Journal of Periodontology - 2018 - Monje - Significance of Keratinized Mucosa Gingiva On Peri Implant and Adjacent
Journal of Periodontology - 2018 - Monje - Significance of Keratinized Mucosa Gingiva On Peri Implant and Adjacent
DOI: 10.1002/JPER.18-0471
CASE SERIES
Results: Overall, 37 patients with 45 edentulous gaps restored with 66 implants and
90 adjacent teeth were analyzed. On comparing a KM band of <2 mm versus ≥2 mm,
with the exception of suppuration (P = 0.6), all the clinical and radiographic param-
eters were significantly increased when the KM band was <2 mm (P < 0.001). A
significant correlation was observed between KM and KT (r = 0.55), though a lack of
KM did not condition a lack of KT. In the presence of peri-implantitis, only bleeding
on probing at the adjacent dentate sites was identified to be increased.
KEYWORDS
alveolar bone, dental implants, diagnostic, implant stability, peri-implant mucositis, peri-implantitis
attended to the supportive periodontal/peri-implant treatment. • Bone level ≥3 mm apical to the most coronal portion of the
Along the recruitment period, three patients resulted to be cur- intraosseous part of the implant.
rent smokers and hence were invited to adhere to a regular sup-
portive peri-implant maintenance therapy but excluded from
the study. 2.4 Clinical assessment
The following clinical parameters and indexes were recorded
2.2 Eligibility criteria at the buccal sites of the studied implants and teeth:
The following inclusion criteria were applied: implant-
• Probing depth (PD) recorded in millimeters using a North
supported single-crown and fixed prostheses, patients aged
Carolina probe.
18 to 80 years; non-smokers; absence of infectious disease
at the time of implant placement or during the maintenance • Modified sulcular bleeding index (mBI) scored from 0 to 3
program; absence of systemic disorders or medication known according to the extent and severity of bleeding on probing
to alter bone metabolism; and partially edentulous patients (BOP).31
with gaps associated to at least one mesial and one distal • Plaque index (PI) scored from 0 to 3 according to the visi-
adjacent tooth, without sign of active periodontal disease and bility and severity of plaque accumulation.32
with or without a history of chronic periodontitis. Subjects • Keratinized mucosa (KM) around dental implants, mea-
in turn were excluded for the following reasons: pregnancy; sured from the free mucosal margin to the mucogingival
lactation; past or present heavy smoking; uncontrolled med- junction at the mid-buccal, -mesial, and -distal line angles,
ical conditions such as diabetes mellitus; inadequate three- and recorded to the nearest millimeter using a North Car-
dimensional implant positioning impeding accurate recording olina probe. If unclear, Lugol iodine was used to stain the
of probing depth; cement-retained restorations or restorations mucosa to better discern the mucogingival margin. The firm
lacking KM on the lingual implant sites. and resilient KM was identified as attached mucosa (AM).
• Keratinized gingival tissue (KT) around natural dentition,
2.3 Case definition of peri-implant health, measured from the free mucosal margin to the mucogin-
mucositis, and peri-implantitis gival junction at the mid-buccal, mesial, and distal line
Based on the consensus report of Workgroup 4 of the 2017 angles, and recorded to the nearest millimeter using a North
World Workshop on the Classification of Periodontal and Carolina probe. If unclear, Lugol iodine was used to stain
Peri-Implant Diseases and Conditions,30 the diagnosis of the mucosa to better discern the mucogingival margin.
health required: • Vestibular depth (VD) measured using a North Carolina
probe from the mucosal margin to the point of greatest
• No clinical signs of inflammation. concavity of the mucobuccal fold while retracting with a
• No bleeding and/or suppuration on gentle probing bilateral retractor. Vestibular depth was rated as shallow
(0.15 Ncm). (<4 mm) or deep (≤4 mm).
• No increase in probing depth compared with previous • Suppuration (SUP) around implants and teeth, recorded by
examinations. a dichotomous (1/0) scale using a North Carolina probe.
