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Amélie Keller (AK) MPH*, Jeanett F Rohde (JFR) MSc*† , Kyle Raymond (KR) PhD*, Berit
“NOTE: this is the author’s version of a work that was accepted for publication in the Journal of
Periodontology. Changes resulting from the publishing process, such as peer review, editing,
corrections, structural formatting, and other quality control mechanisms may not be reflected in this
document. Minor changes may have been made to this manuscript since it was accepted for
*
Institute of Preventive Medicine, Bispebjerg and Frederiksberg Hospital, Copenhagen, Denmark
†
Institute of Public Health, University of Southern Denmark, Copenhagen, Denmark
‡
The Boden Institute of Obesity, Nutrition, Exercise & Eating Disorders, The University of Sydney, Australia
1
Abstract
Introduction: Periodontitis and obesity are among the most common chronic disorders
affecting the world’s populations, and recent reviews suggest a potential link between
previous reviews were primarily based on cross-sectional studies, with only few
The objective was to examine the time-dependent association between obesity and
periodontitis and how weight-changes may affect the development of periodontitis in the
general population. Therefore, longitudinal and experimental studies that assessed the
Method: Intervention and longitudinal studies with overweight or obesity as their exposure
and periodontitis as their outcome were searched through the platforms Pubmed/Medline
Results: Eight longitudinal and five intervention studies were included. Two of the
and subsequent risk of developing periodontitis, and further three studies found a direct
intervention studies on the influence of obesity on periodontal treatment effects found that
the response to non-surgical periodontal treatment was better among lean than obese
patients, the remaining three studies did not report treatment differences between obese
and lean. Among the eight longitudinal studies, one study adjusted for CRP and biological
markers of inflammation such as CRP, IL-6 and TNFα and inflammation markers were
2
Conclusion: This systematic review suggests that overweight, obesity, weight gain and
increased waist circumference may be risk factors for development or worsening with
3
Introduction
Overweight and obesity are defined as excessive accumulation of fat that may impair
health. An adult is considered overweight if its body mass index (BMI= weight kg/height2m),
is ≥ 25 and obese if its BMI is ≥30 Kg/m2.1 The prevalence of overweight and obesity has
increased worldwide during the last decades, raising concern due to its health and
and has been found to predispose to major chronic diseases such as cardiovascular
teeth resulting from the interaction between pathogenic bacteria and the host’s immune
response 4, 5 that may results in partial or complete loss of teeth.6 With a prevalence of
47.2% in the general ≥30 years-old US population in 2009, 7 periodontitis, like obesity, is
one of the most common chronic disorders in the world. 8-10 The exact mechanism
underlying the development of periodontitis has not yet been established and different
reported in 197712, when changes in the periodontium of obese rats was found.12 In
humans, cross-sectional studies suggest that obesity may be directly associated with
cannot be determined in cross-sectional studies, and the risk of reverse causation is high.
26
During the past years, two systematic reviews 3, 27 and other non-systematic reviews 6, 11,
28-36
summarizing the results from studies of association between overweight/obesity and
4
time of previous reviews, mainly cross-sectional studies were included. 3,27 Reviews based
on cross-sectional studies are useful to summarize current findings. However, the level of
the evidence cannot be assessed due to the low hierarchy of evidence from this study
design.
and how weight-changes may affect the development of periodontitis in the general
population, longitudinal and experimental studies that assessed the association between
overweight, obesity, weight gain, waist circumference and periodontitis were reviewed.
Methods
Only cohort studies and intervention studies among children, adolescents and adults
The literature search was performed during December 2013 and June 2014 through the
platforms Pubmed/Medline and Web of Knowledge. The following key terms were used:
AND
Another search combined the abovementioned key words with AND Inflammation OR
Inflammation Mediator
Filters: Humans
5
The selection of articles was performed by two researchers (AK, JFR). First, relevant titles
in the databases were selected. Second and third, all abstracts and full texts were
researcher (BLH) was involved. Reference lists of the included articles and other reviews
Data on overweight; obesity; waist circumference (WC); weight gain; periodontitis status,
measures and treatment were extracted. Furthermore, data on inflammatory markers, age,
socioeconomic status (SES), smoking, gender, oral hygiene and diabetes were sought.
