Diagnóstico Caso Salud, Mucositis, Periimplantitis

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Received: 3 October 2017 | Revised: 4 January 2018 | Accepted: 1 February 2018

DOI: 10.1111/jcpe.12956

2017 WORLD WORKSHOP

Peri‐implant health, peri‐implant mucositis, and peri‐implantitis:


Case definitions and diagnostic considerations

Stefan Renvert1,2,3 | G. Rutger Persson1,4 | Flavia Q. Pirih5 | Paulo M. Camargo5

1
School of Health and Society, Department
of Oral Health Sciences, Kristianstad Abstract
University, Kristianstad, Sweden The objective of this review is to identify case definitions and clinical criteria of peri‐
2
School of Dental Science, Trinity College,
implant healthy tissues, peri‐implant mucositis, and peri‐implantitis. The case defini‐
Dublin, Ireland
3 tions were constructed based on a review of the evidence applicable for diagnostic
Blekinge Institute of Technology,
Karlskrona, Sweden considerations. In summary, the diagnostic definition of peri‐implant health is based
4
Departments of Periodontics and Oral on the following criteria: 1) absence of peri‐implant signs of soft tissue inflammation
Medicine, School of Dentistry, University of
Washington, Seattle, WA, USA (redness, swelling, profuse bleeding on probing), and 2) the absence of further addi‐
5
School of Dentistry, Section of tional bone loss following initial healing. The diagnostic definition of peri‐implant mu‐
Periodontics, University of California, Los cositis is based on following criteria: 1) presence of peri‐implant signs of inflammation
Angeles, Los Angeles, CA, USA
(redness, swelling, line or drop of bleeding within 30 seconds following probing),
Correspondence combined with 2) no additional bone loss following initial healing. The clinical defini‐
Prof. Stefan Renvert, Department of Health
Sciences, Kristianstad University, 29188 tion of peri‐implantitis is based on following criteria: 1) presence of peri‐implant signs
Kristianstad, Sweden. of inflammation, 2) radiographic evidence of bone loss following initial healing, and 3)
Email: stefan.renvert@hkr.se
increasing probing depth as compared to probing depth values collected after place‐
The proceedings of the workshop were ment of the prosthetic reconstruction. In the absence of previous radiographs, radio‐
jointly and simultaneously published in
graphic bone level ≥3 mm in combination with BOP and probing depths ≥6 mm is
the Journal of Periodontology and Journal of
Clinical Periodontology. indicative of peri‐implantitis.

KEYWORDS
diagnosis, peri‐implant health, peri‐implant mucositis, peri‐implantitis

I NTRO D U C TI O N peri‐implant diseases. With such context in mind, the reader is to


be reminded that this manuscript focuses solely on biofilm‐induced
Osseointegrated dental implants have become an increasingly popu‐ inflammatory lesions around dental implants.
lar modality of treatment for the replacement of absent or lost teeth. Biological complications associated with dental implants are
Dental implants have high rates of long‐term survival (≥10 years) mostly inflammatory conditions of the soft tissues and bone sur‐
when used to support various types of dental prostheses. However, rounding implants and their restorative components, which are
the long‐term success of dental implants is not the same or as high induced by the accumulation of bacterial biofilm. Such conditions,
as their survival, as functional implants and their restorations may be which have been named peri‐implant mucositis and peri‐implantitis,
subject to mechanical and biological complications. 1 need to be clearly defined and differentiated from a state of peri‐im‐
It is recognized that there are also unusual peri‐implant prob‐ plant health, so that the clinician may assign a proper diagnosis and
lems (e.g., peri‐implant peripheral giant‐cell granuloma, pyogenic select a proper treatment modality in cases where disease is present.
granuloma, squamous cell carcinoma, metastatic carcinomas, malig‐ In a survey of registered specialists in periodontology in Australia
nant melanoma) or other conditions such as implant fractures that and the United Kingdom about the etiology, prevalence, diagno‐
may mimic or share certain clinical features with biofilm‐associated sis and management of peri‐implant mucositis and peri‐implantitis,

© 2018 American Academy of Periodontology and European Federation of Periodontology

S278 | wileyonlinelibrary.com/journal/jcpe J Clin Periodontol. 2018;45(Suppl 20):S278–S285.


