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

DOI: 10.1002/JPER.16-0424

2017 WORLD WORK SHOP

Peri-implant health
Mauricio G. Araujo1 Jan Lindhe2

1 Department of Dentistry, State University of

Abstract
Maringa, Maringa, Brazil
2 Department of Periodontology, Sahlgren- Objective: The aim is to define clinical and histologic characteristics of peri-implant
ska, Academy at University of Gothenburg, tissues in health and describe the mucosa–implant interface.
Gothenburg, Sweden
Importance: An understanding of the characteristics of healthy peri-implant tissues
Correspondence
Dr. Mauricio Araujo, Department of Dentistry, facilitates the recognition of disease (i.e., departure from health).
State University of Maringa, Maringa, Brazil.
Email: [email protected] Findings: The healthy peri-implant mucosa is, at the microscopic level, comprised
The proceedings of the workshop were of a core of connective tissue covered by either a keratinized (masticatory mucosa) or
jointly and simultaneously published in the non-keratinized epithelium (lining mucosa). The peri-implant mucosa averages about
Journal of Periodontology and Journal of
3 to 4 mm high, and presents with an epithelium (about 2 mm long) facing the implant
Clinical Periodontology.
surface. Small clusters of inflammatory cells are usually present in the connective tis-
sue lateral to the barrier epithelium. Most of the intrabony part of the implant appears
to be in contact with mineralized bone (about 60%), while the remaining portion faces
bone marrow, vascular structures, or fibrous tissue. During healing following implant
installation, bone modeling occurs that may result in some reduction 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 osseointe- was to define clinical and histologic characteristics of peri-
grated dental implants. They are divided into soft and hard implant tissues in health and describe the mucosa–implant
tissue compartments. The soft tissue compartment is denoted interface.
“peri-implant mucosa” and is formed during the wound heal- A search in MEDLINE-PubMed was used to retrieve the
ing process that follows implant/abutment placement.1 The evidence to support the present review. The following key
hard tissue compartment forms a contact relationship to the words were used for the literature search: dental implants
implant surface to secure implant stability.2 Due to their (Mesh) AND biological width OR mucosa OR soft tissue OR
histologic and anatomic features, peri-implant tissues carry attachment OR keratinized mucosa OR peri-implant mucosa
out two basic functions: the mucosa protects the under- OR probing depth OR microbiota OR collagen fibers OR
lining bone, while the bone supports the implant. Indeed, epithelium OR adhesion OR seal OR bone OR osseointegra-
the destruction of peri-implant tissues can jeopardize the tion AND humans OR animals. The two main reasons for
implant success and survival,3 and the understanding of exclusion of studies were: 1) not published in English, and 2)
the characteristics of healthy peri-implant tissues allows the lack of detailed clinical, histologic, or microbiologic descrip-
recognition of disease. Thus, the aim of the present review tion of healthy peri-implant tissues.
© 2018 American Academy of Periodontology and European Federation of Periodontology

J Periodontol. 2018;89(Suppl 1):S249–S256. wileyonlinelibrary.com/journal/jper S249

