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Accepted Article
Article Type: Original Article
Prediabetes and well controlled diabetes are not associated with periodontal disease: the
SHIP Trend Study
Running title: Prediabetes and periodontitis
Bernd Kowall 1,2, Birte Holtfreter 3, Henry Völzke 4 , Sabine Schipf 4, Torsten Mundt5,
Wolfgang Rathmann 1 , Thomas Kocher 3
1
German Diabetes Center, Institute of Biometrics and Epidemiology, Düsseldorf, Germany
2
Center of Clinical Epidemiology, c/o Institute of Medical Informatics, Biometry and
Epidemiology (IMIBE), University Hospital Essen, Germany
3
Unit of Periodontology, Department of Restorative Dentistry, Periodontology, and
Endodontology, University Medicine, Ernst-Moritz-Arndt-University Greifswald, Germany
4
Institute for Community Medicine, University Medicine, Ernst-Moritz-Arndt-University
Greifswald, Germany
5
Department of Prosthodontics, Gerodontology and Biomaterials, Dental School, University
Medicine, Ernst-Moritz-Arndt-University Greifswald, Germany
Correspondence author:
Dr. Bernd Kowall
Center of Clinical Epidemiology
c/o Institute of Medical Informatics, Biometry and Epidemiology (IMIBE)
Hufelandstraße 55
45147 Essen
Tel: +49-201-92239-295
This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1111/jcpe.12391
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Fax: +49-201-92239-333
Mail: bernd.kowall@uk-essen.de
Abstract
Aim. To examine associations of prediabetes and well controlled diabetes with periodontitis.
Materials and methods. The Study of Health in Pomerania (SHIP)-Trend is a cross-sectional
survey in North-Eastern Germany including 3,086 participants (49.4% men; age 20–82 years).
Clinical attachment loss (CAL) and periodontal probing depth (PPD) were assessed applying a
random half-mouth protocol. The number of teeth was determined. Prediabetes comprised
impaired fasting glucose and impaired glucose tolerance. Previously known diabetes was
defined as well controlled if glycated hemoglobin (HbA1c) was <7.0%. Participants were
categorized as follows: normal glucose tolerance (NGT), prediabetes, newly detected type 2
diabetes (T2DM), known T2DM with HbA1c<7.0%, known T2DM with HbA1c≥7.0%.
Results. Prediabetes was neither associated with mean CAL and PPD in multivariable
adjusted linear regression models nor with edentulism (OR=1.09 (95%-CI: 0.69-1.71)) and
number of teeth (OR=0.96 (95%-CI: 0.75-1.22), lowest quartile versus higher quartiles) in
logistic regression models. Associations with mean CAL and edentulism were stronger in
poorly controlled previously known diabetes than in well controlled previously known
diabetes (for edentulism: OR=2.19 (95%-CI: 1.18-4.05), and OR=1.40 (95%-CI: 0.82-2.38),
respectively, for comparison with NGT).
Conclusions. Periodontitis and edentulism were associated with poorly controlled T2DM, but
not with prediabetes and well controlled diabetes.
Keywords: periodontitis; periodontal diseases; periodontal attachment loss;; mouth,
edentulous; prediabetic state; hyperglycemia; glucose intolerance; diabetes mellitus
1. Introduction
There is strong evidence that periodontitis is associated with diabetes mellitus (Khader2006;
Chavarry et al 2009; Demmer et al 2010; Lalla & Papapanou 2011; Preshaw et al 2012;
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Borgnakke et al. 2013). Two meta-analyses showed that mean periodontal probing depth
(PPD) and mean clinical attachment loss (CAL) are higher in subjects with than in subjects
without diabetes (Khader et al 2006; Chavarry et al 2009). Because the association between
diabetes and periodontitis is bidirectional, periodontitis also has a negative impact on
glucose regulation. Thus, periodontal treatment such as scaling and root planing was
suggested to improve glycemic control. Indeed, these interventions reduced glycated
hemoglobin (HbA1c) in type 2 diabetes patients by roughly 0.4%, as reported in recent metaanalyses (Teeuw et al 2010; Engebretson & Kocher 2013; Wang et al 2014). However, little is
known about associations between periodontitis and moderate glycemic disorders such as
prediabetes and well controlled diabetes.
Prediabetes is a state of elevated levels of blood glucose that still are below the threshold
for manifest diabetes (WHO 1999; American Diabetes Association 2014). Prediabetes may be
identified by impaired fasting glucose (IFG) and/or impaired glucose tolerance (IGT), two
conditions that are both highly prevalent in Western countries (International Diabetes
Federation 2014). There are only few studies on the association between periodontal
disease and prediabetes reporting conflicting results. In addition, some studies have
methodical flaws such as small sample sizes or incomplete/insufficient adjustment for
confounders. Results are ambiguous for associations between periodontitis and IGT (Nelson
et al 1990; Emrich et al 1991; Noack et al 2000; Maragumeet al 2003; Saito et al 2004; Saito
et al 2005; Saito et al 2006) as well as for associations between periodontitis and IFG (Zadik
et al 2003; Choi et al 2011; Wang et al 2009). For example, in two reports from the same
research group on the association between IGT and PPD, findings were contrasting: an
association was seen in a mixed-sex Japanese study group (Saito et al 2004), but not in
Japanese women (Saito et al 2005). Likewise, an association between IFG and periodontitis
was reported in only one (Choi et al 2011) of two recent studies from the National Health
and Nutrition Examination Survey (NHANES) (Choi et al 2011; Arora et al 2014).
