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CLINICAL

A Cross-Sectional Analysis on Factors Associated With Peri-


Implant Pathologies at the Implant Level
Bruno César de Vasconcelos Gurgel*
Salomão Israel Monteiro Lourenço Queiroz*
Sheyla Christinne Lira Montenegro
Patrı́cia dos Santos Calderon
Kenio Costa Lima

Pathologies in peri-implant tissues are common and may disturb long-term implant supported rehabilitation. We aimed to evaluate the

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occurrence of such peri-implant diseases and their associated factors in this study. Peri-implantitis and mucositis were diagnosed based
on clinical and radiological findings. Statistical analysis was performed with the X2 and logistic regression. Peri-implant mucositis and
peri-implantitis were observed in 43.4% and 13.8% of patients with implants evaluated, respectively. Univariate analysis found
associations with systemic changes (P ¼ .016; yes), medication use (P ¼ .010; yes), implant location (P , .0001; upper jaw), implant region
(P ¼ .008; posterior), previous augmentation procedure (P ¼ .023; yes), time of prostheses use (P , .0001; .2 years), keratinized mucosa
(P , .0001; absence); and gingival bleeding index (P ¼ .005; .30%). In the multiple analysis, independent predictors were: .2 years of
prostheses use (P , .0001; PR ¼ 1.720), upper jaw location (P , .0001; PR ¼ 1.421), gingival bleeding index .30% (P ¼ .001; PR ¼ 1.496),
and use of medication (P , .0001; PR ¼ 1.261). The frequency of peri-implant pathologies is high (approximately 57.2%) with several
aspects of the occurrence being related to the patients’ prosthesis. Prostheses type and the complexity of rehabilitation are worth
highlighting. Factors include the location of the dental implant, gingival bleeding index, patient’s use of medication(s), and the time of
prostheses use.

Key Words: risk factors, peri-implantitis, peri-implant mucositis

INTRODUCTION and local factors that contribute to peri-implant pathologies, to


provide robust scientific evidence regarding disease etiology.12

D
ental implants have become a good strategy for
Studies of the possible impacts of systemic and local factors
replacing missing teeth in patients. However, bio- on the occurrence of peri-implant pathologies are important to
logical complications such as peri-implantitis and optimize the long-term prognosis of dental implant treatment.
peri-implant mucositis are more frequent during the Therefore, this study aimed to investigate the occurrence of
late stages of implant rehabilitation, potentially leading to peri-implant pathologies in dental implants, as well as possible
implant failure.1,2 Several reports indicate that these patholo- factors associated.
gies are a common finding in such patients.3–6 The occurrence
of peri-implantitis varies between 8.9% and 56% in subjects
and/or dental implants while mucositis presents a frequency of METHODS
43% to 80%.3–7 Divergences regarding this prevalence may be This cross-sectional study (STROBE checklist was used; STROBE
due to a number of factors, including the diagnostic criteria stands for an international, collaborative initiative of epidemi-
employed and the characteristics of the population evaluated. ologists, methodologists, statisticians, researchers, and journal
In addition to the dental biofilm, some factors have been editors involved in the conduct and dissemination of observa-
associated with the onset and progression of peri-implant tional studies, with the common aim of STrengthening the
pathologies.3,6,8,9 Periodontal disease, smoking, lack of sup- Reporting of OBservational studies in Epidemiology; Supple-
ment 1) was previously approved by the Research Ethics
portive periodontal therapy, diabetes, the type of rehabilitation,
Committee of the Federal University of Rio Grande do Norte,
and parafunctional habits can all affect the incidence of peri-
Brazil (protocol: 186/10-P). The patients were selected in the
implant disease.1,7,10,11 Nevertheless, additional epidemiologi- period from 2000 to 2011.
cal and clinical studies are required to investigate the biological
Exclusion and inclusion criteria
Department of Dentistry, Federal University of Rio Grande do Norte, Patients undergoing periodontal therapy or on antibiotic
Natal, Brazil.
therapy during the 2 months prior to the clinical examination
* C orresponding a utho r, e- mail: bcgurgel@yaho o.com .br and
salomaoisrael10@gmail.com were excluded. Individuals that had received implant prosthe-
https://doi.org/10.1563/aaid-joi-D-19-00233 ses during the last 6 months were included.

