Relação entre Diabetes e Doença Periodontal

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Tooth and Periodontal Clinical
Attachment Loss Are Associated With
Hyperglycemia in Patients With Diabetes
Javier Enrique Botero,* Fanny Lucia Yepes,* Natalia Roldán,* Cesar Augusto Castrillón,*
Juan Pablo Hincapie,* Sandra Paola Ochoa,* Carlos Andrés Ospina,* Marı́a Alejandra Becerra,*
Adriana Jaramillo,† Sonia Jakeline Gutierrez,† and Adolfo Contreras†
Background: Periodontal disease has been associated with
diabetes, but there is still controversy on the relationship be-
tween periodontal clinical parameters and glycemic control.
The purpose of this study is to assess the relationship between
blood glucose levels and clinical parameters of periodontal
disease in individuals with diabetes.
Methods: A total of 65 individuals with diabetes and 81
individuals without diabetes were included in the study. A
full-mouth periodontal examination and preprandial fasting
glycemia values were recorded for each individual. Glycosy-
lated hemoglobin was only measured in patients with diabe-
tes. A comparative analysis between groups (Mann-Whitney
U test) and a correlation analysis between glycemia and peri-
odontal parameters were performed (Spearman test).
Results: Patients without diabetes presented more teeth
than individuals with diabetes (P <0.05). Patients with diabetes
with periodontitis displayed loss of periodontal clinical attach-
ment compared to patients without diabetes, but the highest
value was observed in patients with periodontitis that reported
a smoking habit. Furthermore, patients with diabetes with
periodontitis presented higher glycemia and glycated hemo-
globin values in contrast to patients with gingivitis. Patients
with diabetes with hyperglycemia had a higher risk to develop
periodontitis (odds ratio = 2.24; 95% confidence interval =
1.02 to 4.93). A positive correlation was observed between
glycemia and clinical attachment loss (AL), whereas a nega-
tive correlation between glycemia and the number of teeth
present was found (P <0.05).
Conclusions: Tooth and periodontal AL were increased by
hyperglycemia in individuals with diabetes. This study con-
tributes additional evidence that diabetes could aggravate
periodontal disease and affect the systemic health of individ-
uals. J Periodontol 2012;83:1245-1250.
KEY WORDS
Blood glucose, levels; diabetes mellitus; gingivitis;
hyperglycemia; periodontal attachment loss; periodontitis.
P
eriodontal disease is an inflamma-
tory process that may lead to the
breakdown of the tooth-supporting
tissues.1 This breakdown is clinically
observed as an increase in probing depth
(PD), clinical attachment level (CAL),
and radiographic bone loss. The main
etiologic factor of periodontal disease is
biofilm accumulation around the teeth
and near the gingival margin accom-
panied with microbial overgrowth of
specific periodontopathic organisms.2
However, systemic conditions have
been shown to increase the susceptibil-
ity to periodontal disease. This is the
case with diabetes, in which the me-
tabolism of glucose and lipids are im-
paired.3,4 Several biologic mechanisms,
including the production of advanced
glycation end products (AGEs), hyper-
inflammatory reaction, poor collagen
quality, microvascular alterations, host
defense dysfunction, and increased
production of matrix metalloproteinases,
have been proposed to explain this
susceptibility.5-7
The prevalence of periodontitis in indi-
viduals with diabetes is higher compared
to patients without diabetes,8,9 but it has
been moderately associated with im-
paired fasting glucose (odds ratio [OR] =
1.39; 95% confidence interval [CI] =
1.00 to 1.92) when clinical attachment
loss (AL) increased.10 In addition, the
effect of type 1 and 2 diabetes on
* Faculty of Dentistry, Universidad de Antioquia, Medellin, Colombia.
† Periodontal Medicine Group, Universidad del Valle, Cali, Colombia.
doi: 10.1902/jop.2012.110681
J Periodontol • October 2012
1245
periodontal disease development is strongly empha-
sized.11-15 However, other studies have found no cor-
relation between diabetic parameters and periodontal
disease, thus resulting in conflicting conclusions.16-18
In addition, the relationship between hyperglycemia
and periodontal disease has not been fully studied.
Therefore, the purpose of this study is to assess the
relationship between blood glucose levels and clini-
cal parameters of periodontal disease in patients with
diabetes.
MATERIALS AND METHODS
This study consisted of a cross-sectional design with
a convenience sample approved by the Institutional
Review Boards of Universidad de Antioquia (Medellin,
Colombia) and Universidad del Valle (Cali, Colum-
bia). Participants (64 males and 82 females; mean
age: 50.1 – 7 years) selected from February 2010
to March 2011 were informed about the nature of
the study and signed written consent at enrollment ac-
cording to the World Medical Association Declaration
of Helsinki, as revised in 2002.
