Into the Paradigm of Local Factors as Contributors for

Peri-implant Disease: Short Communication

Alberto Monje, DDS1/Pablo Galindo-Moreno, DDS, PhD2/Tolga Fikret Tözüm, DDS, PhD3/
Fernando Suárez-López del Amo, DDS4/Hom-Lay Wang, DDS, MS, PhD5

Although some systemic conditions have been associated with peri-implant disease, local contributing
factors largely remain to be determined. This study aimed at evaluating, based on clinical photographs
obtained from peri-implantitis treatment publications, the possible local contributing factors involved in its
development based upon a survey obtained from three experienced clinicians (> 20 years of expertise).
Cohen’s kappa index was used to test the interexaminer reliability. “Too-buccal implant position” was the
only parameter to reach almost perfect interexaminer agreement (κ = 0.81). “Thin-tissue biotype” and
“minimal presence of keratinized mucosa” demonstrated moderate agreement (κ = 0.43 and κ = 0.58,
respectively). The rest of the parameters studied based on clinical photographs were fair or poor. Therefore,
based on this clinicians’ survey, implants too buccally placed, minimal or a lack of keratinized mucosa, and
thin-tissue biotype might contribute to a higher susceptibility of developing peri-implantitis. These factors
must be the focus of attention in future cross-sectional studies on the incidence of peri-implant diseases.
Int J Oral Maxillofac Implants 2016;31:288–292. doi: 10.11607/jomi.4265

Keywords: endosseous implants, evidence-based, implantology, osseointegration, peri-implantitis, risk factor

B y definition, peri-implantitis represents a chronic

inflammatory process that causes peri-implant tis-
sue breakdown, jeopardizing implant functional sta-
bility. As was foreseen by many experts in this area,1–4
the popularity of implants for restoring oral function
is increasing the prevalence of peri-implantitis. Long-
term studies have shown a range of 2.7% up to 47.1% of
implants.5 This relatively high prevalence is most likely
to occur in the presence of a history of periodontitis,
smoking, poor plaque control, genetic factors (ie, IL-1RN
1Resident
and Research Fellow, Graduate Periodontics,
Department of Periodontics and Oral Medicine, School of
Dentistry, University of Michigan, Ann Arbor, Michigan, USA.
2Professor, Department of Oral Surgery and Implantology, The
University of Granada, Granada, Spain.
3 Professor, Graduate Periodontics, Department of
Periodontics, College of Dentistry, University of Illinois,
Chicago, Illinois, USA.
4Resident, Graduate Periodontics, Department of Periodontics
and Oral Medicine, School of Dentistry, University of Michigan,
Ann Arbor, Michigan, USA.
5Professor and Program Director, Department of Periodontics
and Oral Medicine, School of Dentistry, University of Michigan,
Ann Arbor, Michigan, USA.
Correspondence to: Dr Hom-Lay Wang, Department of
Periodontics and Oral Medicine, University of Michigan
School of Dentistry, 1011 North University Avenue,
Ann Arbor, MI 48109-1078, USA. Fax: (734) 936-0374.
Email: homlay@umich.edu
©2016 by Quintessence Publishing Co Inc.
gene polymorphism), diabetes, occlusal overload, and
residual cement.6 Additionally, much is discussed about
its most accurate treatment, but so far, no agreement
has been reached.7 As a matter of fact, it remains a
controversy in the outcome of peri-implant treatment.
This is largely because the etiologic factors that trigger
peri-implant progressive bone loss have not yet been
identified nor removed.8 For instance, minimal or a
lack of keratinized mucosa has been shown to have a
higher rate of peri-implant pathology.9 Occlusion, in
animal models, also has demonstrated triggering of
peri-implant crestal bone loss that may lead to peri-
implantitis.10,11 Other factors, such as thin-tissue bio-
type or nonideal three-dimensional implant position,
have recently been widely discussed among clinicians
as possible contributing factors to peri-implantitis. For
example, Spray et al demonstrated that a minimum dis-
tance of 1.8 mm from the implant flange to the buccal
bone aspect is required to prevent future bone loss.12
The bottom line of this study is that bone resorption
may trigger implant thread exposure in the areas of
thinnest tissues or bone. As a consequence, putative
bacteria that causes peri-implant disease may then pop-
ulate and lead to the development of chronic inflam-
mation.13 Nonetheless, little is known about how local
contributing factors might contribute to the develop-
ment of peri-implant disease. Hence, this survey study
was designed in an attempt to explore which local
factors might serve as the local contributors for peri-
implant disease.