Journal of Oral Implantology 223


Factors Associated with Peri-Implant Pathologies

Radiographic and clinical evaluation maximum: 88 years). Systemic changes were reported for
34.2% (n ¼ 53) of patients and dry mouth feeling for 17.4% (n ¼
The medical and dental histories of all patients were updated 27). Smokers totaled 12.9% (n ¼ 20) of patients and 36.1% (n ¼
upon inclusion in the study. Parameters were recorded as 56) drank alcoholic drinks. Table 1 presents the descriptive
follows: Probing depth (PD) measured in mm at 6 sites per analysis of data.
implant and teeth; full-mouth visible plaque index (VPI);13 full The teeth count in the mouth ranged from zero to 31 and
gingival bleeding index (GBI);13 bleeding on probing (BOP), the highest amount of implants per patient was 11. The mean
described as presence (1) or absence (0) at 6 sites per teeth and full-mouth VPI was 48.83% (626.60) and the mean GBI was 8%
implants; presence of suppuration (S), described as presence (1) (613.71). The average time of prosthesis use was 47.42 months
or absence (0); keratinized mucosa (KM), described as presence (626.45; minimum: 6; maximum: 120 months) (see Table 1).
(1) or absence (0). The bleeding and plaque score indexes were Periodontitis was observed in 50% of patients, gingivitis
divided into 2 categories as follows: 0–30% and .30%. A was detected in 43% and 7% presented healthy tissues. Five
professional performed all clinical examinations using a WHO hundred and twenty-five implants were evaluated, of these
(World Health Organization) periodontal probe (PD: ICC [intra- 56.6% (n ¼ 296) presented peri-implant pathology and 43.4%
class correlation coefficient] ¼ 0.89 and KM: ICC ¼ 1.00) and a were healthy (n ¼ 227); diagnoses, according to the amount of

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conventional millimeter periodontal probe (PCP-UNC 15; Hu- implants, are presented in Table 1. Associations between the
Friedy). dependent variable, ‘‘peri-implant pathology,’’ and demograph-
Periapical radiograph was used for the evaluation of the ic independent variables also related to dental implants are
implants (paralleling and positioners). The height of the bone presented in Table 2. Associations between the dependent
was evaluated (length of exposed implant threads). Character- variable and prosthetic variables are presented in Table 3, and
istics established by the American Academy of Periodontolo- associations between the dependent variable and clinical
gy14 were used to classify periodontal disease. Bleeding on variables are shown in Table 4.
probing was present with no attachment loss for gingivitis. The univariate analysis showed that variables, such as use
Probing pocket depth was .4 mm, the clinical attachment level of medications (yes), systemic alterations (yes), time of
was 3 mm and bleeding on probing classified periodontitis. prosthesis use (.2 years), location of the implant (upper jaw),
The references for peri-implant diagnosis were based on region (posterior), accomplishment of previous reconstructive
those of a study by Mombelli et al15 Bleeding on probing and/ surgery (such as augmentation procedure) (yes), GBI (.30%),
or gingival and/or suppuration, with no radiographic bone loss and keratinized mucosa (absence) were associated more with
were employed to diagnose mucositis, while PD  5 mm and/ the occurrence of peri-implant pathologies (Tables 2 and 4).
or suppuration, and radiographically visible bone loss were The binary logistic regression indicated that the predictive
used to identify peri-implantitis. Estimating a real proportion of variables of peri-implant pathology; GBI of .30%, .2 years of
0.4 and a ratio of the null hypothesis of 0.6 and significance prostheses use, upper jaw location, and use of medications
level of 0.05, this sample presented a power of 99.99%. were independent factors that were associated with peri-
implant pathology, when adjusted by augmentation procedure
Statistical analysis and sex (Table 5).

