Received: 3 July 2016 | Revised: 22 August 2017 | Accepted: 8 September 2017

DOI: 10.1111/jcpe.12952

2017 WORLD WORKSHOP

Peri‐implant health

Mauricio G. Araujo1 | Jan Lindhe2

1
Department of Dentistry, State University
of Maringa, Maringa, Brazil Abstract
2
Department of Objective: The aim is to define clinical and histologic characteristics of peri‐implant
Periodontology, Sahlgrenska,
tissues in health and describe the mucosa–implant interface.
Academy at University of Gothenburg,
Gothenburg, Sweden Importance: An understanding of the characteristics of healthy peri‐implant tissues
facilitates the recognition of disease (i.e., departure from health).
Correspondence
Dr. Mauricio Araujo, Department of Findings: The healthy peri‐implant mucosa is, at the microscopic level, comprised of
Dentistry, State University of Maringa,
a core of connective tissue covered by either a keratinized (masticatory mucosa) or
Maringa, Brazil.
Email: [email protected] non‐keratinized epithelium (lining mucosa). The peri‐implant mucosa averages about
3 to 4 mm high, and presents with an epithelium (about 2 mm long) facing the implant
The proceedings of the workshop were
jointly and simultaneously published in
surface. Small clusters of inflammatory cells are usually present in the connective
the Journal of Periodontology and Journal of tissue lateral to the barrier epithelium. Most of the intrabony part of the implant ap‐
Clinical Periodontology.
pears to be in contact with mineralized bone (about 60%), while the remaining por‐
tion faces bone marrow, vascular structures, or fibrous tissue. During healing
following implant installation, bone modeling occurs that may result in some reduc‐
tion of the marginal bone level.
Conclusions: The characteristics of the peri‐implant tissues in health are properly
identified in the literature, including tissue dimensions and composition. Deviation
from the features of health may be used by the clinician (and researcher) to identify
disease, including peri‐implant mucositis and peri‐implantitis.

KEYWORDS
connective tissue biology, diagnosis, implantology, osseointegration

Peri‐implant tissues are those that occur around osseointegrated the aim of the present review was to define clinical and histologic
dental implants. They are divided into soft and hard tissue compart‐ characteristics of peri‐implant tissues in health and describe the mu‐
ments. The soft tissue compartment is denoted “peri‐implant mu‐ cosa–implant interface.
cosa” and is formed during the wound healing process that follows A search in MEDLINE‐PubMed was used to retrieve the evidence
1
implant/abutment placement. The hard tissue compartment forms to support the present review. The following key words were used for
a contact relationship to the implant surface to secure implant sta‐ the literature search: dental implants (Mesh) AND biological width
bility. 2 Due to their histologic and anatomic features, peri‐implant OR mucosa OR soft tissue OR attachment OR keratinized mucosa OR
tissues carry out two basic functions: the mucosa protects the un‐ peri‐implant mucosa OR probing depth OR microbiota OR collagen
derlining bone, while the bone supports the implant. Indeed, the fibers OR epithelium OR adhesion OR seal OR bone OR osseointegra‐
destruction of peri‐implant tissues can jeopardize the implant suc‐ tion AND humans OR animals. The two main reasons for exclusion of
cess and survival,3 and the understanding of the characteristics of studies were: 1) not published in English, and 2) lack of detailed clinical,
healthy peri‐implant tissues allows the recognition of disease. Thus, histologic, or microbiologic description of healthy peri‐implant tissues.

© 2018 American Academy of Periodontology and European Federation of Periodontology

S230 | wileyonlinelibrary.com/journal/jcpe J Clin Periodontol. 2018;45(Suppl 20):S230–S236.