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MATERIALS AND METHODS
Information Sources and Development of
Focused Question
An electronic literature search was conducted by one
reviewer (AM) in several databases, including MEDLINE,
EMBASE, Cochrane Central Register of Controlled Trials,
and Cochrane Oral Health Group Trials Register databases
for articles with no language restriction up to September
2014. The PICO question could not be developed since no
intergroup comparisons were being evaluated.
Screening Process
Combinations of controlled terms (MeSH and EMTREE)
from the National Library of Medicine (2014) and keywords
were used whenever possible. The search terms used,
where “[mh]” represented the MeSH terms and “[tiab]” rep-
resented title and/or abstract, for the PubMed search were:
(“peri-implantitis”[mh] OR ((“dental implantation”[mh]
OR “dental implants” [mh]) AND (“peri implant” [tiab]
OR “peri-implantitis” [tiab]))) AND (“treatment” [tiab] OR
“therapy” [tiab] OR “therapeutics”[mh]). In addition, a
screening of the references of included papers was con-
ducted for publications not identified.
Eligibility Criteria
Briefly, articles were included in this qualitative analysis if
they aimed at treating nonsurgical and surgical (resective
and regenerative) peri-implantitis, with no restriction of
sample size, and showing clear clinical photographs where
the following implant parameters could be analyzed.
Horizontal position. This is a point parallel to the
occlusal plane of the adjacent dentition or in a buccolin-
gual position that preserves the buccal and lingual plates
after postplacement resorption takes place.14,15 As such,
implants would be classified using this landmark:
• Too buccal: thin buccal plate (< 2 mm), which might
represent implant malpositioning that triggered
greater buccal bone resorption;12 or improper
occlusal situation, which might lead to occlusal
overloading16
• Correct: in a range of ≥ 2 mm from the buccal plate
and >1 mm from the lingual plate or in the ideal
occlusal plane
• Too lingual: thin lingual plate (< 1 mm) and improper
occlusal situation, which might lead to occlusal
overloading16
Vertical position. After the remodeling process estab-
lishing the biologic width takes place, this is the vertical
point where the implant can maintain a healthy condition
under regular maintenance. As such, implants would be
classified according to their relation to the adjacent tooth
cementoenamel junction (CEJ):
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Monje et al
• Too apical: ≥ 4 mm from adjacent tooth CEJ or 2 mm
below the residual ridge around adjacent dentition/
implants
• Correct: in a range from 4 to 2 mm from the
adjacent CEJ or from 2 mm below the residual ridge
to crestal position (0 mm)
• Too coronal: Supracrestal implant placement
(applicable only for rough-surface neck implants).
For smooth-collar implants, these were not
considered “too coronal” as long as only the smooth
surface was above the crestal level
Angulation. When a reference was used, the adjacent
tooth long axis, or in the lack of this, in a perpendicular
position regarding the ridge parallelism.
• Straight: From 70 to 90 degrees from the adjacent
tooth long axis or from the ridge parallelism
• Tilted: < 70 degrees from the adjacent tooth long
axis or from the ridge parallelism
Keratinized mucosa. Its minimum presence (≥ 2 mm)
has been shown to prevent inflammation and plaque
accumulation9,17:
• Adequate: ≥ 2 mm in the implant midbuccal level
• Minimal: < 2 mm in the implant midbuccal level
• Lack: No presence of keratinized mucosa
Relation to adjacent dentition. Although controversy
exists in this regard due to advances in implant-abutment
connections,18 1.5 mm was generally accepted as the mini-
mum implant-tooth distance to minimize peri-implant
bone loss.19
• Adequate: ≥ 1.5 mm from adjacent tooth (if present)
• Inadequate: < 1.5 mm from adjacent tooth
(if present)
Relation to adjacent implant. As it occurs adjacent to
natural dentition, owing to novel implant-abutment con-
nection designs, there is no consensus about this matter.
