UNIVERSIDADE ESTADUAL PAULISTA
“JÚLIO DE MESQUITA FILHO”
Instituto de Ciência e Tecnologia
Campus de São José dos Campos
ORIGINAL ARTICLE DOI: https://doi.org/10.4322/bds.2024.e3960
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Braz Dent Sci 2024 Jan/Mar;27 (1): e3960
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
Detecção molecular do nível de IL-10 para determinar a gravidade da periodontite em pacientes com Diabetes Mellitus tipo 2
Titiek BERNIYANTI1 , Retno PALUPI1 , Baleegh Abdulraoof ALKADASI2 , Riski Rossa APRILIANI3 , Naufal Ikbar YAASIR3
1 - Universitas Airlangga, Faculty of Dental Medicine, Department of Dental Public Health, Surabaya City, Indonesia
2 - Ibb University, Faculty of Dentistry, Department of Periodontology and Oral Medicine, Ibb City, Yemen
3 - Universitas Airlangga, Faculty of Dental Medicine, Surabaya City, Indonesia
How to cite: Berniyanti T, Palupi R, Alkadasi BA, Apriliani RR, Yaasir NI. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients. Braz Dent Sci. 2024;27(1):e3960. https://doi.org/10.4322/bds.2024.e3960
ABSTRACT
Objective: The prevalence of periodontal disease is increasing in most countries including developing and developed
countries. It affects 20-50-% of the global population. Patients with type 2 Diabetes Mellitus (DM) with severe
periodontal disease had a 3.2 times higher risk of death than individuals without periodontitis. Periodontitis contributes
to small-scale systemic inammation. The objective of this study was to determine the severity of periodontitis using
IL-10 (Interleukin-10) level in type 2 diabetes mellitus. Materials and Methods: This study was cross-sectional. All
methods were performed following the guidelines and regulations of the Ethics Committee, Faculty of Dental Medicine,
Universitas Airlangga. The samples were 90 subjects. The instruments used were questionnaires, periodontal status
measurements based on Community Periodontal Index (CPI), and random blood glucose measurements. Data on the
IL-10 level was obtained using Gingival Crevicular Fluid (GCF). Results: There was a signicant difference in lifestyle
in each group. The highest IL-10 level was found in the periodontitis group, followed by the periodontitis with the
type 2 DM group. Conclusion: The level of IL-10 can be used to determine periodontitis severity in type 2 DM. Most
respondents with the highest level of IL-10 were found in periodontitis followed by periodontitis with type 2 DM
group. High levels of IL-10 will decrease the synthesis of Tumor Necrosis Factor Alpha (TNF-α), Interleukin-1 (IL-1),
Interleukin-6 (IL-6), activation of macrophages, and Polymorphonuclear neutrophil (PMN).
KEYWORDS
IL-10; Periodontitis; Diabetes Mellitus; Medicine; Health risk.
RESUMO
Objetivo: A prevalência da doença periodontal tem aumentado na maioria dos países, incluindo países em desenvolvimento
e desenvolvidos, Afetando 20-50% da população global. Pacientes com Diabetes Mellitus tipo 2 (DM) com doença
periodontal grave apresentaram risco 3,2 vezes maior de morte do que indivíduos sem periodontite. O objetivo deste
estudo foi determinar a gravidade da periodontite utilizando o nível de IL-10 (Interleucina-10) no diabetes mellitus tipo 2.
Materiais e Métodos: Este estudo transversalfoi realizadoseguindo as orientações e regulamentos do Comitê de Ética da
Faculdade de Medicina Dentária da Universitas Airlangga. Noventa participantes,responderam um questionário e foram
examinados , para o estado periodontal, baseadas no Índice Periodontal Comunitário (IPC) e medidas aleatórias de glicemia.