ARAUJO and LINDHE | S231

PE R I ‐ I M PL A NT M U COSA with mainly neutrophils and limited amounts of macrophages. The

number of inflammatory cells subsequently subsided, and the wound
Most information regarding the structural features of the peri‐im‐ surface became characterized by its dense layer of fibroblasts that
plant mucosa is derived from animal studies using dog models.4‒15 In appeared to be in intimate contact with the implant surface. In the
such studies implants were placed in the edentulous ridge (alterna‐ 2nd to 3rd week of healing, the density of fibroblasts was reduced,
tively, the fresh extraction socket), the outer osseous part of which the amount of collagen and matrix components increased, and epi‐
was covered with masticatory mucosa. It was also shown that the thelial cells, extending from the oral epithelium, had started to oc‐
healed peri‐implant mucosa on the buccal aspect averaged about 3 cupy marginal parts of the connective tissue wound. Collagen fibers
to 4 mm high when measured from the mucosal margin to the crest in the previous wound area became organized in bundles after about
of the peri‐implant bone. In addition, this mucosa contains a core 4 weeks. After 6 to 8 weeks the mucosal adhesion appeared mature,
of connective tissue, mainly comprised of collagen fibers and ma‐ and the interface zone at tissue–implant was comprised of a com‐
trix elements (85%), comparatively few fibroblasts (3%), and vas‐ bined epithelial and connective tissue adhesion to the implant sur‐
cular units (5%). The outer (oral) surface of the connective tissue is face. Since the build‐up of the soft tissue adhesion did not change
covered by an often orthokeratinized epithelium. The portion of the much after the first month, it is suggested that a homeostasis had
peri‐implant mucosa that is facing the implant (abutment) contains been reached at this interval.1
two distinct parts, a “coronal” portion that is lined by a thin barrier
epithelium (similar to the junctional epithelium of the gingiva) and
D I M E N S I O N O F TH E PE R I ‐ I M PL A NT
sulcular epithelium, and a more “apical” segment in which the con‐
M U COSA
nective tissue appears to be in direct contact with the implant sur‐
face. This apical portion of the peri‐implant mucosa is designated
Animal studies
zone of connective tissue adhesion.
In the connective tissue immediately lateral to the barrier and The dimension of the peri‐implant mucosa, often called the biologi‐
sulcular epithelium, a delicate plexus of vascular structures, simi‐ cal width or dimension,5 was examined in biopsies mainly obtained
16 17
lar to the dentogingival vascular plexus, is consistently present, from studies in dogs.19‒26 Such measurements disclosed that a cer‐
while the connective tissue adhesion zone appears to harbor only tain width of soft tissue may be required to cover the peri‐implant
limited amounts of vascular structures. At implants placed into mas‐ bone. The studies referred to the length of the epithelium (from the
ticatory mucosa, the main collagen fiber bundles are anchored in the peri‐implant mucosa margin to the apical portion of the junctional
crestal bone and extend in a marginal direction parallel to the sur‐ epithelial) as about 2 mm, while the height of the zone of connective
face of the metal device. It is assumed that circular fibers may also be tissue adhesion exhibited more variation (between 1 and 2 mm). The
present in this type of peri‐implant mucosa. experiments in the animal model included the study of different vari‐
Moon et al.18 analyzed under electron scanning microscope the ables such as material used for the fabrication of the implant and/
zone of connective tissue adhesion confined to a 200‐μm wide zone or the abutment, surgical placement protocol, implants/abutments
of the connective tissue facing the implant. The findings demon‐ with different surface texture,5,19‒23 as well as so‐called implants
strated that the adhesion includes two distinct layers: one inner with a “platform switching” implant/abutment design. 24‒26 The re‐
layer, about 40 μm wide, which harbors large amounts of fibroblasts sults obtained documented that while abutments made of gold alloy
(32% of volume) that appear to be in intimate contact with the sur‐ and dental porcelain failed to establish appropriate soft tissue adhe‐
face of the implant; and one outer layer, about 160 μm wide, that is sion, 23 other variables had apparently limited effect on the dimen‐
dominated by collagen fibers (83%), smaller amounts of fibroblasts sions of the peri‐implant mucosa.
(11%), and larger volumes of vascular structures (3%).18 It should be noted, however, that although animal models may
Valid histologic information is not currently available regarding provide valuable data valid for proof‐of‐principle issues, they may
the peri‐implant mucosa when implants are placed in non‐kerati‐ not completely recreate the anatomic, physiologic, biomechanical/
nized lining or alveolar mucosa. functional, or pathologic environment of the clinical conditions in
humans. 27

