Feasibility Controlling Hemoglobin A1c by Oral Hygiene
Improvement: A Pilot StudyOJDOH: April-2019: Page No: 08-15

Open Journal of Dentistry and Oral HealthResearch Article

Open Access

Feasibility Controlling Hemoglobin A1c by Oral Hygiene Improvement: A
Pilot Study
Ayako Okada1,2, Yoshiaki Nomura1*, Mayu Miyanohara1, Masahide Uraguchi1,3,
Hisanori Tadokoro4, Tetsuya Nagai5, Yoshihito Fujii6, Masahiro Miura7, Ryo Kawachi8,
Takanori Matsui3, Kunio Takayanagi3, Masashi Yamamoto3, Takatsugu Yamamoto2
and Nobuhiro Hanada1
1

Department of Translational Research, Tsurumi University School of Dental Medicine, Yokohama,Japan
2
Department of Operative Dentistry, Tsurumi University School of Dental Medicine, Yokohama,Japan
3
Medical Group Seiwa, Tokyo, Japan
4
Kyodo Dental Clinic, Tokyo, Japan
5
Nagayama Center Dental Clinic, Tokyo, Japan
6
Station Dental Clinic, Sagamihara, Japan
7
Seiwa Dental Clinic, Tokyo, Japan
8
Machida-Kitaguchi Dental Clinic, Tokyo, Japan*Correspondig Author: Yoshiaki Nomura, Department of Translational Research, Tsurumi
University School of Dental Medicine, 2-1-3 Tsurumi, Tsurumi-ku, Yokohama 230-8501, Japan, Tel:(+81)45-580-8462; Fax: (+81)45-573-2473; E-mail: nomura-y@tsurumi-u.ac.jp
Received Date: Apr 14, 2019 / Accepted Date: May 02, 2019 / Published Date: May 04, 2019

Abstract
Purpose: Patients with diabetes mellitus are prone to be bacteremia. The major side effect of diabetes
mellitus is caused by bacteremia. However, conventional periodontal treatment does not focus mainlyon the elimination of pathogenic bacteria. Therefore, the aim of this study was to the management oforal bacteria improve some symptoms of diabetes mellitus.
Material and Method: We monitored Hemoglobin A1c (HbA1c) of five subjects after removed oral
bacteria on the tooth surface by antibiotics using custom made tray. By using the results, simulation
model was constructed.
Result: By the simulation, HbA1c levels declined over time and decreased to 6.0%. However, it took
at least 600 days to come up to 6.0%. The higher the level of HbA1c at baseline, the more time takes
to improve HbA1c level. Subjects with 7.3% HbA1c at baseline required 2,400 days to achieve 6.0%
HbA1c.
Conclusion: The results of this study suggest that HbA1c may be improved by oral bacterial control.
Clinical studies suggest that a long observational period is required to obtain high quality evidence.
Keywords: Oral hygiene; Hemoglobin A1c; Mixed effect model

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Feasibility Controlling Hemoglobin A1c by Oral Hygiene
Improvement: A Pilot StudyOJDOH: April-2019: Page No: 08-15

Cite this article as: Ayako Okada, Yoshiaki Nomura, Mayu Miyanohara, et al. 2019. Feasibility
Controlling Hemoglobin A1c by Oral Hygiene Improvement: A Pilot Study. Open J Dent Oral Health.
1: 08-15.
Copyright: 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 author and source are credited. Copyright © 2019; Ayako Okada

Introduction
The relationship between diabetes mellitus andperiodontal disease has been intensively
investigated [1-5]. These two diseases arecross-correlated. Evidence that diabetes is
associated with an increased risk ofperiodontitis has been demonstrated by many
epidemiological studies [6-8]. In contrast,
efficacy of treatment of periodontitis forglycemic control of patients with diabetes
mellitus is still elusive [9,10]. Systematic
reviews and meta-analyses of the effect of
periodontal treatment on glycemic control
results in the consistent finding that periodontal
treatment has been associated with a decreaseof about 0.4% in Hemoglobin A1c (HbA1c)[11-17]. One of the review papers conducted by
Cochrane Database of Systematic Review
concluded that glycemic control improves in
HbA1c with diabetes mellitus by the treatmentof periodontal disease; with a mean percentage
reduction rate of HbA1c is 0.29% after 3 to 4
months. The contents of periodontal treatment
were scaling and root planning. However,quality evidence was low. In addition, thisreview paper concluded that evidence to provethat observational period for the improvement
and maintenance of HbA1c after 4 months is
insufficient [13]. In another systematic review
concluded that auxiliary use of systemic
antibiotics does not result in a statisticallysignificant benefit in terms of HbA1c
improvement in periodontal treatment ofpatients with diabetes mellitus [18]. However,most of the observational periods of the study
used for the review was insufficient. The
majority of the observation period of the study
used for the review was three months. Diabetes

