Introduction
Diabetes mellitus is a well-predicted risk factor
for periodontal disease, and conversely, periodontitis is thought
to affect the systemic inflammatory condition, insulin resistance,
and lipid and glucose metabolism (1,2). Being
a chronic metabolic disease, it is caused by the body's failure
either to produce the insulin hormone or to use insulin production
effectively. Insulin is a hormone produced by the pancreas which
enables the body to direct glucose from the bloodstream to cells
for energy. Without this vital hormone, glucose builds up in the
bloodstream and can lead to life-threatening and debilitating
complications (3). Glycemic control
is a key issue in the care of people with type 2 diabetes mellitus
(T2DM). Hyperglycemia is the main cause of the progressive
microvascular complications associated with diabetes (retinopathy,
nephropathy, neuropathy) (4-9).
Periodontitis is a chronic inflammation of the
tissues surrounding the teeth, due to the biofilm accumulation, in
the absence of proper oral hygiene, that leads to formation of
pockets between the teeth and gums, loss of periodontal support and
bone [clinical attachment loss (CAL) and bone loss] which could
lead to tooth mobility and subsequently the need to remove the
teeth.
The biofilm is composed of more than 1,000 different
species of microorganisms but some strictly anaerobic bacteria such
as Porphyromonas gingivalis, Tannerella forsythia,
Treponema denticola and Aggregatibacter
atinomycetemcomitans are frequently associated with the
initiation and perpetuation of periodontitis (10-12).
A bi-directional association between periodontitis
and diabetes has been postulated (13). The relationship between diabetes and
chronic periodontitis has recently attracted the attention of
researchers worldwide. Many studies have suggested a two-way
relationship between diabetes mellitus and chronic periodontitis.
Over the years, epidemiological studies have consistently reported
that increased incidence, prevalence and acuity of periodontitis is
found among adults with T2DM (14).
The incidence of periodontitis increases as diabetic patients age
and is both more frequent and more severe in T2DM patients with
advanced systemic complications (15). Poor glycemic control may be
associated with an increased risk of periodontal disease or
increased severity of periodontal disease in patients with
diabetes. T2DM is therefore considered to be one of the risk
factors for periodontal disease (16), and improving glycemic control can
reduce the pathological progression of periodontal disease
(17,18). There is also a vice versa assumption
that periodontitis is considered to increase the risk of developing
diabetes mellitus (14).
Current scientific evidence suggests that better
metabolic control brings significant benefits to the treatment of
chronic periodontitis. In consequence, the main aim of the current
research study was to assess the correlation between glycemic
control and clinical periodontal aspects in patients with T2DM
associated with generalized chronic periodontitis; moreover, some
particular aspects regarding this association were followed,
suggesting the possibility of a protocol that associates the
treatment of chronic periodontal disease as a diagnostic
criterion/follow-up of subjects with T2DM.
Patients and methods
This study was approved by the Ethics Commission of
the Emergency Clinical County Hospital of Oradea, Oradea, Romania,
and was conducted respecting the World Medical Association (WMA)
Code of Ethics, Declaration of Helsinki 1967(19). All patients were verbally informed,
and they signed an informed consent form.
From the initial group of 279 patients, due to the
selection criteria, 182 patients (age range, 40-68 years) diagnosed
with T2DM and generalized chronic periodontitis completed the study
and were evaluated in two private dental clinics in Oradea,
Romania, from July 2018 to February 2020.
The inclusion criteria were as follows: i) ≥40 yeas
of age; ii) confirmed type 2 diabetes for at least 5 years; iii)
diagnosis of chronic generalized periodontitis; iv) history of T2DM
therapy.
The exclusion criteria were as follows: i) Smoker or
tobacco use in any form, in the preceding 5 years; ii) pregnant or
lactating; iii) mouth washing with antimicrobial agent in the past
2 months; iv) chronic disease, excluding DM, associated periodontal
disease; v) periodontal or/and antibiotic therapy in the preceding
6 months.
The participants were divided into two groups,
according to the determined HbA1c levels. Group 1 included patients
with HbAc1 <7% (considered to have a good glycemic control) and
Group 2 comprised of patients with HbAc1 ≥7% (considered to have a
poor glycemic control).