Data were statistically analyzed using the SPSS software (SPSS


Inc), and the implant was used as a statistical unit. All statistics, DISCUSSION
as well as all results and conclusions, were reviewed by a
person with experience in the field. Recent reports have shown frequencies of peri-implantitis and
To verify significant associations, the chi-square test was mucositis of 43.2%7 and 45.6% in patients with implants.16 A
used. Associations with a value of P , .20 were selected for meta-analysis by Lee et al (2017)17 found a mean prevalence of
multiple logistic regression analysis (hierarchical method), implant-based peri-implantitis of 9.25% (95% confidence
which allows us to estimate a probability associated with the interval [CI]: 7.57–0.93) and a mean implant-based mucositis
occurrence of a given event in a set of explanatory variables. prevalence of 29.48% (CI: 22.65–36.32). These pathologies are
This method was used to insert variables in the model even present in elevated frequencies and associated with the lack of
when no statistically significant differences were detected a regular maintenance.
(dependent on the model adaptation capacity, according to the The variability in the reports of peri-implantitis may be
Hosmer and Lemeshow model). To measure the effect of explained by the fact that different clinical parameters are used
multiple analysis, the adjusted odds ratio was transformed into to evaluate and define this pathology; furthermore, the lack of
the adjusted prevalence ratio, with the objective of avoiding standardization of these parameters makes comparisons
overestimation of the effect. The level of significance estab- among reports difficult.18 Despite recent publications classify-
lished for all statistical tests was 5%. ing periodontal and peri-implant pathologies and condi-
tions,7,19,20 the standardization of these clinical parameters,
especially when peri-implantitis is evaluated, is still controver-
sial, as variations in the depth of probing may not be confirmed
RESULTS
by radiographic examination. It should also be noted that some
A total 523 implants and 2,718 teeth were evaluated; 79.4% (n ¼ implant platforms undergo a physiological process of bone loss
123) of the subjects were women and the average age of that does not necessarily constitute disease.
patients was 54.05 years (612.61; minimum: 18 years; Plaque control is indispensable, as peri-implant pathologies

224 Vol. XLVII / No. Three / 2021


de Vasconcelos Gurgel et al

are of infectious origin.21,22 However, the contribution of


TABLE 1
plaque accumulation to the increased risk of peri-implant
Descriptive analysis and categorization of the variables of pathologies is not clear. A VPI . 30% was categorized in this
interest relevant to the study* study with the purpose of considering generalized and
Variables Categories n % localized poor plaque control. Despite the failure to demon-
Age 18–50 118 22.6 strate a clear association between the presence of full-mouth
51 405 77.4 plaque (P ¼ .298; VPI) and peri-implant pathologies, in increased
Sex Female 396 75.7 risk of susceptibility, other studies have made similar assess-
Male 127 24.3 ments, where VPI . 25% presented an association with peri-
Drugs No 250 47.8
implant pathology.2,7
Yes 273 52.2
Systemic changes No 282 53.9 Furthermore, statistically significant differences in terms of
Yes 241 46.1 a higher percentage of GBI (P ¼ .005) may justify this parameter
Alcoholic No 364 69.6 as a predictive variable for the occurrence of peri-implant
Yes 159 30.4 pathology, as a GBI of greater than 30% was observed (PR ¼
Smoker No 439 83.9
1.496). Some studies have pointed out a positive correlation