RENVERT et al. | S279

there appears to be no consensus on treatment standards for the be ≤5.0 mm.4 It should also be noted that peri‐implant tissue health
management of peri‐implant diseases. 2 An American survey that can exist following treatment of peri‐implantitis with variable levels
examined the practitioners’ understanding of the etiology of peri‐ of bone support.
implant diseases and the management of peri‐implant mucositis and It has been proposed that the soft tissue cuff around implants
peri‐implantitis by periodontists in the United States revealed the exhibits less resistance to probing than the gingiva at adjacent teeth
absence of a standard therapeutic protocol to treat these condi‐ sites.8,9 This property of the implant mucosal seal may lead to me‐
tions and a significant variation in the empirical use of therapeutic chanically induced bleeding on probing on dental implants that are
modalities that result in moderately effective treatment outcome.3 clinically healthy.9 The clinical relevance of such phenomenon is
Accordingly, there is a need to establish applicable clinical guide‐ that the presence of a local bleeding dot may, therefore, represent
lines for the diagnosis of peri‐implant mucositis, and peri‐implantitis. a traumatic episode rather than a sign of biofilm‐induced inflamma‐
Additionally, there is a need to develop criteria for peri‐implant mu‐ tion. Such trauma‐induced bleeding on probing may not only be the
cositis and peri‐implantitis applicable in not only in for clinical prac‐ result of excessive probing forces, but can also be the consequence
tice but also for clinical and epidemiological research studies. of clinical difficulties in aiming the dental probe at the sulcus/pocket
The objective of this manuscript is to define peri‐implant health, around the implant, which can occur because of the implant‐res‐
peri‐implant mucositis and peri‐implantitis based on their clinical and toration spatial relationship and contours. It has been suggested
radiographic parameters. The case definitions herein described were that the absence of a periodontal ligament around implants and the
constructed based on a systematic review of the scientific evidence prosthetic design makes assessments of pocket probing depth mea‐
that currently correlates clinical and radiographic findings with the surements at dental implants difficult to perform and interpret.10
three diagnostic entities. The scientific evidence for peri‐implant Recognizing the above described issue, a modified bleeding index
health, peri‐implant mucositis and peri‐implantitis has been sum‐ has been proposed using a grading scale of the extent of bleeding
marized in other manuscripts in this volume.4‒6 The case definitions at dental implants,11 where a score of “0” represents healthy con‐
proposed in this paper are intended to apply to situations in which ditions, and a score of “1” representing an isolated dot of bleeding.
there are reasons to believe that the presence of biofilm on implant
surfaces is the main etiological factor associated with the devel‐
What clinical and radiographic findings and what
opment of peri‐implant mucositis and peri‐implantitis. It is obvious
clinical examination steps are necessary to detect the
from previous manuscripts in this volume that there are major pa‐
presence of peri‐implant health?
tient‐specific differences in inflammatory responses to the microbial
challenge of bacterial communities that reside on implants and its
restorations.5,6 1. Clinical evaluation of the soft tissue conditions around implants
should include registration of oral hygiene in general, with
specific focus on the presence of biofilm on implants and their
PE R I ‐ I M PL A NT H E A LTH restorations;
2. Dental implants should be visually evaluated and probed routinely
While peri‐implant health shares many common clinical features and periodically (at least once per year) as part of comprehensive
with periodontal health around natural teeth, it is clear that there are oral exams, similar to natural teeth;
major structural differences between the two scenarios, particularly 3. Pocket probing on dental implants should be conducted with a
with respect to their relationship with surrounding tissues and bio‐ light force (approximately 0.25 N); peri‐implant pocket depths
4
logical attachment. The review by Araujo and Lindhe describes the should in general be ≤5 mm;
different anatomical and histological characteristics associated with 4. Bleeding on probing should not occur at implant sites defined as
the soft and hard tissues around natural teeth and dental implants being healthy. Bleeding on probing should be assessed carefully
and the authors further described how such differences may be re‐ using light forces (0.25 N) to avoid possible effects of trauma
sponsible for the distinct biological mechanisms involved in host re‐ caused by the process. It is difficult to differentiate between bio‐
sponse and tissue homeostasis observed between the two entities. film‐induced peri‐implant inflammation and mechanically‐induced
Araujo and Lindhe 4 also concluded that peri‐implant health re‐ trauma; bleeding “dots” should be interpreted carefully as this
quires the absence of clinical signs of inflammation (i.e. erythema may represent bleeding due to tissue trauma and not bleeding as‐
and swelling) including no bleeding on probing. This determination sociated with tissue inflammation;
is true to evidence from the periodontal literature that the absence 5. Intra‐oral radiographic evaluation of changes in bone levels
of bleeding on probing is consistent with periodontal health.4,7 In around implants (preferably using a standardized film holder) is
clinical health, the peri‐implant mucosa forms a tight seal around the necessary to discriminate between health and disease states. A
trans‐mucosal component of the implant itself, the abutment or the prerequisite for the radiographic evaluation should be an image
restoration. The height of the soft tissue around the implant follow‐ taken at baseline (supra‐structure in place) that clearly allows for
ing placement influences the initial probing depth. In general, how‐ identification of an implant reference point and distinct visualiza‐
ever, the probing depth associated with peri‐implant health should tion of implant threads, for future reference as well as assessment
S280 | RENVERT et al.