mellitus is a chronic disease and duration of thisdisease is long term.
There are several reports that diabetes mellitus
affected on oral microbiome composition. The
impact diabetes mellitus on the oral
microbiome composition has been studied. As
a consensus report from the European
Federation of Periodontology and the American
Academy of Periodontology, concluded that
diabetes has significant impact on the oral
microbiome composition [19]. However, one
reportsuggestedthat
Porphyromonas
gingivalis and Tannerella forsythia increased inpatients with diabetes mellitus [20].
Oral bacteria invade into blood vessels via
destroyed periodontal tissue. This phenomenon
is called dental bacteremia and this often occurs
in healthy subjects [21-23]. The major side
effect of diabetes mellitus is caused bybacteremia. Patients with diabetes mellitus areprone to be bacteremia [24]. Inhibiting
bacteremia can improve some symptoms ofbacteremia. If dental bacteremia can besuppressed by oral hygiene improvement
including periodontal treatment, some
symptoms diabetes mellitus may be improved.
However, conventional periodontal treatment
does not focus mainly on the elimination ofpathogenic bacteria. Therefore, management oforal bacteria may improve some symptoms of
diabetes mellitus. In this pilot study, we
monitored HbA1c after controlled oral bacteria
by antibiotics applicate only on the tooth
surface by an individual tray.

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Materials and Methods
Subjects
Male and four subjects with prediabetes
participated in this study. Subjects were notappropriately controlled by the treatment andhealth instruction. Their demographic data suchas gender, age, number of remaining teeth were
Case 1: Female, 72 years old, 20 tooth, Case 2:
Male, 68 years old, 18 tooth, Case 3: Male, 54
years old, 24 tooth, and Case 4: Male, 58 years
old, 19 tooth. Inclusion criteria was as follows:
without wearing removable dentures, without
periodontal disease symptoms and diabetes
mellitus status was diagnosed by physician as
prediabetes according to the Guideline of thecommittee of the Japan diabetes society on the
diagnostic criteria of diabetes mellitus [25].
Oral hygiene control
Dental plaque was removed by professional
mechanical tooth cleaning (PMTC). After
PMTC, gel containing cetylpyridinium chloride
were applied by individually fabricated try for
5 minutes as professional care. The subjects
were instructed to control dental plaque by drug
application using individual tray after toothbrush every day as a home care [26-29].
HbA1c Measurements
Blood level HbA1c was measures by
ADAMUS A1c HA-8182 (ARKREY, Osaka,
Japan).
Statistical analysis
As HbA1c levels were tested in each anticipantand measured repeatedly. We applied
multilevel analysis [30]. The model used in thisstudy were specified as follows:
Data Structure: subject
Probability distribution: γ
Link function: Log
In what follows, fixed effects (resp. random
effects or error terms) are denoted by Greek
letters (resp. Alphabet)

Model
Subjects, tooth and time are indexed by ijk.
− L1: 𝑃𝑜 (HbA1c)𝑖𝑗𝑘= 𝑃𝑜 (𝜇𝑖𝑗𝑘 ) = 𝜋0𝑖𝑗𝑘+ 𝜋1𝑗𝑘 (subject)𝑖𝑗𝑘 + 𝜀𝑖𝑗𝑘
− L2: 𝜋0𝑗𝑘(𝑚)

= 𝛽00𝑘3(𝑚)+ ∑ 𝛽001 (days indexed by 𝑚)𝑗𝑘
𝑚=2(𝑚)
+ 𝛽002 (HbA1c at baseline indexed by 𝑚)𝑗𝑘 𝑟0𝑗𝑘

− L2: 𝜋1𝑗𝑘 = 𝛽10𝑘
where HbA1c ~𝛾(𝛼𝑖𝑗𝑘 , 𝜏𝑖𝑗𝑘 ) with 𝜇𝑖𝑗𝑘
= 𝛼𝑖𝑗𝑘 /𝜏𝑖𝑗𝑘
𝑒𝑖𝑗𝑘 ~𝑁(0, 𝛿𝑒2 ), 𝑟0𝑗𝑘 ~𝑁(0, 𝛿𝑟2 ), and 𝑢01𝑘 ~𝑁(0, 𝛿𝑢2(𝑚) )Fixed effect: days, HbA1c at baseline
Random effect: days
Covariance Type: AR1
These analyses were carried out by IBM SPSS
Statistics ver 24.0 (IBM, Tokyo, Japan). The
simulation was carried out by IBM SPSS
Modeler ver 18.0 (IBM, Tokyo, Japan).
EthicsThis study was approved by the Ethicalcommittee of Tsurumi University School of
Dental Medicine (Approval Number: 1304).