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Yes 84 16.1
Dry mouth No 448 85.7 between high plaque scores and an increased risk of presenting
Yes 75 14.3 peri-implant pathology.17,23 Therefore, the primary role of
Augmentation procedure No 452 86.4 plaque was highlighted as a dose-dependent association
Yes 71 13.6 between higher plaque scores and worse conditions in peri-
Periodontal diagnosis Health 28 5.4
implant pathologies.3 Gingival bleeding may reflect the
Periodontal disease 389 74.4
NA 106 20.3 represent of biofilm accumulation on the implants reinforces
Peri-implant diagnosis Health 227 43.4 the role of this factor of risk.11
Peri-implant pathology 296 56.6 Whereas changes in volume, such as edema, and color of
GBI 0–30% 477 91.2 marginal peri-implant tissues were considered as signs of
30% 46 8.8
diseases.18,24 The absence of keratinized tissue, or the presence
VPI 0–30% 111 21.2
30% 412 78.8 of scar tissue from previous surgeries, may influence the dental
Number of teeth 17–31 282 53.9 researcher at the time of quantifying the degree of inflamma-
0–16 241 46.1 tion by visual criteria. The inability to reproduce these indices
Number of implants 1–2 105 20.1 has been cited in some other studies.18,25,26
.3 418 79.9
The keratinized mucosa has been identified as a protective
Implant region Posterior 314 60.0
Anterior 209 40.0 factor against the incidence of peri-implant pathologies, and
Implant location Lower jaw 287 54.9 grafting procedures for keratinized mucosa gain are an
Upper jaw 236 45.1 important factor for reducing indices such as bleeding and
Keratinized tissue No 392 75.0 maintenance of bone tissue.27 More recent studies have
Yes 131 25.0
reported that the absence of keratinized mucosa may hamper
Range of keratinized mucosa 0–2 mm 221 42.3
.2 mm 302 57.7 oral hygiene procedures and have shown limited evidence of
Presence of papilla No 300 57.4 the association of this characteristic with peri-implant pathol-
Yes 200 38.2 ogies.7,20 The univariate analysis used in this study showed that
NI 23 4.4 the absence of keratinized mucosa was associated more with
Time of the prosthesis 6–24 156 29.8
the incidence of peri-implant pathologies; however, in the
.24 321 61.4
NI 46 8.8 multivariate analysis, this variable strength was lost within the
Situation of the prosthesis Provisional 39 7.5 context of this study.
Permanent 484 92.5 Other possible factors associated with peri-implant pathol-
Type of prosthesis Unitary 197 37.7 ogies have been reported; this study observed more events in
Removable full 96 18.4
men, but this difference was not statistically significant, as also
Protocol 69 13.2
Multiple partial 161 30.8
observed by other studies.3,6,7,10,28,29 Women display better oral
Adaptation failed No 441 84.3 hygiene, which can improve health30 and may explain the
Yes 82 15.7 higher prevalence of disease in males in this study. It should be
Prosthesis material Metal-ceramic 319 61.0 noted that patients in this study presented with a history of
Resin 204 39.0 periodontal disease and, therefore, this limitation may not have
Type of attachment Screwed 118 22.6
Cemented 309 59.1
the power to correlate the associated factors investigated or
NI 96 18.4 correctly evaluate the effect and cause relationship.
Occlusion type Normal 356 68.1 Systemic changes that could influence peri-implant health
Malocclusion 157 30.0 (osteoporosis, immunocompromised patients, diabetes, cardio-
NI 10 1.9 vascular disorders, and hormonal disorders) were also evaluat-
*GBI indicates gingival bleeding index; NA, not applicable; NI, not ed in this study and were found to be associated more with
informed; VPI, visible plate index. peri-implant pathologies (P ¼ .016), as well as the use of
medications. As these two variables compete between
themselves, the use of medications was chosen for application

Journal of Oral Implantology 225


Factors Associated with Peri-Implant Pathologies

TABLE 2
Univariate analysis between the dependent variable, ‘‘peri-implant pathology,’’ and demographic independent variables also
related to dental implants*
Peri-Implant Pathology

Variables Categories No (%) Yes (%) P PR CI (95%)


Age (years) 18–50 50 (42.4%) 68 (57.6%) .797 0.970 0.764–1.230
51 177 (43.7%) 228 (56.3%)
Sex Female 53 (41.7%) 74 (58.3%) .662 1.053 0.833–1.330
Male 174 (43.9%) 222 (56.1%)
Drugs No 123 (90.1%) 127 (9.9%) .010* 1.292 1.061–1.572
Yes 104 (38.1%) 169 (61.9%)
Systemic changes No 136 (48.2%) 146 (51.8%) .016* 1.277 1.043–1.563
Yes 91 (37.8%) 150 (62.2%)
Alcoholic No 164 (45.1%) 200 (54.9%) .249 1.137 0.910–1.421
Yes 63 (39.6%) 96 (60.4%)