Moreover, only few studies considered whether periodontal health is associated with
glycemic control in persons with diabetes (Sandberg et al 2000; Tsai et al 2002; Chuang et al
2005; Peck et al 2006; Campus et al 2005; Javed et al 2007 ; Silvestre et al 2009; Preshaw et
al 2010 ; Haseeb et al 2012 ; Demmer et al 2012). Most, but not all, of these studies showed
a worse periodontal status in poorly controlled diabetes. However, several of these studies
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suffered from drawbacks such as lack of adjustment for confounders (Haseeb et al 2012;
Campus et al 2005), small sample size (Javed et al 2007; Peck et al 2006), and lack of a
constant, globally accepted HbA1c cut-off value to define poorly controlled diabetes.
Thus, there is still a need for studies with a large sample size and well characterized
participants to clarify the association between periodontal disease and moderate glycemic
disorders. The aim of the present study is to assess whether periodontitis, low number of
teeth and edentulism are more prevalent in subjects with prediabetes and well controlled
diabetes than in subjects with normal glucose tolerance using data from the large,
population-based Study of Health in Pomerania (SHIP)-Trend study.
2. Materials and Methods
Study population
SHIP-Trend is a cross-sectional survey conducted in West Pomerania, a region in the NorthEastern part of Germany (Völzke et al 2011) – a follow-up of the study will run from 2016 2018. Examinations were conducted between 2008 and 2012. A stratified random sample of
10,000 adults aged 20–82 years was drawn from population registries. Inclusion criteria
were residency in the study region and - to ensure the individual had lived in the area (or in
Germany) for a long time - German citizenship. The only exclusion criterion was participation
in SHIP-0, another population study started in 1997. Sample selection was facilitated by
centralization of local population registries in the Federal State of Mecklenburg/West
Pomerania. Stratification variables were age, sex and city/county of residence. Subjects were
sampled from the regional strata with a probability proportional to size design. After
exclusion of migrated (N=851) and deceased (N=323) persons, the net sample included 8,826
persons. Because of several reasons (241 did not answer, 3367 declined participation, 549
did not keep the appointment and 249 agreed without an appointment) 4,420 subjects were
finally enrolled in the study, corresponding to a response rate of 50.1%.
Dental examination
Periodontal probing depth (PPD) and clinical attachment loss (CAL) were assessed at four
sites per tooth (mesiobuccal, midbuccal, distobuccal and midlingual/midpalatinal) according
to the random half-mouth method, excluding third molars. A manual periodontal probe
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(PCPUNC 15, Hu-Friedy, Chicago, IL, USA) was used. Measurements were mathematically
rounded to the nearest (or closest) whole millimeter. PPD was measured as the distance
between the free gingival margin (FGM) and the bottom of the sulcus or periodontal pocket.
If the cemento-enamel junction (CEJ) was located subgingivally, CAL was calculated as PPD
minus the distance between free gingival margin (FGM) and CEJ. If recession was present at
the examined site, CAL was directly measured as the distance between CEJ and the pocket
base. Where the determination of the CEJ was impossible due to wedge-shaped defects or
restorations, attachment level was not recorded. The number of all natural teeth present
(excluding third molars) was recorded, and hence bridge abutments, prostheses, and dental
implants were excluded.
Every 6–12 months, all five examiners performed calibration exercises on subjects not
associated with the study. Intra-rater correlations for CAL measurements ranged from 0.67
to 0.89 and inter-rater correlation was 0.70. For PPD measurements, the examiners yielded
intra-rater correlations between 0.68 and 0.88 and an inter-rater correlation of 0.72.
Definition of periodontitis
We used one periodontitis case definition (Tonetti & Claffey 2005) and various continuous
and dichotomous measures to assess the periodontal and dental status. According to the 5th
European Workshop in Periodontology (EWP) (Tonetti & Claffey 2005), we defined incipient
periodontitis as presence of proximal CAL of ≥3 mm in ≥2 non-adjacent teeth. Manifest
periodontitis was defined as presence of proximal CAL of ≥5 mm in ≥30% of teeth, thereby
identifying “cases with substantial extent and severity” (Tonetti & Claffey 2005). For the EWP
case definition, analyses were restricted to those with at least two sites with CAL
measurements, as it necessitates the presence of at least two teeth (Tonetti & Claffey 2005).
Mean CAL/PPD equals the average CAL/PPD over all assessed sites.