Results
Figure 1 shows the transition of HbA1c levels
after oral hygiene control of four subjects.
HbA1c levels fluctuated, however, the data
seemed to be improved. Using these data, themixed effect model specified by Method wasconstructed. The constructed model was shownin Table 1. Baseline HbA1c level was animportant predictor of changes in HbA1c levels
following oral hygiene treatment. Figure 2
shows a scatter plot of predicted values of
HbA1c levels against observed HbA1c levels.
Linearity was observed for 6.0 - 7.5% of HbA1c
at baseline. Finally, we simulated the transitionof HbA1c after oral hygiene treatment. Using
the simulation data, predicted values were
calculated by the mixed effect model shown inPage: 10
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Table 1. The response surface is illustrated in
Figure 3. HbA1c levels declined over time anddecreased to 6.0%. However, it takes at least
600 days to come up to 6.0%. The higher thelevel of HbA1c at baseline, the more time takes

to improve HbA1c level. Subjects with 7.3%
HbA1c at baseline required 2,400 days toachieve 6.0% HbA1c by simulation.

Figure 1: Transition of HbA1c levels after oral hygiene treatment. HbA1c level was improved for thetwo subjects with more than 6.5% HbA1c level at baseline.

Figure 2: Scatter plot of predictive values against observed values of HbA1c. Predictive values of
HbA1c was calculated by the mixed effect model shown in Table1.

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Table 1: Mixed effect model to predict the HbA1c after oral hygiene treatment.
Coefficient
95%CI
P - value
HbA1c at Baseline
0.187
0.124 - 0.249< 0.001Time< 0.001< 0.001 - < 0.001
0.423Intercept
0.635
0.195 - 1.075
0.006
Coefficient of HbA1c level at baseline was statistically significant. Details of model specification was
described in Method.

Figure 3: The response surface of the simulation of transition of HbA1c. HbA1c levels were decreased
with the time passes and it come up to 6.0%. However, it takes at least 600 days. The higher levels of
HbA1c at baseline, the more time is necessary to improve HbA1c levels. Subjects with 7.3% HbA1c atbaseline, 2400 days were necessary to attain 6.0% HbA1c by the simulation.

Discussion and Conclusion
In this study, the statistical model and its
simulation clearly showed that HbA1c was
improved by controlling oral bacteria. First, weestablished a methodology of selective
elimination mutans streptococci from the oralcavity [28]. By the fabrication of individual
tray, antibiotics can selectively deliver to thetooth surface, without oral mucosal
microbiome. We called this drug delivery
system as dental drug delivery systemabbreviated as 3DS [25-28]. Biofilm that
contains pathogenic oral bacteria selectively
formed on the tooth surface as a biofilm.

Controlling the biofilm on the tooth surface isthe key element of oral hygiene.
This methodology is applicable to periodontal
pathogens. To improve the periodontal
conditions and by the elimination of periodontal
pathogens, dental bacteremia may besuppressed [30,31]. Dental bacteremia causes
the weak but contentious damage to bloodvessels. We are currently studying the effect of
this method to control oral bacteremia to obtainhealthy blood vessels. The relationship between
periodontal disease and systemic health has
been investigated. One of the importantelements of this relationship is dental
bacteremia. Several studies have shown that

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endothelial dysfunction was improved bycontrolling oral bacteria [32-34].
The molecular mechanisms of diabetes mellitus
by dental bacteria is still inconclusive. Whenoral bacteria form patients with diabetes
mellitus transferred to normal germ-free mice,osteoclast genesis and periodontal bone loss
were induced [35]. Diabetes mellitus increases
IL-17 expression, leading to altered virulenceof oral microorganisms and increased
periodontal inflammation [36]. However, oral
pathogens directly affect diabetes mellitus.
Further studies are needed to reveal the effectsof oral pathogens on diabetes mellitus. The
results of simulation in this study showed thatoral bacterial control resulted in improved
HbA1c levels. However, it may take at least 600
days and the subjects with 7.3% of HbA1c atbaseline required 2,400 days to recover to 6.0%
HbA1c.
Even through Cochrane Database of Systematic
Review concluded that treatment of periodontal
disease by scaling and root plaining does
improve glycemic control in patients withdiabetes, with a mean percentage reduction in
HbA1c of 0.29% at 3 - 4 months [12]. The
average decline rate of HbA1c it is 0.29% in 3
- 4 months and quality of this evidence is low.
The papers reviewed in this systematic review,
the observational period for the five studies was
6 months [37] and the observation period of theother studies was 3 to 4 months. Evidence
suggested by clinical studies was low due to theshort observational period.
Another systematic review showed thatcombination therapy of conventional therapy
and systemic antibiotics did not produce
statistically significant benefits in terms of
HbA1c improvement in periodontal treatmentof patients with diabetes [13]. The
observational period of the studies reviewed
were up to 6 months. In addition, contentious
intake antibiotics for periodontal treatment andsubsequent oral microbial improvement may
not apply. In this concept, a specific drugdelivery system is required. The methodology
to control oral bacteria, by using individuallyfabricate tray, without disturbing mucosal
microbiome can be a candidate for long-term
control of oral microbiome.
In conclusion, the results of this preliminary
study indicated that HbA1c levels can becontrolled by improving oral hygiene
conditions. To control oral bacteria, 3DS may
be the best way to control bacteria in the oralcavity. Evidence suggested by clinical studies
was low due to the short observational period.

Acknowledgments
This study was supported by JSPS KAKENHI
Grant Numbers 17K12030.

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