M O R PH O G E N E S I S O F TH E M U COSA L
Human studies
ADHESION
Studies on the morphogenesis and morphology of the mucosa at im‐
The formation of the mucosal adhesion was studied in a dog model.1 plants in humans used block biopsies obtained from mini‐implants
One‐piece implant devices were placed in the edentulous mandible or from soft tissue dissection techniques from conventional or spe‐
of dogs, and healing was monitored using light microscopic exami‐ cially designed abutments. 22,28‒32 Tomasi et al.31,32 presented a de
nation of biopsies sampled at different intervals during a 3‐month novo biopsy technique and reported on the morphogenesis of the
period. In the initial phase of the wound between the implant and cut peri‐implant mucosa at single implant sites in human volunteers. Soft
connective tissue, a fibrin clot/coagulum formed that was infiltrated tissue biopsies were sampled after 2, 4, 8, and 12 weeks of healing
S232 | ARAUJO and LINDHE

following abutment connection. They reported that after 2 weeks subsequent study, stated that the probe penetration into the healthy
large areas of the severed connective tissue were infiltrated with soft tissues at the buccal surface of teeth and implants in dogs was
inflammatory cells, while after 4 weeks the infiltrated areas were alike and similar to the length of the junctional/barrier epithelium.
smaller and a short barrier epithelium had formed in the interface It was assumed that probing the implant–mucosa interface would
zone. Sections representing later phases of observation exhibited sever the soft tissue seal and jeopardize the integrity of the adhe‐
continued healing of the connective tissue wound and the forma‐ sion. This issue was examined in a dog study51 that documented that
tion of a well‐defined barrier and sulcular epithelium in the marginal already after 5 to 7 days following clinical probing, the soft tissue
portion of the soft tissue samples. The height of the peri‐implant seal had regenerated to its full extent.
mucosa, measured along the profile of the soft tissue, increased dur‐
ing the healing phase from 2.7 mm at 2 weeks to between 3.0 and
3.5 mm after 4, 8, and 12 weeks. In the corresponding intervals the BONE SOUNDING
length of the epithelium varied between 2.2 and 2.0 mm, while the
zone of connective tissue adhesion varied between 1.7 and 1.1 mm. Bone sounding or transmucosal sounding (TS) is a measurement that
In summary, results from the available studies in man and from is used to determine the height of the entire soft tissue cuff at vari‐
animal experiments are consistent and document that the peri‐im‐ ous groups of teeth and implants. The dimensions of the peri‐implant
plant mucosa is about 3 to 4 mm high with an epithelium that is mucosa and the gingiva at adjacent tooth sites was studied by clini‐
about 2 mm long. cal measurements performed mainly in partially edentulous subjects
who had been treated with implant‐supported single‐crown restora‐
tions. In such studies the brand of the periodontal probe used for the
PE R I ‐ I M PL A NT TI S S U E S I N C LI N I C A L assessments was identified; PD as well as TS measurements were
H E A LTH used to describe some features of the soft tissue.
Results from such studies52‒60 demonstrated that the PD was
The gingiva and the peri‐implant mucosa and their adhesion (seal) greater at proximal than at facial/buccal surfaces at both tooth and