Laboratory measurements
HbA1c was measured by high-performance liquid chromatography with spectrophotometric
detection (Diamat Analyzer; Bio-Rad, Munich, Germany) and a coefficient of variation of
1.5%. For the oral glucose tolerance test (OGTT), fasting venous blood is sampled, and 75 g
of anhydrous glucose with blackcurrant flavor (Dextro OGT, Boehringer Mannheim,
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Mannheim, Germany) was given orally. Two hours later, a second venous blood sample for
determination of plasma glucose concentrations was taken (WHO1999). Fasting glucose,
total cholesterol, high density lipoprotein (HDL) cholesterol, and triglycerides were
measured photometrically using the Dimension Vista® 500 analytical system (Siemens AG,
Erlangen, Germany).
Covariates assessments
Data on behavioral and socio-economic variables were retrieved from the computer-aided
personal interview. Education was categorized as <10/10/>10 years of schooling. Smoking
was categorized as never, former and current smoking. The self-reported physician’s
diagnosis of diabetes mellitus was recorded.
Weight was measured wearing light clothing without shoes using a calibrated scale (S20,
SOEHNLE-Waagen GmbH) and a linear encoder (SOEHNLE-Waagen GmbH). The body mass
index (BMI; body weight in kg divided by the height in meters squared) was calculated.
Ascertainment of prediabetes and diabetes
Impaired fasting glucose (IFG) and impaired glucose tolerance (IGT) were defined according
to the 1999 WHO diagnostic criteria (IFG: 6.1 – 6.9 mmol/l fasting glucose, IGT: 7.8 – 11.0
mmol/l 2h-glucose). Prediabetes comprised isolated IFG, isolated IGT, and combined IFG and
IGT. Newly detected type 2 diabetes mellitus (T2DM) was defined as ≥7.0 mmol/l fasting or
≥11.1 mmol/l 2 h post glucose load from OGTTs. Known T2DM was defined as self-reported
physician’s diagnosis or anti-diabetic medication (ATC Code A10). Participants with selfreport of diabetes were asked to specify the type of diabetes. T2DM subjects were further
classified as having good (HbA1c<7.0%) or poor metabolic control (HbA1c≥7.0%).
Participants were categorized into five groups as follows: normal glucose tolerance (NGT),
prediabetes, newly detected T2DM, known T2DM with HbA1c<7.0%, and known T2DM with
HbA1c≥7.0%.
Statistical methods
Participants were excluded from analyses in case of 1) missing data on glucose regulation
(n=715) or prevalent type 1 diabetes (n=9), 2) missing data on covariates (n=38), and 3)
missing data on periodontitis (n=572) (or missing data on number of teeth when edentulism
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or number of teeth were the dependent variables (n=35)). The analyses on periodontitis
included 3,086 participants, and the analyses on edentulism and number of teeth included
3,623 participants.
Five sets of binomial logistic regression analyses were done with the following dependent
variables: 1) periodontitis defined by EWP case definition (incipient / manifest vs no), 2)
percentage of sites with CAL ≥ 4mm (upper quartile Q4 versus the three lower quartiles Q1Q3), 3) mean PPD (Q4 vs Q1-Q3), 4) edentulism (yes/no), 5) number of teeth (lowest quartile
Q1 versus the three higher quartiles Q2-Q4). The independent variable was glucose
regulation (known T2DM with HbA1c≥7.0%, known T2DM with HbA1c<7.0%, newly detected
T2DM, prediabetes, and NGT as the reference category). For each of the five sets of logistic
regression analyses, four different models were fitted: 1) an unadjusted model, 2) a model
adjusted for age and sex, 3) a model adjusted for age, sex, and BMI, 4) a model adjusted for
age, sex, BMI, education, smoking, alcohol consumption, total cholesterol, HDL cholesterol,
and triglycerides. Fully adjusted logistic regression analyses were replicated with
subcategories of prediabetes (isolated IFG, isolated IGT, and combined IFG and IGT) instead
of one comprehensive category of prediabetes.
Two sets of linear regression analyses were done with the square root of mean CAL and the
square root of mean PPD, respectively, as dependent variables. CAL and PPD were square
rooted to fulfill the condition that residuals are normally distributed in linear regression
modelling. Categories of glucose regulation and model adjustment were adopted from
logistic regression analyses.
Fully adjusted logistic and linear regression analyses were replicated using three categories
of HbA1c (HbA1c ≥ 6.5%; 5.7% ≤ HbA1c < 6.5%; HbA1c < 5.7%) instead of categories of
glucose regulation (for results and discussion of these analyses cf. supplementary material
2).
The level of statistical significance was 5%. The analyses were carried out using SAS version
9.3 (SAS Institute, Cary, NC).