Os dados do nível de IL-10 foram obtidos utilizando Fluido Crevicular Gengival (GCF). Resultados: Houve uma diferença
signicativa no estilo de vida em cada grupo. O nível mais alto de IL-10 foi encontrado no grupo com periodontite, seguido
pela periodontite com o grupo DM tipo 2. Conclusão: O nível de IL-10 pode ser utilizado para determinar a gravidade da
periodontite no DM tipo 2. A maioria dos participantes com maior nível de IL-10 estava no grupo periodontite seguida
de periodontite com DM tipo 2. Altos níveis de IL-10 diminuiem a síntese do Fator de Necrose Tumoral Alfa (TNF-α),
Interleucina-1 (IL-1), Interleucina-6 (IL-6), ativação de macrófagos e neutrólos polimorfonucleares (PMN).
PALAVRAS-CHAVE
IL-10; Periodontite; Diabetes Mellitus; Medicina; Fatores de risco.
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Berniyanti T et al.
Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
INTRODUCTION
Periodontitis is a disease that includes the
chronic inammatory process and is initiated and
exacerbated by a weak host immune response to
bacterial biolms on teeth. Periodontitis affects
the vitality of the periodontal tissue because the
inammatory process can cause progressive tissue
damage and lead to tooth loss. According to its
pathophysiology, periodontitis is an inammatory
response to an imbalance of microbes in the oral
cavity. The severity of periodontitis occurs in
10-15%, and the prevalence is twice as high in
individuals over 50 years of age [1,2]. The main
features of periodontitis are loss of periodontal
tissue manifested by loss of attachment (LOA)
and bone resorption detected by radiographic
examination, periodontal pockets, and bleeding
on the probing of gingival tissue [3].
Periodontal disease can affect 50% of the
global population, it is the most common oral
disease and has serious damage such as tooth
loss. The prevalence of periodontal disease is
increasing in most countries including developing
and developed countries. It affects 20-50-%
of the global population. Patients with type
2 diabetes mellitus (Type 2 DM) with severe
periodontal disease had a 3.2 times higher risk
of death than individuals without periodontitis.
Previous studies have also shown that there is a
close association between lifestyle and diabetes
mellitus. Lifestyle can determine the severity of
Type 2 DM and it is also a risk factor in Type
2 DM. Good management of lifestyle can lead
to a healthy lifestyle which can prevent the
severity of DM and also delay the complications
of this disease [4]. This association can also lead
to further infection and also delay the wound
healing process. According to the WHO, 80% of
non-communicable diseases including Type 2 DM
can be prevented by changes in lifestyle [4,5].
Periodontitis contributes to small-scale
systemic inammation. The cause of this systemic
inammation is related to the release of bacterial
and virulence factors and/or inflammatory
mediators from the periodontal tissues into the
bloodstream. These factors allow the circulation
of cytokines that lead to increased risk factors for
heart disease, insulin resistance, complications of
diabetes mellitus, and other systemic diseases [6].
Periodontitis is considered a complication of
diabetes mellitus because it is very closely related
to diabetes mellitus, especially uncontrolled
diabetes mellitus. Individuals with systemic
disorders of uncontrolled diabetes mellitus are
more susceptible to infection and impaired
wound healing [1].
Periodontitis has an association with the
imbalances between protein inflammation
such as pro-inammatory cytokines and anti-
inflammatory cytokines that affect systemic
manifestations [6]. Pro-inammatory cytokines
have an important role in inammatory reactions
and show an increased risk of diabetes mellitus
because they can increase the resistance of insulin
in several cells of the body such as adipocyte
cells, muscle cells, and hepatic cells directly,
and will result in the systemic disturbances of
insulin sensitivity and the damage in glucose
homeostasis [7]. The previous study that was
conducted in 2014 showed that 8.5% of adults
aged 18 years and over had diabetes. Meanwhile,
in 2016 diabetes was one of the causes of
death with 1.6 million deaths, and high blood
glucose levels were another cause of 2.2 million
deaths [8].