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Smoker No 190 (43.3%) 249 (56.7%) .897 0.983 0.755–1.279
Yes 37 (44.0%) 47 (56.0%)
Dry mouth No 198 (44.2%) 250 (55.8%) .371 1.143 0.844–1.548
Yes 29 (38.7%) 46 (61.3%)
Number of teeth 17–31 129 (45.7%) 153 (54.3%) .243 1.125 0.922–1.372
0–16 98 (40.7%) 143 (59.3%)
Number of implants 0–2 42 (40.0%) 63 (60.0%) .431 0.904 0.698–1.170
.2 185 (44.3%) 233 (55.7%)
Implant location Lower jaw 153 (53.3%) 134 (46.7%) ,.0001* 1.700 1.368–2.113
Upper jaw 74 (31.4%) 162 (68.6%)
Implant region Anterior 151 (48.1%) 163 (51.9%) .008* 1.322 1.069–1.636
Posterior 76 (36.4%) 133 (63.6%)
Augmentation procedure No 205 (45.4%) 247 (54.6%) .023* 1.464 1.020–2.101
Yes 22 (31.0%) 49 (69.0%)

*P , .05 in chi-square of Pearson.


CI indicates confidence interval; PR, prevalence ratio. Bold indicates statistically significant difference.

in the model of regression, since it demonstrated the best fit to executed, should not be an important factor in the predictability
the model. Indeed, the use of medication was an independent of peri-implant pathology incidence. Other factors such as
factor associated with the occurrence of peri-implant pathol- occlusion, prosthetic condition, adaptation, type, material,
ogies (PR: 1,261). fixation (excess cement), and complexity of rehabilitation have
While, Roos-Jansåker et al1 did not find any significant been more frequently reported;7,17,35,36 however, in our study,
associations among some of these conditions (osteoporosis, these factors were not important predictors, possibly due to the
diabetes, and coronary heart disease) and the onset of disease. fact that our unit of evaluation was the implant itself.
The medications in use that may have an effect on bone The rehabilitation of dental implants in grafted areas, even
turnover and/or healing and remodeling of mucosa could have though this is still considered a challenging practice, is currently
affected the results.1 This aspect was compromised, since the regarded to be a successful procedure, independent of the
medication type was not considered separately in the material used (autogenous, allograft, xenograft, and alloplast).
anamnesis of this study for additional discussion.6,16 Failures in the grafted regions are more associated with
Periodontal and peri-implant pathologies were not signif- contamination of the material, lack of primary stability, lack of
icantly associated with each other, as also observed in other installation technique and inadequate prosthetic rehabilitation,
studies.1,7,11,28 Microorganisms remaining in periodontal pock- as well as disrespect to biomechanical principles.37 It should be
ets can be transferred from to peri-implant sites, ie, pockets as noted that the type of increase (horizontal or vertical),
niches of infection.8,31 An elevated incidence of biological extension of the grafted area, the number of implants, and
complications associated with implants has been observed in countless other variables can influence the success of the
patients with periodontitis, compared to healthy individu- rehabilitation.37 However, the authors conclude that the type of
als.32,33 Additionally, periodontitis as a risk indicator may be platform, smoking, and history of periodontitis are more
attributable to the fact that both pathologies share common important in this context.38 Reports of peri-implant pathologies
host factors or common microbiota.9 occurring in association with the grafted area are scarce in the
The finding that peri-implant pathologies are positively literature and additional studies are needed to elucidate this
correlated with the time of prostheses use5 has also been issue. We, herein, observed a significant association between
confirmed by the present analysis, as peri-implant pathology peri-implant pathologies and grafting area, but this variable lost
was more associated with implants that had been fitted more strength in the model; nevertheless, this association was still
than 2 years before (PR: 1,720). Similar findings were observed in apparent when adjusting the model and, consequently, the
other studies.7,17,34 It is important also to note that the time of magnitude of the strength of the other variables. Several
use of the prosthesis, when the prosthesis is well planned and authors have observed a higher occurrence of peri-implant

226 Vol. XLVII / No. Three / 2021


de Vasconcelos Gurgel et al

TABLE 3
Univariate analysis between the dependent variable ‘‘peri-implant pathology,’’ and ‘‘considerations regarding rehabilitation’’
variables*`
Peri-Implant Pathology

No (%) Yes (%) P PR CI (95%)


Occlusion
Normal 154 (43.3%) 202 (56.7%) .584 0.943 0.767–1.161
Malocclusion 72 (45.9%) 85 (54.1%)
Prosthesis condition
Provisional 210 (43.4%) 274 (56.6%) .981 0.992 0.514–1.915
Permanent 181 (43.6%) 138 (56.4%)
Prosthesis type
Unit 83 (42.1%) 114 (57.9%) .167  
Removable full 35 (36.5%) 61 (63.5%)
Protocol 37 (53.6%) 32 (46.4%)

