahamsson I, Berglundh T, Wennstro € m J, Lindhe J. The
peri-implant hard and soft tissues at different implant sys-
tems. A comparative study in the dog. Clin Oral Implants
Res 1996: 7: 212–219.
2. Abrahamsson I, Berglundh T, Lindhe J. The mucosal barrier
following abutment dis/reconnection. J Clin Periodontol
1997: 24: 568–572.
3. Abrahamsson I, Berglundh T, Glantz PO, Lindhe J. The
mucosal attachment at different abutments. J Clin Peri-
odontol 1998: 25: 721–727.
4. Abrahamsson I, Berglundh T, Moon IS, Lindhe J. Peri-
implant tissues at submerged and non-submerged titanium
implants. J Clin Periodontol 1999: 26: 600–607.
5. Abrahamsson I, Zitzmann NU, Berglundh T, Wennerberg A,
Lindhe J. Bone and soft tissue integration to titanium
implants with different surface topography: an experimen-
tal study in the dog. Int J Oral Maxillofac Implants 2001: 16:
323–332.
6. Abrahamsson I, Zitzmann NU, Berglundh T, Linder E, Wen-
nerberg A, Lindhe J. The mucosal attachment to titanium
implants with different surface characteristics: an experi-
mental study in dogs. J Clin Periodontol 2002: 29: 448–455.
7. Abrahamsson I, Soldini C. Probe penetration in periodontal
and peri-implant tissues. An experimental study in the bea-
gle dog. Clin Oral Implants Res 2006: 17: 601–605.
8. Abrahamsson I, Cardaropoli G. Peri-implant hard and soft
tissue integration to dental implants made of titanium and
gold. Clin Oral Implants Res 2007: 18: 269–274.
9. Adell R, Lekholm U, Rockler B, Branemark PI, Lindhe J,
Eriksson B, et al. Marginal tissue reactions at osseointe-
grated titanium fixtures (I). A 3-year longitudinal prospec-
tive study. Int J Oral Maxillofac Surg 1986: 15: 39–52.
10. Albouy JP, Abrahamsson I, Persson LG, Berglundh T. Spon-
taneous progression of peri-implantitis at different types of
implants. An experimental study in dogs. I: clinical and
radiographic observations. Clin Oral Implants Res 2008: 19:
997–1002.
11. Albouy JP, Abrahamsson I, Persson LG, Berglundh T. Spon-
taneous progression of peri-implantitis at implants with dif-
ferent surface characteristics. An experimental study in
dogs II: histological observations. Clin Oral Implants Res
2009: 20: 366–371.
12. Al-Nsour M, Chang HL, Wang HL. Effect of platform switch-
ing technique on preservation of peri-implantmarginal
bone: a systematic review. Int J Oral Maxillofac Implants
2012: 27: 138–145.
13. Apse P, Zarb GA, Schmitt A, Lewis DW. The longitudinal
effectiveness of osseointegrated dental implants. The Tor-
onto Study: peri-implant mucosal response. Int J Periodon-
tics Restorative Dent 1991: 11: 94–111.
14. Armitage GC, Svanberg GK, Lo € e H. Microscopic evaluation
of clinical measurements of connective tissue attachment
levels. J Clin Periodontol 1977: 4: 173–190.
15. Astrand P, Engquist B, Dahlgren S, Gro € ndahl K, Engquist E,
Feldmann H. Astra Tech and Br anemark system implants: a

5-year prospective study of marginal bone reactions. Clin
Oral Implants Res 2004: 15: 413–420.
16. Berglundh T, Lindhe J, Ericsson I, Marinello CP, Liljenberg
B, Thomsen P. The soft tissue barrier at implants and teeth.
Clin Oral Implants Res 1991: 2: 81–90.
17. Berglundh T, Lindhe J, Jonsson K, Ericsson I. The topogra-
phy of the vascular systems in the periodontal and peri-
implant tissues in the dog. J Clin Periodontol 1994: 21: 189–
193.
18. Berglundh T, Lindhe J. Dimension of the periimplant
mucosa. J Clin Periodontol 1996: 23: 971–973.
19. Berglundh T, Abrahamsson I, Welander M, Lang NP, Lindhe
J. Morphogenesis of the peri-implant mucosa: an experi-
mental study in dogs. Clin Oral Implants Res 2007: 18: 1–8.