are consistently challenged by the oral environment, including the implant sites and greater at implant than at tooth sites. This shows
steady exposure to microorganisms in the biofilm present on the that the soft tissue cuff around implants exhibits less resistance to
22,32‒37
tooth and implant surfaces. In the clinically normal peri‐im‐ probing than the gingiva at adjacent teeth. There are reasons to sug‐
plant mucosa (and gingiva), the continuous host response includes gest that the lack of root cementum on the implant surface as well
both vascular and cellular events. Thus, distinct vascular structures as the difference in the orientation of the collagen fibers in the two
occur in the connective tissue lateral to the epithelium, as well as types of soft tissue may be associated with the variation observed in
small clusters of inflammatory cells (T‐ lymphocyte and B‐lympho‐ the “resistance to probing.”
cyte). Macrophages seem to be present along the entire interface The TS measurements disclosed that the peri‐implant mucosa
zone, while polymorphonuclear leukocytes occur mainly in the con‐ was in most cases 1.0 to 1.5 mm higher than the corresponding gin‐
nective tissue immediately lateral to the epithelium.32 giva at both buccal/facial and proximal sites. It was further demon‐
strated that patients with a “flat‐thick” periodontal phenotype61,62
exhibited greater peri‐implant mucosa dimensions than subjects
PRO B I N G PE R I ‐ I M PL A NT TI S S U E S that belonged to the “scalloped‐thin” biotype.57,63 In addition, the
height of the papilla between an implant‐supported restoration and
For many years it was incorrectly assumed that the tip of the peri‐ a natural tooth was reported to be ≤5 mm52,56,64,65 and related to the
odontal probe in a probing depth (PD) measurement identified the connective tissue adhesion level at the adjacent approximal tooth
apical base of the dento‐gingival epithelium.38 Later research docu‐ surfaces.57,66 The corresponding dimension between two adjacent
mented, however, that this was not the case. At healthy sites the implant restorations averaged 3 mm64,67 and apparently was depen‐
tip of the probe failed to reach the apical portion of the epithelial dent on the outline of the crest of the supporting bone.
barrier, while at diseased sites the probe found the apical base of
the inflammatory cell infiltrate. Hence, PD measurements assess
the depth of probe penetration or the resistance offered by the soft K E R ATI N IZE D M U COSA (K M)
39‒47
tissue.
The influence of the condition (health, disease) of the peri‐im‐ KM is a term used to describe the masticatory mucosa that is present
plant mucosa on the outcome of the probing measurement was at many, but not all, implant sites. KM extends from the margin of the
studied in animal models.48‒50 Lang et al.49 reported that at sites peri‐implant mucosa to the movable lining (oral) mucosa. KM is com‐
with healthy mucosa or mucositis, the tip of the probe identified prised of a lamina propria (fibrous connective tissue that contains
the apical border of the barrier epithelium with an error of approxi‐ fibroblasts and equal amounts of type I and type III collagen) that
mately 0.2 mm, while at sites with peri‐implantitis, the measurement is covered by an orthokeratinized squamous epithelium. The width
error was much greater at 1.5 mm. Abrahamsson and Soldini,50 in a of the KM at the facial/buccal side of teeth is, as a rule, about 1 mm
ARAUJO and LINDHE | S233