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S250 ARAUJO AND LINDHE

PERI-IMPLANT MUCOSA edentulous mandible of dogs, and healing was monitored

using light microscopic examination of biopsies sampled at
Most information regarding the structural features of the different intervals during a 3-month period. In the initial phase
peri-implant mucosa is derived from animal studies using of the wound between the implant and cut connective tissue,
dog models.4–15 In such studies implants were placed in the a fibrin clot/coagulum formed that was infiltrated with mainly
edentulous ridge (alternatively, the fresh extraction socket), neutrophils and limited amounts of macrophages. The number
the outer osseous part of which was covered with mastica- of inflammatory cells subsequently subsided, and the wound
tory mucosa. It was also shown that the healed peri-implant surface became characterized by its dense layer of fibroblasts
mucosa on the buccal aspect averaged about 3 to 4 mm high that appeared to be in intimate contact with the implant sur-
when measured from the mucosal margin to the crest of the face. In the 2nd to 3rd week of healing, the density of fibrob-
peri-implant bone. In addition, this mucosa contains a core lasts was reduced, the amount of collagen and matrix compo-
of connective tissue, mainly comprised of collagen fibers and nents increased, and epithelial cells, extending from the oral
matrix elements (85%), comparatively few fibroblasts (3%), epithelium, had started to occupy marginal parts of the con-
and vascular units (5%). The outer (oral) surface of the con- nective tissue wound. Collagen fibers in the previous wound
nective tissue is covered by an often orthokeratinized epithe- area became organized in bundles after about 4 weeks. After
lium. The portion of the peri-implant mucosa that is facing 6 to 8 weeks the mucosal adhesion appeared mature, and the
the implant (abutment) contains two distinct parts, a “coronal” interface zone at tissue–implant was comprised of a combined
portion that is lined by a thin barrier epithelium (similar to the epithelial and connective tissue adhesion to the implant sur-
junctional epithelium of the gingiva) and sulcular epithelium, face. Since the build-up of the soft tissue adhesion did not
and a more “apical” segment in which the connective tissue change much after the first month, it is suggested that a home-
appears to be in direct contact with the implant surface. This ostasis had been reached at this interval.1
apical portion of the peri-implant mucosa is designated zone
of connective tissue adhesion.
In the connective tissue immediately lateral to the barrier
and sulcular epithelium, a delicate plexus of vascular struc-
DIM ENS IO N OF T H E
tures, similar to the dentogingival vascular plexus,16 is con-
PERI-IMPLANT MUCOSA
sistently present,17 while the connective tissue adhesion zone
appears to harbor only limited amounts of vascular structures.
Animal studies
At implants placed into masticatory mucosa, the main colla- The dimension of the peri-implant mucosa, often called the
gen fiber bundles are anchored in the crestal bone and extend biological width or dimension,5 was examined in biopsies
in a marginal direction parallel to the surface of the metal mainly obtained from studies in dogs.19–26 Such measure-
device. It is assumed that circular fibers may also be present ments disclosed that a certain width of soft tissue may be
in this type of peri-implant mucosa. required to cover the peri-implant bone. The studies referred
Moon et al.18 analyzed under electron scanning microscope to the length of the epithelium (from the peri-implant mucosa
the zone of connective tissue adhesion confined to a 200-𝜇m margin to the apical portion of the junctional epithelial)
wide zone of the connective tissue facing the implant. The as about 2 mm, while the height of the zone of connec-
findings demonstrated that the adhesion includes two distinct tive tissue adhesion exhibited more variation (between 1
layers: one inner layer, about 40 𝜇m wide, which harbors large and 2 mm). The experiments in the animal model included
amounts of fibroblasts (32% of volume) that appear to be in the study of different variables such as material used for
intimate contact with the surface of the implant; and one outer the fabrication of the implant and/or the abutment, surgi-
layer, about 160 𝜇m wide, that is dominated by collagen fibers cal placement protocol, implants/abutments with different
(83%), smaller amounts of fibroblasts (11%), and larger vol- surface texture,5,19–23 as well as so-called implants with
umes of vascular structures (3%).18 a “platform switching” implant/abutment design.24–26 The
Valid histologic information is not currently available results obtained documented that while abutments made of
regarding the peri-implant mucosa when implants are placed gold alloy and dental porcelain failed to establish appro-
in non-keratinized lining or alveolar mucosa. priate soft tissue adhesion,23 other variables had appar-
ently limited effect on the dimensions of the peri-implant
mucosa.
MORPHOGENESIS OF THE It should be noted, however, that although animal models
MUCOSAL AD H E SI O N may provide valuable data valid for proof-of-principle issues,
they may not completely recreate the anatomic, physiologic,
The formation of the mucosal adhesion was studied in a biomechanical/functional, or pathologic environment of the
dog model.1 One-piece implant devices were placed in the clinical conditions in humans.27
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ARAUJO AND LINDHE S251