20. Bosshardt DD, Lang NP. The junctional epithelium: from
health to disease. J Dent Res 2005: 84: 9–20.
21. Botero JE, Gonza lez AM, Mercado RA, Olave G, Contreras A.
Subgingival microbiota in peri-implant mucosa lesions and
adjacent teeth in partially edentulous patients. J Periodon-
tol 2005: 76: 1490–1495.
22. Buser D, Weber HP, Donath K, Fiorellini JP, Paquette DW,
Williams RC. Soft tissue reactions to non-submerged
unloaded titanium implants in beagle dogs. J Periodontol
1992: 63: 225–235.
23. Cochran DL, Simpson J, Weber HP, Buser D. Attachment
and growth of periodontal cells on smooth and rough tita-
nium. Int J Oral Maxillofac Implants 1994: 9: 289–297.
24. Cochran DL, Hermann JS, Schenk RK, Higginbottom FL,
Buser D. Biologic width around titanium implants. a histo-
metric analysis of the implanto-gingival junction around
unloaded and loaded nonsubmerged implants in the
canine mandible. J Periodontol 1997: 68: 186–197.
25. Comut AA, Weber HP, Shortkroff S, Cui FZ, Spector M. Con-
nective tissue orientation around dental implants in a
canine model. Clin Oral Implants Res 2001: 12: 433–440.
26. Ericsson I, Lindhe J. Probing depth at implants and teeth:
an experimental study in the dog. J Clin Periodontol 1993:
20: 623–627.
27. Ericsson L, Randow K, Nilner K, Petersson A. Some clinical
and radiographical features of submerged and non-sub-
merged titanium implants. A 5-year follow-up study. Clin
Oral Implants Res 1997: 8: 422–426.
28. Etter TH, H akanson I, Lang NP, Trejo PM, Caffesse RG.
Healing after standardized clinical probing of the per-
limplant soft tissue seal: a histomorphometric study in
dogs. Clin Oral Implants Res 2002: 13: 571–580.
29. Gargiulo AW, Arrocha R. Histo-clinical evaluation of free
gingival grafts. Periodontics 1967: 5: 285–291.
30. Gracis S, Michalakis K, Vigolo P, Vult von Steyern P, Zwah-
len M, Sailer I. Internal vs. external connections for abut-
ments/reconstructions: a systematic review. Clin Oral
Implants Res 2012: 23: 202–216.
31. Gould TR, Westbury L, Brunette DM. Ultrastructural study
of the attachment of human gingiva to titanium in vivo.
J Prosthet Dent 1984: 52: 418–420.
32. Ha€mmerle CH, Bra €gger U, Bu€ rgin W, Lang NP. The effect of
subcrestal placement of the polished surface of ITI implants
on marginal soft and hard tissues. Clin Oral Implants Res
1996: 7: 111–119.
33. Heitz-Mayfield LJA. Peri-implant diseases: diagnosis and
risk indicators. Clin Oral Implants Res 2008: 35 (Suppl. 8):
292–304.
Comparison of periodontal and peri-implant soft tissues
34. Heitz-Mayfield LJA, Lang NP. Comparative biology of
chronic and aggressive periodontitis vs. peri-implantitis.
Periodontol 2000 2010: 53: 167–181.
35. Heitz-Mayfield LJ, Mombelli A. The therapy of peri-implan-
titis: a systematic review. Int J Oral Maxillofac Implants
2014: 29 (Suppl): 325–345.
36. Hermann JS, Cochran DL, Nummikoski PV, Buser D. Crestal
bone changes around titanium implants. a radiographic
evaluation of unloaded nonsubmerged and submerged
implants in the canine mandible. J Periodontol 1997: 68:
1117–1130.
37. Hermann JS, Buser D, Schenk RK, Cochran DL. Crestal
bone changes around titanium implants. a histometric
evaluation of unloaded non-submerged and submerged
implants in the canine mandible. J Periodontol 2000: 71:
1412–1424.
38. Hermann JS, Buser D, Schenk RK, Schoolfield JD, Cochran
DL. Biologic width around one-and two-piece titanium
implants. Clin Implant Dent Relat Res 2001: 12: 559–571.