However, classically, an interimplant distance of 3 mm has
been considered predictable to avoid peri-implant loss
and to achieve interimplant papillae20:
• Adequate: ≥ 3 mm from adjacent implant
(if present)
• Inadequate: < 3 mm from adjacent implant
(if present)
Tissue biotype. Recent evidence is showing that
thicker peri-implant tissues may impact on marginal
bone loss.21–23 Nonetheless, no cutoff point has been
demonstrated to enhance implant prognosis. Hence, the
The International Journal of Oral & Maxillofacial Implants 289
Monje et al
Identified
Inclusion
1,082 1,036
Exclusion
Titles and
abstracts
Fig 1   Chart of the screening process.
evaluators ranked the presence of thick- or thin-tissue
biotype relatively subjectively according to Linkevicius
et al23 into three major categories:
• Thin: < 2 mm thickness
• Medium: 2 to 3 mm thickness
• Thick: > 3 mm thickness
Prosthesis design. Not enough literature is available
to claim the superiority of implant-supported or implant-
retained prosthesis design (shape, emergence, and adap-
tation) upon peri-implant tissue conditions. Nevertheless,
it is generally accepted that while rectangular-shape
crowns might be more plaque retentive due to the impos-
sibility of maintaining adequate oral hygiene, unduly
triangular-shape crowns might be more prone for food
impaction. Thus, if the prosthesis was placed, examiners
ranked subjectively between two categories:
• Adequate: Easy to perform home care
plaque control
• Inadequate: Difficult to perform home care
plaque control
Implant design. Advances in implant micro- and
macrodesigns have resulted in dental implants having
higher long-term success rates. Although the impact of
current implant surfaces upon failure is still not clear,24
it can be stated that rough titanium-alloy taper- and
straight-threaded implants currently represent the gold
standard due to up-to-date successful outcomes through
achievement of osseointegration. Therefore, although
some subjectively were executed when evaluating this
fact, two categories were considered:
• Rough: Rough implant body, straight- or
taper-threaded dental implant
• Smooth: Smooth implant body
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Potentially relevant
Articles = 30
46 16
Cases = 36
No/deficient
clinical photograph
Study Survey
Three experienced implantologists (> 20 years of expertise)
qualitatively evaluated the selected cases (PG-M, TF-T,
H-LW). This was a double-blinded examination (evaluator
masked from publication authors and from the other
examiners). Cohen’s kappa index was used to test the
interexaminer reliability. One author (AM) collected this
information and evaluated the data to figure out the
putative parameters for the development of peri-implant
disease.25 For each photograph evaluated, only parameters
that were agreed on by all three examiners were reported
as potential factors. Furthermore, only clear parameters
for evaluation were extracted from each article; if not,
they were left blank and considered to be dismissed.
RESULTS
Selected Studies
An overall 46 studies were selected initially. After compre-
hensive appraisal, 30 studies were examined inasmuch
as they provided clinical photos that could be evaluated.
From these, 36 clinical cases that were documented pho-
tographically were extracted and scored by the exam-
iners (Fig 1).
Survey of Parameters
Only the parameter “implant position–too buccal” reached
almost perfect interexaminer agreement (κ = 0.81). Like-
wise, “tissue biotype–thin” and “presence of keratinized
mucosa–minimal” demonstrated moderate agreement
(κ = 0.43 and κ = 0.58, respectively). The rest of the param-
eters studied based on clinical photographs were fair or
poor. Therefore, they were excluded as local contributing
factors for the development of peri-implantitis. Figure 2
displays the relevance of these parameters in the present
findings. Too-buccal implant position, minimal keratin-
ized mucosa, and thin-tissue biotype represented 40.5%,
29%, and 21.5% of the determinants for peri-implantitis,
respectively.
 Monje et al