of mesial and distal bone levels in relation to such reference The conversion from an inflammatory process identified as peri‐
points; and implant mucositis (without evidence of bone loss) to peri‐implantitis
6. Absence of bone loss beyond bone level changes resulting from (with bone loss) remains an enigma. It is, however, generally agreed
initial bone remodeling. Alveolar bone remodeling following the that both peri‐implant mucositis and peri‐implantitis have an infec‐
first year in function may be dependent on the type and position tious etiology through the development of biofilm composed of a
of the implant, but change (loss) of alveolar bone starting after the plethora of bacteria with known pathogenicity. 21‒24
12‒14
implant was placed in function should not exceed 2 mm.
Changes ≥2 mm at any time point during or after the first year
should be considered as pathologic. PE R I ‐ I M PL A NT M U COS ITI S

Case definitions of peri‐implant mucositis were identified in 22 out


of 33 articles listed in Table 1. Bleeding on probing without any other
Peri‐implant health: Case definitions for day‐to‐day
criteria was identified in three out of 22 articles. Bleeding on probing
clinical practice
combined with no radiographic evidence of bone level changes could
The diagnosis of peri‐implant health requires: be identified in seven out of 22 articles as the definition of peri‐
implant mucositis. Three of these articles accounted for remodeling
1. Visual inspection demonstrating the absence of peri‐implant of the marginal alveolar bone adjacent to the implant as a result of
signs of inflammation: pink as opposed to red, no swelling as the surgical procedure. The remaining reports also included probing
opposed to swollen tissues, firm as opposed to soft tissue pocket depths and/or bone loss assessments. In addition to bleed‐
consistency; ing on probing, one study allowed up to 3 mm of bone loss from the
2. Lack of profuse (line or drop) bleeding on probing; implant platform to define peri‐implant mucositis. 25
3. Probing pocket depths could differ depending on the height of the The diagnosis of peri‐implant mucositis should be based on clin‐
soft tissue at the implant location. An increase in probing depth ical signs of inflammatory disease. In routine clinical examinations,
over time, however, conflicts with peri‐implant health; and signs of inflammation should be screened for. In addition, radio‐
4. Absence of further bone loss following initial healing, which graphic images should be evaluated to exclude bone level changes
should not be ≥2 mm. consistent with the definition of peri‐implantitis, as described later
in the manuscript.

