REVIEW ARTICLE

Epithelial Attachment and Downgrowth on Dental Implant

AbutmentsA Comprehensive Review
GERHARD IGLHAUT, DDS*, FRANK SCHWARZ, DDS, PhD, ROBERT R. WINTER, DDS, ILJA MIHATOVIC, DDS,
MICHAEL STIMMELMAYR, DDS, HENNING SCHLIEPHAKE, DDS, MD, PhD

ABSTRACT
The soft tissues around dental implants are enlarged compared with the gingiva because of the longer junctional
epithelium and the hemidesmosonal attachments are fewer, suggestive of a poorer quality attachment. Inflammatory
infiltrates caused by bacterial colonization of the implant-abutment interface are thought to be one of
the factors causing epithelial downgrowth and subsequent peri-implant bone loss. Gold alloys and dental ceramics
as well as the contamination of the implant surface with amino alcohols, appear to promote epithelial
downgrowth. Physical manipulaton of the abutment surfaces, including concave abutment designs, platform switching,
and microgrooved surfaces are believed to inhibit epithelial downgrowth and minimizes bone loss at the implant
shoulder. This paper reviews the factors that are believed to influence the migration of epithelial attachment
the dental implant and abutment surfaces. Exploration of innovative computer-aided design/computer-aided
manufacturing-based concepts such as one abutmentone time and their effect on epithelial downgrowth are
discussed.

CLINICAL SIGNIFICANCE
Based on the review of current literature, the authors recommend inserting definitive abutments at the time of
surgical uncovering. To implement this concept, registration of the implant position should to be taken at the time of
surgical implant placement.
(J Esthet Restor Dent 26:324331, 2014)

INTRODUCTION
Clinical observations of patients without inammatory
conditions over several years showed that substantial
peri-implant tissue loss may occur within no more than
2 to 5 years post-prosthodontic rehabilitation and cause
considerable esthetic compromise. Immediate implant
placement and prosthodontic rehabilitation often
appear to be associated with esthetic problems.1 This
has prompted a search for the factors of peri-implant

tissue recession apparently unrelated to inammatory

processes and the conditions required to ensure stable
long-term results.
The three-dimensional position of the implant appears
to be a critical factor for an acceptable esthetic
outcome.2 Based on studies of the sagittal dimension,
Evans and Chen3 recommend implant placement in a
more palatal position. Implants oriented in a buccal
position were associated with three times more

*Director, Oral Surgery Office, Bahnhofstrasse 20, 87700 Memmingen, Germany

Associate Professor, Department of Oral Surgery, Heinrich-Heine University, Moorenstrasse 5, 40225 Dsseldorf, Germany

Prosthodontist, Private Office, 9942 E Chiricahua Pass, Scottsdale, AZ 85262, USA

Oral Surgeon, Oral Surgery Office, Josef-Heiligbrunnerstrasse 2, 93413 Cham, Germany

Head, Department of Oral and Maxillofacial Surgery, George-Augusta-University Gttingen, Robert-Koch-Strasse 40, 37075 Gttingen, Germany

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EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

soft-tissue recession than implants oriented in a palatal

aspect (1.8 versus 0.6 mm). In the horizontal dimension,
a distance of 1.5 to 2 mm from the roots of the
neighboring teeth has been recommended.4 The
vertical position of the implant shoulder should be
oriented to the buccal bone level of the neighboring
teeth.5 The attachment levels associated with
two-piece implants and standard abutment connections
can be distinguished from abutment connections with
platform switching. This may be related to unfavorable
eects of the microgap between the implant shoulder
and the abutment.6 Thin soft-tissue structures
may, however, lead to unpleasant grayish-livid
discolorations.7
What anatomical tissue dimensions are required
for an acceptable long-term esthetic outcome? One
study8 demonstrated that with a baseline bone
thickness of 1.8 mm or more at the level of the
implant shoulder, there was no loss of bone after
healing, and in some cases, there was a gain in bone.
Comparing bone thickness of 1 and 2 mm at implant
neck, Baone and colleagues9 failed in recent animal
experiments to detect any dierences in bone volume
after a healing time of 3 months. Grunder and
colleagues2 claimed that the vestibular and approximal
bone volume should be sucient to guarantee a circular
bone thickness of 2 mm at the implant shoulder. He
concluded that the proper implant diameter in the
anterior region is normally limited to 4 mm
or less.
The soft-tissue volume also appears to be a factor
aecting peri-implant tissue stability.10 Periodontal soft
tissues are considered as thin biotype if they are less
than 1 mm, and thick biotype if they show a tissue
thickness of 1.0 to 1.3 mm.11 Thin biotype tissue tends
to be associated with substantially more pronounced
recession. This suggests the use of soft-tissue grafts12,13
or combined soft-tissue/onlay grafts to gain tissue
thickness.1416 The width of the attached gingiva is
thought to be yet another factor determining tissue
stability. Therefore, the maintenance or establishment
of a keratinized peri-implant mucosa to a width of
3 mm or more has been recommended in several
studies.1719