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3. Results
Subject characteristics
Table 1 shows the baseline characteristics of the participants according to categories of
glucose regulation. 365 persons (11.8%) of the participants had diabetes, 164 of whom
(44.9%) were unaware of having the disease. In unadjusted comparisons, participants with
poorer glucose regulation tended to be older and more often male, had a higher BMI, and
were less educated. Moreover, they tended to have a greater extent of CAL ≥4 mm, higher
mean PPD, a lower number of teeth or more often periodontitis as defined by the EWP case
definition. Age, BMI, proportion of males, extent of CAL ≥4 mm and the proportion of
manifest periodontitis using the EWP case definition tended to be higher in subjects with
previously known diabetes than in subjects with newly detected diabetes. Only one third of
the participants with previously known diabetes had an HbA1c level ≥7.0%, and among these
64 subjects, 44 had an HbA1c level ≤8.0%, and three had an HbA1c level ≥10.0%.
Associations between prediabetes and binary periodontitis measures
In unadjusted logistic regression models (Table 2, Model 1), subjects with prediabetes and
previously known or newly detected T2DM were more likely to have periodontitis by all
three selected criteria of periodontitis, edentulism and low number of teeth than subjects
with normal glucose tolerance. In age-sex adjusted models (Model 2), odds ratios (ORs) are
strongly reduced for both prediabetes and T2DM. After adjustment for age, sex and BMI
(Model 3), prediabetes was no longer associated with periodontitis, edentulism and low
number of teeth. In fully adjusted models (Model 4), well controlled known diabetes was not
associated with edentulism (OR=1.40 (95%-CI: 0.82-2.38)) as opposed to poorly controlled
known diabetes (OR=2.19, 95%-CI: 1.18 – 4.05). For low number of teeth and all measures of
periodontitis, associations were stronger with uncontrolled than with controlled known
diabetes, albeit not significant after full adjustment. Furthermore, newly detected diabetes
was associated with high mean PPD in the fully adjusted model (OR=1.50, 95%-CI: 1.04 –
2.17). Replications of the fully adjusted logistic regression analyses with subcategories of
prediabetes did not show significant associations between IFG and IGT, respectively, and
periodontitis, edentulism and low number of teeth (cf. supplementary table 1).
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Linear association between prediabetes and mean CAL/PPD
In unadjusted linear regression models (Table 3, Model 1), prediabetes, newly detected and
previously known diabetes, respectively, were statistically significantly associated with mean
CAL and mean PPD (both square rooted). For prediabetes, these associations were no longer
significant after adjustment for age, sex, and BMI (Model 3). Compared to NGT, square root
of mean CAL was significantly higher in poorly controlled (p=0.02), but not in well controlled
known diabetes (p=0.29) in the fully adjusted model 4.
4. Discussion
In SHIP-Trend, a large population-based study, we did not find consistent associations
between prediabetes defined by glucose criteria, i.e. fasting and 2-hour glucose, and
different criteria of periodontitis, edentulism and low number of teeth, respectively.
Furthermore, our results suggest that it is important to differentiate between poorly and
well controlled previously known diabetes. We found no increased prevalence of
periodontitis and edentulism in well controlled diabetes whereas mean CAL and edentulism
were associated with poorly controlled diabetes.
The latter result lends plausibility to the result of no association between periodontitis and
prediabetes. Glucose regulation is better in prediabetes than in well controlled previously
known diabetes as can be seen from the corresponding glucose parameters. Thus, if there is
no increase in prevalence of periodontitis and edentulism in well controlled previously
known diabetes compared to NGT, it is even more unlikely in prediabetes. Associations with
poorly controlled diabetes were somewhat weaker than expected (significant associations
for mean CAL and edentulism, but not for PPD, periodontitis defined by the EWP case
definition, and number of teeth). This may be due to two reasons: the low number of
participants with poorly controlled diabetes in our study, and the fact that most of these
subjects did not have a very severely increased level of HbA1c above 8.0%.
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Diabetes and edentulism
Associations between glucose regulation and tooth loss have only rarely been investigated.
In cross-sectional analyses from the National Health and Nutrition Examination Survey
(NHANES), subjects with diabetes were more likely to be edentulous than subjects without
diabetes (OR=2.25, 95%-CI: 1.19 – 4.21, after adjustment for age, sex, ethnicity,
socioeconomic status, dental insurance, and smoking status) (Patel el al 2013). However, in
the NHANES study, control of HbA1c was not taken into account.
Degree of glycemic control and periodontitis
Our results concerning glycemic control of diabetes and periodontal health are in line with
most other studies on this topic. Only in two studies, no difference in periodontal health
between poorly and well controlled diabetes was reported (Sandberg et al 2000; Chuang et
al 2005). However, studies reporting such a difference partly used very high HbA1c cut-offs
to define poorly controlled diabetes like 8% (Campus et al 2005) or even 9% (Tsai et al 2002;
Chuang et al 2005), were lacking adequate confounder adjustment (Haseeb et al 2012;
Campus et al 2005; Chuang et al 2005; Sandberg et al 2000), or included very few persons
with well controlled type 2 diabetes (Javed et al 2007; Peck et al 2006; Chuang et al 2005;
Sandberg et al 2000). Whereas most studies on glycemic control and periodontitis were
cross-sectional, Demmer et al. (2012) found that PPD and CAL deteriorated over five years in
poorly controlled, but not in well controlled type 2 diabetes. Along the same line, incident
tooth loss was higher in poorly controlled subjects.
