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ecent systematic reviews and meta-
tients are included in this study. The waist/hip ratio (WHR), analyses demonstrated a link among
plaque index, bleeding on probing, probing depth (PD), overweight, obesity, and periodo-
and clinical attachment level (CAL) were measured at base- ntal diseases.1,2 Obesity has been recog-
line and 3 and 6 months after treatment. Univariable and nized as a major public health problem.3
multivariable analyses were used to evaluate the influence Obesity is defined as an abnormal accu-
of sex, age, baseline percentage of PD >3 mm, WHR, and mulation of body fat and is associated with
obesity on periodontal treatment outcomes. increased risk of illness, disability, and
Results: Demographic and periodontal characteristics at death and is considered a risk factor for
baseline were similar in both groups. All periodontal param- cardiovascular diseases, some cancers,
eters were improved during treatment in both groups. PD re- and type 2 diabetes.4,5 People are con-
duction and CAL gain were 0.88 and 0.84 mm in NW sidered overweight (preobese) if their
individuals and 0.79 and 0.68 mm in obese individuals. body mass index (BMI) stands between
The difference in moderate-to-deep pocket (PD >5 mm) per- 25 and 30 kg/m2 and obese when BMI is
centages between the baseline and 6-month examinations >30 kg/m2. However, there are some
was 9.1% in NW individuals and 6.08% for obese individuals. limitations to the use of BMI. In fact, BMI
Multivariable analysis showed that obesity negatively influ- does not measure the corpulence of the
enced changes of PD >5 mm percentages. This influence individual and provides only limited data
was also observed at 3 months for improving sites (PD de- on body composition that varies with
crease >2 mm between examinations) if WHR was also con- age, sex, and physical activity.6 Recent
sidered in the analysis. data suggest that waist circumference
Conclusions: A negative association between adiposity and waist/hip ratio (WHR) are more
measurements and periodontal treatment outcomes was ob- convenient indicators of abdominal fat
served mainly for moderate-to-deep pockets. Consideration distribution and its associated health
of WHR and other influencing factors amplified the negative problems.5
effect of obesity on periodontal treatment outcomes. J Peri- Periodontitis is an infectious and in-
odontol 2015;86:1030-1037. flammatory disease that is one of the
most common chronic diseases through-
KEY WORDS
out the world7 and is closely related to
Obesity; periodontal diseases; treatment outcome; waist-hip diabetes8 and stroke.9 These diseases
ratio. have some common risk factors, such as
smoking.10 Periodontitis appears to affect
* Department of Periodontology, Dental Faculty, Strasbourg, France. more frequently and be more severe in
† National Institutes of Health and Medical Research, Osteoarticular and Dental
Regenerative Nanomedicine, Strasbourg, France. obese individuals than in normal-weight
(NW) individuals.1 The risk factor het-
erogeneity of the observed population in
the different investigations on obesity and
adiposity effects could affect the magni-
tude of the increased risk rather than
doi: 10.1902/jop.2015.140734
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J Periodontol • September 2015 Bouaziz, Davideau, Tenenbaum, Huck
precluding the risk.11 Some systemic conditions as- level (CAL) ‡3 mm19; 2) ‡12 teeth; 3) aged >18
sociated with adiposity, such as metabolic syndrome, years; 4) non-smoker (or former smoker since ‡5
dyslipidemia, and insulin resistance, are able to influ- years); 5) have a regular medical follow-up (at least
ence this relationship.12 Interestingly, increased WHR one time per year); and 6) have recent blood samples
seemed to exacerbate the association between obesity that enable control of glycemic or hemoglobin A1c
and periodontal disease.13,14 (HbA1c) (in the previous 3 months).
Presently, few studies have been conducted on the Patients were excluded from the study for the
effect of obesity on periodontal treatment. Some following: 1) diagnosed with diabetes mellitus and
studies have shown that obesity negatively influ- HbA1c level >6.5%; 2) chronic inflammatory disease
enced periodontal treatment outcomes,15,16 but or infection; 3) pregnancy or lactation; 4) physical or
other studies did not demonstrate such an influ- mental handicaps that could interfere with adequate
ence.17,18 The inclusion of other risk factors in some oral hygiene control; 5) currently smoking or a former
studies, such as diabetes18and smoking,15,18 may smoker of <5 years; 6) the use of systemic or topical
influence the results. Furthermore, the variability of steroidal and non-steroidal anti-inflammatory drugs
demographic characteristics, such as age and sex, or antibiotics during the past 6 months; 7) any imm-
and the definition of periodontal status, treatment unologic condition requiring prophylactic antibiotic
modalities (2-15 to 6-month16 follow-up), and out- treatment before invasive dental procedures; 8) any
comes could also modify data interpretation. Finally, history of periodontal treatment; and 9) any diet ful-
the definition of obesity and control patients varied filled to lose weight (or intention to fulfill a diet).