• No bone loss beyond crestal bone level changes resulting
Moreover, the patients were interviewed by one examiner
from initial bone remodeling.
(AM) using a visual analog scale (VAS) to assess brushing
The diagnosis of peri-implant mucositis in turn was estab- comfort before assessing the clinical condition to minimize
lished from the following: bias. The VAS recorded a characteristic (comfort) ranging
across a continuum of values, and which is not easy to mea-
• Presence of bleeding and/or suppuration on gentle probing sure directly. The score ranged from 0 (maximum discomfort)
(0.15 Ncm). to 100 (maximum comfort) and was recorded around teeth and
• No bone loss beyond crestal bone level changes resulting implants.
from initial bone remodeling.
2.5 Radiographic assessment
Lastly, the diagnosis of peri-implantitis in turn was estab-
lished from the following: One examiner (AM) assessed the radiographic bone level
(intra-rater Cohen kappa value >90% – almost perfect). Peri-
• Presence of bleeding and/or suppuration on gentle probing implant radiographic marginal bone loss (MBL) was deter-
(0.15 Ncm). mined by taking linear measurements from the most mesial
• Probing depth ≥6 mm. and distal point of the implant platform to the crestal bone on
19433670, 2019, 5, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.18-0471 by Luiz Guilherme Fiorin - Universidade Estadual Paulista , Wiley Online Library on [23/12/2024]. 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
448 MONJE AND BLASI
each periapical radiograph, corrected according to the known Overall, 45 edentulous gaps were analyzed of which, 26
height and width of each implant using an image processing were assessed in the posterior mandible, followed by 17 in the
program (National Institutes of Health). posterior maxilla and a vast minority in the anterior regions
(2). In the posterior mandible, 53.8% accounted for <2 mm
2.6 Statistical analysis of KM, while in the posterior maxilla 17.6%. On the other
side, 82.4% and 100% of the posterior and anterior maxil-
A priori statistical power analysis was performed assuming
lary sites, respectively, and 46.2% and 0% in the posterior
an intra-class correlation coefficient (ICC) of 0.25, based on a
and anterior mandibular sites, respectively, displayed ≥2 mm
previous study.33 The Kolmogorov-Smirnov test was applied
of KM.
to assess normality between the parameters KM and KT. Pear-
son correlation coefficient was used to assess the correlations
between the presence/lack of KM in the edentulous gap and 3.2 Significance of KM in relation
the other clinical and radiographic parameters or KT of the to peri-implant condition
adjacent teeth. The Mann-Whitney U-test was applied to val-
The vast majority of the implants examined presenting a band
idate the homogeneity of the clinical parameters for teeth and
of ≥2 mm of KM displayed mucosal attachment (92%), while
implants. In the event of a non-homogeneous distribution, we
AM could not be found in implants with <2 mm of KM (0%).
used the Spearman correlation test. The Kruskal-Wallis test
When comparing a KM band of <2 mm versus ≥2 mm, with
was applied to assess homogeneity of one of the variables in
the exception of SUP, all the clinical and radiographic param-
≥3 independent samples.
eters were significantly increased when the band was < 2 mm
The inferential analysis involved estimation by generalized
(Table 1 and Fig. 1). Moreover, KM was positively associ-
estimating equations (GEEs) of multilevel logistic regres-
ated with VD. A lack of KM was significantly associated with
sion models. Calculations were made to assess any parameter
peri-implantitis (P < 0.001).
recorded at implant-level in relationship to KM. The level of
The width of the KM band was significantly associated
significance was defined as 5% (𝛼 = 0.05).