What clinical and radiographic findings and what


PE R I ‐ I M PL A NT D I S E A S E S
clinical examination steps are necessary to detect the
presence of peri‐implant mucositis?
The scientific literature has provided the evidence to define the di‐
agnosis of peri‐implant conditions and diseases, and the reviews by
Heitz‐Mayfield and Salvi,5 and Schwarz et al.6 were used as the basis 1. Visually, local swelling, redness, and shininess of the soft tissue
for the present report. In addition, two recent systematic reviews re‐ surface are classical signs of clinical inflammation. A common
porting on the prevalence of peri‐implant mucositis and peri‐implan‐ symptom reported by patients is soreness;
titis were also evaluated.15,16 Through these reports, we identified 2. A local dot of bleeding resulting from probing may be the result of
33 articles defining clinical and radiographic criteria for the diagnosis a traumatic (probing) injury that should not be considered, in the
of peri‐implant mucositis and peri‐implantitis (Table 1). absence of other inflammatory changes, a definitive criterion to
The American Academy of Periodontology has defined peri‐im‐ characterize a peri‐implant soft tissue lesion;
plant mucositis as a disease that includes inflammation of the soft 3. Any bleeding on probing that is combined with visual inflamma‐
tissues surrounding a dental implant, without additional bone loss tory changes of the tissues at the site of probing;
after the initial bone remodeling that may occur during healing fol‐ 4. Clear evidence of bleeding such as a line of bleeding or drop
lowing the surgical placement of the implant.17 The etiology of peri‐ bleeding should be used as an indication of an inflammatory peri‐
implant mucositis is the accumulation of a bacterial biofilm around implant soft tissue lesion;
5
the implant. 5. Suppuration upon clinical examination (e.g., application of light
Peri‐implantitis has been defined as an inflammatory lesion of pressure to the tissues or following probing); and
the mucosa surrounding an endosseous implant and with progres‐ 6. Intra‐oral radiographic evaluation of bone levels around implants
sive loss of supporting peri‐implant bone.6,17‒20 It is generally per‐ should always be included in the presence of clinical signs of in‐
ceived that following implant installation and initial loading, some flammation. In addition, a pre‐requisite for the evaluation is that a
crestal bone height is lost (between 0.5 and 2 mm) in the healing radiograph be taken at baseline (supra‐structure in place) and
process.12,13 Any additional radiographic evidence of bone loss sug‐ used for future assessment of mesial and distal bone levels in re‐
gests peri‐implant disease. lation to defined references. Accounting for the remodeling
RENVERT et al. | S281

TA B L E 1 Criteria used for the case definitions of peri‐implantitis and peri‐implant mucositis from studies selected in the review

Case definition of peri‐implant


Study Case definition of peri‐implantitis mucositis

Fransson et al. (2005)29 Bone level change > 3 threads after first year in function ND
Roos‐Jansåker et al. (2006)31 Bone level change > 1.8 mm after first year in function + BOP + PD > 4 mm + no bone loss after
BOP first year on function
Ferreira et al. (2006) 32 PD > 5 mm + BOP and/or suppuration (SUP) BOP
33
Gatti et al. (2008) Bone level change > 2 mm from last radiographic assessment ND
+ Pus/ BOP + PD > 5 mm
Maximo et al. (2008)34 Bone level change ≥3 threads + BOP and/or SUP + PD ≥5 BOP + absence of radiographic bone
mm loss and no SUP
Koldsland et al. (2010)35 Bone level change ≥2 mm from platform + BOP + PD ≥4 mm BOP + no bone loss from platform
35
Koldsland et al. (2010) Bone level change ≥2 mm from platform + BOP + PD ≥6 mm BOP + no bone loss from platform
Koldsland et al. (2010)35 Bone level change ≥3 mm from platform + BOP + PD ≥4 mm BOP + no bone loss from platform
35
Koldsland et al. (2010) Bone level change ≥3 mm from platform + BOP + PD ≥6 mm BOP + no bone loss from platform
Simonis et al. (2010)36 Bone level change > 2.5 mm (or ≥3 threads) from platform + ND
BOP and/or SUP + PD ≥5 mm
Wahlström et al. (2010)37 Bone level change > 2 mm after first year in function + BOP BOP + PD < 4 mm + no bone loss after
and/or SUP + PD ≥4 mm first year on function
Zetterqvist et al. (2010)38 Bone level change > 5 mm from the platform + BOP/SUP + ND
PD > 5mm
Pjetursson et al. (2012)39 Bone level change ≥2 mm after bone remodeling equals Level 1: BOP + PD > 5 mm
marginal bone levels of ≥5 mm below the implant shoulder Level 2: BOP + PD > 6 mm
Mir‐Mari et al (2012) 40 Bone level change > 2 threads from platform + BOP and or BOP + bone level change < two threads
suppuration from platform
Swierkot et al. (2012) 41 Bone level change > 0.2 mm annually after first year in BOP + PD > 5 mm + no bone level
function, + PD ≥5 mm with or without BOP change
Fardal and Grytten (2013) 42 Bone level change > 3 threads after bone remodeling + BOP ND
or suppuration
Marrone et al. (2013) 43 Bone level change > 2 mm from the platform + BOP + BOP + bone level change ≤2 mm from
PD > 5 mm platform. PPD ≤5 mm
Cecchinato et al. (2014) 44 Progressive bone loss > 0.5 mm +BOP + PD ≥4 mm BOP
45
Martens et al. (2014) Bone level change > 2 mm from the platform + PD > 4 mm ND
Meijer et al. (2014) 46 Bone level change ≥2 mm from the platform + BOP BOP + bone level change < 2 mm from
platform
Passoni et al. (2014) 47 Bone level change > 2 + BOP and/or SUP + PD ≥ 5 mm BOP + no bone level change
48
Renvert et al. (2014) Bone level change ≥2 mm from the platform + PD ≥ 4 mm + BOP + bone level change < 2 mm from
BOP and or suppuration platform
Aguirre‐Zorzano et al. (2015) 49 Bone level change > 1.5 mm after 6 months in function + BOP + no bone loss
often associated with suppuration, increased probing depth
and bleeding on probing
Canullo et al. (2015)50 Bone level change > 3 mm following implant integration ND
Daubert et al. (2015)51 Bone level change > 2 mm after remodeling + BOP and or BOP and/or gingival inflammation + no
SUP + PD ≥4 mm bone level change after remodeling
Ferreira et al. (2015)52 Bone level change > 2 mm after remodeling + BOP and/or + BOP and no bone loss
PD ≥4 mm
Frisch et al. (2015)53 Bone level change ≥2 mm after remodeling + BOP +PD ≥5 BOP
mm
Konstantinidis et al. (2015)54 Bone level change > 2 mm from the platform (at tissue level BOP
implants > 2 mm from the polished collar+ BOP + PD > 4
mm
Rinke et al. (2015)55 Bone level change ≥ 3.5 mm from platform ND