Study quality and grading of the strength of the evidence (grade I (good/strong) to V (not
assignable)) was assessed by two researchers (AK, JFR) using the “Quality Criteria
Checklist: Primary Research and Primary Research – Non human Subjects” of the
Academy of Nutrition and Dietetics 37. (More information in Supplement: Method and
Supplement: Table 2)
Results
After full texts selection, thirteen papers, eight prospective cohort studies (referred to as
longitudinal studies)38-45 and five clinical trials (referred to as intervention studies)46-50 were
between overweight/obesity and development of periodontitis. Four clinical trials46, 47, 49, 50
examined the outcome of non-invasive periodontal treatment (NIPT) between obese and
non-obese patients. The fifth study48 investigated NIPT outcome between bariatric surgery
patients and controls. Four longitudinal studies38-41 included men only; the remaining
included both gender.42-45 Four46, 48-50 intervention studies included both gender; one47
included women, only. Two studies were from the same authors group (Gorman et al.).38,
6
39
The list of excluded articles is given in Supplement: Table 1. Characteristics of included
Three longitudinal studies38, 40, 42 found a direct association between obesity at baseline
and subsequent periodontitis development 38, 40, 42, and two studies40, 42 found a direct
95%CI 1.05-2.21), alveolar bone loss (ABL) (adjusted-HR=1.60 95%CI 1.07-2.38) and
probing pocket depth (PD) (adjusted-HR=1.40 95%CI 1.02-1.91) was worse for obese
developing periodontitis over 20 years among obese men. A 5-year study of Japanese
women HR=3.24; (95%CI 1.32-7.94), but not men (HR=1.44; (95%CI 0.97-2.14)).
Similarly, increased risk of developing periodontal disease was observed for overweight
men in one study40 and for overweight men and women in another.48 No associations were
Three studies38, 39, 45 found that weight-gain was directly associated with development of
periodontitis, and men with moderate to large weight-gains, developed more PD or ABL
events than low weight-gainers. 38, 39, 45 A fourth41 study did not find an association
between weight gain from age 21 to 60-70 years and thresholds of periodontitis in adjusted
models.41 (Table 5)
7
Regarding WC, one study38 found that a 1% increment in baseline waist-height-ratio was
over 27 years, and an augmentation of 1cm in WC was associated with a 1-2% increase in
the hazard of AL and PD.38 Another study among overweight men found39 that increased
years. Similarly, a third study40 found that, men in the extreme quintile of change in WC
and waist-to-hip-ratio had a 27% and 34% increased risk of developing periodontitis,
Two cohort studies44, 45 focusing on youth, were identified. 44, 45 In one study, no
association between overweight and obesity and the odds of developing gingivitis, calculus
or PD were found in the adjusted model at eight years.44. However, there was an
association between the number of episodes of obesity, which was calculated by counting
the number of times each participant was considered obese during follow-up, between age
15-24 years, and the simultaneous risk of presenting dental calculus at age 2444. WC was
also directly associated with the odds of developing gingivitis (OR 2.03 (1.20-3.45)) and
calculus (PR 1.08 (1.01-1.15)) at eight year. 44 Mixed results were found in the other study
45
with an increase in BMI over 3 years being directly associated with simultaneous
development of periodontitis when assessed using the Community Periodontal Index score
Among intervention studies46-50, two 48, 50 found that the response to NIPT was better
among lean than obese, whereas three other studies did not find significant differences. 46,
47, 49
(Table 2) One study 50 showed less improvement in clinical parameters following
8
NIPT among obese than among overweight patients, and obese had on average 3.2%
more sites with PD >4mm than normal-weight patients following treatment. Furthermore,
for every BMI difference of 10 kg/m2, the mean percentage of sites with PD >4mm two
months following treatment increased by 2.5%. 50 Another study found response to NIPT in
bariatric patients compared to controls with greater improvement in mean gingival index,
PD, AL and bleeding on probing. 48 Two studies46,49, did not show differences in
periodontal healing between obese and non-obese patients undergoing NIPT (p>0.05). At
baseline, plasma levels of the inflammation markers TNFα and leptin were significantly
higher in the obese (p<0.05; p<0.01) 46, whereas IL-6 and CRP levels were identical. 46 At
follow-up, only IL-6 was significantly lower in the non-obese compared to the obese.46 In
the fifth study 47, there was a trend towards better systemic response to treatment among
normal-weight women compared to obese women, however the difference was not
significant. CRP levels were significantly higher among obese women at baseline,
One longitudinal study44 adjusted for C-reactive protein (CRP), the other studies38-43, 45
as CRP, IL-6 and TNFα were analyzed separately in three46, 47, 49 of the intervention
studies.