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SOFT-TISSUE INTERFACE AROUND

ORAL IMPLANTS
Gargiulo and colleagues20 showed in a human histologic
study the average apicocoronal soft-tissue dimension
around teeth, and consequently the soft-tissue cu
above the bone level, to have a mean width of 2.73 mm,
with a mean epithelium portion of 1.66 mm, and a
mean connective tissue portion of 1.06 mm. In total the
connective tissue attachment and the epithelial
attachment showed an average mean width of 2.04 mm
and was described as biologic width. Vacek and
colleagues21 found similar dimensions of dentogingival
junction. Thus, the epithelium is about 1 mm in
distance to the alveolar bone. The attachment to the
root cementum possibly acts as a seal and may help to
exclude microorganisms. The junctional epithelium is
mechanically attached to the tooth surface (enamel and
root cementum) by hemidesmosomes,22 whereas the
connective tissue is mechanically and chemically
attached to the root cementum by perpendicularly
oriented collagen bers described as Sharpeys bers.23
Measuring clinically the soft-tissue width between the
bone margin and the gingival margin, Kois24 subdivided
it in three biotypes: Based on clinical probing, he
described a buccal probing depth of approximately
3 mm as normal crest type (85% of subjects), a probing
depth of 3.5 to 4 mm as low crest type (13% of
subjects), and a probing depth of 2 to 2.5 mm as high
crest type (2% of subjects).
In animal experiments,25 the peri-implant soft-tissue
dimension was slightly enlarged (33.5 mm). A barrier
epithelium facing the abutment surface showed a height
about 2 mm followed by a connective tissue portion of
1 to 1.5 mm above the alveolar bone crest, apparently in
direct contact to the TiO2 layer of the implant. A
comparison of dierent implant systems did not show
any variations.26 The barrier epithelium seems to be
attached to titanium surfaces by hemidesmosomes23
and provide a mucosal attachment. As there is no root
cement, connective tissue attachment to implants
diers from that to natural teeth: Unlike compared
natural teeth, the collagen ber bundles are not
perpendicularly arranged, but rather parallel to the
implant surface.25 Mechanical and chemical

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attachment to the titanium surface is absent.

Instead, a proteoglycane layer the thickness of 20 m
could be shown. The connective tissue composition also
shows dierences: Around natural teeth tissue is
comprised of approximately 60% collagen bers and 5
to 15% broblasts, compared with 85% collagen
bers and 1 to 3% broblasts around titanium implants.
Thus, mucosal connective tissue resembles scar tissue.
Blood vessels were shown less abundant in peri-implant
soft tissue. The vasculary blood supply to gingival
structures is provided by large supraperiosteal blood
vessels and by the vascular plexus of the periodontal
ligament. The vascular system of the peri-implant soft
tissue is limited to the large supraperiosteal blood
vessel. Due to the lack of periodontal ligament, a
vascular plexus is missing at the interface of crestal
bone and implant surface. This nding was supported
by Moon and colleagues.27 In a zone of 40 m close to
the titanium surface, the number of blood vessels was
extremely low (0.3%). As a result, immune responses
around oral implants may be reduced.28 Schwarz
and colleagues29 showed in a dog study, that
well-vascularized subepithelial connective tissue could
develop around chemically modied, acid-etched as
well as chemically modied grit-blasted and
acid-etched titanium surfaces. After 14 days of open
healing, collagen bers radial oriented to the implant
surface were histologically proved. Highly hydrophilic
surfaces appear to promote proper soft-tissue
integration.