Human studies apical portion of the epithelial barrier, while at diseased sites
the probe found the apical base of the inflammatory cell infil-
Studies on the morphogenesis and morphology of the mucosa
trate. Hence, PD measurements assess the depth of probe pen-
at implants in humans used block biopsies obtained from
etration or the resistance offered by the soft tissue.39–47
mini-implants or from soft tissue dissection techniques from
The influence of the condition (health, disease) of the peri-
conventional or specially designed abutments.22,28–32 Tomasi
implant mucosa on the outcome of the probing measurement
et al.31,32 presented a de novo biopsy technique and reported
was studied in animal models.48–50 Lang et al.49 reported
on the morphogenesis of the peri-implant mucosa at single
that at sites with healthy mucosa or mucositis, the tip of the
implant sites in human volunteers. Soft tissue biopsies were
probe identified the apical border of the barrier epithelium
sampled after 2, 4, 8, and 12 weeks of healing following
with an error of approximately 0.2 mm, while at sites with
abutment connection. They reported that after 2 weeks large
peri-implantitis, the measurement error was much greater at
areas of the severed connective tissue were infiltrated with
1.5 mm. Abrahamsson and Soldini,50 in a subsequent study,
inflammatory cells, while after 4 weeks the infiltrated areas
stated that the probe penetration into the healthy soft tissues
were smaller and a short barrier epithelium had formed in the
at the buccal surface of teeth and implants in dogs was alike
interface zone. Sections representing later phases of obser-
and similar to the length of the junctional/barrier epithelium.
vation exhibited continued healing of the connective tissue
It was assumed that probing the implant–mucosa interface
wound and the formation of a well-defined barrier and sul-
would sever the soft tissue seal and jeopardize the integrity of
cular epithelium in the marginal portion of the soft tissue
the adhesion. This issue was examined in a dog study51 that
samples. The height of the peri-implant mucosa, measured
documented that already after 5 to 7 days following clinical
along the profile of the soft tissue, increased during the heal-
probing, the soft tissue seal had regenerated to its full extent.
ing 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
length of the epithelium varied between 2.2 and 2.0 mm, while
the zone of connective tissue adhesion varied between 1.7 and
BONE S O UNDING
1.1 mm.
Bone sounding or transmucosal sounding (TS) is a measure-
In summary, results from the available studies in man and
ment that is used to determine the height of the entire soft
from animal experiments are consistent and document that the
tissue cuff at various groups of teeth and implants. The dimen-
peri-implant mucosa is about 3 to 4 mm high with an epithe-
sions of the peri-implant mucosa and the gingiva at adja-
lium that is about 2 mm long.
cent tooth sites was studied by clinical measurements per-
formed mainly in partially edentulous subjects who had been
PERI-IMPLANT TISSUES IN treated with implant-supported single-crown restorations. In
C L I N I CA L HE A LT H such studies the brand of the periodontal probe used for the
assessments was identified; PD as well as TS measurements
The gingiva and the peri-implant mucosa and their adhe- were used to describe some features of the soft tissue.
sion (seal) are consistently challenged by the oral environ- Results from such studies52–60 demonstrated that the PD
ment, including the steady exposure to microorganisms in the was greater at proximal than at facial/buccal surfaces at both
biofilm present on the tooth and implant surfaces.22,32–37 In tooth and implant sites and greater at implant than at tooth
the clinically normal peri-implant mucosa (and gingiva), the sites. This shows that the soft tissue cuff around implants
continuous host response includes both vascular and cellular exhibits less resistance to probing than the gingiva at adja-
events. Thus, distinct vascular structures occur in the connec- cent teeth. There are reasons to suggest that the lack of root
tive tissue lateral to the epithelium, as well as small clusters cementum on the implant surface as well as the difference in
of inflammatory cells (T- lymphocyte and B-lymphocyte). the orientation of the collagen fibers in the two types of soft
Macrophages seem to be present along the entire interface tissue may be associated with the variation observed in the
zone, while polymorphonuclear leukocytes occur mainly in “resistance to probing.”
the connective tissue immediately lateral to the epithelium.32 The TS measurements disclosed that the peri-implant
mucosa was in most cases 1.0 to 1.5 mm higher than
PROBING PERI-IMPLANT TISSUES the corresponding gingiva at both buccal/facial and prox-
imal sites. It was further demonstrated that patients with
For many years it was incorrectly assumed that the tip of a “flat-thick” periodontal phenotype61,62 exhibited greater
the periodontal probe in a probing depth (PD) measurement peri-implant mucosa dimensions than subjects that belonged
identified the apical base of the dento-gingival epithelium.38 to the “scalloped-thin” biotype.57,63 In addition, the height
Later research documented, however, that this was not the of the papilla between an implant-supported restoration and
case. At healthy sites the tip of the probe failed to reach the a natural tooth was reported to be ≤5 mm52,56,64,65 and
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S252 ARAUJO AND LINDHE