The previous report that was obtained from
12,254 participants in the Third National Health
and Nutrition Examination Survey (NHANES
III) showed that all the participants of those
study who had severe periodontitis also had an
increase in both fasting glucose (≥ 100 but <
126 mg/dl) and were diagnosed with diabetes
mellitus (≥ 126 mg/dl). Studies showed that
pro-inammatory cytokines have an important
role in inammatory reactions and could increase
the risk of diabetes mellitus [7]. Several studies
have shown that inammatory mediators such
as fibrinogen, C-reactive protein (CRP), and
pro-inammatory cytokines (IL-6 and TNF-α)
are associated with metabolic syndromes such as
diabetes mellitus and dyslipidemia [9]. IL-10 is
one of the anti-inammatory cytokines that have
a role in the response of anti-inflammatory
in metabolic syndrome and diabetes mellitus.
There is low production of IL-10 in response to
proinammatory cytokine activity on IL-10 which
is associated with high levels of HbA1c and can
be a predictor of hyperglycemia [9,10].
IL-10 deciency can result in an accelerated
bone resorption process and inhibition of the
bone formation process. IL-10 stimulates the
production of osteoprotegerin (OPG) which
can inhibit bone resorption by preventing
the attachment of the Receptor activator of
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Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
nuclear factor kappa-Β ligand (RANK/RANKL).
In addition, IL-10 is also considered to be an
important regulator of bone homeostasis under
both inammatory and homeostatic conditions.
Some studies have shown that the decrease in
IL-10 levels is considered insufcient to inhibit
the synthesis of pro-inammatory cytokines and
collagenases that impact the development of
osteoporosis [11,12]. The increased levels of
IL-10 can reduce the severity of periodontitis
and diabetes mellitus certainly. This condition
occurs due to the reduction of synthesis of pro-
inammatory cytokines such as IL-6 and TNF-α
because TNF-α can downregulate the tyrosine
kinase activity of the insulin receptor and can
cause insulin resistance [9,13]. The findings
from Toker
et al
in 2017 which stated that the
levels of IL-10 GCF in periodontitis patients
were higher than in the control group without
periodontitis. In his research, Toker suggested
that the polymorphism of the IL-10 gene that
affects the amount of IL-10 depends on several
factors such as cell type, stimulation time, type
of stimulus, and the presence of other cytokines.
Another study by Miranda et al in 2018 also
conducted a similar study and found that the
highest levels of IL-10 were found in the control
group without periodontitis and diabetes mellitus
and lower levels were found in the group with
chronic periodontitis, while lower levels were
found in the control group and a group with
periodontitis and diabetes mellitus [6,14]. Based
on the background, this study has an objective
to determine the role of IL-10 in the severity of
periodontitis in patients with diabetes mellitus.
MATERIALS AND METHODS
This study was an observational analytic
with a cross-sectional approach. The instruments
used were questionnaires, periodontal status
measurements based on CPI, and random blood
glucose measurements. Data on the IL-10 level
was obtained using GCF. The population of
this study was divided into four groups; 1)
periodontitis patients with clinical examination
of periodontal pockets 4 mm without diabetes
mellitus, 2) patients with diabetes mellitus only
without periodontitis, 3) patients with both
periodontitis and diabetes mellitus, 4) while
the control group samples were normal patients
without periodontitis and diabetes mellitus. This
study used a cluster random sampling technique
to obtain the sample. The total sample that was
used in this study was 156.
Data collection procedure
Blood glucose examination was carried
out on the population of patients with diabetes
mellitus and periodontitis at the Surabaya Public
Health Center. Informed consent was given to the
respondent as an agreement to become a research
subject. Examination of blood glucose levels was
carried out using Point of Care Testing (POCT)
and glucose strips to determine random blood
glucose values.
Performing an intra-oral examination using
a WHO periodontal probe to determine the
pocket depth, bleeding on probing (BOP), loss
of attachment, and a dental mirror to assess
the severity of the respondent’s periodontitis,
then recorded on the periodontal status sheet.
The examinations carried out were the presence
or absence of pockets and bleeding on probing.
The criteria to determine pocket depth was ≥ 4 mm.
Conducting interviews with respondents to
ll out questionnaires related to the respon-
dent’s history of diabetes mellitus
The patients declared that they did not have oth-
er systemic diseases other than type 2 diabetes
mellitus and not use any drugs that affected on
IL10 during the last 6 months.