The present study, SHIP-Trend, was carried out in the same region as SHIP-0, another
population-based study which took place about ten years earlier, but examined a population
sample independent of SHIP-0. In SHIP-0, the association between previously known
diabetes as a whole and periodontal health was stronger than in the present study (Kaur et
al 2009). This may be explained by the fact that the proportion of poorly controlled diabetes
was considerably higher in SHIP-0 than in SHIP-Trend (47% versus 32%). Thus, the
association between diabetes and periodontitis may become weaker if control of diabetes
improves, and for an appropriate assessment of this association, poorly and well controlled
diabetes should be differentiated.
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Studies on the association between prediabetes and periodontitis
The few other studies on the association between prediabetes and periodontitis led to
conflicting results. Partly, this may be due to different definitions of periodontitis or
prediabetes (e.g., IFG defined as fasting glucose 100-125mg/dl or 110-125mg/dl; subjects
with IGT were partly included in the IFG category when 2-hour glucose was not measured).
Moreover, some studies have important limitations:
In a study of Israeli males, Zadik et al. (2010) found an association between IFG and alveolar
bone loss. However, there was apparently no adjustment for potential confounders. Other
studies suffered from small sample sizes. In a study of German patients by Noack et al
(2000), participants with IGT did not differ from those with normal glucose tolerance with
regard to probing depth. However, only 56 subjects with IGT and only 27 controls were
included in the analysis. In a Japanese study (Saito et al 2006), IGT was associated with high
alveolar bone loss but only 38 persons with IGT were included. In a study among Japanese
men by Maragume et al (2003), IGT was not associated with alveolar bone loss, but IGT was
compared to NGT + IFG and not to NGT alone. Several studies were based on only one
criterion of periodontitis. However, probing depth and attachment loss, although strongly
correlated, differ in their meaning. Probing depth reflects current inflammation, whereas
attachment loss reflects history of periodontal destruction. Therefore, both probing depth
and attachment loss should be considered in analyses.
Two recent studies using NHANES data also provided inconclusive results. In multivariable
adjusted models, Choi et al (2011) found a higher prevalence of IFG when the highest
quintile of CAL was compared to the lowest quintile (OR=1.55, 95%-CI: 1.16 – 2.07), whereas
Arora et al. (2014) found no association between different criteria of periodontitis and IFG.
In the latter study, however, mean PPD, but not mean CAL was associated with IGT: persons
with mean PPD above the 75th percentile were more likely to have IGT than persons with
smaller mean PPD after multivariable adjustment (OR=2.05, 95%-CI: 1.24 – 3.39).
Limitations and strengths
Strengths of our study are its population-based approach, the large sample size, the use of
several measures of periodontitis, and the comprehensive adjustment for potential
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confounders. This is important because in several earlier studies exploring whether
prediabetes and degree of glycemic control, respectively, are related to periodontal health,
confounder adjustment was limited and sample size was low.
One limitation of the study is its cross-sectional design, because of which no causative
relationships could be established. Further, the number of subjects with poorly controlled
previously known diabetes was quite low in SHIP-Trend which may reflect improved
management of diabetes in Pomerania over the last decade. In addition, known diabetes
was not validated by contacting physicians. However, in general, self-reported diagnoses of
diabetes are known to be valid, and large positive predictive values were reported (Pastorino
et al 2014; Espelt et al 2012). Moreover, periodontal measurements were recorded halfmouth at four sites per tooth, which is known to be associated with an underestimation of
periodontal disease severity (Kingmann et al 2008). Specifically, only one lingual site,
namely mid-lingually but no approximal located lingual site was probed, which most likely
has led to substantial underestimation of periodontal disease. The associated misclassification
might further result in the dilution of effect estimates towards the null effect (Beck et al
1999).
Conclusion
In this population-based SHIP-Trend study, there was no association between glucose-based
prediabetes and periodontitis. Associations with periodontitis were seen in poorly, but not in
well controlled previously known diabetes. Both results together suggest that only severe
glycemic disorders are related to a greater prevalence of periodontitis and tooth
loss/edentulism. There is still a need for longitudinal studies to assess changes in periodontal
status in subjects with prediabetes and well controlled diabetes.
Conflict of interest and sources of funding statement. The authors declare that there are no
conflicts of interest in this study. This work is part of the research project Greifswald
Approach to Individualized Medicine (GANI_MED). The GANI_MED consortium is funded by
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the Federal Ministry of Education and Research and the Ministry of Cultural Affairs of the
Federal State of Mecklenburg – West Pomerania (03IS2061A). SHIP is part of the Community
Medicine Research net (CMR) of the University of Greifswald, Germany, which is funded by
the Federal Ministry of Education and Research (grant no. ZZ9603) and the Ministry of
Cultural Affairs as well as the Social Ministry of the Federal State of Mecklenburg-West
Pomerania (http://www.community-medicine.de). BH was supported by an unlimited
educational grant from GABA, Switzerland.