related to the connective tissue adhesion level at the adjacent nection between living bone and the surface of a load-carrying
approximal tooth surfaces.57,66 The corresponding dimension implant.”
between two adjacent implant restorations averaged 3 mm64,67 In animal experiments88,89 the process of hard tissue heal-
and apparently was dependent on the outline of the crest of the ing around implants made of c.p.titanium was described. The
supporting bone. individual device had the shape of a solid screw with a modi-
fied surface configuration and U-shaped invaginations (wound
chambers) that allowed the ingrowth of bone. The wound
K E R AT I N I Z E D M U CO SA (K M ) chambers were first occupied with a coagulum that after 4
days had been replaced with granulation tissue that contained
KM is a term used to describe the masticatory mucosa that is inflammatory cells and also numerous mesenchymal cells and
present at many, but not all, implant sites. KM extends from newly formed vessels. After about 1 week of healing, fin-
the margin of the peri-implant mucosa to the movable lining gerlike projections of woven bone occurred around vascular
(oral) mucosa. KM is comprised of a lamina propria (fibrous structures in the center of the chambers and also in direct
connective tissue that contains fibroblasts and equal amounts contact with small areas of the implant. After 2 to 4 weeks
of type I and type III collagen) that is covered by an orthok- the chambers were filled with woven bone extending from
eratinized squamous epithelium. The width of the KM at the the old bone to reach the surface of the titanium device. In
facial/buccal side of teeth is, as a rule, about 1 mm greater the 6- to 12-week interval the woven bone was replaced with
than at contralateral implant sites.54,59,60 It is suggested that lamellar bone and marrow and bone-to-implant contact had
loss of crestal bone following tooth extraction is the main rea- been established. At the end of the experiment about 60% of
son for dimunition of the KM. The thickness of facial KM, the moderately rough implant surface was occupied with min-
determined with a probe at the base of the PD, is greater at eralized bone and the marginal bone-to-implant contact was
implants than at teeth (2.0 mm vs 1.1 mm, respectively).54 located about 0.3 mm from the abutment/implant level. Addi-
The need for a minimum amount of keratinized mucosa to tional preclinical studies90,91 have confirmed that rough sur-
maintain peri-implant tissue health is apparently a controver- faces enhance early bone formation and bone-to-implant con-
sial issue.68–72 Several studies failed to associate the lack of tact. Findings from studies in man92–97 confirmed the animal
a minimum amount of KM with mucosal inflammation,73–80 results by documenting that the amount of direct bone (min-
while other studies suggested that plaque build-up and eralized tissue)-to-implant contact was about 60% of the cir-
marginal inflammation were more frequent at implant sites cumference of the implanted device after a healing period of
with < 2 mm of KM.81–85 6 weeks to 3 months.

Crestal bone-level change

BONE TISSUE A ROUND IMPLANTS
Following implant installation and loading, modeling of the
Bone tissue in the edentulous ridge bone occurs, and during this process some crestal bone height
is lost. Studies in animals have demonstrated the location
In a study involving partially edentulous subjects, hard tis-
of the implant–abutment interface (microgap) determines the
sue biopsies were sampled from the maxilla and the mandible
amount of this initial marginal bone loss.26,98–100 Thus, the
with the use of trephine drills.86 The bone tissue was found
crestal bone reduction that occurs in this healing phase appar-
to include a blend of mainly lamellar bone (46%) and bone
ently varies between brands and seems to be related to the
marrow (23%) with less amounts of fibrous (12%) and osteoid
design of the implant system used.101–112 After this initial
(4%) tissue. Bone marrow was the dominant tissue element
period about 75% of implants experience no additional bone
in the anterior maxilla, while dense lamellar bone character-
loss but osseointegration takes place. Most implant sites that
ized the anterior portion of the mandible. The cortical cap was
exhibit crestal bone loss of > 1 mm appear to be associated
consistently comprised of lamellar bone and was wider in the
with soft tissue inflammation although some sites may have
mandible than in the maxilla (1.8 mm vs 0.8 mm, respectively)
an apparently healthy peri-implant mucosa.3
and substantially more narrow in the anterior maxilla than in
the anterior mandible.