GCF was obtained using paper points in
the deepest periodontal pocket for 30 seconds.
First, done the isolation and used paper points.
Paper points were immersed in an Eppendorf
tube containing 100μL of PBS solution, stored
at -300C, and mixed using a vortex mixer for
1 minute. The solution was added to each well.
The solution then was incubated for 90 minutes
at 370C. After incubation, the solution then was
transferred and was added 100μL of Biotinylated
Detection Ab/Ag then was incubated again for
1 hour at 370C. The solution was then aspirated
and washed 3 times. The solution was added
by 100μL HRP Conjugate and was incubated
for 30 minutes at 370C. The solution was then
aspirated and washed 5 times. 90μL of substrate
reagent was added and incubated for 15 minutes
at 370C. 50μL of Stop Solution was added and
the OD value was determined at a wavelength
of 450 nm. All the procedures had to be done
sequentially.
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Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
Data analysis
The results were calculated. The data that
was obtained then was tested using a statistical
analysis program SPSS 25 software.
RESULTS
Random blood glucose levels were divided
into 3 categories (Figure 1), namely 69-140 mg/dl,
141-199 mg/dl, and ≥ 200 mg/dl. The distribution
of health status based on random blood glucose
levels resulted in 4 groups of respondents
(Figure 1). Most random blood glucose levels of
respondents were in the 69-140 mg/dl category.
At 69-140 mg/dl category, the highest number
was in the Periodontitis group without type 2 DM,
and the least was in the type 2 DM group without
periodontitis. In the category of random blood
glucose levels of 141-199 mg/dl the most was
in the Periodontitis group without type 2 DM
and the least in the Normal and Type 2 Diabetes
Mellitus groups. In the category of random blood
glucose levels ≥ 200 mg/dl, the most common
was the Periodontitis with Type 2 Diabetes
Mellitus group.
Most respondents in this study had
periodontitis with type 2 diabetes mellitus
(Table I) and the least respondents were normal
respondents without periodontitis or type
2 diabetes mellitus or both. The comparison test
results in clinical examination between groups
(Table II) showed signicant results. It means
that there were differences in clinical examination
results (Pocket, LOA, and BOP) between groups.
In and BOP results showed that the mean of
the periodontitis group was the highest pocket
4.00 ±1.285, and 1.34 ± 0.48 respectively.
Meanwhile, in the result of LOA, the highest mean
was in periodontitis with type 2 diabetes mellitus
group (1.13 ± 0.619). Periodontitis remained
the main consistent occurrence. A comparative
test of these variables in periodontitis showed
signicant results in all groups.
There are 14 subjects who have suffered from
Type 2 DM for 0-3 years by 46.7% and as many as
16 other subjects for 3-7 years by 53.3% (Table III).
Table I - Comparison of Distribution in Each Group
Group N Percentage (%)
Normal 42 26.9%
Periodontitis 50 32%
Type 2 Diabetes Mellitus 27 17.3%
Periodontitis with Type 2 Diabetes Mellitus 37 23.8%
Total 156 100%
Table II - Comparison of pocket, loss of attachment, and bleeding on probing between all group
Variable Group Mean ± SD p-value
Pocket
Normal 1.84 ± 0.765
0.000*
Periodontitis 4.00 ±1.285
Type 2 Diabetes Mellitus 2.50 ±0.760
Periodontitis with Type 2 Diabetes Mellitus 2.31 ± 0.704
LOA
Normal 0.00 ± 0.00
0.000*
Periodontitis 0.83 ± 0.803
Type 2 Diabetes Mellitus 0.00 ± 0.00
Periodontitis with Type 2 Diabetes Mellitus 1.13 ± 0.619
BOP
Normal 1.00 ± 0.00
0.001*
Periodontitis 1.34 ± 0.48
Type 2 Diabetes Mellitus 1.00 ± 0.00
Periodontitis with Type 2 Diabetes Mellitus 1.06 ± 0.25
*p < 0.05 represents a significant statistical difference.