DISCUSSION
Too-buccal position: 40.5%
Upon the definition of risk factor,26 this short com-
munication does not attempt to mislead the clinicians
by stating that local factors such as too buccal of an
implant position, minimal presence of keratinized
mucosa, and/or thin-tissue biotype are the etiologic Other factors:
Thin-tissue
9%
factors for peri-implant pathology , since authors agree biotype:
21.5%
that biofilm represents the primary etiologic factor
for peri-implant diseases. However, implants with
the aforementioned variables seem to have a higher
incidence of peri-implant pathology. It is of paramount
importance to understand the concepts of peri-implan-
titis and peri-implant marginal bone loss (MBL). While
the first unarguably includes the second, the latest
can occur at earlier stages (aka physiologic bone loss) Minimal keratinized: 29%
without the occurrence of disease (ie, inflammation).8,27
Recently, it was shown that 96% of implants with an
MBL of > 2 mm at 18 months had a loss of 0.44 mm or Fig 2  Radar-type graph for the factors involved in the devel-
more at 6 months postloading.28 Thus, factors affecting opment of peri-implant disease. Implant position (too buccal),
early MBL may lead and contribute to the development keratinized mucosa (minimal), and tissue biotype (thin) repre-
sented 40.5%, 29%, and 21.5% of the determinants for peri-
of peri-implantitis due to a standing peri-implant bone implantitis, respectively.
loss progression.
Based upon the present findings, the most determi-
nant parameter for the presence of peri-implant disease
was implant positioning. Implants placed too buccally,
using the buccal bone flange as the standard position,
developed more peri-implantitis. The authors’ hypoth- is related to a thicker-tissue biotype and, in other words,
esis was that, although most of the implants analyzed a more resistant environment for peri-implant contami-
might have been completely within the bony housing nation and inflammation.
at insertion, there is a bone remodeling process that The authors could not accurately evaluate other fac-
occurs regardless of the implant placement protocol tors such as implant-prosthesis connection/design,31
(buccolingual resorption of 1.9 mm for delayed and occlusion,32 or type of implant-prosthesis retention,
3.06 mm for immediate).28 This may trigger thread among others.33 However, these factors cannot be over-
exposure, leading to an auspicious environment for the looked since they seem also to play an important role in
pathogenic bacteria to cause the disease with further peri-implant stability.33 Hence, it is the authors’ purpose
bone loss. As a matter of fact, it needs to be mentioned to stress the need for human studies to examine these
that approximately 40% of the implants appraised were unknown possible contributing factors.34
in the anterior maxillary area, where many clinicians
opt for immediate implant placement. The thickness of
alveolar maxillary bone in this area ranges from 1.08 to CONCLUSIONS
1.3 mm.29 Therefore, based on this evidence, the vast
majority of the implants placed in the anterior area This work highlights the importance of local factors
may have thread exposure that may eventually result as contributors to peri-implant disease development:
in peri-implantitis and/or peri-implant bone loss due implants too buccally placed followed by minimal
to biofilm accumulation. or a lack of keratinized mucosa, and thin-tissue bio-
Additionally, it seems evident that a lack of or mini- type. These factors must be the focus of attention
mal keratinized mucosa, and what in many cases repre- in future cross-sectional studies on the incidence of
sents its counterpart, a thin-tissue biotype, represents a peri-implant diseases.
common situation over implants with peri-implantitis.
Although controversial, the presence of keratinized
mucosa as well as peri-implant tissue biotype around ACKNOWLEDGMENTS
implants seems to play a role in protecting the peri-
implant environment and ultimately reducing the The authors do not have any financial interests, either directly
or indirectly, in the products or information listed in the article.
crestal bone loss.9,30 This increase in keratinized mucosa

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Monje et al
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