Peri-implant diseases have received much attention since dental implants are generally used in contemporary dentistry. Several contributing factors associated with the development of peri-implant diseases have also been investigated. The prevalence of peri-implantitis has been reported but with great heterogeneity because of a lack of a universally accepted classification system that could define the extent and severity of peri-implantitis. Several parameters—including radiographic bone loss, probing depth, bleeding on probing, and suppuration—have been introduced in these reports to assist with clinical diagnosis. This article provides an objective evaluation of these parameters based on currently available evidence, offers further recommendations, and proposes a multidomain scale for diagnosis of peri-implantitis. Future investigations and modifications may be needed to develop a comprehensive, evidence-based classification system that addresses the multifactorial etiology of peri-implant diseases.

Introduction

Peri-implant diseases have received much attention since dental implants began extensive use in contemporary dentistry.13  The American Academy of Periodontology Academy Statement3  defines peri-implant mucositis as the presence of inflammation confined to the soft tissues surrounding a dental implant with no signs of bone loss following initial bone remodeling. Peri-implantitis is defined as an inflammatory process around an implant, which includes both soft tissue inflammation and progressive bone loss following initial bone remodeling.3  The etiology of peri-implant diseases is multifactorial. Similar to the etiology of gingivitis and periodontitis, the primary etiology of peri-implant diseases is reported to be bacterial in nature with subsequent activation of the host immune response.35 

Several contributing factors associated with the development of peri-implant diseases have also been investigated, including but not limited to a history of periodontitis,6,7  smoking,8,9  and residual cement.10  In addition, occlusal overload is often as a significant factor when bone loss is observed proximal to dental implants.11  Other factors that have been linked to peri-implant bone loss are implant malposition,12  compression necrosis,13  and even foreign body reaction.14  However, these remain controversial with regards to their true association with peri-implant bone loss or even peri-implantitis.

The prevalence of peri-implantitis has been widely reported but with great heterogeneity.3,15  Since there is no universally accepted classification system to define the extent and severity of peri-implantitis, most clinical publications define a disease status based on their own criteria (Table 1).1631  According to these publications, the prevalence of peri-implantitis ranges from 6.2% to 39.3% at the implant level and 10.5% to 47.8% at the patient level. Several parameters have been introduced in these reports to assist with clinical diagnosis. Among the most widely used parameters are radiographic bone loss (RBL), probing depth (PD), bleeding on probing (BOP), and suppuration. This article's goal is to provide an objective evaluation of these parameters based on currently available evidence, provide further recommendations, and propose a multidomain scale for future diagnosis of peri-implantitis.

Table 1

Studies reporting the prevalence and criteria for peri-implantitis*

Studies reporting the prevalence and criteria for peri-implantitis*
Studies reporting the prevalence and criteria for peri-implantitis*

Radiographic Bone Loss

Peri-implant bone loss is the major criterion that differentiates peri-implantitis from peri-implant mucositis. As a result, radiographic bone loss (RBL) is introduced to determine the peri-implant bone level due to its convenience and lack of invasiveness. However, there is no consensus on the ideal threshold of RBL that defines disease status. In 1986, Albrektsson et al32  proposed that a successful implant must present no mobility, no peri-implant radiolucency, bone loss of less than 0.2 mm per year after the first year of loading, and no persistent pain, discomfort, or infection. In their study, the authors reported 1 mm of RBL during the first year after abutment connection. It is important to note that the authors proposed these criteria based on observations made on pure titanium implants, which are different from those often used today (namely, rough or coated surface implants). Similarly, Adell et al33  reported an average of 1.5 mm of RBL during the first year of healing when a pure titanium implant was used and only 0.1 mm of RBL annually thereafter. This “first-year bone loss” after connection of the restoration was then further investigated and is now considered part of “physiologic bone remodeling.”1 

Since physiologic bone remodeling is an inevitable process, four different patterns have been proposed to describe this phenomenon.34  Although bone remodeling occurs primarily within the first year after placement of the abutment connection,32  the reasons for its occurrence and the unpredictability of the amount of RBL are still not fully understood. Several factors—including the level of implant placement, tissue biotype, types of abutment connections, implant macro- and microdesigns, and implant surface topography—have all been analyzed.2,3,15,21,28,35  A recent animal study reported that different types of implant designs and depth of implant placement have significant impact on this remodeling process.35  These findings underscore that using a certain level of RBL (ie, 2 mm) from a fixed reference point (ie, implant shoulder) to define “acceptable” bone remodeling is challenging.2,25  Consequently, the prevalence of peri-implantitis reported throughout the literature is inconsistent because of the diverse cut-off values for RBL defined in individual studies.