Figure 1 - Result of Random Blood Glucose Test.
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Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
According to Table IV, most of the respondents that
had a bad life style were on periodontitis with
type 2 diabetes mellitus group. P-value showed
that there was signicant difference of life style
in each groups (p-value < 0.05).
Lifestyle of respondents showed that
bad lifestyle was highest in the periodontitis
group and followed by periodontitis and type
2 diabetes mellitus group (Table IV). According to
Table V, IL-10 levels were divided into 3 groups
mean±SD 3.44 ± 13.19, 13.20 ± 21.00, and
21.01 ± 96.36 pg/ml. In all categories, the mean of
periodontitis category had the highest IL-10 level.
It means that at all levels, people with periodontitis
can produce IL-10 levels actively and progressively.
The type 2 DM category had the least levels of
IL-10 in the mean ± SD group of 13.20 ± 21.00.
Overall based on Table V, the highest IL-10 level
was found in the periodontitis without type 2 DM
group, followed by Periodontitis with type 2 DM
group was the same as the normal group, while
in the type 2 DM group was the least.
DISCUSSION
Chronic diseases such as Type 2 Diabetes
Mellitus showed insulin resistance. However, not
all parents and elderly who have type 2 diabetes
mellitus as a disease history also reduce insulin
resistance. This condition occurs due to several
factors that induce the occurrence of type 2 diabetes
mellitus such as diet, lifestyle, and physical
activity [15,16]. The highest level of IL-10 was
found in the periodontitis group. According
to Passoja, the host-pathogen interaction is
complex. Its effect depends on the strength and
nature of the immune response and the nature
of the microbial pathogen that causes it [16].
The downregulation of IL-10 can be inuenced
by an increased concentration of TNF- α [16,17].
Meanwhile, a previous studies found that there was
a higher concentration of IL-10 in the Periodontitis
group [13,14]. In the previous study equalized age,
and gender in each group of subjects and limited
the subject’s BMI to <30 kg/m2. Excessive BMI or
obesity can affect inammation. In obesity, there is
an overexpression of pro-inammatory cytokines.
Adipose tissue responds to additional nutritional
stimulation through adipocyte hyperplasia and
hypertrophy. Due to the morphological structure of
adipose tissue which is composed of immune cells,
endothelium cells, and adipocyte cells that can
easily lead to progressive adipocyte enlargement,
the blood supply to adipocytes will be reduced
Table III - Distribution based on the history of diabetes mellitus
History of diabetes mellitus N Percentage Total N (Percentage of Re-
spondents with type 2 DM)
0-3 years 14 46.7% 30 (100% / 30%)
3-7 years 16 53.3%
Table IV - Differences of the lifestyle in each group
Life style
Normal Periodontitis Diabetes Mellitus Periodontitis-Diabetes
Mellitus p-value
N (%) (Mean±SD) N (%) (Mean±SD) N (%) (Mean±SD) N (%) (Mean±SD)
Good 7 (19.4%) 50.05±13.24 25 (69.4%) 41.45±16.17 2 (5.6%) 49.52±11.92 2 (5.6%) 45.59±12.45 0.000*
Bad 12 (22.2%) 16 (29.6%) 12 (22.2%) 14 (25.9%)
*p < 0.05 represents a significant statistical difference
Table V - Distribution of IL-10
IL-10
Mean±SD
Group (N)
Normal Periodontitis Type 2 Diabetes Mel-
litus
Periodontitis with Type 2
Diabetes Mellitus
3.44-13.19 9 25 6 5
13.20-21.00 4 8 6 5
21.01-96.36 6 8 2 6
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Berniyanti T et al.
Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
resulting in hypoxia. Hypoxia is an etiology that
triggers necrosis and inltration of macrophages
into adipose tissue, which can then lead to pro-
inflammatory mediator overproduction. This
will lead to local inflammation in the adipose
tissue area, and it progressively spreads and
results in systemic inammation along the body
that has an association with the comorbidities
obesity-related [13,18,19].