Osseointegration M AJ O R DIF F ERENCES BET W EE N

HEALTHY PERI-I MPLANT AND
The term osseointegration was coined by Brånemark et al.87 P ERIO DO NTA L T IS S UES
and was described as bone-to-implant contact on the light
microscopic level. Later, Albrektsson and Sennerby2 defined The implant device lacks tooth characteristic structures such
osseointegration as, “a direct functional and structural con- as root cementum, periodontal ligament, and bundle bone
 19433670, 2018, S1, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.16-0424 by CAPES, Wiley Online Library on [18/12/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ARAUJO AND LINDHE S253

(alveolar bone proper).113 The dento-alveolar and the dento- 8. Berglundh T, Lindhe J, Ericsson I, Marinello CP, Liljenberg B,
gingival fiber bundles connect the soft tissues with the tooth Thomsen P. The soft tissue barrier at implants and teeth. Clin Oral
Implants Res. 1991;2:81–90.
(root cementum), while no such fiber bundles are apparent in
the peri-implant tissues. At periodontally healthy sites, the 9. Berglundh T, Lindhe J. Dimension of the periimplant mucosa. Bio-
logical width revisited. J Clin Periodontol. 1996;23:971–973.
margin of the gingiva follows the outline of the cemento-
enamel junction, while at a corresponding implant site the 10. Buser D, Weber HP, Donath K, Fiorellini JP, Paquette DW,
Williams RC. Soft tissue reactions to non-submerged unloaded
mucosal margin follows the contour of the crestal bone (mul-
titanium implants in beagle dogs. J Periodontol. 1992;63:225–235.
tiple implants) or relates to the connective tissue adhesion at
11. Ericsson I, Persson LG, Berglundh T, Marinello CP, Lindhe
adjacent teeth (single implants). The tooth is mobile within
J, Klinge B. Different types of inflammatory reactions in peri-
its socket, while the implant is rigidly anchored (ankylosed)
implant soft tissues. J Clin Periodontol. 1995;22:255–261.
to the surrounding host bone.
12. Ericsson I, Nilner K, Klinge B, Glantz PO. Radiographical and
histological characteristics of submerged and nonsubmerged tita-
nium implants. An experimental study in the Labrador dog. Clin
CONC LU SI ON S Oral Implants Res. 1996;7:20–26.
13. Hermann JS, Buser D, Schenk RK, Schoolfield JD, Cochran DL.
The healthy peri-implant mucosa is comprised of a core of Biologic width around one- and two-piece titanium implants. Clin
connective tissue covered by either a keratinized or non- Oral Implants Res. 2001;12:559–571.
keratinized epithelium. Most of the intrabony part of the 14. Scipioni A, Bruschi GB, Giargia M, Berglundh T, Lindhe J.
implant is in contact with mineralized bone, while the remain- Healing at implants with and without primary bone contact. An
ing portion faces bone marrow, vascular structures, or fibrous experimental study in dogs. Clin Oral Implants Res. 1997;8:
tissue. The characteristics of peri-implant tissues in health are 39–47.
properly identified in the literature. According to the available 15. Vignoletti F, de Sanctis M, Berglundh T, Abrahamsson I, Sanz
definitions114 of peri-implant mucositis and peri-implantitis, M. Early healing of implants placed into fresh extraction sockets:
an experimental study in the beagle dog. III: soft tissue findings.
the absence of signs of clinical inflammation is necessary for
J Clin Periodontol. 2009;36:1059–1066.
concluding that a site has peri-implant health.
16. Egelberg J. The blood vessels of the dento-gingival junction.
J Periodontal Res. 1966;1:163–179.
ACKNOW LEDGMENTS AND DISCLOSURES 17. Berglundh T, Lindhe J, Jonsson K, Ericsson I. The topography of
The authors report no conflicts of interest related to this the vascular systems in the periodontal and peri-implant tissues in
review paper. the dog. J Clin Periodontol. 1994;21:189–193.
18. Moon IS, Berglundh T, Abrahamsson I, Linder E, Lindhe J. The
barrier between the keratinized mucosa and the dental implant.
REFERENCES An experimental study in the dog. J Clin Periodontol. 1999;26:
1. Berglundh T, Abrahamsson I, Welander M, Lang NP, Lindhe J. 658–663.
Morphogenesis of the peri-implant mucosa: an experimental study 19. Abrahamsson I, Zitzmann NU, Berglundh T, Linder E, Wenner-
in dogs. Clin Oral Implants Res. 2007;18:1–8. berg A, Lindhe J. The mucosal attachment to titanium implants
2. Albrektsson T, Sennerby L. State of the art in oral implants. J Clin with different surface characteristics: an experimental study in
Periodontol. 1991;18:474–481. dogs. J Clin Periodontol. 2002;29:448–455.
3. Derks J, Håkansson J, Wennström JL, Tomasi C, Larsson M, 20. Abrahamsson I, Cardaropoli G. Peri-implant hard and soft tissue
Berglundh T. Effectiveness of implant therapy analyzed in a integration to dental implants made of titanium and gold. Clin Oral
Swedish population: early and late implant loss. J Dent Res. Implants Res. 2007;18:269–274.
2015;94:44S-51S. 21. Cochran DL, Obrecht M, Weber K, et al. Biologic width
4. Abrahamsson I, Berglundh T, Wennström J, Lindhe J. The peri- adjacent to loaded implants with machined and rough col-
implant hard and soft tissues at different implant systems. A com- lars in the dog. Int J Periodontics Restorative Dent. 2014;34:
parative study in the dog. Clin Oral Implants Res. 1996;7:212–219. 773–779.
5. Abrahamsson I, Berglundh T, Lindhe J. The mucosal barrier fol- 22. Schwarz F, Mihatovic I, Becker J, Bormann KH, Keeve PL, Fried-
lowing abutment dis/reconnection. An experimental study in dogs. mann A. Histological evaluation of different abutments in the pos-
J Clin Periodontol. 1997;24:568–572. terior maxilla and mandible: an experimental study in humans.
6. Abrahamsson I, Berglundh T, Glantz PO, Lindhe J. The mucosal J Clin Periodontol. 2013;40:807–815.
attachment at different abutments. An experimental study in dogs. 23. Welander M, Abrahamsson I, Berglundh T. The mucosal barrier at
J Clin Periodontol. 1998;25:721–727. implant abutments of different materials. Clin Oral Implants Res.
7. Abrahamsson I, Berglundh T, Moon IS, Lindhe J. Peri-implant tis- 2008;19:635–641.
sues at submerged and non-submerged titanium implants. J Clin 24. Baffone GM, Botticelli D, Pantani F, Cardoso LC, Schweikert MT,
Periodontol. 1999;26:600–607. Lang NP. Influence of various implant platform configurations on
 19433670, 2018, S1, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.16-0424 by CAPES, Wiley Online Library on [18/12/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
S254 ARAUJO AND LINDHE