Most recent studies introduced the concept of 2 mm of bone loss from a fixed point (such as the implant shoulder, the platform level, or the most apical extension of the polished surface) as the reference point from which to measure the RBL after the first year of loading (Table 2). However, this definition often makes clinical diagnosis difficult since the amount of physiologic bone remodeling cannot be predicted from the reference point due to its multifactorial nature. To date, the only consensus report aiming to define this threshold is the VIII European Workshop on Periodontology.2  In this consensus report, peri-implantitis was defined as “changes in the level of the crestal bone in conjunction with BOP with or without concomitant deepening of peri-implant pockets”36  if a baseline radiograph is available. However, in the absence of previous radiographic records, a threshold of 2 mm of vertical bone loss from the expected marginal bone level was suggested. Although this report provides a clear diagnostic guideline for clinicians, other issues such as “expected marginal bone level” and “acceptable amount of annual bone loss” after the first year of loading are subjective. One study suggested that “RBL >2 mm from the implant platform for bone-level implants or >2 mm from the apical termination of the polished collar for tissue-level implants” could be used as the threshold indicating peri-implantitis.25  In addition, an annual bone loss of less than 0.2 mm after physiologic remodeling could be considered acceptable.1  Therefore, a modified scale that incorporates the type of implant design and years of service would be beneficial in deriving a more uniform diagnosis.

Table 2

Currently available scales defining peri-implantitis*

Currently available scales defining peri-implantitis*
Currently available scales defining peri-implantitis*

In our proposed multidomain scale (Table 3), clinicians should evaluate whether or not a baseline radiograph taken at least 1 year after definite crown delivery is available. If this baseline radiograph is available, the acceptable RBL will be no more than 0.2 mm annually compared to the baseline radiograph. On the contrary, if a baseline radiograph is not available, a threshold of 2 mm RBL from a fixed point (eg, implant platform for bone-level and termination of polished collar for tissue-level implants) should be used to determine the disease status. It is worth taking a baseline radiograph whenever possible since it provides valuable information in terms of bone level after the physiologic bone remodeling process. The threshold of “2 mm RBL from a fixed point” should be applied only when a baseline radiograph is not retrievable. A clinical case with a baseline radiograph is demonstrated in Figure 1 as an example.

Table 3

Proposed multi-domain scale defining peri-implantitis*

Proposed multi-domain scale defining peri-implantitis*
Proposed multi-domain scale defining peri-implantitis*
Figure

A 67-year-old Caucasian female received dental implant placement to replace the missing teeth #29 and #30. (a) Periapical radiograph was taken at the time of implant placement. (b) Another periapical radiograph was taken 1 year after definite restoration. This periapical radiograph is served as a baseline radiograph to represent radiographic bone level. (c) Periapical radiograph taken 2 years after crown delivery showed progressive peri-implant bone loss at distal aspect of #29. No apparent peri-implant bone loss was seen at #30. (d) A clinical picture taken 2 years after crown delivery showed inflamed peri-implant tissue with suppuration at #29 and #30. Based on the proposed multi-domain scale, #29 was determined with peri-implantitis and #30 was determined with peri-implant mucositis.

Figure

A 67-year-old Caucasian female received dental implant placement to replace the missing teeth #29 and #30. (a) Periapical radiograph was taken at the time of implant placement. (b) Another periapical radiograph was taken 1 year after definite restoration. This periapical radiograph is served as a baseline radiograph to represent radiographic bone level. (c) Periapical radiograph taken 2 years after crown delivery showed progressive peri-implant bone loss at distal aspect of #29. No apparent peri-implant bone loss was seen at #30. (d) A clinical picture taken 2 years after crown delivery showed inflamed peri-implant tissue with suppuration at #29 and #30. Based on the proposed multi-domain scale, #29 was determined with peri-implantitis and #30 was determined with peri-implant mucositis.