In this study, the second higher results of
IL-10 were found in the periodontitis-diabetes
Mellitus group and normal group. This result is
possible because of the consumption of drugs by
patients with diabetes mellitus in this group and
the inuence of inammation from the periodontal
tissue in this group. This condition occurred due
to the anti-inammatory effect of the antidiabetic
drugs consumed by most of our subjects. It is known
that several types of antidiabetic medications such
as insulin, metformin, sulfonylureas, and others,
besides functioning to lower blood glucose also
have anti-inammatory mechanisms [13]. One of
the drugs often given by doctors is metformin.
Metformin inhibits Nuclear Factor Kappa B (NFkB)
activation through blockade of the phosphoinositide
3-kinase (PI3K)-Akt pathway in human blood
vessel wall cells, the study then continued that
in macrophage-activated lipopolysaccharide,
metformin can inhibit the production of the IL-1β
precursor molecule. and other pro-inammatory
cytokines meanwhile enhance the induction of
the anti-inammatory cytokine IL-10. Meanwhile,
the normal group can be inuenced due to local
factors such as oral hygiene that leads to tissue
inammation [17-19].
Another result that can be found in this
study is the higher mean IL-10 in the group with
chronic periodontitis compared to the diabetes
mellitus group. IL-10 is a protein that has an
important role as an anti-inammatory cytokine, it
represents part of the anti-inammatory response
in several diseases including metabolic syndrome
and diabetes mellitus. There is low production of
IL-10 in response to proinammatory cytokine
activity on IL-10 which has a correlation with
high levels of HbA1c and can be a predictor of
hyperglycemia [9,10]. Most patients with a high
level of IL-10 were diagnosed with periodontitis
and also periodontitis in the type 2 diabetes
mellitus group. The severity of periodontitis that
can be detected by IL-10 level can be decreased
with control of lifestyle and also maintenance of
oral health which can decrease the inammation
of periodontal tissue and lower the IL-10 level
in periodontal tissue. High levels of IL-10 will
decrease the synthesis of TNF-α, IL-1, and IL-6,
activation of macrophages, and PMN. Lifestyles
such as drinking alcohol, smoking, lower physical
activity, bad diet habits, and insufcient sleep had
a close correlation with periodontal inammation,
especially in diabetes mellitus patients. Several
cells contribute in the severity of inammation
in patients with type 2 DM. Macrophages as cells
that are very important in wound healing have
the function of bacterial phagocytosis and dead
tissue will turn into efferocytotic macrophages
(M2) which secrete anti-inammatory cytokines
such as IL-10. IL-10 in patients with diabetes
mellitus is less responsive so it is possible to
cause the concentration of IL-10 in the diabetes
mellitus group to be lower than in the healthy state
(without metabolic and inammatory disorders)
and the effect of antidiabetic drugs in the diabetes
mellitus group is less dominating, unlike in the
periodontitis-diabetes Mellitus group. It should
also be noticed that the results obtained also
depend on the host-pathogen interaction which is
complex and its effect depends on the strength and
nature of the immune response and the nature of
the microbial pathogen that causes it [7].
Most of the respondents in the Periodontitis
group have a bad lifestyle, its score was the
highest. It showed that lifestyle is also a risk factor
in periodontitis [12]. This result also showed that
respondents with bad lifestyles were found high in
periodontitis with type 2 DM group which indicated
that the lifestyle of patients with periodontitis
and diabetes mellitus was worse. Lifestyle has
an association with type 2 DM. Lifestyle can
worsen the condition of diabetes mellitus and also
suppress the immune which can lead to periodontal
inammation and tooth loss [4,5,10]. It was in line
with the theory stating that lifestyle is the main risk
factor for diabetes mellitus [12].
CONCLUSION
The level of IL-10 can be used to determine
the periodontitis severity in patients with type
2 diabetes mellitus. Respondents with the highest
level of IL-10 were found in periodontitis followed
by periodontitis with type 2 DM group. High levels of
IL-10 will decrease the synthesis of Tumor Necrosis
Factor Alpha (TNF-α), Interleukin-1 (IL-1),
Interleukin-6 (IL-6), activation of macrophages,
and Polymorphonuclear neutrophil (PMN).