Clinical relevance
Scientific rationale for the study: In a large adult study population in North-Eastern Germany,
the associations between prediabetes, well and poorly controlled T2DM and periodontal
disease and edentulism, respectively, were assessed.
Principal findings: The risk of having periodontitis and edentulism was increased in poorly
controlled T2DM (i.e., HbA1c≥7.0%), but not in well controlled T2DM (HbA1c<7.0%) and
prediabetes.
Practical implications: A diabetes check should be made in patients with periodontitis, and
the patients’ periodontal health status should be checked in the management of type 2
diabetes. However, further longitudinal studies are warranted to assess effects of
improvements of glycemic control on periodontitis.
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Table 1. Characteristics of participants with complete periodontal data by categories of glucose
regulation (N=3,086) a
N (%)
Age
Sex (male) (%)
Known T2DM,
HbA1c < 7.0%
Known
T2DM,
HbA1c ≥
7.0%
164
137
64
(18.7%)
(5.3%)
(4.4%)
(2.1%)
44.8 ± 13.6
54.6 ± 12.7
60.1 ± 9.7
63.6 ± 9.3
63.4 ± 8.8
46.3
54.9
57.3
61.3
59.4
NGT
Prediabetes
2145
(69.5%)
576
Newly
detected
T2DM
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BMI (kg/m2)
26.4 ± 4.4
29.6 ± 4.9
30.9 ± 5.1
32.8 ± 5.0
34.1 ± 5.7
Education
11.1 / 57.9
/ 31.0
20.7 / 54.0 /
25.4
29.9 / 44.5 /
25.6
46.7 /36.5 /
16.8
43.8 / 43.8 /
12.5
35.3 / 32.6
/ 32.0
42.5 / 38.7 /
18.8
47.0 / 38.4 /
14.6
34.3 / 56.2 /
9.5
31.3 / 54.7 /
14.1
Alcohol consumption
(g/d)
8.8 ± 13.0
10.3 ± 13.3
10.0 ± 17.0
7.4 ± 11.0
7.7 ± 13.6
Total cholesterol
(mmol /l)
5.4 ± 1.1
5.7 ± 1.1
5.7 ± 1.2
5.1 ± 1.2
5.2 ± 1.1
Total cholesterol
(mg/dl)
207.3± 41.7
219.1 ± 41.5
218.9 ± 45.4
198.4 ± 47.3
202.5 ± 44.1
HDL cholesterol
(mmol /l)
1.5 ± 0.4
1.4 ± 0.4
1.3 ± 0.4
1.3 ± 0.3
1.2 ± 0.3
HDL cholesterol
(mg/dl)
57.1± 14.2
54.0 ± 13.9
50.9 ± 14.3
49.2 ± 11.5
44.7 ± 10.9
Triglycerides
1.15
(0.83¸1.66)
1.51
1.95
1.83
2.63
(1.14; 2.11)
(1.35; 2.74)
(1.35; 2.72)
(1.88; 3.46)
134.8
174.1
163.4
234.8
(120.5,244.6)
(120.5,242.9)
(167.9,308.9)
<10/10/>10 years
(%)
Smoking
Never/former/
current (%)
(mmol /l)
Triglycerides
(mg/dl)
102.7
(74.1,148.2) (101.8,188.4)
Fasting plasma
glucose (mmol/l)
5.2 ± 0.4
5.9 ± 0.6
7.3 ± 1.4
7.6 ± 2.2
11.5 ± 3.9
Fasting plasma
glucose (mg/dl)
93.5 ± 8.0
106.9 ± 10.5
130.6 ± 25.2
136.7 ± 39.8
208.1 ± 69.6
HbA1c value [%]
5.08 ± 0.53
5.31 ± 0.54
5.83 ± 0.84
6.02 ± 0.54
8.02 ± 1.27
4.2
19.8
32.3
40.5
57.3
(0, 25.0)
(4.0, 50.0)
(10.9, 64.6)
(16.7, 80.0)
(22.7, 89.6)
18.2
32.8
43.9
50.4
60.9
Percentage of sites
with CAL ≥ 4 mm (%)
Percentage of sites
with CAL ≥ 4 mm
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Accepted Article
> 37.5 (%)b
Percentage of sites
with CAL ≥ 5 mm (%)
0
5.0
12.5
20.0
26.0
(0, 8.5)
(0, 25.5)
(0, 40.1)
(5.8, 54.2)
(7.7, 70.4)
1.7
2.5
3.0
3.2
3.6
(1.1, 2.7)
(1.7, 3.6)
(2.1, 4.1)
(2.3, 4.9)
(2.7, 5.5)
4.2
9.1
15.0
12.5
17.1
(0, 15.0)
(2.1, 22.8)
(2.1, 31.5)
(2.8, 32.5)
(4.6, 33.0)
0
0
0
0
0
(0,0)
(0, 1.9)
(0, 3.2)
(0, 2.3)
(0, 4.5)
2.3
2.5
2.6