Other risk factors than inflammation cited were age, smoking, SES, oral hygiene and
diabetes. All but one 44 longitudinal studies adjusted for age. Six38-42, 44 adjusted for
cigarette smoking and two43, 45 others included only non-smokers. Five studies adjusted for
SES. 38, 39, 41, 43, 44 Oral hygiene was adjusted for in four studies. 38, 41, 43, 45 Four studies38,
40-42
adjusted for diabetes and three38, 43, 45 studies included non-diabetic participants only.
9
The quality score was positive for nine38-41, 43, 44, 46, 47, 49 studies and neutral for four42, 45, 48,
50
(Supplement: table 2). Studies with neutral quality scores presented either undetailed
was graded limited to fair, fair for weight gain and good for WC. Regarding periodontal
treatment among overweight/obese patients, the strength of the evidence was graded
All studies but one had a statement regarding conflict of interest. All studies were publicly
funded and one study further reported partial private funding. 50 (Supplement: table 5)
Discussion
The results of the present review suggest that overweight, obesity, weight gain and
such as PB, ABL, AL or plaque index. Evidence from longitudinal studies, with a follow-up
≥ 20 years38-40 was clearer than evidence from studies with shorter follow-ups or from
intervention studies. 41-45 Long-term follow-up minimizes the risk of reverse causation or
confounding from chronic disease at baseline. Short-term longitudinal studies might not
periodontitis increases with age, probably due to longer exposure-time of the periodontal
10
tissue to bacterial plaque.28 Furthermore, as fat increases and lean mass decreases with
age, even minor weight-gains might involve important adverse changes in body
composition that may influence periodontal health.51 Therefore, studies with a longer
follow-up time, and among older participants, might be more likely to show a direct
association. However, as most included studies38-43, 45 adjusted for age, there seems to be
Associations were more consistent for visceral than general adiposity suggesting that
periodontitis incidence than BMI. This is in line with the fact that pro-inflammatory
adipocytokines such as TNF-α and IL-6 are primarily produced by the abdominal adipose
tissue. Several mechanisms are linked to increased levels of TNF-α that may contribute to
the onset of periodontitis. The stimulation of osteoclasts formation and effect on host
bones and participate in connective tissues degradation. Regarding IL-6, its association
with periodontitis onsets remains unclear due to its dual pro and anti-inflammatory effect.
29
Seemingly, the role of other cytokines on the pathway between overweight/obesity and
periodontitis has not yet been clarified. 4, 31 The mechanism of how obesity affects the
periodontium is still poorly understood, and this association may be bidirectional. 29, 31,53
markers by the adipose tissue that may increase gingival inflammation and promote
bacterial proliferation on the tooth root surface. But, periodontitis also induces the
production of pro-inflammatory cytokines that might prompt obesity and other chronic
11
Low SES may both influence the propensity to obesity and risk of developing periodontitis.
A recent review 28 concluded that there was a clear association between low SES and
gingivitis but the association was less direct for periodontitis. 28 In the present review,
five38, 39, 41, 43, 44 longitudinal studies controlled for SES in their analyses, showing
discrepant effects.