FACTORS AFFECTING EPITHELIAL

DOWNGROWTH
Epithelial downgrowth on titanium surfaces is
attributable to coronalapical proliferation and
migration of epithelial cells derived from the mucosa
surrounding the wound surface forming a junctional
epithelium of a thickness of about 2 mm.30 The
presence of granulation tissue in contact with the
transmucosal titanium surfaces is thought to be a
primary factor limiting apical epithelial migration.31
Animal experiments conrmed the important role
connective tissue plays in preventing epithelial
downgrowth.32,33 The location of the junctional

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epithelium appears to be determined by the initial

phases of wound healing.34
Results of animal studies demonstrate the inuence of
the physical design of the implant systems on the height
of the junctional epithelium, i.e., two-part bone-level
versus single-part tissue-level implants, have varied
widely. Hermann and colleagues6 found signicantly
more apical epithelial migration around bone-level
implants and postulated that the transmucosal
abutmentimplant interface (microgap) was a
negative factor explaining peri-implant bone loss. This
contrasts with several other studies documenting
soft-tissue adaptation at the abutment level.25,26,30,35
However, inammatory cell inltrates were seen only
around bone-level implants; they were absent around
tissue-level implants.35 The inltrates appear to be
caused by bacterial colonization translocated from the
oral cavity to the abutmentimplant interface.3639
Harder and colleagues40,41 conrmed that endotoxin
microleakage also occurred at conical
abutmentimplant connections and detected
lipopolysaccharide-mediated proinammatory cytokine
gene expression. Endotoxins of gram-negative bacteria
may induce alveolar bone resorption via the
osteoclast-activating pathway.42 These small molecule
complexes of lipopolysaccharides and proteins can
penetrate small gaps and are known to play a major role
in bone destruction processes.
Material properties appear to be another factor
aecting epithelial downgrowth. Animal experiments
showed a peri-implant cu of about 3.5 mm in width to
be present around abutments of pure titanium and
Al2O3 ceramics. Around abutments of gold and gold
alloys fused with dental ceramics, the soft-tissue
attachment migrated toward the implant neck and
associated bone loss was noted.43 Kohal and colleagues44
reported favorable soft-tissue formation on both
titanium and ZrO2 surfaces. In a further animal study,
the soft-tissue dimension at Ti and ZrO2 abutments
remained stable after 5 months of healing. However, at
gold/platinum alloys abutment sites, an apical shift of
the barrier epithelium and marginal bone lost
occurred.45 In a 4-year prospective clinical study, Vigolo
and colleagues46 evaluated abutments of titanium versus

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EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

gold alloy when used with cemented single implant

crowns. Statistical analysis revealed no signicant
dierences regarding peri-implant bone loss and
soft-tissue level. In a systematic review, Linkevicius and
colleagues47 evaluated available evidence for dierences
related to peri-implant tissue stability around titanium
abutments versus gold alloy, zirconium oxide, or
aluminum oxide. The included studies failed to give
evidence that titanium abutments maintain a higher
bone level in comparison with other materials.

Farronato and colleagues54 found signicantly less

epithelial attachment and less peri-implant bone loss
for implants with platform switching than for those
with standard abutmentimplant connections.
Connective tissue adaptation by contrast, was of similar
width. In a systematic review and meta-analysis,55
implants with a mismatch of 0.4 mm were found to be
associated with less bone loss (mean 0.37 mm). Despite
the maintenance of the soft-tissue level, the clinical
relevance appears in question.

The negative eect of abutment surface contamination

and eective cleaning has also been discussed.48 In this
context, the removal of rmly adherent amino alcohols
appears to be a problem factor.49 Amino-alcohol
solution was supplied in vitro on machined titanium
surfaces and four dierent methods were used to
remove the adsorbed alcohol. Rinsing in water, saline
solution, and 5% H2O2 solution failed to remove the
amino-alcohol; however, ozone exposure resulted in
complete removal of the alcohol from the titanium
surface. Using an ultrasonic cleaning (Clemson
bioengineering cleaning [CBC]) protocol on both
titanium and aluminum oxide surfaces removed an
average 99.96% of contaminants.50 A further study
evaluated the eect of multiple sterilization on in vitro
cell attachment on pure titanium surfaces.51 Ultraviolet
sterilized surfaces showed no changes related to cell
attachment levels. In contrast, both ethylene oxide and
steam autoclave sterilization altered the titanium
surface and decreased levels of cell attachment. In an
animal study, contaminated titanium abutments were
cleaned ultrasonically in butanol and ethanol or only
rinsed in saline solution, before being implanted in the
abdominal wall of rats.52 New uncontaminated titanium
abutments were inserted as a control group.
Irrespective of cleaning procedure, all contaminated
components induced an altered tissue response
compared to controls.