Patients with a previous (>2 years) and confirmed
diagnosis (fasting glucose ‡126 mg/dL or hemoglo-
bin A1c [HbA1c] ‡6.5%) of type 1 or 2 diabetes melli-
tus from the Hospital Universitario San Vicente de
Paul (Medellin, Colombia) were invited to participate
in the study. Patients without diabetes were from the
School of Dentistry at the Universidad del Valle. For
enrollment, participants met the following inclusion
criteria: 1) ‡18 years old; 2) voluntary participation;
3) confirmed type 1 or 2 diabetes mellitus; 4) other
controlled systemic diseases (e.g., hypertension);
and 5) ‡10 teeth present. Individuals without diabetes
met the same inclusion criteria except the diabetes
diagnosis. Individuals were excluded when they pre-
sented any systemic disease that contraindicated
the clinical examination, had any previous (3 months)
consumption of antibiotics and/or anti-inflammatory
drugs, received previous periodontal treatment (6
months), and were pregnant or positive for human
immunodeficiency virus. Because cigarette smoking
is a confounding variable for periodontal disease, it
was not considered an exclusion criterion but was re-
corded when indicated by the patient and analyzed
independently.
A full clinical periodontal examination was per-
formed by two calibrated clinicians (SPO and CAO)
in all participants. The recording of clinical parame-
ters was calibrated until intraclass and interclass
k values were between 0.80 and 0.90. Periodontal
clinical parameters were recorded in six sites around
each tooth excluding third molars as follows: PD (mil-
limeters) and CAL (millimeters) measurements were
averaged in each participant; bleeding on probing
(BOP) (percentage) was recorded as positive/nega-
tive and presented as the percentage of total bleeding
sites; and the number of teeth present was also re-
corded. Periapical radiographs were taken to evaluate
bone loss. Periodontal probing was performed using
a marked periodontal probe,‡ and measurements
were rounded to the next millimeter. In addition,
values for fasting preprandial glycemia (FPG) (milli-
grams per deciliter) in all participants and glyco-
sylated hemoglobin (HbA1c; percentage) only in
individuals with diabetes were recorded. Blood glucose
levels were analyzed as follows: normal fasting glucose
<100 mg/dL, impaired fasting glucose ‡100 but <126
mg/dL, and hyperglycemia (diabetes) ‡126 mg/dL.19
A periodontal diagnosis was given to each partici-
pant according to the American Academy of Peri-
odontology20 and Page and Eke.21 Gingivitis was
defined as the presence of PD £3 mm, CAL £3 mm,
BOP, and absence of noticeable radiographic bone
loss. Chronic periodontitis was defined as the pres-
ence of ‡2 sites in non-adjacent teeth with PD ‡4
mm, CAL ‡4 mm, BOP, and evidence of radiographic
bone loss.20
Demographic variables and clinical parameters
are presented as the mean – SD or median and in-
terquartile range in each group. Periodontal and dia-
betic clinical parameter comparisons between
groups with and without diabetes were performed us-
ing the Kruskal-Wallis with Dunn multiple comparisontest and Mann-Whitney U test when indicated. Al-
though the type of diabetes was known, patients with
type 1 and type 2 diabetes were considered in the
same group because previous studies have found
that they are equally susceptible to periodontal dis-
ease.22-24 Patients that reported the habit of cigarette
smoking were allocated to the smokers group and
treated separately for the analysis.
The relationship between periodontitis and diabe-
tes was tested in a 2 · 2 table, and the OR was calcu-
lated (95% CI). CAL was considered the primary
outcome, and PD and number of teeth present were
the secondary outcomes. To establish the relationship
between glycemia (independent variable) and peri-
odontal clinical parameters (dependent variable),
a linear regression analysis and the Spearman corre-
lation test were used. A statistical software§ was used
to analyze all data. Statistical differences were as-
sumed when P <0.05.
RESULTS
Table 1 depicts the demographic description of the
patients studied. A total of 146 patients (65 individ-
uals with diabetes and 81 individuals without diabe-
tes), were included and allocated to the following
‡ UNC-15 probe, Hu-Friedy, Chicago IL.
§ GraphPad Prism version 5.00 for Windows; GraphPad Software, San
Diego, CA.
Tooth Loss and Periodontitis in Patients With Diabetes Volume 83 • Number 10
1246
groups: patients with diabetes with gingivitis or peri-
odontitis; patients without diabetes with gingivitis,
periodontitis, or patients with periodontitis who
smoke. None of the patients with diabetes reported
a smoking habit. No differences for age were observed
among groups. In the groups with diabetes, there was
a higher frequency of females in contrast to the group
without diabetes. The proportion of type 2 diabetes
patients was slightly higher, but it was not statistically
significant.