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Multiple partial 72 (44.7%) 89 (55.3%)
Prosthesis material
Metal-ceramic 138 (43.3%) 181 (56.7%) .934 0.992 0.812–1.212
Resin 89 (43.6%) 115 (56.4%)
Fixation type
Screwed 60 (50.8%) 58 (49.2%) .131 1.190 0.956–1.482
Cemented 132 (42.7%) 177 (57.3%)
Failure to adapt
No 188 (42.6%) 253 (57.4%) .408 0.896 0.697–1.153
Yes 39 (47.6%) 43 (52.4%)
Time of prosthesis use (months)
6–24 98 (62.8%) 58 (37.2%) ,.0001* 1.785 1.474–2.161
.24 113 (35.2%) 208 (64.8%)

*P , .05 chi-square of Pearson.


Not possible to calculate PR and CI.
`CI indicates confidence intervals; PR, prevalence ratio. Bold indicates statistically significant difference.

pathology in the upper jaw.1,7,10,11,12 This study also showed an CONCLUSION


association between location in the upper jaw and peri-implant
pathology. Serino and Turri39 demonstrated that bone charac- Even in the case of a cross-sectional study, with the limitations
teristics and quantity may influence the progression of peri- inherent to this type of study (evaluation of the specific
implantitis, especially in areas with smaller bone density and moment), the factors associated with peri-implant pathologies
lower density, which are probably more susceptible to the are important to highlight. Potential risk factors should be
inflammatory process and occlusal stresses. confirmed with specific studies for this type of analysis; as such

TABLE 4
Univariate analysis between the dependent variable, ‘‘peri-implant pathology,’’ and clinical variables*
Peri-Implant Pathology

No Yes P PR CI (95%)
VPI
0–30% 53 (47.7%) 58 (52.3%) .298 1.131 0.903–1.416
.30% 174 (42.2%) 238 (57.8%)
GBI
0–30% 216 (45.3%) 261 (54.7%) .005* 1.894 1.120–3.201
.30 % 11 (23.9%) 35 (76.1%)
Periodontal disease
No 12 (42.9%) 16 (57.1%) .973 0.992 0.637–1.545
Yes 168 (43.2%) 221 (56.8%)
Keratinized mucosa
Yes 81 (61.2%) 50 (38.2%) ,.001* 1.660 1.378–2.000
No 146 (37.2%) 246 (62.8%)
Papilla
Yes 81 (40.5%) 119 (59.5%) .225 0.880 0.715–1.084
No 138 (46.0%) 162 (54.0%)

*P , .05, according to Pearson’s chi-square.


CI indicates confidence interval; GBI, gingival bleeding index; PR, prevalence ratio; VPI, visible plate index. Bold indicates statistically significant difference.

Journal of Oral Implantology 227


Factors Associated with Peri-Implant Pathologies

TABLE 5
Binary logistic regression model for peri-implant pathologies*
PR IC (95%) P PR adjusted CI (95%) P
More than 2 years since fitting of prosthesis 1.785 (1.474–2.161) ,.001 1.720 (1.413–2.167) ,.0001
Upper jaw 1.700 (1.368–2.113) ,.001 1.421 (1.203–1.678) ,.0001
GBI . 30% 1.894 (1.120–3.201) .005 1.496 (1.170–1.914) .001
Augmentation procedure 1.464 (1.020–2.101) .023 1.095 (0.908–1.320) .341
Use of medication 1.292 (1.061–1.572) .010 1.261 (1.1321–1.554) ,.0001
Sex 1.053 (0.833–1.330) .662 0.930 (0.772–1.120) .443

*Hosmer and Lemeshow test: 1.000; Nagelkerke R Square: 0.218; Chi-square: 84.455 (6): P , .0001.
CI indicates confidence interval; GBI, gingival bleeding index; PR, prevalence ratio.

the present study represents an important starting point for the tube-in-tube connection: a cross-sectional analysis of 512 implants. Clin Oral
development of new research in the area. The frequency of Implants Res. 2017;28:24–28.

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NOTE
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