In an animal study, Schwarz and colleagues29

demonstrated evidence that 14 days after soft-tissue
healing, perpendicularly oriented collagen bers could
be promoted to high hydrophilic titanium surface.
In a following study,56 however, the resistance to
probing was quite poor. Clinical probing more than two
times increased mean-probing depth and markedly
disrupted the epithelial and connective tissue
attachment. Nevins and colleagues57 examined the
attachment of soft tissues to titanium surfaces
microgrooved with a pulsed laser histologically and
microscopically by polarized light and scanning electron
microscopy. They showed evidence that after 6 months
of healing, the soft tissue in humans was attached
mechanically by perpendicular collagen ber bundles
on a microgrooved surface. In a clinical study up to

Animal experiments and clinical studies conrmed the

eect of the abutment design on epithelial downgrowth.
Becker and colleagues53 showed the junctional
epithelium to end at the mismatch of the implant
shoulder of tapered implants (platform switching,
mismatch 0.30.5 mm). In another animal experiment,

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FIGURE 1. Histologic specimen showing peri-implant soft

and hard tissues around a titanium abutment with a laser
microgrooved surface.

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EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

2,200.00

100.00
o2

2,000.00

80.00

Percentage

1,800.00
1,600.00
1,400.00

40.00

1,200.00
1,000.00

20.00
M

LP
Type

LC

FIGURE 2. Comparative histomorphometric data of the

junctional epithelium around machined (M) and laser
microgrooved surfaces with a width of 0.7 mm (LaserLok
partial [LP]) and 2.9 mm (LaserLok complete [LC]).

100.00

Percentage

80.00
60.00
40.00
20.00
0.00
M

LP

LC

FIGURE 4. Soft-tissue attachment in percent to machined

(M) and laser microgrooved surfaces with a width of 0.7 mm
(LP) and 2.9 mm (LC) after two abutment reconnections.

37 months, Pecora and colleagues58 found a positive

eect on probing depth and maintenance of
peri-implant bone around implants with a
microstructured shoulder surface in contrast to
implants with machined surface. The high mechanical
stability of this attachment suggests the formation of a
soft-tissue seal above the crestal bone.
Kim and colleagues59 compared the eects of abutment
shapes relative with bone levels. They compared
concave microgrooved transmucosal proles, convex

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60.00

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LP

LC

FIGURE 3. Soft-tissue attachment in percent to machined

(M) and laser microgrooved surfaces with a width of 0.7 mm
(LP) and 2.9 mm (LC).

machined proles, and straight anodically oxidized

proles of bone-level implants. Around convex
machined proles, the junctional epithelium was found
longer, around concave microgrooved proles
connective tissue attachment was more extended and
the bone-level stable. Two animal studies60,61 apparently
support positive eects of concave microgrooved
abutment surfaces related to the maintenance of
peri-implant soft- and hard-tissue structures. In a
recent animal study, Iglhaut and colleagues61 compared
soft- and hard-tissue stability around abutments with
machined versus 0.8 mm microgrooved versus 2.8 mm
microgrooved titanium surface. The author concluded
that the width of microgrooved abutment surfaces was
negatively correlated to the extent of epithelial
downgrowth (Figures 1 and 2), and was positively
correlated to the extent of connective tissue attachment
and crestal bone level (Figure 3).
Abutment dis/reconnection seems to have an important
eect on tissue-level maintenance adjacent to dental
implants. In an animal study, Abrahamsson and
colleagues62 demonstrated apical epithelial downgrowth
and peri-implant bone loss when abutments were
dis/reconnection with alcohol disinfection ve times at
monthly intervals. Iglhaut and colleagues61 observed a
negative eect even after two abutment
dis/reconnections (Figure 4). In contrast, Hermann and
colleagues63 found in a dog study no negative eect on

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EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

the peri-implant tissue after ve abutment

dis/reconnections without alcohol disinfection. In a
further animal study, Hermann and colleagues64
described unfavorable eects of micromobile abutments
independent of the width of the microgap. Based on
these studies, tissue loss was hypothesized to be
minimized by one-stage insertion of denitive
abutments and immediate prosthodontic rehabilitation
(one abutmentone time concept). Clinical studies6365
conrmed that this procedure seems to have a positive
eect on the maintenance of peri-implant soft and hard
tissue. However, Canullo and colleagues66 mentioned
that the dierence of 0.2 mm might have a poor clinical
eect.
Based on the review of current literature, the authors
recommend inserting denitive abutments at the time
of surgical uncovering. To implement this concept,
registration of the implant position should to be taken
at the time of surgical implant placement.

6.

7.

8.

9.

10.

11.
12.

DISCLOSURE
The authors have no nancial interest in any of the
companies whose products were mentioned in this
paper.

13.

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Reprint requests: Gerhard Iglhaut, DDS, Oral Surgery Office,

Bahnhofstrasse 20, 87700 Memmingen, Germany; Tel.: +498331-2864;
Fax: +498331-44528; email: dr.iglhaut@t-online.de

Journal of Esthetic and Restorative Dentistry

Vol 26 No 5 324331 2014

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