In terms of the severity of peri-implantitis, several parameters have been proposed.28,37,38  Froum and Rosen37  and Decker et al38  used the percentage of RBL relative to the total implant length to define the severity of peri-implantitis. Derks et al28  proposed the amount of RBL (>0.5 mm as mild/slight and >2 mm as moderate/severe) to address the severity. A comparison of these systems and a proposed scale is listed in Table 2. Since there is no available consensus report to elaborate on this issue, we suggest using the percentage of RBL relative to the total implant length, proposed by the aforementioned articles,37,38  to define severity since it is relatively objective and easy to determine radiographically.

Probing Depth

Probing depth is another parameter that has been used to determine peri-implant tissue health. Although this parameter is reproducible and repeatable within 1 mm of accuracy at periodontal sites,39  the accuracy of PD around dental implants remains challenging. Since the reproducibility of PD depends on several factors—such as probing force, probing angulation, probe tip diameter, and tissue inflammatory status—implant-supported restorations might hinder the ability to attain accurate measurements. It has been reported that implant and abutment designs might increase difficulty in obtaining accurate PD measurements, further underestimating the extent of the peri-implant lesion.36 

Due to the absence of periodontal ligament fibers, supracrestal connective tissue fibers are arranged in a circular pattern40,41  around the peri-implant tissues, thus decreasing the resistance to clinical probing compared to natural teeth.36,41  In an animal model, Schou et al41  reported that the probe tip was closer to the bone around implants than around teeth in diseased sites, and even mild inflammation was associated with deeper probe penetration around implants. Histologically, the probe tip stopped at the apical extent of the connective tissue attachment in the mucositis sites, and close to the crestal bone level in the peri-implantitis sites. Therefore, using an absolute cut-off number for PD (ie, ≥4 mm) to define disease status is challenging and difficult for monitoring disease progression. Additionally, a deeper PD has been reported for implants placed subcrestally compared to those placed crestally,42  which indicates that a baseline PD should be established as a basis for comparison before applying PD as a diagnostic criterion.

In terms of the correlation between PD and peri-implant bone loss, Serino et al43  reported a high linear and statistically significant correlation between PD recorded after removal of a prosthesis and the bone level; however, this correlation was not seen if the PD was recorded without removal of the prosthesis. Additionally, the authors also reported that only 37% of sites presented similar measurements between PD recorded with and without implant-supported prostheses, whereas 39% of sites presented a difference of 1 mm, and in 25% of sites, a 2-mm discrepancy was detected. Thus, PD measurements at sites with peri-implantitis with concomitant prosthetic reconstruction should be interpreted cautiously, since the accuracy and correlation with peri-implant bone loss is not consistent.

Based on the current evidence,42,43  PD may not be a reliable indicator for peri-implant disease status. Two studies that explored this topic2,28  suggested that there should be no cut-off value or specific PD for defining peri-implantitis. In our multidomain scale of diagnostic criteria (Table 3), we propose using a deepening PD and with progressive RBL when a baseline PD is available; if a baseline PD is not available, use a PD consistent with concomitant RBL to diagnose peri-implantitis. In a situation with a deepening PD but without signs of progressive RBL, a diagnosis of peri-implant mucositis should be made. However, if progressive RBL is detected, a diagnosis of peri-implantitis is indicated. In any case, we do not recommend using a PD cut-off number only to define disease status; RBL should always be used to define the progression of peri-implantitis.