between the different studies, with some basing the Periodontal measurements and anthropometric data
distinction on BMI alone15,16 and others using BMI in were collected by the same trained examiner (WB). The
association with other adiposity measurements data collection was done at baseline and 3 and 6
(WHR, body fat),17,18 which could explain in part the months. At baseline, non-surgical treatment was per-
variability of results1 and the need for additional formed, including oral hygiene education and scaling
studies considering the influence of these factors. and root planing (SRP). First, a trained periodontist
The aim of this study is to evaluate the association (WB) instructed the patient regarding brushing tech-
among adiposity measurements, non-surgical peri- nique (Bass technique) and use of interproximal hy-
odontal treatment outcomes, and influencing factors giene devices. SRP was performed using an ultrasonic
in patients suffering from moderate-to-severe chronic device‡ and manual curets.§ Treatment was performed
periodontitis (CP). in two to three sessions under local anesthesia for
probing depth (PD) >5 mm lasting 1 hour each. The
MATERIALS AND METHODS aim of each session was to remove biofilms and cal-
Study Groups culus of scaled roots. All sessions were performed
Patients diagnosed at the Department of Periodon- within 7 days. Patients were instructed to rinse with
tology, Dental Faculty, University of Strasbourg, a chlorhexidine mouthwash (0.12%)i twice a day for 7
France, as having moderate-to-severe generalized days. The treatment protocol did not include antibiotics
CP are included in this study. The study protocol was treatment. Oral hygiene was controlled at each ap-
accepted by the Ethical Committee of the Faculty of pointment, and hygiene instructions were repeated if
Medicine (2014-61), University of Strasbourg. This needed. At the 3-month examination, reinstruction of
study was conducted from January 2011 to June oral hygiene methods was performed if needed, and
2012. Participants were informed about the objec- residual pockets ‡4 mm were systematically scaled
tives of the study and its design and provided written and planed.20 All treatments procedures were per-
informed consent. The patients (20 males and 20 formed by the same periodontist (WB).
females, aged 22 to 78 years; mean age: 51 – 15
Data Collection
years) were selected and placed in two groups: 1) an
Periodontal examination. To calibrate the examiner,
obese group including patients with BMI ‡30 and 2)
a total of 250 sites were evaluated randomly in six
an NW group including patients with a BMI ‡18.5 and
patients (one quadrant per patient). The examiner
£25. Obese patients were first enrolled and matched
(WB) evaluated the PD parameters on two occasions
by sex and age with NW patients. The maximum
at 1-week intervals with an agreement >0.90 as
allowable difference between an obese patient and
calculated with the k-light score.
the corresponding matched NW patient was 10 years.
Full-mouth clinical measurements included the
The matching ratio was 1:1.
following: 1) plaque index (PI); 2) bleeding on probing
To be enrolled in the study, participants from
both groups had to fulfill all the inclusion criteria: 1)
‡ Suprasson Newtron, Satelec, Acteon, Merignac, France.
a clinical diagnosis of moderate-to-severe general- § Hu-Friedy, Chicago, IL.
ized CP with ‡30% of sites with clinical attachment i Eludril, Pierre Fabre, Castres, France.
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Adiposity and Midterm Periodontal Treatment Outcomes Volume 86 • Number 9
1032
J Periodontol • September 2015 Bouaziz, Davideau, Tenenbaum, Huck
0.79 – 0.60
6.08 – 8.87
0.68 – 0.74
achieving statistical significance at the 0.20 level in
the univariable analysis for at least one of the se-
lected variables were included in multivariable
analysis. WHR was forced in the different models
considering its effect on obesity morbidity.13 Differ-
0.27 – 0.75
0.76 – 0.39
0.88 – 0.98
9.10 – 14.3
0.84 – 0.78
ences were considered as significant when P <0.05.
6 Months, Mean – SD
† RESULTS
Obese (n = 18)
15.71 – 13.08*
0.41 – 0.45*†
10.36 – 9.92*
2.43 – 0.49*
1.30 – 2.21*
3.37 – 1.15*
Patients’ Demographic Characteristics
23.16 – 5.79
7.00 – 7.26*
2.45 – 0.53*
12.76 – 11.0*
2.81 – 3.56*
3.23 – 0.98*
0.44 – 0.58
14.6 – 8.08
4.81 – 7.83
0.35 – 0.48
0.61 – 0.94
0.53 – 0.70
2.58 – 3.06*
3.70 – 1.14*
creased (<1 kg) in the obese group, but WHR did not
23.22 – 5.75
2.78 – 0.55
change.
Periodontal Characteristics at Baseline and
Response to Non-Surgical Periodontal Treatment
0.75 – 0.54*
3.54 – 0.86*
2.71 – 0.40
3.82 – 3.66
3.22 – 0.76
7.39 – 9.78
4.04 – 1.17
3.33 – 0.92
4.07 – 1.15
Teeth (n)
BOP (%)
Table 2.
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Adiposity and Midterm Periodontal Treatment Outcomes Volume 86 • Number 9
Bold type indicates statistically significant differences at P £0.2, and, other than for % PD >3 mm, indicate the parameters that will be included in multivariate analysis models. Negative values indicat poorer
<0.001
0.14
0.40
0.57
0.25
amination were 18.0 and 10.5 in the NW and
P
obese groups, respectively.