(Continues)
S282 | RENVERT et al.

TA B L E 1 (Continued)

Case definition of peri‐implant


Study Case definition of peri‐implantitis mucositis

Papantonopoulos et al. (2015)56 Bone level change ≥3 mm from platform + BOP and/or SUP ND
+PD ≥5 mm
Trullenque‐Eriksson et al. (2015)25 Bone level change ≥3 mm from the platform + BOP and/or BOP + bone level change < 3 mm from
SUP + PD ≥ 5 mm platform level
van Velzen et al. (2015)57 Bone level change > 1.5 mm after first year in function + ND
BOP
Derks et al. (2016)1 Bone loss > 0.5 mm after up to 24 months + BOP/ BOP + no bone loss
suppuration.
In addition, bone level change > 2 mm + BOP was consid‐
ered moderate/severe peri‐implantitis
Dalago et al. (2017)58 Bone level change > 2 mm from abutment installation + ND
PD > 5 mm + BOP/SUP
Rokn et al. (2017)59 Bone level change > 2 mm from platform level + BOP and/or BOP and/or SUP + bone level change ≤2
SUP mm from platform level
Tenenbaum et al. (2017)60 Bone level change > 4.5 mm from platform + BOP + PD ≥5 BOP + no bone level change from
mm platform

BOP = bleeding on probing, PD = probing depth, SUP = suppuration, ND = not defined.