Bleeding on Probing

The presence of BOP or suppuration is generally used as one of the criteria to define peri-implant tissue inflammation. The clinical value of BOP has been studied extensively in the periodontal literature. Lang et al44  reported that BOP is a good indicator for predicting future attachment level loss in natural dentition, with a 30% chance if BOP is present at the same site on four consecutive recall appointments. In addition, although BOP has a low positive predictive value, its negative predictive value was almost 100%,45,46  indicating that the absence of BOP is a good measure of periodontal health. It has been presumed that the same correlations apply to peri-implant tissues; however, this has not been clinically validated.46 

Since peri-implant tissue is less resistant to probing forces than is the periodontium,47  simply using the presence of BOP may not adequately characterize the inflammatory status of the peri-implant tissues. Furthermore, previous studies have reported that BOP around dental implants was significant despite reduced signs of tissue inflammation.48,49  Therefore, because BOP does not accurately reflect the status of the peri-implant tissues, other measures (ie, redness, swelling, suppuration) are needed to evaluate the inflammatory condition around implants.

Suppuration

Suppuration is the most common parameter used with BOP to confirm the status of peri-implant tissue inflammation. Interestingly, though the value of this parameter has been investigated at periodontal sites,50  there is currently no standardized method to measure this parameter at peri-implant sites. In an early study,50  Kaldahl et al introduced the use of an egg ball burnisher to exert lateral pressure against the gingival margin to detect suppuration. A positive suppuration value was recorded if visible nonclear exudate was seen at the gingival crevice. Their study showed that gingival suppuration was a better prognosticator of future attachment loss than gingival bleeding or supragingival plaque. The authors further concluded that suppuration is an indicator of active attachment loss; however, lack of suppuration did not ensure health or the absence of breakdown.50 

With regards to peri-implant tissues, Derks et al28  reported a positive value if an observation of suppuration was noted within 15 seconds following pocket probing. Other parameters—such as the plaque index, bleeding index, or gingival index—have also been used27,29  as adjunctive criteria to determine peri-implant tissue health. Based on the current evidence,46,4850  the presence of suppuration presumably provides a higher sensitivity for peri-implant tissue breakdown than the presence of BOP. However, further clinical trials are needed to analyze the predictive values of these parameters at peri-implant sites.

Summary

Based upon the currently available evidence, we propose a multidomain diagnostic scale for peri-implantitis (Table 3) that incorporates the use of RBL, PD, and BOP/suppuration. In terms of RBL, if a baseline radiograph taken at the time of abutment connection is available, we recommend less than 0.2 mm annual bone loss after physiologic bone remodeling as the acceptable threshold. If a baseline radiograph is not present, a threshold of 2 mm from the expected bone level (based on bone-level or tissue-level implants) is proposed. With respect to PD, since this parameter might not reliably reflect disease status, a threshold PD is not used as a criterion. Instead, a deepening PD with progressive RBL (if a baseline PD is available) or a PD consistent with concomitant RBL (if a baseline PD is not available) is proposed as an adjunctive parameter to define peri-implantitis. The presence of suppuration remains one of the criteria to define peri-implant tissue inflammation in our scale since this parameter tends to be more sensitive than BOP for detecting tissue breakdown. However, we suggest the inclusion of other clinical signs of tissue inflammation (ie, BOP, redness, swelling) to confirm the inflammatory status around implants. A severity scale of peri-implantitis based on the percentage of RBL relative to total implant length is also included in our proposed multidomain scale.

Since there is a high prevalence of peri-implant diseases in contemporary dentistry, a generally accepted diagnostic scale is crucial to achieve consistent diagnosis and further guide clinical practice. Although our proposed scale is based on the available evidence, future investigations and modifications may be warranted; namely, a comprehensive, evidence-based classification system is needed to address the multifactorial etiology of peri-implant diseases.

Abbreviations

    Abbreviations
     
  • BOP

    bleeding on probing

  •  
  • PD

    probing depth

  •  
  • RBL

    radiographic bone loss

Note

The authors report no conflicts of interest related to this study.