39. Jansen VK, Conrads G, Richter EJ. Microbial leakage and
marginal fit of the implant abutment interface. Int J Oral
Maxillofac Implants 1997: 12: 527–540.
40. Jepsen S, Ru € hling A, Jepsen K, Ohlenbusch B, Albers HK.
Progressive peri-implantitis. Incidence and prediction of
peri-implant attachment loss. Clin Oral Implants Res 1996:
7: 133–142.
41. Joss A, Adler R, Lang NP. Bleeding on probing. A parameter
for monitoring periodontal conditions in clinical practice. J
Clin Periodontol 1994: 21: 402–408.
42. Karayiannis A, Lang NP, Joss A, Nyman S. Bleeding on prob-
ing as it relates to probing pressure and gingival health in
patients with a reduced but healthy periodontium. A clini-
cal study. J Clin Periodontol 1992: 19: 471–475.
43. Kim P, Ivanovski S, Latcham N, Mattheos N. The impact of
cantilevers on biological and technical success outcomes of
implant-supported fixed partial dentures. A retrospective
cohort study. Clin Oral Implants Res 2013: 25: 175–184.
44. Klinge B, Meyle J. Soft-tissue integration of implants. Con-
sensus report of Working Group 2. Clin Oral Implants Res
2006: 17: 93–96.
45. Kronstro € m M, Svenson B, Hellman M, Persson GR. Early
implant failures in patients treated with Branemark System
titanium dental implants: a retrospective study. Int J Oral
Maxillofac Implants 2001: 16: 201–207.
46. Lang NP, Adler R, Joss A, Nyman S. Absence of bleeding on
probing. An indicator of periodontal stability. J Clin Peri-
odontol 1990: 17: 714–721.
47. Lang NP, Nyman S, Senn C, Joss A. Bleeding on probing as
it relates to probing pressure and gingival health. J Clin
Periodontol 1991: 18: 257–261.
48. Lang NP, Bra €gger U, Walther D, Beamer B, Kornman KS.
Ligature-induced peri-implant infection in cynomolgus
monkeys. I. Clinical and radiographic findings. Clin Oral
Implants Res 1993: 4: 2–11.
49. Lang NP, Wetzel AC, Stich H, Caffesse RG. Histologic probe
penetration in healthy and inflamed peri-implant tissues.
Clin Oral Implants Res 1994: 5: 191–201.
50. Lang NP, Berglundh T, on Behalf of Working Group 4 of the
Seventh European Workshop on Periodontology. Periim-
plant diseases: where are we now? – Consensus of the
Seventh European Workshop on Periodontology. J Clin
Periodontol 2011: 38 (Suppl. 11): 178–181.
13
Ivanovski & Lee
51. Lazzara RJ, Porter SS. Platform switching: a new concept in
implant dentistry for controlling postrestorative crestal
bone levels. Int J Periodontics Restorative Dent 2006: 26:
9–17.
52. Lekholm U, Adell R, Lindhe J, Br anemark PI, Eriksson B,
Rockler B, Lindvall AM, Yoneyama T. Marginal tissue reac-
tions at osseointegrated titanium fixtures. (II) A cross-sec-
tional retrospective study. Int J Oral Maxillofac Surg 1986:
15: 53–61.
53. Leonhardt A, Renvert S, Dahle n G. Microbial findings at
failing implants. Clin Oral Implants Res 1999: 10: 339–345.
54. Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C.
Experimental breakdown of peri-implant and periodontal
tissues. A study in the beagle dog. Clin Oral Implants Res
1992: 3: 9–16.
55. Lindhe J, Berglundh T. The interface between the mucosa
and the implant. Periodontol 2000 1998: 17: 47–54.
56. Linkevicius T, Vindasiute E, Puisys A, Linkeviciene L,
Maslova N, Puriene A. The influence of the cementation
margin position on the amount of undetected cement. A
prospective clinical study. Clin Oral Implants Res 2013: 24:
71–76.
57. Listgarten MA, Lang NP, Schroeder HE, Schroeder A. Peri-
odontal tissues and their counterparts around endosseous
implants. Clin Oral Implants Res 1991: 21: 1–19.
58. Listgarten MA, Buser D, Steinemann SG, Donath K, Lang
NP, Weber HP. Light and transmission electron microscopy
of the intact interfaces between non-submerged titanium-
coated epoxy resin implants and bone or gingiva. J Dent Res
1992: 71: 364–371.