2.6
2.8
(2.1, 2.7)
(2.2, 2.9)
(2.3, 3.1)
(2.3, 3.2)
(2.3, 3.1)
Mean PPD > 2.75
mm (%) c
19.8
32.8
42.7
40.9
48.4
Number of teeth
25
24
21
21
19
(22, 28)
(19, 26)
(17, 25)
(14, 24)
(11, 23)
40.9 / 39.9
/ 19.2
22.1 / 44.1 /
33.9
12.8 / 40.9 /
46.3
12.4 / 34.3 /
53.3
6.3 / 31.3 /
62.5
Mean CAL (mm)
Percentage of sites
with
PPD ≥ 4 mm (%)
Percentage of sites
with
PPD ≥ 6 mm (%)
Mean PPD (mm)
EWP case definition
(no/ incipient /
manifest
periodontitis)
NGT: normal glucose tolerance; T2DM: type 2 diabetes mellitus; CAL: clinical attachment loss; PPD,
periodontal probing depth EWP: European Workshop in Periodontology
a
mean ± standard deviation, median (first quartile, third quartile), or proportion (%)
b
For each individual, the proportion of teeth with CAL ≥ 4 mm was measured. 37.5% is the third
quartile of these proportions in the whole study group.
c
2.75 mm is the third quartile of mean PPD in the whole study group.
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Accepted Article
Table 2. Odds ratios (95% confidence intervals) for having different measures of periodontitis and
tooth loss/edentulism by categories of glucose control
Model 1
Model 2
Model 3
Model 4
OR (95% CI)
OR (95% CI)
OR (95% CI)
OR (95% CI)
2.57 (0.91 – 7.28)
2.14 (0.75 – 6.10)
1.60 (0.55 – 4.63)
1.17 (0.67 – 2.03)
1.01 (0.58 – 1.78)
0.94 (0.52 – 1.67)
EWP case definition (incipient / manifest vs no)
Known T2DM,
HbA1c ≥ 7.0%
Known T2DM,
HbA1c < 7.0%
10.39
(3.76 – 28.70)
4.89
(2.92 – 8.19)
newly detected
T2DM
4.72 (2.96 – 7.52)
1.48 (0.90 – 2.42)
1.35 (0.82 – 2.23)
1.27 (0.76 – 2.12)
Prediabetes
2.45 (1.98 – 3.04)
1.27
1.19 (0.93 – 1.53)
1.16 (0.90 – 1.50)
1
1
(0.997– 1.62)
NGT (reference)
1
1
Percentage of sites with CAL ≥ 4mm (Q4 vs Q1-Q3)
Known T2DM,
HbA1c ≥ 7.0%
7.00 (4.19 –
11.70)
1.95 (1.12 – 3.42)
1.71 (0.96 – 3.04)
1.36 (0.75 – 2.49)
Known T2DM,
HbA1c < 7.0%
4.55 (3.20 – 6.48)
1.13 (0.76 – 1.68)
1.02 (0.68 – 1.54)
0.94 (0.61 – 1.45)
newly detected
T2DM
3.51 (2.53 – 4.87)
1.19 (0.83 – 1.72)
1.11 (0.76 – 1.61)
1.05 (0.71 – 1.55)
Prediabetes
2.19 (1.78 – 2.69)
1.05 (0.83 – 1.33)
1.00 (0.78 – 1.27)
0.98 (0.77 – 1.26)
1
1
1
1
Known T2DM,
HbA1c ≥ 7.0%
3.80 (2.30 – 6.28)
1.92 (1.14 – 3.24)
1.48 (0.87 – 2.52)
1.31 (0.75 – 2.30)
Known T2DM,
HbA1c < 7.0%
2.80 (1.96 – 4.00)
1.37 (0.94 – 2.01)
1.10 (0.75 – 1.64)
1.13 (0.75 – 1.71)
newly detected
T2DM
3.01 (2.17 – 4.18)
1.73 (1.23 – 2.44)
1.49 (1.05 – 2.12)
1.50 (1.04 – 2.17)
NGT (reference)
Mean PPD (Q4 vs Q1-Q3)
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Prediabetes
1.98 (1.61 – 2.42)
1.36 (1.10 – 1.69)
1.23 (0.98 – 1.53)
1.24 (0.99 – 1.57)
1
1
1
1
12.23
3.82
3.03 (1.75 – 5.22)
2.19 (1.18 – 4.05)
(7.53 – 19.87)
(2.26 – 6.43)
6.98
1.98
1.59 (0.97 – 2.62)
1.40 (0.82 – 2.38)
(4.49 – 10.83)
(1.23 – 3.17)
newly detected
T2DM
4.01 (2.37 – 6.81)
1.47 (0.85 – 2.56)
1.26 (0.72 – 2.22)
1.13 (0.63 – 2.06)
Prediabetes
2.64 (1.76 – 3.95)
1.32 (0.86 – 2.01)
1.18 (0.77 – 1.82)
1.06 (0.68 – 1.67)
1
1
1
1
2.89 (1.89 – 4.43)
2.16 (1.40 – 3.35)
1.49 (0.92 – 2.40)
NGT (reference)