peri-implant tissue dimensions: an experimental study in dog. Clin 40. Armitage GC, Svanberg GK, Löe H. Microscopic evaluation
Oral Implants Res. 2011;22:438–444. of clinical measurements of connective tissue attachment levels.
25. Siar CH, Toh CG, Ali TBT, Seiz D, Ong ST. Dimensional profile J Clin Periodontol. 1977;4:173–190.
of oral mucosa around combined tooth-implant-supported bridge- 41. Robinson PJ, Vitek RM. The relationship between gingival inflam-
work in macaque mandible. Clin Oral Implants Res. 2012;23:438– mation and resistance to probe penetration. J Periodontal Res.
446. 1979;14:239–243.
26. Cochran DL, Mau LP, Higginbottom FL, et al. Soft and hard tis- 42. Spray JR, Garnick JJ, Doles LR, Klawitter JJ. Microscopic demon-
sue histologic dimensions around dental implants in the canine stration of the position of periodontal probes. J Periodontol.
restored with smaller-diameter abutments: a paradigm shift in peri- 1978;49:148–152.
implant biology. Int J Oral Maxillofac Implants. 2013;28:494– 43. Magnusson I, Listgarten MA. Histological evaluation of prob-
502. ing depth following periodontal treatment. J Clin Periodontol.
27. Berglundh T, Stavropoulos A. Preclinical in vivo research in 1980;7:26–31.
implant dentistry. Consensus of the eighth European workshop on 44. Polson AM, Caton JG, Yeaple RN, Zander HA. Histological deter-
periodontology. J Clin Periodontol. 2012;39(Suppl. 1):1–5. mination of probe tip penetration into gingival sulcus of humans
28. Glauser R, Schüpbach P, Gottlow J, Hämmerle CHF. Periim- using an electronic pressure-sensitive probe. J Clin Periodontol.
plant soft tissue barrier at experimental one-piece mini-implants 1980;7:479–488.
with different surface topography in humans: a light-microscopic 45. van der Velden U, Jansen J. Microscopic evaluation of pocket
overview and histometric analysis. Clin Implant Dent Relat Res. depth measurements performed with six different probing forces
2005;7(Suppl. 1):S44-S51. in dogs. J Clin Periodontol. 1981;8:107–116.
29. Schupbach P, Glauser R. The defense architecture of the human 46. Fowler C, Garrett S, Crigger M, Egelberg J. Histologic probe posi-
periimplant mucosa: a histological study. J Prosthet Dent. tion in treated and untreated human periodontal tissues. J Clin
2007;97:S15-S25. Periodontol. 1982;9:373–385.
30. van Brakel R, Meijer GJ, Verhoeven JW, Jansen J, de Putter C, 47. Schou S, Holmstrup P, Stoltze K, Hjorting-Hansen E, Fiehn
Cune MS. Soft tissue response to zirconia and titanium implant NE SL. Probing around implants and teeth with healthy or
abutments: an in vivo within-subject comparison. J Clin Periodon- inflamed peri-implant mucosa / gingiva: a histologic comparison
tol. 2012;39:995–1001. in cynomolgus monkeys (Macaca fascicularis). Clin Oral Implants
31. Tomasi C, Tessarolo F, Caola I, Wennstrom J, Nollo G, Berglundh Res. 2002;13:113–126.
T. Morphogenesis of peri-implant mucosa revisited: an experi- 48. Ericsson I, Lindhe J. Probing depth at implants and teeth. An
mental study in humans. Clin Oral Implants Res. 2014;25:997– experimental study in the dog. J Clin Periodontol. 1993;20:623–
1003. 627.
32. Tomasi C, Tessarolo F, Caola I, et al. Early healing of peri-implant 49. Lang NP, Wetzel AC, Stich H, Caffesse RG. Histologic probe pen-
mucosa in man. J Clin Periodontol. 2016;43:816–824. etration in healthy and inflamed peri-implant tissues. Clin Oral
33. Seymour GJ, Gemmell E, Lenz LJ, Henry P, Bower R, Yamazaki Implants Res. 1994;5:191–201.
K. Immunohistologic analysis of the inflammatory infiltrates 50. Abrahamsson I, Soldini C. Probe penetration in periodontal and
associated with osseointegrated implants. Int J Oral Maxillofac peri-implant tissues. An experimental study in the beagle dog. Clin
Implants. 1989;4:191–198. Oral Implants Res. 2006;17:601–605.
34. Tonetti MS, Gerber L, Lang NP. Vascular adhesion molecules and 51. Etter TH, Håkanson I, Lang NP, Trejo PM, Caffesse RG. Healing
initial development of inflammation in clinically healthy human after standardized clinical probing of the perlimplant soft tissue
keratinized mucosa around teeth and osseointegrated implants. seal: a histomorphometric study in dogs. Clin Oral Implants Res.
J Periodontal Res. 1994;29:386–392. 2002;13:571–580.
35. Tonetti MS, Imboden M, Gerber L, Lang NP. Compartmental- 52. Tarnow DP, Magner AW, Fletcher P. The effect of the dis-
ization of inflammatory cell phenotypes in normal gingiva and tance from the contact point to the crest of bone on the pres-
peri-implant keratinized mucosa. J Clin Periodontol. 1995;22: ence or absence of the interproximal dental papilla. J Periodontol.
735–742. 1992;63:995–996.
36. Liljenberg B, Gualini F, Berglundh T, Tonetti M, Lindhe J. Com- 53. Tarnow D, Elian N, Fletcher P, et al. Vertical distance from the
position of plaque-associated lesions in the gingiva and the peri- crest of bone to the height of the interproximal papilla between
implant mucosa in partially edentulous subjects. J Clin Periodon- adjacent implants. J Periodontol. 2003;74:1785–1788.
tol. 1997;24:119–123. 54. Chang M, Wennström JL, Odman P, Andersson B. Implant sup-
37. Zitzmann NU, Berglundh T, Marinello CP, Lindhe J. Exper- ported single-tooth replacements compared to contralateral natural
imental peri-implant mucositis in man. J Clin Periodontol. teeth. Crown and soft tissue dimensions. Clin Oral Implants Res.
2001;28:517–523. 1999;10:185–194.
38. Waerhaug J. The gingival pocket; anatomy, pathology, deepening 55. Grunder U. Stability of the mucosal topography around single-
and elimination. Odontol Tidskr. 1952;60(Suppl. 1):1–186. tooth implants and adjacent teeth: 1-year results. Int J Periodontics
39. Listgarten MA, Mao R, Robinson PJ. Periodontal probing and the Restorative Dent. 2000;20:11–17.
relationship of the probe tip to periodontal tissues. J Periodontol. 56. Choquet V, Hermans M, Adriaenssens P, Daelemans P, Tarnow
1976;47:511–513. DP, Malevez C. Clinical and radiographic evaluation of the
 19433670, 2018, S1, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.16-0424 by CAPES, Wiley Online Library on [18/12/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ARAUJO AND LINDHE S255