There were statistical differences for the number of
teeth present, glycemia values, PD, and CAL among
all groups (Table 2). Patients without diabetes pre-
sented more teeth than patients with diabetes, and
the difference was statistically significant between
patients with gingivitis and periodontitis compared
to patients with diabetes (P <0.01). Patients with peri-
odontitis with a cigarette smoking habit expressed
increased PDs compared to the same category in
patients with and without diabetes (P <0.01). No dif-
ference for PD was observed for periodontitis patients
with and without diabetes. Patients with diabetes with
periodontitis displayed increased loss of CAL com-
pared to patients without diabetes, but the highest
value was observed for patients with periodontitis
who smoke, and these differences were statistically
significant (P <0.01). Furthermore, individuals with
diabetes with periodontitis had higher glycemia
and glycated hemoglobin values in contrast to pa-
tients with gingivitis, but the difference was not sta-
tistically significant.
To test whether there was a relationship between
glycemia and periodontal clinical parameters, corre-
lation and regression analyses were performed (Fig.
1; Table 3). Patients with diabetes with hyperglycemia
had higher risk to develop periodontitis (OR = 2.24;
95% CI = 1.02 to 4.93) (Fig. 1). A positive correlation
was observed between glycemia and AL (Fig. 1A;
Table 3) (P <0.01), whereas a negative correlation
between glycemia and the number of teeth present
was found (Fig. 1C; Table 3) (P <0.01). Conversely,
no correlation was found between glycemia and PDs
(Fig. 1B; Table 3).
DISCUSSION
The current study shows that high levels of blood
glucose are associated with a worse periodontal con-
dition in patients with diabetes. The proportion of peri-
odontitis was higher (75.3%) in patients affected by
diabetes than in patients without diabetes (64.1%),
and this is in agreement with previous studies.8,9 This
contributes additional evidence that diabetes could
increase the prevalence of periodontal disease and
seriously affect the systemic health of individuals. It
is important to note that, although age was similar
among groups, patients with diabetes reported a long
duration of the disease (>10 years), and this could ex-
plain the increased prevalence and severity of peri-
odontitis compared to patients without diabetes.
Duration of diabetes is considered a main factor when
addressing the susceptibility to periodontal disease
and other systemic complications,25,26 but control
of glycemia is one of the principal etiologic mecha-
nisms associated with periodontal breakdown.27 High
blood glucose (hyperglycemia) results in the produc-
tion of AGEs, interleukin-1, tumor necrosis factor,
prostaglandin E2, and altered collagen turnover, thus
affecting the homeostasis of periodontal tissues in
patients with diabetes.28 Patients in this study present
values for glycemia (170.9 mg/dL) and glycated
hemoglobin (7.7%) above the accepted values for
a good control of blood glucose in individuals with
diabetes (FPG ‡126 mg/dL; HbA1c ‡6.5%)19 and
were more likely to develop periodontitis (OR =
2.24; 95% CI = 1.02 to 4.93). This finding is in con-
junction with long diabetes duration, adding to the
evidence linking diabetes and hyperglycemia as risk
factors for periodontal breakdown.
Table 1.
Demographic Description of the Patients Included in the Study
Patients With Diabetes Patients Without Diabetes
Variable Gingivitis Periodontitis Gingivitis Periodontitis Periodontitis-Smokers
Number of patients 16 49 29 30 22
Sex (female/male) 14/2 31/18 8/21 14/16 15/7
Age (mean – SD) 55.7 – 13.2 57.9 – 9.8 42.7 – 7.1 45.5 – 10.7 49 – 13.3
Diabetes mellitus type 1 5 (31.2%) 24 (48.9%) NA NA NA
Diabetes mellitus type 2 11 (68.8%) 25 (51.1%) NA NA NA
Diabetes duration in years (mean – SD) 13.6 – 9.3 13.7 – 8.4 NA NA NA
J Periodontol • October 2012 Botero, Yepes, Roldán, et al.
1247
The oral condition and function in patients with
diabetes were deteriorated as teeth were lost through
time. Patients with diabetes with periodontitis had lost
more teeth and presented increased periodontal AL
compared to patients without diabetes, although the
cross-sectional nature of this study does not allow es-
tablishing the precise reason for tooth extraction in the
group of patients examined. Nonetheless, the diagno-
sis of periodontal disease results from the analysis of
PD and AL that represents past destruction of peri-
odontal tissues, and this constitutes one of the main
causes of tooth loss. In addition, patients with diabetes
from this study report that teeth were extracted when
they presented increased mobility (data not shown).
Teeth that are severely affected by periodontitis are
frequently extracted during dental visits, and conse-
quently this explains the low number of teeth present
in patients with diabetes. To support this finding,
results from the correlation and regression analysis
show that there is a positive correlation between
Table 2.