process of alveolar bone during the first year after installation, – as assessed from radiographs – was a necessary criterion for the
the change in bone level since the placement of the prosthetic diagnosis of peri‐implantitis in 13 reports.
supra‐structure should not be > 2.0 mm. Presence of bone loss Without accounting for the initial (remodeling‐associated) bone
beyond crestal bone level changes resulting from the intial re‐ loss, the remaining articles identified bone loss using the implant
modeling process of alveolar bone after implant installation sug‐ platform level as reference. Bone loss requirements varied between
gests either progressive peri‐implant infection, or other local 1.8 to 4.5 mm to diagnose the implant as having peri‐implantitis.
factors such as excess cement and looseness/fracture of implant Different cut‐off levels for probing pocket depth around implants
components. were also required in 20 of the articles to define a diagnosis of peri‐
implantitis. It is clear from the data summarized in Table 1 that there
is a large variation in the requirements to define a case as having
either peri‐implant mucositis or peri‐implantitis. Such variation
Peri‐implant mucositis: Case definitions for day‐to‐
in the application of individual clinical judgement is confirmed by
day clinical practice
Ramanauskaite et al. 26 who concluded that there is currently no sin‐
The diagnosis of peri‐implant mucositis requires: gle uniform definition of peri‐implantitis, or parameters that could be
used to define peri‐implant disease entities.
1. Visual inspection demonstrating the presence of peri‐implant Understanding the wide heterogeneity in defining peri‐implanti‐
signs of inflammation: red as opposed to pink, swollen tissues tis, the most uniform consensus in characterizing peri‐implantitis is
as opposed to no swelling, soft as opposed to firm tissue as follows; 1) peri–implantitis lesions present with the same clinical
consistency; signs of inflammation as peri‐implant mucositis and 2) the distinc‐
2. Presence of profuse (line or drop) bleeding and/or suppuration on tive difference between a diagnosis of peri‐implant mucositis and
probing; peri‐implantitis is the presence of bone loss in peri‐implantitis, as
3. An increase in probing depths compared to baseline; and identified from dental radiographs.6
4. Absence of bone loss beyond crestal bone level changes resulting During the last 10 to 15 years, there has been a general agreement
from the intial remodeling. that following the first year in function, bone loss around dental im‐
plants ≥2 mm represents peri‐implantitis.14,27,28 Recent data suggest
that the pattern of bone loss in general is not linear.1,29 Typically, the
development of peri‐implantitis appears within the first few years
PE R I ‐ I M PL A NTITI S after which the implant is in function. This suggests that it is im‐
portant to carefully monitor changes that may occur around dental
To assign a diagnosis of peri‐implantitis, most reports listed in Table 1 implants in the early post‐restorative phase, with focus on bleeding
(30 out of 33) require bleeding on probing in addition to bone loss. on probing/suppuration and in combination with radiographic evi‐
Following the initial healing, additional bone loss 0.5 mm to 5 mm dence of bone loss. From the clinical perspective, it is important to
RENVERT et al. | S283

recognize that there is no predictable model or algorithm to predict 4. In the absence of initial radiographs and probing depths, radio‐
the progression of peri‐implantitis based on diagnostic methodolo‐ graphic evidence of bone level ≥3 mm and/or probing depths ≥6
gies currently available in daily practice. mm in conjunction with profuse bleeding represents
Furthermore, experiences from the knowledge about the pro‐ peri‐implantitis.
gression of periodontitis can only be extrapolated to peri‐implan‐
titis with extreme care. For decades, it has been recognized that For day to day clinical practice it may be valuable to assess the
the progression of periodontitis is unpredictable, as lesions alter‐ yearly rate of bone loss. This can be calculated if it is known when the
nate phases of dormancy and bursts of disease activity, which may implant was placed in function.
be slow or rapid. 30 Based on this knowledge and in attempting to
extrapolate it to peri‐implantitis, any bone loss greater than the
measurement error (≥2 times its standard deviation) or approxi‐ C R ITE R I A TO B E U S E D I N E PI D E M I O LO G I C
mately 2 mm is indicative of peri‐implantitis. 28 (S U RV E I LL A N C E ) S T U D I E S

The same criteria used to define peri‐implant health and peri‐implant


What clinical and radiographic findings and what
mucositis in day‐to‐day practice should be applied in epidemiological
clinical examination steps are necessary to detect the
studies. In epidemiological studies, radiographic and clinical infor‐
presence of peri‐implantitis?
mation from the time point when the supra‐structure was placed
may not be available. Under such circumstances a distance from
1. The visual inspection with assessment of the presence of clas‐ the implant platform to bone contact ≥3 mm, and in conjunction
sical signs and symptoms of inflammation, i.e. redness, swelling, with bleeding on probing would be required for the diagnosis of
pain, and bleeding on probing (characteristics of the latter, peri‐implantitis.
described for peri‐implant mucositis, also apply to the diagnosis
of peri‐implantitis);
AC K N OW L E D G M E N T S A N D D I S C LO S U R E S
2. The differential diagnosis between peri‐implant mucositis and
peri‐implantitis is based on evidence that alveolar bone loss This paper was self‐funded by the authors and their institutions. The
following initial healing and bone remodeling has occurred authors report no conflicts of interest related to this case definition
and requires a radiographic evaluation of the bone level paper.
around dental implants over time. This is in addition to the
presence of inflammatory changes and bleeding on probing on
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