papilla level adjacent to single-tooth dental implants. A retro- 72. Thoma DS, Mühlemann S, Jung RE. Critical soft-tissue dimen-
spective study in the maxillary anterior region. J Periodontol. sions with dental implants and treatment concepts. Periodontol
2001;72:1364–1371. 2000. 2014;66:106–118.
57. Kan JYK, Rungcharassaeng K, Umezu K, Kois JC. Dimen- 73. Krekeler G, Kappert HF, Schilli W. Scanning electron microscopic
sions of peri-implant mucosa: an evaluation of maxillary ante- study of the reaction of human bone to a titanium implant. Int J
rior single implants in humans. J Periodontol. 2003;74:557– Oral Surg. 1985;14:447–450.
562. 74. Mericske-Stern R. Clinical evaluation of overdenture restorations
58. DeAngelo SJ, Kumar PS, Beck FM, Tatakis DN, Leblebicioglu B. supported by osseointegrated titanium implants: a retrospective
Early soft tissue healing around one-stage dental implants: clini- study. Int J Oral Maxillofac Implants. 1990;5:375–383.
cal and microbiologic parameters. J Periodontol. 2007;78:1878– 75. Mericske-Stern R, Steinlin Schaffner T, Marti P, Geering AH.
1886. Peri-implant mucosal aspects of ITI implants supporting over-
59. Chang M, Wennström JL. Soft tissue topography and dimensions dentures. A five-year longitudinal study. Clin Oral Implants Res.
lateral to single implant-supported restorations. A cross-sectional 1994;5:9–18.
study. Clin Oral Implants Res. 2013;24:556–562. 76. Wennström JL, Bengazi F, Lekholm U. The influence of the masti-
60. Parpaiola A, Cecchinato D, Toia M, Bressan E, Speroni S, Lindhe catory mucosa on the peri-implant soft tissue condition. Clin Oral
J. Dimensions of the healthy gingiva and peri-implant mucosa. Implants Res. 1994;5:1–8.
Clin Oral Implants Res. 2015;26:657–662. 77. Heckmann SM, Karl M, Wichmann MG, Winter W, Graef F, Tay-
61. Ochsenbein C, Ross S. A re-evaluation of osseous surgery. In: lor TD. Cement fixation and screw retention: parameters of passive
Prichard J, ed. Dental Clinics of North America. Philadelphia, PA: fit. An in vitro study of three-unit implant-supported fixed partial
W.B. Saunders Co; 1973:87–102. dentures. Clin Oral Implants Res. 2004;15:466–473.
62. Seibert JS, Lindhe J. Esthetics and periodontal therapy. In: Lindhe 78. Kim B-S, Kim Y-K, Yun P-Y, et al. Evaluation of peri-
J, ed. Textbook of Clinical Periodontology. 2nd edition. Copen- implant tissue response according to the presence of keratinized
hagen, DK: Munksgaard; 1989:477–514. mucosa. Oral Surg Oral Med Oral Pathol Oral Radiol Endod.
63. Romeo E, Lops D, Rossi A, Storelli S, Rozza R, Chiapasco M. 2009;107:e24-e28.
Surgical and prosthetic management of interproximal region with 79. Zigdon H, Machtei EE. The dimensions of keratinized mucosa
single-implant restorations: 1-year prospective study. J Periodon- around implants affect clinical and immunological parameters.
tol. 2008;79:1048–1055. Clin Oral Implants Res. 2008;19:387–392.
64. Gastaldo JF, Cury PR, Sendyk WR. Effect of the vertical and hor- 80. Schrott AR, Jimenez M, Hwang J-W, Fiorellini J. Weber H-P. Five-
izontal distances between adjacent implants and between a tooth year evaluation of the influence of keratinized mucosa on peri-
and an implant on the incidence of interproximal papilla. J Peri- implant soft-tissue health and stability around implants support-
odontol. 2004;75:1242–1246. ing full-arch mandibular fixed prostheses. Clin Oral Implants Res.
65. Ryser MR, Block MS, Mercante DE. Correlation of papilla to 2009;20:1170–1177.
crestal bone levels around single tooth implants in immediate or 81. Chung DM, Oh T-J, Shotwell JL, Misch CE, Wang H-L. Signif-
delayed crown protocols. J Oral Maxillofac Surg. 2005;63:1184– icance of keratinized mucosa in maintenance of dental implants
1195. with different surfaces. J Periodontol. 2006;77:1410–1420.
66. Palmer RM, Farkondeh N, Palmer PJ, Wilson RF. Astra Tech 82. Bouri A, Bissada N, Al-Zahrani MS, Faddoul F, Nouneh I. Width
single-tooth implants: an audit of patient satisfaction and soft tis- of keratinized gingiva and the health status of the supporting
sue form. J Clin Periodontol. 2007;34:633–638. tissues around dental implants. Int J Oral Maxillofac Implants.
67. Degidi M, Novaes AB, Nardi D, Piattelli A. Outcome analysis of 2008;23:323–326.
immediately placed, immediately restored implants in the esthetic 83. Boynueğri D, Nemli SK, Kasko YA. Significance of keratinized
area: the clinical relevance of different interimplant distances. J mucosa around dental implants: a prospective comparative study.
Periodontol. 2008;79:1056–1061. Clin Oral Implants Res. 2013;24:928–933.
68. Wennström JL, Derks J. Is there a need for keratinized mucosa 84. Adibrad M, Shahabuei M, Sahabi M. Significance of the width
around implants to maintain health and tissue stability. Clin Oral of keratinized mucosa on the health status of the supporting tis-
Implants Res. 2012;23(Suppl 6):136–146. sue around implants supporting overdentures. J Oral Implantol.
69. Gobbato L, Avila-Ortiz G, Sohrabi K, Wang C-W, Karimbux N. 2009;35:232–237.
The effect of keratinized mucosa width on peri-implant health: a 85. Roccuzzo M, Grasso G, Dalmasso P. Keratinized mucosa around
systematic review. Int J Oral Maxillofac Implants. 2013;28:1536– implants in partially edentulous posterior mandible: 10-year
1545. results of a prospective comparative study. Clin Oral Implants Res.
70. Lin G-H, Chan H-L, Wang H-L. The significance of keratinized 2015.
mucosa on implant health: a systematic review. J Periodontol. 86. Lindhe J, Bressan E, Cecchinato D, Corrá E, Toia M, Liljenberg
2013;84:1755–1767. B. Bone tissue in different parts of the edentulous maxilla and
71. Brito C, Tenenbaum HC, Wong BKC, Schmitt C, Nogueira-Filho mandible. Clin Oral Implants Res. 2013;24:372–377.
G. Is keratinized mucosa indispensable to maintain peri-implant 87. Brånemark PI, Adell R, Breine U, Hansson BO, Lindström J, Ohls-
health? A systematic review of the literature. J Biomed Mater Res son A. Intra-osseous anchorage of dental prostheses. I. Experimen-
B Appl Biomater. 2014;102:643–650. tal studies. Scand J Plast Reconstr Surg. 1969;3:81–100.
 19433670, 2018, S1, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.16-0424 by CAPES, Wiley Online Library on [18/12/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
S256 ARAUJO AND LINDHE

88. Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo alve- a 10-year period. Scand J Plast Reconstr Surg Suppl. 1977;16:1–
olar bone formation adjacent to endosseous implants. Clin Oral 132.
Implants Res. 2003;14:251–262. 102. Adell R, Lekholm U, Rockler B, Brånemark PI. A 15-year study
89. Abrahamsson I, Berglundh T, Linder E, Lang NP, Lindhe J. Early of osseointegrated implants in the treatment of the edentulous jaw.
bone formation adjacent to rough and turned endosseous implant Int J Oral Surg. 1981;10:387–416.
surfaces. An experimental study in the dog. Clin Oral Implants 103. Adell R, Lekholm U, Brånemark PI, et al. Marginal tissue reac-
Res. 2004;15:381–392. tions at osseointegrated titanium fixtures. Swed Dent J Suppl.
90. Cochran DL, Schenk RK, Lussi A, Higginbottom FL, Buser D. 1985;28:175–181.
Bone response to unloaded and loaded titanium implants with a 104. Lekholm U, Zarb GA. Patient selection and preparation. In:
sandblasted and acid-etched surface: a histometric study in the Branemark PI, Zarb GA, Albrektson T, eds. Tissue-Integrated
canine mandible. J Biomed Mater Res. 1998;40:1–11. Prostheses: Osseointegration in Clinical Dentistry. Chicago:
91. Buser D, Broggini N, Wieland M, et al. Enhanced bone apposi- Quintessence Publising Co.; 1985:199–209.
tion to a chemically modified SLA titanium surface. J Dent Res. 105. Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-
2004;83:529–533. term efficacy of currently used dental implants: a review and
92. Jensen OT, Sennerby L. Histologic analysis of clinically retrieved proposed criteria of success. Int J Oral Maxillofac Implants.
titanium microimplants placed in conjunction with maxillary sinus 1986;1:11–25.
floor augmentation. Int J Oral Maxillofac Implants. 1998;13:513– 106. Albrektsson T, Zarb GA. Current interpretations of the osseoin-
521. tegrated response: clinical significance. Int J Prosthodont.
93. Ivanoff CJ, Hallgren C, Widmark G, Sennerby L, Wennerberg A. 1993;6:95–105.
Histologic evaluation of the bone integration of TiO(2) blasted and 107. Jemt T, Lekholm U. Implant treatment in edentulous maxillae: a
turned titanium microimplants in humans. Clin Oral Implants Res. 5-year follow-up report on patients with different degrees of jaw
2001;12:128–134. resorption. Int J Oral Maxillofac Implants. 1995;10:303–311.
94. Bosshardt DD, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, 108. Roos J, Sennerby L, Lekholm U, Jemt T, Gröndahl K, Albrektsson
Lang NP. The role of bone debris in early healing adjacent to T. A qualitative and quantitative method for evaluating implant
hydrophilic and hydrophobic implant surfaces in man. Clin Oral success: a 5-year retrospective analysis of the Brånemark implant.
Implants Res. 2011;22:357–364. Int J Oral Maxillofac Implants. 1997;12:504–514.
95. Lang NP, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, 109. Bryant SR, Zarb GA. Crestal bone loss proximal to oral implants
Bosshardt DD. Early osseointegration to hydrophilic and in older and younger adults. J Prosthet Dent. 2003;89:589–597.
hydrophobic implant surfaces in humans. Clin Oral Implants Res.
110. Ekelund J-A, Lindquist LW, Carlsson GE, Jemt T. Implant treat-
2011;22:349–356.
ment in the edentulous mandible: a prospective study on Bråne-
96. Cecchinato D, Bressan EA, Toia M, Araújo MG, Liljenberg B, mark system implants over more than 20 years. Int J Prosthodont.
Lindhe J. Osseointegration in periodontitis susceptible individu- 2003;16:602–608.
als. Clin Oral Implants Res. 2012;23:1–4.
111. Attard NJ, Zarb GA. Long-term treatment outcomes in edentu-
97. Donati M, Botticelli D, La Scala V, Tomasi C, Berglundh T. Effect lous patients with implant-fixed prostheses: the Toronto study. Int
of immediate functional loading on osseointegration of implants J Prosthodont. 2004;17:417–424.
used for single tooth replacement. A human histological study.
112. Jemt T, Johansson J. Implant treatment in the edentulous maxillae:
Clin Oral Implants Res. 2013;24:738–745.
a 15-year follow-up study on 76 consecutive patients provided with
98. Hermann JS, Cochran DL, Nummikoski PV, Buser D. Crestal bone fixed prostheses. Clin Implant Dent Relat Res. 2006;8:61–69.
changes around titanium implants. A radiographic evaluation of
113. Schroeder HE. The Periodontium. Berlin: Springer-Verlag; 1986.
unloaded nonsubmerged and submerged implants in the canine
mandible. J Periodontol. 1997;68:1117–1130. 114. Sanz M, Chapple IL. Clinical research on peri-implant dis-
eases: consensus report of Working Group 4. J Clin Periodontol.
99. Broggini N, McManus LM, Hermann JS, et al. Persistent acute
2012;39(Suppl. 1):202–206.
inflammation at the implant-abutment interface. J Dent Res.
2003;82:232–237.
100. Broggini N, McManus LM, Hermann JS, et al. Peri-implant
inflammation defined by the implant-abutment interface. J Dent How to cite this article: Araujo MG, Lindhe J.
Res. 2006;85:473–478. Peri-implant health. J Periodontol. 2018;89(Suppl 1):
101. Brånemark PI, Hansson BO, Adell R, et al. Osseointegrated S249–S256. https://doi.org/10.1002/JPER.16-0424
implants in the treatment of the edentulous jaw. Experience from