References

References
1
Iacono
VJ.
Committee on Research S, Therapy tAAoP. Dental implants in periodontal therapy
.
J Periodontol
.
2000
;
71
:
1934
1942
.
2
Sanz
M.
Chapple
IL.
Working Group 4 of the VEWoP. Clinical research on peri-implant diseases: consensus report of Working Group 4
.
J Clin Periodontol
.
2012
;
39
(
suppl 12
):
202
206
.
3
American Academy of Periodontology Academy Statement
.
Peri-implant mucositis and peri-implantitis: a current understanding of their diagnoses and clinical implications
.
J Periodontol
.
2013
;
84
:
436
443
.
4
Heitz-Mayfield
LJ.
Lang
NP.
Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis
.
Periodontol 2000
.
2010
;
53
:
167
181
.
5
Salvi
GE.
Aglietta
M.
Eick
S.
Sculean
A.
Lang
NP.
Ramseier
CA.
Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans
.
Clin Oral Implants Res
.
2012
;
23
:
182
190
.
6
Karoussis
IK.
Salvi
GE.
Heitz-Mayfield
LJ.
Bragger
U.
Hammerle
CH.
Lang
NP.
Long-term implant prognosis in patients with and without a history of chronic periodontitis: a 10-year prospective cohort study of the ITI Dental Implant System
.
Clin Oral Implants Res
.
2003
;
14
:
329
339
.
7
Van der Weijden
GA.
van Bemmel
KM.
Renvert
S.
Implant therapy in partially edentulous, periodontally compromised patients: a review
.
J Clin Periodontol
.
2005
;
32
:
506
511
.
8
Klokkevold
PR.
Han
TJ.
How do smoking, diabetes, and periodontitis affect outcomes of implant treatment?
Int J Oral Maxillofac Implants
.
2007
;
22
(
suppl
):
173
202
.
9
Strietzel
FP.
Reichart
PA.
Kale
A.
Kulkarni
M.
Wegner
B.
Kuchler
I.
Smoking interferes with the prognosis of dental implant treatment: a systematic review and meta-analysis
.
J Clin Periodontol
.
2007
;
34
:
523
544
.
10
Wilson
TG
Jr.
The positive relationship between excess cement and peri-implant disease: a prospective clinical endoscopic study
.
J Periodontol
.
2009
;
80
:
1388
1392
.
11
Miyata
T.
Kobayashi
Y.
Araki
H.
Ohto
T.
Shin
K.
The influence of controlled occlusal overload on peri-implant tissue. Part 3: A histologic study in monkeys
.
Int J Oral Maxillofac Implants
.
2000
;
15
:
425
431
.
12
Monje
A.
Galindo-Moreno
P.
Canullo
L.
Greenwell
H.
Wang
HL.
Editorial: from early physiological marginal bone loss to peri-implant disease: on the unknown local contributing factors
.
Int J Periodontics Restorative Dent
.
2015
;
35
:
764
765
.
13
Bashutski
JD.
D'Silva
NJ.
Wang
HL.
Implant compression necrosis: current understanding and case report
.
J Periodontol
.
2009
;
80
:
700
704
.
14
Wilson
TG
Jr,
Valderrama
P.
Burbano
M.
et al.
Foreign bodies associated with peri-implantitis human biopsies
.
J Periodontol
.
2015
;
86
:
9
15
.
15
Salvi
GE.
Cosgarea
R.
Sculean
A.
Prevalence and mechanisms of peri-implant diseases
.
J Dent Res
.
2017
;
96
:
31
37
.
16
Fransson
C.
Lekholm
U.
Jemt
T.
Berglundh
T.
Prevalence of subjects with progressive bone loss at implants
.
Clin Oral Implants Res
.
2005
;
16
:
440
446
.
17
Roos-Jansaker
AM.
Lindahl
C.
Renvert
H.
Renvert
S.
Nine- to fourteen-year follow-up of implant treatment. Part II: presence of peri-implant lesions
.
J Clin Periodontol
.
2006
;
33
:
290
295
.
18
Koldsland
OC.
Scheie
AA.
Aass
AM.