Fasting blood glucose (FBG) from venous blood was
determined using glucose oxidase method, expressed in milligrams
per deciliter (mg/dl), while HbA1c was determined using
high-performance liquid chromatography (HPLC) and expressed as a
percentage. All the patients underwent a periodontal evaluation
using a manual periodontal probe (PCP-UNC15; Hu Friedy). The
periodontal parameters recorded were as follows: PI (plaque index),
BoP (bleeding on probing), PD (probing depth) and CAL (clinical
attachment level). The percentage of PD ≥5 mm and CAL ≥5 mm sites
and the number of remaining teeth for each individual were also
recorded.
From the point of view of statistical analysis, in
order to examine the data distribution, the normality
Kolmogorov-Smirnov test was used; also, because the data had a
normal distribution (P>0.05), analysis was performed using
parametric methods. PD and CAL were dichotomized into <5 or ≥5
mm. The full-mouth mean percentage of sites with visible plaque,
BoP, PD ≥5 mm, CAL ≥5 mm and SUP, the full-mouth mean PD and CAL
were determined for each subject. The clinical parameters were also
grouped into subsets of glycemia, according to two, <7% (good
glycemic control) and ≥7% (poor glycemic control) levels of HbA1c.
Values for each clinical parameter were averaged separately within
the two glycemic categories. The clinical parameters between HbA1c
subsets <7 and ≥7% were compared by Student's t-test. The
Chi-square test was used to detect differences in the frequencies
of sex and DM treatment regimen among the glycemic groups. A value
of P<0.05 was considered statistically significant.
Results
A total of 279 patients were screened at two private
dental clinics in Oradea, Romania from July 2018 to February 2020.
The study was completed by 182 participants on the basis of
inclusion/exclusion criteria, divided in two groups. The percentage
of uncontrolled diabetic subjects (Group 2) was higher than that of
the well-controlled subjects (Group 1) (57.15 vs. 42.85%);
uncontrolled diabetes being correlated with increased levels of
HbAc1 and FPG. Age, sex, duration of DM, and diet did not have any
statistical significance between the two groups; for the numerical
variables we applied a Student t-test and for the qualitative
variable we applied the Chi-square test. Data resulted are depicted
in Table I.
 | Table IDiabetes parameters. |
Table I
Diabetes parameters.
| Parameters | HbA1c <7% (Group
1) | HbA1c ≥7% (Group
2) | P-value |
|---|
| No. of subjects
(%) | 78 (42.85%) | 104 (57.15%) | <0.01 |
| Mean age (years) | 54.2±6.8 | 53.7±7.1 | 0.63 |
| Sex (% men) | 48.1 | 49.03 | 0.9 |
| Duration of DM
(years) | 6.3±1.5 | 5.9±1.8 | 0.11 |
| Diet (%) | 100 | 100 | >0.05 |
| Diet + oral
hypoglycemic agents (%) | 58.23 | 50.00 | 0.27 |
| Diet + insulin
(%) | 29.11 | 35.58 | 0.35 |
| Diet + insulin + oral
hypoglycemic agents (%) | 12.66 | 14.42 | 0.73 |
| Mean FPG (mg/dl) | 124±34.8 | 146±46.8 | <0.01 |
The mean full-mouth plaque accumulation index
(74.2±25.2 vs. 62.5±28.7%, P<0.01), as well as the mean PD
(3.78±0.9 vs. 3.42±0.8 mm, P<0.01), and mean CAL (4.5±1.2 vs.
4.1±1.2 mm, P=0.02) were significantly higher in Group 2 patients
when compared with Group 1 patients. The sites with PD ≥5 mm were
statistically more prevalent in patients with HbA1c ≥7% than that
in patients with HbA1c <7% (27.8±6.2 vs. 23.4±5.8%, P<0.01).
The mean number of remaining teeth was statistically significantly
lower in Group 2 patients (18.5±3.2 vs. 20.4±4.1, P<0.01) than
in that in Group 1 patients. For the numerical variables, a
Student's t-test was applied and for the qualitative variable we
used the Chi-square test. The results that were obtained are
presented in Table II.
| Table IIPeriodontal parameters. |
Table II
Periodontal parameters.