Among the eight longitudinal studies38-45, four were on men only38-41, and the remaining
included men and women.42-45 Among the latter, one study42 analyzed men and women
separately whereas the other three43-45 did not. In this study, Saxlin et al. (2010) 43 tested
for modification by gender but found no significant interaction, suggesting that gender did
not seem to influence the association between obesity and periodontitis. In a recent study
54
, overweight, obesity and waist-to-hip ratio were associated with increased risk of tooth
loss among men and women. However, the results suggested that markers of
inflammation such as CRP and IL-6 may be mediators of the association between obesity
Some studies indicate 28, 55 that men are more at risk for developing periodontitis than
women; whereas others28,56 suggest that women might, during certain periods, be more
gingival inflammation. From the results of this review, it is not possible to make a clear
Smoking has been found to contribute to the destruction of the periodontal tissue which
increases periodontitis progression. 28 Studies also show that smokers have a higher
furcation defects than non-smokers. 57, 58 However, smokers tend to weigh less and gain
12
less weight, limiting the possibility that the association between obesity and risk of
periodontitis is related to smoking. 59 Studies either had excluded smokers, or adjusted for
The strength of our review lies in its systematic approach and the inclusion of longitudinal
and intervention studies only, limiting the risk of reverse causation. However, among
longitudinal studies, two38, 45 reported results from simultaneous changes in exposure and
outcome, therefore being more prone to reverse causation due to their design resembling
a cross-sectional one. 60
To strengthen the quality of this systematic review, the article search was performed
independently by two researchers (AK, JFR) and a validated quality assessment tool was
used. A limitation of our study is the inclusion of only published studies and restriction to
English language. Publication bias cannot be excluded, as studies with positive results
studies used different measures and cut-offs to define periodontitis, making a meta-
analysis difficult. Generally PD was the most common measure with seven studies using it.
However, among these studies, the cut-offs used for PD varied from ≥3mm to≥5mm.
(Supplement: table 6) Furthermore, variations regarding the sites and numbers of teeth
examined were present. Such differences in definition and cut-offs might influence study
results, and no clear pattern could be established. Different measures of associations were
also used that were difficult to combine in a meta-analysis and some of the statistical
analyses performed could have introduced bias. In one study38, the time to periodontal
progression was defined as the number of years from the baseline exam to the first exam
where periodontal progression was noted. Therefore, the time to periodontal progression
13
was interval censored, i.e. it occurred sometime between examinations. It is difficult to
assess the nature, direction and size of such bias that arises from the imputation, but
potentially it led to attenuation rather than inflation of the association, giving credit to the
used in the model associated with the event were treated as time-dependent covariates.
However, the values of the covariates were only obtained at each examination. This
implies that the authors use the last observation carried forward. Again, the magnitude of
the bias associated with such an imputation is difficult to assess. In another study42, the
authors used Cox regression to assess the 5-year incidence of periodontal disease.
However, the data collected is an example of current status data, 62 a special case of
interval censoring where individual's status is observed at one time point . The only
information pertaining to the event of interest corresponds to whether it has occurred in the
5-year period between the baseline and follow-up exam. The choice of model does not
account for the characteristics of the data collected. The subsequent bias arising from both
Conclusion
Evidence from longitudinal studies, particularly those with a follow-up ≥ twenty years,
suggest that overweight, obesity, weight gain and increased waist circumference, may be
risk factors for developing periodontitis or worsening with regard to periodontal measures.