(P < 0.001) with the health and peri-implantitis rates, but
not with peri-implant mucositis (Fig. 2). Interestingly, under
the presence of KM, on comparing a band ranging from 0 to
3 RESULTS 1.99 mm versus ≥2 mm, only mucositis was found to be sig-
nificantly greater (P <0.05) in the <2 mm group. Neither peri-
3.1 Study population implantitis nor healthy implants differed between these study
Based on the a priori sample size calculation, 37 white groups.
patients (37.6% females, 32.4% males; mean age: 49.9 ± 12.9
years) with 45 edentulous gaps restored with 66 implants
3.3 Significance of KM in relation to comfort
(mean follow-up: 5.73 ± 2.89 years) and 90 adjacent teeth
upon brushing
were analyzed. Of these, 30 (81.1%), six (16.2%), and
one (16.2%) patients, respectively, had one, two, and three In the presence of a KM band of <2 mm, the VAS score
implant-supported edentulous gaps. Overall, 18 (48.6%), 11 decreased significantly (P <0.001). Interestingly, when the
29.7%), seven (18.9%), and one (2.7%) patients carried one, mean KM band was 2.5 mm, all the patients reported
two, three, and five implants, respectively. In turn, 30 (81.1%), maximum comfort (VAS = 100).
six (16.2%), and one (16.2%) patients, respectively, had two,
four, and six teeth examined. A total of 196 implants sites and
3.4 Association between KM and KT of the
360 tooth sites were recorded.
adjacent dentition
Overall, eight (21.62%) out of the 37 patients presented
with active periodontal disease (residual pockets ≥5 mm with The mean KM band width was 2.35 ± 1.83 mm (range
bleeding on probing), 16 (43.24%) were controlled individu- 0 to 6.33 mm), with a median of 2.2 mm. In 40% of the
als with history of chronic periodontitis (no residual pockets edentulous implant-supported sites, the mean KM band
≥5 mm) and 13 (35.14%) were not diagnosed with active or was <2 mm, while the remaining 60% presented a KM band
history of periodontitis (no pockets ≥5 mm). Regarding the width of ≥2 mm. On the other hand, the KT band width was
level of radiographic attachment loss, 5.40% (two patients) substantially greater, with a mean value of 3.49 ± 1.12 mm
presented advanced loss of support in the dentition (>50%), (range 1 to 6.50 mm) and a median of 3.50 mm.
24.33% (nine patients) with moderate loss (30% to 50%) and The correlation between KM and KT of the adjacent teeth
70.27% (26 patients) with mild attachment loss (<30%). The was statistically significant (P = 0.002; r = 0.55). In other
grade of attachment loss was neither associated with the width words, in scenarios characterized by a lack or narrow band
of the KT and/nor the KM (P = 0.22). of KM, the KT band of the adjacent teeth was significantly
19433670, 2019, 5, Downloaded from https://aap.onlinelibrary.wiley.com/doi/10.1002/JPER.18-0471 by Luiz Guilherme Fiorin - Universidade Estadual Paulista , Wiley Online Library on [23/12/2024]. 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
MONJE AND BLASI 449
TABLE 1 Descriptive analysis of the clinical and radiographic parameters according to the width of keratinized mucosa
Keratinized mucosa
<2 mm ≥2 mm Differential coefficient P value r (P value)
n 26 40
PD (mm) 4.86 ± 1.06 (5.00) 3.65 ± 1.06 (3.33) −1.21 ± 0.28 <0.001*** −0.57 (P < 0.001*** )
mBI 1.15 ± 0.69 (1.17) 0.46 ± 0.57 (0.17) −0.69 ± 0.17 <0.001*** −0.54 (P < 0.001*** )
SUP 0.08 ± 0.20 (0.00) 0.06 ± 0.18 (0.00) −0.02 ± 0.04 0.666 −0.11 (P = 0.463)
PI 1.08 ± 0.86 (1.00) 0.28 ± 0.41 (0.00) −0.79 ± 0.21 <0.001*** −0.60 (P < 0.001*** )
MBL (mm) 2.03 ± 1.65 (2.10) 0.64 ± 0.93 (0.20) −1.39 ± 0.41 0.001** −0.55 (P < 0.001*** )
VAS (%) 53.8 ± 30.7 (60.0) 97.0 ± 8.5 (100.0) 43.2 ± 6.49 <0.001*** 0.703 (P < 0.001*** )
VD <4 mm 95.7% 18.9% <0.001***
**
P < 0.01; ***