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Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
The higher level of IL-10 showed the more severe
of inammation in periodontal tissue in patients
with type 2 DM.
Acknowledgements
All the authors would like to express their
gratitude towards all the parties who supported
this research including the Rector, the Director of
the Research and Innovation Center, the Dean, and
the Department of Dental Public Health, Faculty
of Dental Medicine, Universitas Airlangga.
Author’s Contributions
TB, RP: Conceptualization. TB, RP Data
Curation. TB: Formal Analysis. TB, RP: Supervision.
RP, NIY: Methodology. RP: Visualization. TB,
RP, BAA: Writing – Review & Editing. RP, BAA:
Validation. RRA, NIY: Resources. RRA, NIY:
Writing – Original Draft Preparation. RRA: Project
Administration. NIY: Investigation. NIY: Funding
Acquisition.
Conict of Interest
The authors declare that they do not have
to compete with interests.
Funding
This study was supported by a grant from
the Ministry of Higher Education, with grant number
(No. 428/UN3/2020); Jakarta, Indonesia. The
funder of this study did not have any role in the
study design, data collection, data analysis, and
interpretation, preparation of the manuscript, and
the decision to submit the paper for publication.
Regulatory Statement
This study has been approved ethically by
Ethics Committee, Faculty of Dental Medicine,
Universitas Airlangga, Surabaya, Indonesia
(Number: 172/HRECC.FODM/IV/2019).
REFERENCES
1. Teeuw WJ, Kosho MXF, Poland DCW, Gerdes VEA, Loos BG.
Periodontitis as a possible early sign of diabetes mellitus.
BMJ Open Diabetes Res Care. 2017;5(1):e000326. http://doi.
org/10.1136/bmjdrc-2016-000326. PMid:28316794.
2. Llanos AH, Silva CGB, Ichimura KT, Rebeis ES, Giudicissi M,
Romano MM,etal. Impact of aggressive periodontitis and chronic
periodontitis on oral health-related quality of life. Braz Oral Res.
2018;32(0):e006. http://doi.org/10.1590/1807-3107bor-2018.
vol32.0006. PMid:29451591.
3. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine
DH, et al. Periodontitis: consensus report of workgroup 2 of
the 2017 World Workshop on the Classification of Periodontal
and Peri-Implant Diseases and Conditions. J Clin Periodontol.
2018;45(Suppl 20):162-70. PMid:29926490.
4. Samudera WS, Efendi F, Indarwati R. Effect of community
and peer support based healthy lifestyle program (CP-HELP)
on self care behavior and fasting blood glucose in patient
with type 2 Diabetes Mellitus. J Diabetes Metab Disord.
2021;20(1):193-9. http://doi.org/10.1007/s40200-021-
00729-y. PMid:34178831.
5. World Health Organization (WHO). 2013. Available from: https://
www.who.int/publications/i/item/WHO-NMH-MND-13.2
6. Miranda TS, Haleuy SL, Cruz DF, da Silva HDP, Feres M, Figueiredo
LC,etal. The ratios of pro-inflammatory to anti-inflammatory
cytokines in the serum of chronic periodontitis patients with
and without type 2 diabetes and/or smoking habit. Clin Oral
Investig. 2018. http://doi.org/10.1007/s00784-018-2471-5.
PMid:29737428.
7. Al-Shukaili A, Al-Ghafri S, Al-Marhoobi S, Al-Abri S, Al-Lawati
J, Al-Maskari M. Analysis of inflammatory mediators in type 2
diabetes patients. Int J Endocrinol. 2013;2013:976810. http://
doi.org/10.1155/2013/976810. PMid:23762057.
8. World Health Organization. Global Report On Diabetes. Geneve:
WHO Press; 2014.
9. van Exel E, Gussekloo J, de Craen AJ, Frolich M, Bootsma-
Van Der Wiel A, Westendorp RG. Low production
capacity of interleukin-10 associates with the metabolic
syndrome and type 2 diabetes: the Leiden 85-Plus Study.