0.16
0.83
0.54
P
0.74
0.24
DISCUSSION
<0.001
0.14
0.68
0.87
0.23
0.16
0.27
0.71
P
0.21
0.25
0.51
Covariable
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J Periodontol • September 2015 Bouaziz, Davideau, Tenenbaum, Huck
0.001
<0.001
6 months.16 In the present investigation, various
0.98
0.25
0.07
0.76
0.48
0.44
0.06
P
kinetics of periodontal parameter changes during
<0.001
0.02
associated with PD >5 mm percentage changes and
0.48
0.17
0.08
0.51
0.85
0.15
P
<0.001
0.005
0.04
0.01
0.78
0.16
0.18
P
<0.001
0.04
0.02
0.51
0.70
0.11
0.08
P
<0.001
0.256
0.12
0.13
0.39
0.41
0.41
0.24
<0.001
0.27
0.12
0.24
0.63
0.56
0.20
0.09
changes.
P
at baseline
Sex (female)
Sex (female)
Table 4.
Obese
Model 1
Model 2
WHR
Age
Age
Model
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Adiposity and Midterm Periodontal Treatment Outcomes Volume 86 • Number 9
with diabetes (HbA1c >6.5%) were excluded, as was decreases serum levels of tumor necrosis factor-a,
done in the study by Gonc xalves et al.16 Smokers have IL-6, and leptin.18 Interestingly, periodontal treat-
been also excluded. 16,17 Univariable analysis of the ment did not decrease others inflammatory markers,
studied population showed that the initial severity of such as C-reactive protein (CRP), or did not modify
periodontal disease (percentage of PD >3 mm) posi- the lipid profile at 3 months.18 This observation may
tively influenced changes of deep pockets and the be explained by the continuous production of in-
number of improving sites. Obesity alone did not in- flammatory products by adipocytes30 that may affect
fluence periodontal outcomes, as shown previously.15 periodontal tissue response as suggested for patients
In multivariable analysis models taking into account with diabetes.31 Interestingly, the nullification of systemic
age, sex, and initial severity of periodontitis, a signifi- effects by obesity in response to periodontal treatment
cant negative influence of obesity was observed for has been demonstrated in the PAVE (Periodontitis
deep pocket changes, but this influence was not ob- and Vascular Events) study for high-sensitivity CRP
served for mean PD and percentages of PD >3 mm reduction.32
changes (data not shown). Similarly, in the study by Some limitations could be attributed to the present
Gonc xalves et al.,16 the observed difference of mean PD study. The specific profile of the obese patients (non-
reduction between obese and non-obese patients is diabetic, non-smoker) may restrain the extrapolation
more marked for initially deep sites than for initially of the results to the whole obese population. Fur-
moderate sites.16 This could be explained by the se- thermore, the small sample size and the impossibility
verity of the initial periodontal status, although initial to achieve investigator masking regarding the visible
mean PD and percentage of PD >4 mm appeared more aspect of obesity may also limit the strength of this
severe in the study by Suvan et al.15 (4 mm and 50%), study. However, the matched design (for age and
in the study by Gonc xalves et al.16 (3.5 mm and 23.5%), sex), the absence of other risk factors (smoking,
and in the study by Altay et al.18 (3.1 mm and 18%) diabetes) in the studied population, and the stan-
compared with the present study (3.2 mm and 17.5%) dardization of periodontal treatment modalities may
(data not shown). These data suggested that the effect reduce the influence of those issues.
of obesity was more pronounced in the case of severe
periodontitis. CONCLUSIONS
In previous studies, the definition of obese versus Within the limitations of this study, it could be con-
non-obese patients was only based on BMI, as in the cluded that adiposity measurements and non-surgical
study by Suvan et al.,15 or did not include other periodontal treatment outcomes were associated
adiposity measurements, such as body fat,18 WHR,16 in patients suffering from moderate-to-severe CP.
or both.17 Interestingly, the inclusion of the WHR Obese patients without diabetes had a poorer response
variable in multivariable analysis amplified the neg- to initial periodontal treatment than NW patients. This
ative association between periodontal treatment effect was mainly observed for moderate-to-deep
outcomes and obesity. Previous studies have shown pockets, suggesting that, the more severe peri-
that WHR or waist circumference could independently odontitis was, the more negative the effect of adiposity
influence periodontal status. 13,14 However, in the was on periodontal treatment outcomes. Interestingly,
present study, WHR alone is not associated with the consideration of WHR and other influencing factors
periodontal treatment outcomes. The study by Jimenez amplified the negative effect of obesity on periodontal
et al.13 has shown that WHR exacerbated the link treatment outcomes.
between periodontitis and obesity in males. These
results suggested that the definition of obesity and ACKNOWLEDGMENTS
adiposity could influence their predictive value for The authors thank Dr. Francxois Séverac (Department
periodontal treatment outcomes. Adiposity contrib- of Public Health, Hôpitaux Universitaires de Stras-
uted to systemic inflammation through modulation of bourg, Strasbourg, France) for his helpful comments.
immune and metabolic parameters, increasing peri- The authors report no conflicts of interest related to
odontitis susceptibility,18 including resistin, leptin, and this study.
adiponectin.28 It has been demonstrated previously
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