P < 0.001, in brackets: median value
TABLE 2 Correlations between the clinical and radiographic parameters between implants and their adjacent dentition
Implants
PD mBI SUP PI MBL KM VAS
Dentition PD 0.32 (0.034* ) 0.10 (0.504) −0.10 (0.532) 0.21 (0.176) 0.19 (0.216) −0.23 (0.137) −0.26 (0.09)
mBI 0.47 (0.001** ) 0.42 (0.005** ) 0.11 (0.454) 0.38 (0.011* ) 0.25 (0.103) −0.25 (0.10) −0.16 (0.307)
SUP — — — — — — —
PI 0.39 (0.009** ) 0.37 (0.013* ) 0.16 (0.293) 0.43 (0.001** ) 0.20 (0.188) −0.10 (0.519) 0.09 (0.541)
KT −0.14 (0.367) 0.01 (0.927) −0.14 (0.358) 0.18 (0.242) −0.10 (0.520) 0.45 (0.002** ) 0.16 (0.283)
VAS (%) −0.03 (0.871) 0.15 (0.321) 0.02 (0.902) 0.05 (0.770) 0.13 (0.380) 0.20 (0.179) 0.40 (0.007** )
*
P < 0.05; **
P < 0.01
FIGURE 4 Case showing the clinical poor oral hygiene (left) in an erratic maintenance complier, where in the presence of a wide band of
keratinized mucosa, marginal bone loss has not progressed to a pathological condition (right)
since under conditions of adequate supportive peri-implant KM. In this sense, it should be highlighted that future stud-
maintenance, the association might be negligible. ies should monitor the peri-implant clinical and radiographic
Likewise, there seems to be consensus on the brushing parameters in a longitudinal basis to assess the changes over
comfort conferred by ≥2 mm of KM.46 In the absence of time in the presence/lack of KM. Furthermore, it would be of
KM, there is a mobile lining mucosa rich in elastic fibers particular interest to evaluate the dynamics of the band of KM
and poor in collagen.47 This agrees with the findings of a according to the peri-implant condition. Moreover, it must be
recent cross-sectional comparative study in which implant noted that these findings are not applicable to good mainte-
sites with a KM band width of <2 mm were found to be nance compliers, where conflicting results have been reported
more prone to brushing discomfort, plaque accumulation regarding the significance of KM.
and peri-implant soft tissue inflammation.16 In contrast, two
recent studies failed to support the association between the
absence of KM and discomfort during brushing.33,48 This 5 CONC LU SI ON S
is certainly an area of controversy where the patient pain
threshold, brushing strength, mucosal thickness and other The presence of <2 mm of KM around dental implants in
anatomy-related factors may play important roles. erratic maintenance compliers seems to be associated with
The positive association between KM and VD is of key peri-implant diseases. The lack of KM constitutes a site-
importance, since it implies that a shallow VD could inter- specific phenomenon independent of the keratinized tissue
fere with proper oral hygiene techniques, thus leading to more present in the adjacent dentition.
plaque accumulation. This finding is in agreement with a pre-
vious clinical study reporting the association between VD and ACKNOW LEDGMENTS
a lack of KM, and also increased bone loss and mucosal reces- The authors wish to acknowledge the Foundation for the
sion around implants15 and natural dentition.49 Study and Development of Implantology and Oral and
Although a correlation was observed between KM and KT, Maxillofacial Surgery (Badajoz, Spain) for financial support
a complete absence of KM was not associated with a lack of of the statistical analysis. The authors have no direct financial
KT – thus defining the former as a site-specific condition. This interests with the products and instruments listed in the paper.
critical finding suggests that there is a remodeling of soft tis-
sues in the same way as there is a remodeling of hard tissues
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on peri-implant soft-tissue health and stability around implants