Results from intervention studies on periodontal clinical response between obese and
normal weight patients undergoing non-surgical periodontal treatment are few and the
evidence for an effect limited. Inflammation, gender and socioeconomic status are likely to
14
play a role in the pathogenesis of obesity and periodontitis. Therefore, more studies
Conflict of interest
This review was supported by Tryg foundation, Virum, Denmark. The authors declare not
15
Table 1: included studies with weight (overweight/obesity/weight gain) as the main exposure and periodontitis as the outcome
Reference Study Dataset Population Follow-up Outcome RR/HR/OR/PR /β Exposure Results¥ Inflammation Confounders Q
(author design used and characteristics (+) direct association
and date) country (no anaylized, (NS) no association
gender, age) (-) inverse association
Gorman et Cohort VA Dental 893 30 years Periodontitis Mean±SD Weight gain +** - Age A
al. 2012 39 Longitudinal Adults (1968-1998) (PD) β-coefficient WC +** Smoking
Study, USA M Education
21-84 y.o Oral hygiene
Linden et Cohort Prospective 1362 12 years Periodontits OR Weight change from NS - Age A
al. 2007 41 Epidemiologi Adults (1991-2003) (lth‡/hth#) age 21 to 60-70 y.o Smoking
cal Study of M Education
Myocardial 50-60 y.o SES
Infarction Oral hygiene
(PRIME), Diabetes
Northern
Ireland
Morita et Cohort Nagoya, 2787 5 years Periodontitis HR Overweight + ♂ ** - Age B
al. 2011 42 Japan Adults (2001/2002- (PD) + ♀** Smoking
M+F 2006/2007 Obesity NS ♂ Diabetes
21-69 y.o +♀*
Saxlin et Cohort Health 2000 396 4 years Periodontitis IRR Overweight NS - Age A
al. 2010 43 Survey, Adults (2000-2004) (PD) Obesity NS Gender
Finland M+F Education
30-59 y.o Dental plaque
Oral hygiene
Ttt
N teeth
16
de Cohort Oral health 720 8 years Periodontitis PR Overweight NS CRP Smoking A
Castilhos Study Adolescents/ (GI, calculus, Obesity NS Gender
et al. 2012 (OHS), young adults PD) WC + GI only Education
44
Brazil M+F SES
15-23 y.o Race
Diet
Ekuni et al. Cohort Japan 224 3 years Periodontitis OR BMI increase + CPI* - Age B
2014 45 Adolescents/ (CPI;%BOP, NS;%BOP, PD Gender
young adults PD) Oral hygiene
M+F
17-19 years
World Health Organization (2000) classification: normal weight equated to BMI ≥18.5<25 kg/m2, overweight ≥25 to ≤30 kg/m2 and obese >30 kg/m2. WC normal (men < 94 cm, women < 80 cm), level 1 (men 94 and <102
cm, women 80 and <88 cm) and level 2 (men 102 cm; women 88 cm). Lean et al. 1995
¥ adjusted models
(+) direct association; (NS) no association; * P<.05; **P<.01
Q=Quality: A: Positive – low bias level; B: Neutral – intermediate bias level; C: Negative – high bias level
‡
Lth=Low-threshold: at least two teeth with non-contiguous inter-proximal sites with ≥6mm loss of attachment and with at least one pocket of ≥5 mm
#
Hth: High-threshold: ≥15% of all sites measured had loss of attachment ≥6mm and there was at least one site with deep pocketing (≥6 mm)
M=male; F=female; RR=risk/rate ratio; HR=hazard ratio; OR=odds ratio; PR prevalence ratio; IRR=incidence risk ratio
TTT= treatment; WHtS=waist-height ratio; WHR=waist-hip ratio; CP= chronic periodontitis; TL= tooth loss; PI=plaque index; GI=gingivitis/gingival regression; tertile 2= moderate weight gain; tertile 3=large weight gain;
CPI=Community Periodontal Index; BOP=bleeding on probing
17
Table 2: included studies on periodontal treatment outcomes among participants with different weight status (overweight/obesity/weight gain)
Reference Study Dataset Population Follow- Outcome Periodo RR/ Intervention/ Exposure Results¥ Inflammation Quality