Diabetes. 2002;51(4):1088-92. http://doi.org/10.2337/
diabetes.51.4.1088. PMid:11916930.
10. Wang X, Bao W, Liu J, Ouyang YY, Wang D, Rong S, et al.
Inflammatory markers and risk of type 2 diabetes: a systematic
review and meta-analysis. Diabetes Care. 2013;36(1):166-75.
http://doi.org/10.2337/dc12-0702. PMid:23264288.
11. Fenol A, Sasidharan RK, Krishnan S. Levels of interleukin -10
in gingival crevicular fluid and its role in the initiation and
progression of gingivitis to periodontitis. J Oral Hyg Health.
2014;2(3):3. http://doi.org/10.4172/2332-0702.1000135.
12. Zhang Q, Chen B, Yan F, Guo J, Zhu X, Ma S,etal. Interleukin-10
inhibits bone resorption: a potential therapeutic strategy in
periodontitis and other bone loss diseases. BioMed Res Int.
2014;2014:284836. http://doi.org/10.1155/2014/284836.
PMid:24696846.
13. Acharya AB, Thakur S, Muddapur MV. Evaluation of serum
interleukin-10 levels as a predictor of glycemic alteration in
chronic periodontitis and type 2 diabetes mellitus. J Indian
Soc Periodontol. 2015;19(4):388. http://doi.org/10.4103/0972-
124X.150876. PMid:26392685.
14. Toker H, Gorgun EP, Korkmaz EM, Yüce HB, Poyraz O. The effects
of IL-10 gene polymorphism on serum, and gingival crevicular
fluid levels of IL-6 and IL-10 in chronic periodontitis. J Appl Oral
Sci. 2018;26(0):e20170232. http://doi.org/10.1590/1678-7757-
2017-0232. PMid:29489938.
15. Bokhari SAH, Suhail AM, Malik AR, Imran MF. Periodontal disease
status and associated risk factors in patients attending a
dental teaching Hospital in Rawalpindi, Pakistan. J Indian Soc
Periodontol. 2015;19(6):678-82. http://doi.org/10.4103/0972-
124X.156882. PMid:26941520.
16. Holt R, Cockram C, Flyvbjerg A, Goldstein B. Textbook of
diabetes (5th ed.). Chichester: John Wiley& Sons Ltd; 2017.
http://doi.org/10.1002/9781118924853.
8
Braz Dent Sci 2024 Jan/Mar;27 (1): e3960
Berniyanti T et al.
Molecular detection of IL-10 level to determine severity of periodontitis in type 2 Diabetes Mellitus patients
Berniyanti T et al. Molecular detection of IL-10 level to determine severity of
periodontitis in type 2 Diabetes Mellitus patients
17. Passoja A, Puijola I, Knuuttila M, Niemela¨ O, Karttunen R, Raunio
T,etal. Serum levels of interleukin-10 and tumour necrosis factor-a
in chronic periodontitis. J Clin Periodontol. 2010;37(10):881-7.
http://doi.org/10.1111/j.1600-051X.2010.01602.x. PMid:20718895.
18. Xourgia E, Tzouganatou E-M, Papazafeiropoulou A, Melidonis
A. Anti-inflammatory properties of antidiabetic agents. World
J Metaanal. 2019;7(4):129-41. http://doi.org/10.13105/wjma.
v7.i4.129.
19. Mohammed SE, Patimah I, Khaza’ai H, Rahmat A, Abed Y. Obesity
and inflammation: the linking mechanism and the complications.
Arch Med Sci. 2017;13(4):851-63. http://doi.org/10.5114/
aoms.2016.58928. PMid:28721154.
Titiek Berniyanti
(Corresponding address)
Universitas Airlangga, Faculty of Dental Medicine, Department of Dental Public
Health, Surabaya, Indonesia
Email: titiek-b@fkg.unair.ac.id Date submitted: 2023 July 13
Accept submission: 2024 Mar 27