Prevalence of peri-implantitis related to severity of the disease with different degrees of bone loss
.
J Periodontol
.
2010
;
81
:
231
238
.
19
Simonis
P.
Dufour
T.
Tenenbaum
H.
Long-term implant survival and success: a 10–16-year follow-up of non-submerged dental implants
.
Clin Oral Implants Res
.
2010
;
21
:
772
777
.
20
Atieh
MA.
Alsabeeha
NH.
Faggion
CM
Jr,
Duncan
WJ.
The frequency of peri-implant diseases: a systematic review and meta-analysis
.
J Periodontol
.
2013
;
84
:
1586
1598
.
21
Renvert
S.
Aghazadeh
A.
Hallstrom
H.
Persson
GR.
Factors related to peri-implantitis – a retrospective study
.
Clin Oral Implants Res
.
2014
;
25
:
522
529
.
22
Schuldt Filho G, Dalago HR, Oliveira de Souza JG, Stanley K, Jovanovic S, Bianchini MA
.
Prevalence of peri-implantitis in patients with implant-supported fixed prostheses
.
Quintessence Int
.
2014
;
45
:
861
868
.
23
Aguirre-Zorzano
LA.
Estefania-Fresco
R.
Telletxea
O.
Bravo
M.
Prevalence of peri-implant inflammatory disease in patients with a history of periodontal disease who receive supportive periodontal therapy
.
Clin Oral Implants Res
.
2015
;
26
:
1338
1344
.
24
Daubert
DM.
Weinstein
BF.
Bordin
S.
Leroux
BG.
Flemming
TF.
Prevalence and predictive factors for peri-implant disease and implant failure: a cross-sectional analysis
.
J Periodontol
.
2015
;
86
:
337
347
.
25
Konstantinidis
IK.
Kotsakis
GA.
Gerdes
S.
Walter
MH.
Cross-sectional study on the prevalence and risk indicators of peri-implant diseases
.
Eur J Oral Implantol
.
2015
;
8
:
75
88
.
26
Schwarz
F.
Becker
K.
Sahm
N.
Horstkemper
T.
Rousi
K.
Becker
J.
The prevalence of peri-implant diseases for two-piece implants with an internal tube-in-tube connection: a cross-sectional analysis of 512 implants
.
Clin Oral Implants Res
.
2017
;
28
:
24
28
.
27
Dalago
HR.
Schuldt Filho
G
,
Rodrigues
MA
,
Renvert
S
,
Bianchini
MA
.
Risk indicators for peri-implantitis. A cross-sectional study with 916 implants
.
Clin Oral Implants Res
.
2017
;
28
:
144
150
.
28
Derks
J.
Schaller
D.
Hakansson
J.
Wennstrom
JL.
Tomasi
C.
Berglundh
T.
Effectiveness of implant therapy analyzed in a Swedish population: prevalence of peri-implantitis
.
J Dent Res
.
2016
;
95
:
43
49
.
29
Rokn
A.
Aslroosta
H.
Akbari
S.
Najafi
H.
Zayeri
F.
Hashemi
K.
Prevalence of peri-implantitis in patients not participating in well-designed supportive periodontal treatments: a cross-sectional study
.
Clin Oral Implants Res
.
2017
;
28
:
314
319
.
30
Meijer
HJ.
Raghoebar
GM.
de Waal
YC.
Vissink
A.
Incidence of peri-implant mucositis and peri-implantitis in edentulous patients with an implant-retained mandibular overdenture during a 10-year follow-up period
.
J Clin Periodontol
.
2014
;
41
:
1178
1183
.
31
Ferreira
SD.
Silva
GL.
Cortelli
JR.
Costa
JE.
Costa
FO.
Prevalence and risk variables for peri-implant disease in Brazilian subjects
.
J Clin Periodontol
.
2006
;
33
:
929
935
.
32
Albrektsson
T.
Zarb
G.
Worthington
P.
Eriksson
AR.
The long-term efficacy of currently used dental implants: a review and proposed criteria of success
.
Int J Oral Maxillofac Implants
.
1986
;
1
:
11
25
.
33
Adell
R.
Lekholm
U.
Rockler
B.
Branemark
PI. A
15-year study of osseointegrated implants in the treatment of the edentulous jaw
.
Int J Oral Surg
.