(author design used and characteristi up ntal TTT HR/OR/
and date) country cs PR
(no Β
anaylized,
gender, age)
Altay, Clinical trial Turkey 46 3 Periodontitis non- Median value Test : Obese + CP Control : Non NS CRP, IL-6, TNF- A
Gürgan Adults months (AL, PD, PI, invasive Mean±SD obese + CP α, leptin
and M+F GI, BOP)
Agbaht >25 y.o
2013 46
Al-Zahrani Clinical trial Saudi 40 2 Periodontitis non- Mean±SD Test : Obese + CP Control : Non NS CRP A
& Arabia Adults months (AL, PD, PI, invasive obese + CP
AlGhamdi F BOP)
2012 47 >35 y.o
Lakkis et Clinical trial US 30 6 weeks Periodontitis non- Mean±SD Test : ¶Obese+ CP Control : Obese + +** - B
al. 2012 48 Adults (PD, AL, GI, invasive + BS CP
M+F PI, BOP)
35-59 y.o
Zuza et al. Clinical trial Brazil 52 3 Periodontitis non- Mean±SD Test : Obese + CP Control : Non NS Il-1β, IL-6, A
2011 49 Adults months (PD, AL, GI, invasive obese + CP TNFα, IFNγ
M+F PI, BOP)
35-55 y.o
Suvan et Secondary UK, Italy 260 2 Periodontitis non- coefficient (95% CI) Test : Control : Normal - B
al. 2014 50 analysis Adults months (PD, invasive Overweight + weight
(pooled M+F %PD>4mm obese
data of 5 27-77 y.o AL, FMBS)
clinical
trials)
World Health Organization (2000) classification1: normal weight equated to BMI <25 kg/m2, overweight ≥25 to ≤30 kg/m2 and obese >30 kg/m2
¥ adjusted model
(+) direct association; (NS) no association; * P<.05; **P<.01
Quality: A: Positive – low bias level; B: Neutral – intermediate bias level; C: Negative – high bias level
‡
Lth=Low-threshold: at least two teeth with non-contiguous inter-proximal sites with ≥6mm loss of attachment and with at least one pocket of ≥5 mm
#
Hth: High-threshold: ≥15% of all sites measured had loss of attachment ≥6mm and there was at least one site with deep pocketing (≥6 mm)
¶
The intervention group are obese people with a loss of 40% excess weight after BS; The control group are obese people without BS nor weight loss
M=male; F=female; RR=risk/rate ratio; HR=hazard ratio; OR=odds ratio; PR prevalence ratio; IRR=incidence risk ratio; SD=standard deviation; SE=standard error
WhtS=waist-height ratio; WHC=waist-hip ratio; CP= chronic periodontitis; TL= tooth loss; PI=plaque index; GI=gingivitis/gingival regression; BOP=bleeding on probing; BS=bariatric surgery; FMBS=full-mouth gingival
bleeding scores
18
Table 3: Association between obesity and periodontitis by gender
F M
Gorman et al 27 21-84 Obesity Periodontitis (PD) + 1.40 (1.02-1.91)
201238
Jimenez et al 20 40-75 Obesity Periodontitis + 1.30 (1.17-1.45)
201240
Morita et al 5 21-69 Obesity Periodontitis + NS 3.24 (1.32-7.94)
201142 1.44 (0.97-2.14)
Saxlin et al 4 30-59 Obesity Periodontitis NS NS 1.3 (0.7-2.1)
201043
Castilhos et al 8 15-23 Obesity Periodontitis NS NS 1.01 (0.25-4.0)
201244
F: female; M: male
F M
19
Table 5: Association between weight gain and periodontitis by gender
F M
Gorman et al 27 21-84 Weight gain Periodontitis + 1.05 (1.01-1.09)
201238
Gorman et al 30 21-84 Weight gain Periodontitis + P<.01
201239
Linden et al 12 50-60 Weight gain Periodontitis NS 1.33 (0.95-1.86)
200741
Ekuni et al 3 17-19 Weight gain Periodontitis + + 1.95 (1.05-3.57)
201445 (BMI)
F:female; M: male
F M
Gorman et al 30 21-84 Waist circumference Periodontitis + P<.05
201239
Gorman et al 27 21-84 Waist circumference Periodontitis + 1.03 (1.01-1.05)
201238
Jimenez et al 20 40-75 Waist circumference Periodontitis + 1.27 (1.11-1.46)
201240
Castilhos et al 8 15-23 Waist circumference Periodontitis + + 2.03 (1.20-3.45)
201244
F:female; M: male
20
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