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

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 Monje et al

MATERIALS AND METHODS • Too apical: ≥ 4 mm from adjacent tooth CEJ or 2 mm

below the residual ridge around adjacent dentition/
Information Sources and Development of implants
Focused Question • Correct: in a range from 4 to 2 mm from the
An electronic literature search was conducted by one adjacent CEJ or from 2 mm below the residual ridge
reviewer (AM) in several databases, including MEDLINE, to crestal position (0 mm)
EMBASE, Cochrane Central Register of Controlled Trials, • Too coronal: Supracrestal implant placement
and Cochrane Oral Health Group Trials Register databases (applicable only for rough-surface neck implants).
for articles with no language restriction up to September For smooth-collar implants, these were not
2014. The PICO question could not be developed since no considered “too coronal” as long as only the smooth
intergroup comparisons were being evaluated. surface was above the crestal level

Screening Process Angulation. When a reference was used, the adjacent

Combinations of controlled terms (MeSH and EMTREE) tooth long axis, or in the lack of this, in a perpendicular
from the National Library of Medicine (2014) and keywords position regarding the ridge parallelism.
were used whenever possible. The search terms used,
where “[mh]” represented the MeSH terms and “[tiab]” rep- • Straight: From 70 to 90 degrees from the adjacent
resented title and/or abstract, for the PubMed search were: tooth long axis or from the ridge parallelism
(“peri-implantitis”[mh] OR ((“dental implantation”[mh] • Tilted: < 70 degrees from the adjacent tooth long
OR “dental implants” [mh]) AND (“peri implant” [tiab] axis or from the ridge parallelism
OR “peri-implantitis” [tiab]))) AND (“treatment” [tiab] OR
“therapy” [tiab] OR “therapeutics”[mh]). In addition, a Keratinized mucosa. Its minimum presence (≥ 2 mm)
screening of the references of included papers was con- has been shown to prevent inflammation and plaque
ducted for publications not identified. accumulation9,17:

Eligibility Criteria • Adequate: ≥ 2 mm in the implant midbuccal level

Briefly, articles were included in this qualitative analysis if • Minimal: < 2 mm in the implant midbuccal level
they aimed at treating nonsurgical and surgical (resective • Lack: No presence of keratinized mucosa
and regenerative) peri-implantitis, with no restriction of
sample size, and showing clear clinical photographs where Relation to adjacent dentition. Although controversy
the following implant parameters could be analyzed. exists in this regard due to advances in implant-abutment
Horizontal position. This is a point parallel to the connections,18 1.5 mm was generally accepted as the mini-
occlusal plane of the adjacent dentition or in a buccolin- mum implant-tooth distance to minimize peri-implant
gual position that preserves the buccal and lingual plates bone loss.19
after postplacement resorption takes place.14,15 As such,
implants would be classified using this landmark: • Adequate: ≥ 1.5 mm from adjacent tooth (if present)
• Inadequate: < 1.5 mm from adjacent tooth
• Too buccal: thin buccal plate (< 2 mm), which might (if present)
represent implant malpositioning that triggered
greater buccal bone resorption;12 or improper Relation to adjacent implant. As it occurs adjacent to
occlusal situation, which might lead to occlusal natural dentition, owing to novel implant-abutment con-
overloading16 nection designs, there is no consensus about this matter.
• Correct: in a range of ≥ 2 mm from the buccal plate However, classically, an interimplant distance of 3 mm has
and >1 mm from the lingual plate or in the ideal been considered predictable to avoid peri-implant loss
occlusal plane and to achieve interimplant papillae20:
• Too lingual: thin lingual plate (< 1 mm) and improper
occlusal situation, which might lead to occlusal • Adequate: ≥ 3 mm from adjacent implant
overloading16 (if present)
• Inadequate: < 3 mm from adjacent implant
Vertical position. After the remodeling process estab- (if present)
lishing the biologic width takes place, this is the vertical
point where the implant can maintain a healthy condition Tissue biotype. Recent evidence is showing that
under regular maintenance. As such, implants would be thicker peri-implant tissues may impact on marginal
classified according to their relation to the adjacent tooth bone loss.21–23 Nonetheless, no cutoff point has been
cementoenamel junction (CEJ): demonstrated to enhance implant prognosis. Hence, the

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Monje et al

Identified Potentially relevant

Inclusion

Articles = 30
1,082 1,036 46 16
Cases = 36

Exclusion
Titles and No/deficient
abstracts clinical photograph

Fig 1   Chart of the screening process.

evaluators ranked the presence of thick- or thin-tissue Study Survey

biotype relatively subjectively according to Linkevicius Three experienced implantologists (> 20 years of expertise)
et al23 into three major categories: qualitatively evaluated the selected cases (PG-M, TF-T,
H-LW). This was a double-blinded examination (evaluator
• Thin: < 2 mm thickness masked from publication authors and from the other
• Medium: 2 to 3 mm thickness examiners). Cohen’s kappa index was used to test the
• Thick: > 3 mm thickness interexaminer reliability. One author (AM) collected this
information and evaluated the data to figure out the
Prosthesis design. Not enough literature is available putative parameters for the development of peri-implant
to claim the superiority of implant-supported or implant- disease.25 For each photograph evaluated, only parameters
retained prosthesis design (shape, emergence, and adap- that were agreed on by all three examiners were reported
tation) upon peri-implant tissue conditions. Nevertheless, as potential factors. Furthermore, only clear parameters
it is generally accepted that while rectangular-shape for evaluation were extracted from each article; if not,
crowns might be more plaque retentive due to the impos- they were left blank and considered to be dismissed.
sibility of maintaining adequate oral hygiene, unduly
triangular-shape crowns might be more prone for food
impaction. Thus, if the prosthesis was placed, examiners RESULTS
ranked subjectively between two categories:
Selected Studies
• Adequate: Easy to perform home care An overall 46 studies were selected initially. After compre-
plaque control hensive appraisal, 30 studies were examined inasmuch
• Inadequate: Difficult to perform home care as they provided clinical photos that could be evaluated.
plaque control From these, 36 clinical cases that were documented pho-
tographically were extracted and scored by the exam-
Implant design. Advances in implant micro- and iners (Fig 1).
macrodesigns have resulted in dental implants having
higher long-term success rates. Although the impact of Survey of Parameters
current implant surfaces upon failure is still not clear,24 Only the parameter “implant position–too buccal” reached
it can be stated that rough titanium-alloy taper- and almost perfect interexaminer agreement (κ = 0.81). Like-
straight-threaded implants currently represent the gold wise, “tissue biotype–thin” and “presence of keratinized
standard due to up-to-date successful outcomes through mucosa–minimal” demonstrated moderate agreement
achievement of osseointegration. Therefore, although (κ = 0.43 and κ = 0.58, respectively). The rest of the param-
some subjectively were executed when evaluating this eters studied based on clinical photographs were fair or
fact, two categories were considered: poor. Therefore, they were excluded as local contributing
factors for the development of peri-implantitis. Figure 2
• Rough: Rough implant body, straight- or displays the relevance of these parameters in the present
taper-threaded dental implant findings. Too-buccal implant position, minimal keratin-
• Smooth: Smooth implant body ized mucosa, and thin-tissue biotype represented 40.5%,
29%, and 21.5% of the determinants for peri-implantitis,
respectively.

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 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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