59. Luterbacher S, Mayfield L, Bra €gger U, Lang NP. Diagnostic
characteristics of clinical and microbiological tests for mon-
itoring periodontal and peri-implant mucosal tissue condi-
tions during supportive periodontal therapy (SPT). Clin
Oral Implants Res 2000: 11: 521–529.
60. Maeda Y, Miura J, Taki I, Sogo M. Biomechanical analysis
on platform switching: is there any biomechanical ratio-
nale? Clin Oral Implants Res 2007: 18: 581–584.
61. Magnusson I, Listgarten MA. Histological evaluation of
probing depth following periodontal treatment. J Clin Peri-
odontol 1980: 7: 26–31.
62. Mombelli A, van Oosten MA, Schurch E Jr, Land NP. The
microbiota associated with successful or failing osseointe-
grated titanium implants. Oral Microbiol Immunol 1987: 2:
145–151.
63. Mombelli A, Buser D, Lang NP. Colonization of osseointe-
grated titanium implants in edentulous patients. Early
results. Oral Microbiol Immunol 1988: 3: 113–120.
64. Mombelli A, De caillet F. The characteristics of biofilms in
peri-implant disease. J Clin Periodontol 2011: 38 (Suppl.
11): 203–213.
65. Moon IS, Berglundh T, Abrahamsson I, Linder E, Lindhe J.
The barrier between the keratinized mucosa and the dental
implant. An experimental study in the dog. Osteoporos Int
1999: 9: 290–295.
66. Nevins M, Nevins ML, Camelo M, Boyesen JL, Kim DM.
Human histologic evidence of a connective tissue attach-
ment to a dental implant. Int J Periodontics Restorative Dent
2008: 28: 110–121.
67. Nevins M, Kim DM, Jun SH, Guze K, Schupbach P, Nevins
ML. Histologic evidence of a connective tissue attachment
14
to laser microgrooved abutments: a canine study. Int J Peri-
odontics Restorative Dent 2010: 30: 245–255.
68. Nevins M, Camelo M, Nevins ML, Schupbach P, Kim DM.
Connective tissue attachment to laser-microgrooved abut-
ments: a human histologic case report. Int J Periodontics
Restorative Dent 2012: 32: 385–392.
69. Oh TJ, Yoon J, Misch CE, Wang HL. The causes of early
implant bone loss: myth or science? J Periodontol 2002: 73:
322–333.
70. Persson LG, Lekholm U, Leonhardt A, Dahle n G, Lindhe J.
Bacterial colonization on internal surfaces of Br anemark
system implant components. Clin Oral Implants Res 1996:
7: 90–95.
71. Piattelli A, Cosci F, Scarano A, Trisi P. Localized chronic
suppurative bone infection as a sequel of peri-implantitis in
a hydroxyapatitecoated dental implant. Biomaterials 1995:
16: 917–920.
72. Polson AM. Interrelationship of inflammation and tooth
mobility (trauma) in pathogenesis of periodontal disease.
J Clin Periodontol 1980: 7: 351–360.
73. Pontes AE, Ribeiro FS, Iezzi G, Piattelli A, Cirelli JA, Marcan-
tonio E Jr. Biologic width changes around loaded implants
inserted in different levels in relation to crestal bone: histo-
metric evaluation in canine mandible. Clin Oral Implants
Res 2008: 19: 483–490.
74. Qian J, Wennerberg A, Albrektsson T. Reasons for marginal
bone loss around oral implants. Clin Implant Dent Relat
Res 2012: 14: 792–807.
75. Quirynen M, van Steenberghe D. Bacterial colonization of
the internal part of two stageimplants. An in vivo study.
Clin Oral Implants Res 1993: 4: 158–161.
76. Renvert S, Roos-Jans aker AM, Claffey N. Non-surgical treat-
ment of peri-implant mucositis and peri-implantitis: a liter-
ature review. J Clin Periodontol 2008: 35 (Suppl): 305–315.
77. Renvert S, Polyzois I, Claffey N. How do implant surface
characteristics influence periimplant disease? J Clin Peri-
odontol 2011: 38 (Suppl. 11): 214–222.
78. Rosenberg ES, Torosian JP, Slots J. Microbial differences in
2 clinically distinct types of failures of osseointegrated
implants. Clin Oral Implants Res 1991: 2: 135–144.