Comparison of Periodontal Clinical and Diabetic Parameters Between Groups
Patients With Diabetes Patients Without Diabetes
Parameters
Gingivitis
(n = 16)
Periodontitis
(n = 49)
Gingivitis
(n = 29)
Periodontitis
(n = 30)
Periodontitis-
Smokers
(n = 22) P Value*
No. of teeth: median
(interquartile range)
21.5 (14.2 to 24.7)† 20 (17.5 to 23)‡ 26 (24 to 28) 25 (23 to 27) 24 (20.5 to 27) 0.0001
BOP (%): median
(interquartile range)
22.3 (15.7 to 37.1) 58.3 (42.1 to 81.2) 45.8 (23.1 to 54.7) 75 (37.9 to 91.6) 66.6 (42.6 to 87.7) NS
PD (mm): median
(interquartile range)
1.9 (1.7 to 2.1)† 2.8 (2.4 to 3.5) 2.5 (2.3 to 2.7) 2.9 (2.6 to 3.3) 3.7 (3.1 to 4.1)i 0.0001
CAL (mm): median
(interquartile range)
2.3 (1.8 to 2.9) 3.0 (2.5 to 3.7)§ 2.1 (1.6 to 2.5) 2.6 (1.7 to 3.6) 4.0 (3.4 to 4.6)i 0.0001
Glycemia (mg/dL): median
(interquartile range)
158 (138 to 175)† 170.9 (129 to 227)§ 90 (80.5 to 98.5) 88 (77.7 to 99.2) 89 (78 to 100) 0.0001
HbA1c (%): median
(interquartile range)
7.0 (6.5 to 7.6) 7.7 (6.3 to 9.3) NA NA NA ND
NS = non-significant; ND = not determined; NA = not applicable.
*Kruskal-Wallis with Dunn multiple comparison test.
† P <0.01 compared to gingivitis in patients without diabetes (Mann-Whitney U test).
‡ P <0.01 compared to periodontitis in patients without diabetes and patients with periodontitis who smoke (Mann-Whitney U test).
§ P <0.01 compared to periodontitis in patients without diabetes (Mann-Whitney U test).
i P <0.01 compared to periodontitis in patients with diabetes and patients without diabetes (Mann-Whitney U test).
Figure 1.
Linear regression model and comparison between clinical parameters and glycemia. Continuous line indicates the best fit slope, and dotted line indicates
the 95% CI. The OR for the development of periodontitis in individuals with hyperglycemia was OR = 2.24; 95% CI = 1.02 to 4.93.
Tooth Loss and Periodontitis in Patients With Diabetes Volume 83 • Number 10
1248
higher glycemia values and AL (P <0.01). In ad-
dition, the correlation between glycemia and number
of teeth present was inversely proportional (P <0.01).
This means that poor glycemic control may create
a susceptibility condition that leads to AL and tooth
loss with time. These findings are further supported
by others.29,30 A study analyzed the National Health
and Nutrition Examination Survey III and found a sim-
ilar association in the United States.10 Moreover, the
observational nature of this study provides circum-
stantial evidence that needs to be reproduced in ana-
lytic investigations.
Cigarette smoking is considered an important risk
factor for periodontal disease and has been associated
with two to eight times more AL in a dose-dependent
manner.31-33 In the present investigation, a group of
patients with periodontitis but without diabetes re-
ported being active smokers and were analyzed sepa-
rately. Although glycemia values in smokers were
normal, they presented the higher PDs and CAL. It is
important to consider the sum of different risk factors
in patients with diabetes because it has been observed
that the risk of AL is increased from 4.4 to 12.3 times
more when patients had HbAc1 >8% and smoked.34
However, it was not possible to perform an additional
analysis with this parameter because patients with di-
abetes were non-smokers, and this may be a weakness
of the study.
Considering that diabetes and periodontal disease
are chronic and may share multiple risk factors, the in-
terdisciplinary approach in the treatment of the patient
with diabetes will result in an improved systemic and
oral condition of these patients. Recent studies suggest
that good control of the glycemia improves the peri-
odontal condition and vice versa,35,36 but this still needs
tobe furtherevaluated in long-term interventionstudies.
CONCLUSIONS
Tooth and periodontal AL were increased by hypergly-
cemia in patients with diabetes. This study contributes
evidence that diabetes could aggravate periodontal
disease and affect the systemic health of individuals.
ACKNOWLEDGMENTS
This study was funded by Universidad de Antioquia Re-
search Development Committee Grant CODI 14-2009
and Universidad del Valle Grant 1638. The authors
report no conflicts of interest related to this study.
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CAL 0.37 0.20 to 0.52 <0.0001
Number of teeth
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Correspondence: Javier Enrique Botero, Faculty of Den-
tistry, Universidad de Antioquia, Calle 64 52-59, Medellı́n,
Colombia. E-mail: drjavo@yahoo.com.
Submitted November 17, 2011; accepted for publication
December 12, 2011.
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