Edentulism (yes / no)
Known T2DM,
HbA1c ≥ 7.0%
Known T2DM,
HbA1c < 7.0%
NGT (reference)
Number of teeth (Q1 vs Q2-Q4)
Known T2DM,
HbA1c ≥ 7.0%
9.37
(6.40 – 13.72)
Known T2DM,
HbA1c < 7.0%
6.28 (4.76 – 8.28)
1.65 (1.20 – 2.27)
1.30 (0.93 – 1.80)
1.05 (0.74 – 1.50)
newly detected
T2DM
4.02 (3.01 – 5.36)
1.41 (1.01 – 1.95)
1.18 (0.85 – 1.65)
1.05 (0.73 – 1.49)
Prediabetes
2.26 (1.86 – 2.74)
1.10 (0.88 – 1.39)
0.98 (0.77 – 1.23)
0.96 (0.75 – 1.22)
1
1
1
1
NGT (reference)
EWP: European Workshop in Periodontology; NGT: normal glucose tolerance; T2DM: type 2 diabetes
mellitus; Q4: highest quartile; Q1: lowest quartile; OR: odds ratio; CI: confidence interval; CAL: clinical
attachment loss; PPD: periodontal probing depth
Model 1: no adjustment
Model 2: adjusted for age and sex
Model 3: adjusted for age, sex, and BMI
Model 4: Adjusted for age, sex, BMI, education, smoking, alcohol consumption, total cholesterol, HDL
cholesterol, and triglycerides
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Accepted Article
Table 3. Beta regression coefficients (95% confidence intervals) for the association between
categories of glucose regulation, and square root of mean clinical attachment loss and mean
periodontal probing depth, respectively a
Model 1
Model 2
Model 3
Model 4
Square root of mean clinical attachment loss
Known
T2DM,
HbA1c ≥
7.0%
Known
T2DM,
HbA1c <
7.0%
newly
detected
T2DM
Prediabetes
ß (95%
CI)
p
ß (95% CI)
p
ß (95% CI)
p
ß (95%
CI)
p
0.62
<0.001
0.18
<0.001
0.16
0.002
0.13
0.02
(0.49;
0.74)
0.50
(0.0838;
0.2850)
<0.001
(0.42;
0.59)
0.40
<0.001
0
0.05
0.05
<0.001
0.02
0.14
0.04
0
0.22
0.21
0.02
0.28
0
0.29
0.03
0.39
(-0.04;
0.09)
0.42
(-0.02;
0.05)
-
0.04
(-0.03;
0.11)
(-0.03;
0.10)
(-0.02;
0.06)
-
(0.02;
0.23)
(-0.03;
0.12)
(-0.02;
0.11)
(0.21;
0.30)
NGT
(reference)
0.08
(-0.01;
0.13)
(0.33;
0.48)
0.25
0.06
(0.06;
0.27)
0.02
0.41
(-0.02;
0.05)
-
0
-
Square root of mean periodontal probing depth
Known
T2DM,
HbA1c ≥
7.0%
Known
T2DM,
HbA1c <
7.0%
newly
detected
ß (95%
CI)
p
ß (95% CI)
p
ß (95% CI)
p
ß (95%
CI)
p
0.13
<0.001
0.06
0.007
0.04
0.11
0.02
0.35
(0.09;
0.18)
0.10
(0.02;
0.10)
<0.001
(0.06;
0.13)
0.10
0.02
(-0.01;
0.08)
0.13
(-0.01;
0.06)
<0.001
0.04
0.004
(-0.02;
0.07)
0.80
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0.03
0.83
(-0.03;
0.03)
(-0.03;
0.003
0.004
0.04
0.03
0.08
Accepted Article
T2DM
(0.07;
0.13)
Prediabetes
0.06
(0.02;
0.07)
<0.001
(0.04;
0.08)
NGT
(reference)
0
0.02
(0.001;
0.06)
0.01
(0.01;
0.04)
-
0
0.01
(-0.003;
0.05)
0.14
(-0.004;
0.03)
-
0
0.01
0.17
(-0.005;
0.03)
-
0
-
CI: confidence interval; T2DM: type 2 diabetes
a
Change in square root of mean clinical attachment loss and square root of mean periodontal
probing depth, respectively, with normal glucose tolerance as reference category
Model 1: no adjustment
Model 2: adjusted for age and sex
Model 3: adjusted for age, sex, and BMI
Model 4: Adjusted for age, sex, BMI, education, smoking, alcohol consumption, total cholesterol, HDL
cholesterol, and triglycerides
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