79. Salvi GE, Lang NP. Diagnostic parameters for monitoring
peri-implant conditions. Int J Oral Maxillofac Implants
2004: 19 (Suppl): 116–127.
80. Sanz M, Chapple IL; Working Group 4 of the VIII European
Workshop on Periodontology. Clinical research on peri-
implant diseases: consensus report of working group 4.
J Clin Periodontol 2012: 39 (Suppl. 12): 202–206.
81. Schou S, Holmstrup P, Reibel J, Juhl M, Hjørting-Hansen E,
Kornman KS. Ligature-induced marginal inflammation
around osseointegrated implants and ankylosed teeth:
stereologic and histologic observations in cynomolgus
monkeys (Macaca fascicularis). J Periodontol 1993: 64: 529–
537.
82. Schou S, Holmstrup P, Stoltze K, Hjørting-Hansen E, Fiehn
NE, Skovgaard LT. Probing around implants and teeth with
healthy or inflamed peri-implant mucosa/gingiva. A histo-
logic comparison in cynomolgus monkeys (Macaca fascicu-
laris). Clin Oral Implants Res 2002: 13: 113–126.
83. Schroeder HE, Listgarten MA. The gingival tissues: the
architecture of periodontal protection. Periodontol 2000
1997: 13: 91–120.

84. Schwarz F, Herten M, Sager M, Wieland M, Dard M, Becker
J. Histological and immunohistochemical analysis of initial
and early subepithelial connective tissue attachment at
chemically modified and conventional SLA titanium
implants. A pilot study in dogs. Clin Oral Investig 2007: 11:
245–255.
85. Schwarz F, Mihatovic I, Becker J, Bormann KH, Keeve PL,
Friedmann A. Histological evaluation of different abut-
ments in the posterior maxilla and mandible: an experi-
mental study in humans. J Clin Periodontol 2013: 40: 807–
815.
86. Seymour GJ, Powell RN, Davies WI. The immunopathogen-
esis of progressive chronic inflammatory periodontal dis-
ease. J Oral Pathol 1979: 8: 249–265. Review.
87. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres
M. Composition of supra- and subgingival biofilm of sub-
jects with healthy and diseased implants. Clin Oral
Implants Res 2008: 19: 975–982.
88. Tesmer M, Wallet S, Koutouzis T, Lundgren T. Bacterial
colonization of the dental implant fixture-abutment
interface: an in vitro study. J Periodontol 2009: 80: 1991–
1997.
89. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of
material characteristics and or surface topography on bio-
film development. Clin Oral Implants Res 2006: 17 (Suppl.
2): 68–81.
Comparison of periodontal and peri-implant soft tissues
90. Tomasi C, Tessarolo F, Caola I, Wennstro €m J, Nollo G, Ber-
glundh T. Morphogenesis of peri-implant mucosa revisited:
an experimental study in humans. Clin Oral Implants Res
2014: 25: 997–1003.
91. Vacek JS, Gher ME, Assad DA, Richardson AC, Giambarresi
LI. The dimensions of the human dentogingival junction.
Int J Periodontics Restorative Dent 1994: 14: 154–165.
92. Vigolo P, Givani A, Majzoub Z, Cordioli G. A 4-year prospec-
tive study to assess peri-implant hard and soft tissues adja-
cent to titanium versus gold-alloy abutments in cemented
single implant crowns. J Prosthodont 2006: 15: 250–256.
93. Watzak G, Zechner W, Tangl S, Vasak C, Donath K, Watzek
G. Soft tissue around three different implant types after
1.5 years of functional loading without oral hygiene: a pre-
liminary study in baboons. Clin Oral Implants Res 2006: 17:
229–236.
94. Welander M, Abrahamsson I, Berglundh T. The mucosal
barrier at implant abutments of different materials. Clin
Oral Implants Res 2008: 19: 635–641.
95. Wilson TG Jr. The positive relationship between excess
cement and peri-implant disease: a prospective clinical
endoscopic study. J Periodontol 2009: 80: 1388–1392.
96. Zitzmann NU, Berglundh T. Definition and prevalence of
peri-implant diseases. J Clin Periodontol 2008: 35 (Suppl. 8):
286–291.
15