1981
;
10
:
387
416
.
34
Schwartz-Arad
D.
Herzberg
R.
Levin
L.
Evaluation of long-term implant success
.
J Periodontol
.
2005
;
76
:
1623
1628
.
35
Hermann
JS.
Jones
AA.
Bakaeen
LG.
Buser
D.
Schoolfield
JD.
Cochran
DL.
Influence of a machined collar on crestal bone changes around titanium implants: a histometric study in the canine mandible
.
J Periodontol
.
2011
;
82
:
1329
1338
.
36
Lang
NP.
Berglundh
T.
Working Group 4 of the Seventh European Workshop on Periodontology. Periimplant diseases: where are we now? Consensus of the Seventh European Workshop on Periodontology
.
J Clin Periodontol
.
2011
;
38
(
suppl 11
):
178
181
.
37
Froum
SJ.
Rosen
PS.
A proposed classification for peri-implantitis
.
Int J Periodontics Restorative Dent
.
2012
;
32
:
533
540
.
38
Decker
AM.
Sheridan
R.
Lin
GH.
Sutthiboonyapan
P.
Carroll
W.
Wang
HL.
A prognosis system for periimplant diseases
.
Implant Dent
.
2015
;
24
:
416
421
.
39
Jeffcoat
MK.
Reddy
MS.
Advances in measurements of periodontal bone and attachment loss
.
Monogr Oral Sci
.
2000
;
17
:
56
72
.
40
Berglundh
T.
Lindhe
J.
Ericsson
I.
Marinello
CP.
Liljenberg
B.
Thomsen
P.
The soft tissue barrier at implants and teeth
.
Clin Oral Implants Res
.
1991
;
2
:
81
90
.
41
Schou
S.
Holmstrup
P.
Stoltze
K.
Hjorting-Hansen
E.
Fiehn
NE.
Skovgaard
LT.
Probing around implants and teeth with healthy or inflamed peri-implant mucosa/gingiva. A histologic comparison in cynomolgus monkeys (Macaca fascicularis)
.
Clin Oral Implants Res
.
2002
;
13
:
113
126
.
42
Huang
B.
Meng
H.
Piao
M.
Xu
L.
Zhang
L.
Zhu
W.
Influence of placement depth on bone remodeling around tapered internal connection implant: a clinical and radiographic study in dogs
.
J Periodontol
.
2012
;
83
:
1164
1171
.
43
Serino
G.
Turri
A.
Lang
NP.
Probing at implants with peri-implantitis and its relation to clinical peri-implant bone loss
.
Clin Oral Implants Res
.
2013
;
24
:
91
95
.
44
Lang
NP.
Joss
A.
Orsanic
T.
Gusberti
FA.
Siegrist
BE.
Bleeding on probing
.
A predictor for the progression of periodontal disease? J Clin Periodontol
.
1986
;
13
:
590
596
.
45
Lang
NP.
Adler
R.
Joss
A.
Nyman
S.
Absence of bleeding on probing. An indicator of periodontal stability
.
J Clin Periodontol
.
1990
;
17
:
714
721
.
46
Lang
NP.
Wilson
TG.
Corbet
EF.
Biological complications with dental implants: their prevention, diagnosis and treatment
.
Clin Oral Implants Res
.
2000
;
11
(
suppl 1
):
146
155
.
47
Gerber
JA.
Tan
WC.
Balmer
TE.
Salvi
GE.
Lang
NP.
Bleeding on probing and pocket probing depth in relation to probing pressure and mucosal health around oral implants
.
Clin Oral Implants Res
.
2009
;
20
:
75
78
.
48
Bragger
U.
Burgin
WB.
Hammerle
CH.
Lang
NP.
Associations between clinical parameters assessed around implants and teeth
.
Clin Oral Implants Res
.
1997
;
8
:
412
421
.
49
Karoussis
IK.
Muller
S.
Salvi
GE.
Heitz-Mayfield
LJ.
Bragger
U.
Lang
NP.
Association between periodontal and peri-implant conditions: a 10-year prospective study
.
Clin Oral Implants Res
.
2004
;
15
:
1
7
.
50
Kaldahl
WB.
Kalkwarf
KL.
Patil
KD.
Molvar
MP.
Relationship of gingival bleeding, gingival suppuration, and supragingival plaque to attachment loss
.
J Periodontol
.
1990
;
61
:
347
351
.