greater than at contralateral implant sites. 54,59,60 It is suggested that abutment/implant level. Additional preclinical studies90,91 have
loss of crestal bone following tooth extraction is the main reason for confirmed that rough surfaces enhance early bone formation and
dimunition of the KM. The thickness of facial KM, determined with bone‐to‐implant contact. Findings from studies in man92‒97 con‐
a probe at the base of the PD, is greater at implants than at teeth firmed the animal results by documenting that the amount of di‐
(2.0 mm vs 1.1 mm, respectively).54 rect bone (mineralized tissue)‐to‐implant contact was about 60%
The need for a minimum amount of keratinized mucosa to main‐ of the circumference of the implanted device after a healing period
tain peri‐implant tissue health is apparently a controversial issue.68‒72 of 6 weeks to 3 months.
Several studies failed to associate the lack of a minimum amount of
KM with mucosal inflammation,73‒80 while other studies suggested
Crestal bone‐level change
that plaque build‐up and marginal inflammation were more frequent
at implant sites with < 2 mm of KM.81‒85 Following implant installation and loading, modeling of the bone oc‐
curs, and during this process some crestal bone height is lost. Studies
in animals have demonstrated the location of the implant–abutment
B O N E TI S S U E A RO U N D I M PL A NT S
interface (microgap) determines the amount of this initial marginal
bone loss. 26,98‒100 Thus, the crestal bone reduction that occurs in
Bone tissue in the edentulous ridge
this healing phase apparently varies between brands and seems to
In a study involving partially edentulous subjects, hard tissue biop‐ be related to the design of the implant system used.101‒112 After this
sies were sampled from the maxilla and the mandible with the use initial period about 75% of implants experience no additional bone
of trephine drills.86 The bone tissue was found to include a blend loss but osseointegration takes place. Most implant sites that exhibit
of mainly lamellar bone (46%) and bone marrow (23%) with less crestal bone loss of > 1 mm appear to be associated with soft tissue
amounts of fibrous (12%) and osteoid (4%) tissue. Bone marrow was inflammation although some sites may have an apparently healthy
the dominant tissue element in the anterior maxilla, while dense la‐ peri‐implant mucosa.3
mellar bone characterized the anterior portion of the mandible. The
cortical cap was consistently comprised of lamellar bone and was
wider in the mandible than in the maxilla (1.8 mm vs 0.8 mm, respec‐ M A J O R D I FFE R E N C E S B E T W E E N H E A LTH Y
tively) and substantially more narrow in the anterior maxilla than in PE R I ‐ I M PL A NT A N D PE R I O D O NTA L
the anterior mandible. TI S S U E S

The implant device lacks tooth characteristic structures such as root

Osseointegration
cementum, periodontal ligament, and bundle bone (alveolar bone
The term osseointegration was coined by Brånemark et al.87 and was proper).113 The dento‐alveolar and the dento‐gingival fiber bundles
described as bone‐to‐implant contact on the light microscopic level. connect the soft tissues with the tooth (root cementum), while no
Later, Albrektsson and Sennerby2 defined osseointegration as, “a di‐ such fiber bundles are apparent in the peri‐implant tissues. At peri‐
rect functional and structural connection between living bone and odontally healthy sites, the margin of the gingiva follows the outline
the surface of a load‐carrying implant.” of the cemento‐enamel junction, while at a corresponding implant
In animal experiments 88,89 the process of hard tissue healing site the mucosal margin follows the contour of the crestal bone (mul‐
around implants made of c.p.titanium was described. The individ‐ tiple implants) or relates to the connective tissue adhesion at adja‐
ual device had the shape of a solid screw with a modified surface cent teeth (single implants). The tooth is mobile within its socket,
configuration and U‐shaped invaginations (wound chambers) that while the implant is rigidly anchored (ankylosed) to the surrounding
allowed the ingrowth of bone. The wound chambers were first oc‐ host bone.
cupied with a coagulum that after 4 days had been replaced with
granulation tissue that contained inflammatory cells and also nu‐
merous mesenchymal cells and newly formed vessels. After about CO N C LU S I O N S
1 week of healing, fingerlike projections of woven bone occurred
around vascular structures in the center of the chambers and also The healthy peri‐implant mucosa is comprised of a core of connec‐
in direct contact with small areas of the implant. After 2 to 4 weeks tive tissue covered by either a keratinized or non‐keratinized epi‐
the chambers were filled with woven bone extending from the old thelium. Most of the intrabony part of the implant is in contact with
bone to reach the surface of the titanium device. In the 6‐ to 12‐ mineralized bone, while the remaining portion faces bone marrow,
week interval the woven bone was replaced with lamellar bone vascular structures, or fibrous tissue. The characteristics of peri‐
and marrow and bone‐to‐implant contact had been established. implant tissues in health are properly identified in the literature.
At the end of the experiment about 60% of the moderately rough According to the available definitions114 of peri‐implant mucositis
implant surface was occupied with mineralized bone and the mar‐ and peri‐implantitis, the absence of signs of clinical inflammation is
ginal bone‐to‐implant contact was located about 0.3 mm from the necessary for concluding that a site has peri‐implant health.
S234 | ARAUJO and LINDHE

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