| Parameters | HbA1c <7% (Group
1) | HbA1c ≥7% (Group
2) | P-value |
|---|
| Mean full-mouth
plaque accumulation (%) | 62.5±28.7 | 74.2±25.2 | <0.01 |
| Mean full-mouth PD
(mm) | 3.42±0.8 | 3.78±0.9 | <0.01 |
| Mean full-mouth CAL
(mm) | 4.1±1.2 | 4.5±1.2 | 0.02 |
| Mean full-mouth BoP
(%) | 45.24±27.5 | 47.90±30.1 | 0.53 |
| Mean full-mouth SUP
(%) | 2.7±2.1 | 3.1±2.8 | 0.28 |
| Sites with PD ≥5 mm
(%) | 23.4±5.8 | 27.8±6.2 |
<0.01 |
| Sites with CAL ≥5
mm (%) | 43.7±12.1 | 42.6±13.5 | 0.56 |
| Number of teeth
(n) | 20.4±4.1 | 18.5±3.2 |
<0.01 |
Discussion
Current literature suggests two-way
inter-relationships between diabetes mellitus and periodontitis
(20). Previous longitudinal
studies have shown associations between baseline periodontitis and
diabetes incidence (21-24)
whereas one showed no association (25). Few cross-sectional studies showed
periodontitis to be associated with precursors of diabetes
(26-30).
Consequently, since periodontitis-diabetes interactions may have a
negative effect on patient glycemic control, the management of
highly prevalent periodontal disease in diabetic patients is
beneficial in improving overall health status.
The exact mechanisms by which glycemic control
influences periodontal disease and its treatment may affect
glycemic control, in patients with type 2 diabetes mellitus (T2DM),
have not been fully elucidated. A popular hypothesis involves
inflammatory pathways common to periodontitis and insulin
resistance pathogenesis (20).
Botero et al showed that the reduction in
HbA1c values (0.23 to 1.03%) was significant for the treatment of
T2DM (31). However, it was
observed that for every percentage point decrease in HbAlc (e.g. 9
to 8%), there was a 35% reduction in the risk of complications,
with periodontal disease being a major complication of diabetes
(32). Therefore, it is
biologically plausible that periodontitis may exacerbate glycemia
in T2DM patients, and that treatment may improve glycemic control
by reducing circulating cytokine levels (33).
Preshaw et al and Winning et al
reported similar results with our findings. Therefore, the number
of poor glycemic control patients was higher than the number of
good glycemic control patients. Increased values were found in poor
glycemic control patients, when comparing the periodontal
parameters of the two groups (PD, CAL, BoP and SUP) (20,21).
The most striking changes in uncontrolled diabetes
are the reduction in defense mechanism and the increased
susceptibility to infections, leading to destructive periodontal
disease. The glucose content of gingival fluid and blood is higher
in individuals with diabetes than in those without diabetes, with
similar plaque and GI scores (34).
The increased glucose in the gingival fluid and blood of diabetic
patients could change the environment of the microflora, inducing
qualitative changes in bacteria that could contribute to the
severity of periodontal disease observed in those with poorly
controlled diabetes. In patients with poorly controlled diabetes,
the function of polymorphonuclear granulocytes (PMNs) and
monocytes/macrophages is impaired (35), and as a result, the primary defense
(PMNs) against periodontal pathogens is diminished, and bacterial
proliferation is more likely.
The correlation between worsening periodontitis and
poor glycemic control in the Group 2 patients was also reflected in
the reduced number of teeth (mean value of 20.4 in Group 1 vs. 18.5
in Group 2). This result was in accordance with a study performed
by Joshipura et al (13).
The presence of periodontitis increases the risk of worsening of
glycemic control over time. For example, in a 2-year longitudinal
trial, diabetic subjects with severe periodontitis at baseline had
a six-fold increased risk of worsening of glycemic control over
time compared to diabetic subjects without periodontitis (36).
Group 2 patients had significantly worse periodontal
status, deeper periodontal pocket and higher attachment loss.
Increased bleeding on probing and suppuration index were also
increased for Group 2 patients. These results are in concordance
with the findings reported by Wu et al in a systematic
review (37).
Periodontitis may also be associated with an
increased risk of other diabetic complications, as seen in a
longitudinal case-control study in which 82% of diabetic patients
with severe periodontitis experienced the onset of one or more
major cardiovascular, cerebrovascular, or peripheral vascular
events compared to only 21% of diabetic subjects without
periodontitis (13).
Although many diabetic patients show improvement in
clinical parameters of disease immediately after therapy, patients
with poorer glycemic control may have a more rapid recurrence of
deep pockets and a less favorable long-term response (38).
As the present research proves once again by the
results obtained, it is recommended that the criterion of inclusion
of patients with periodontal treatment may be an important part of
the protocol for the management of diabetic patients.
In conclusion, the severity and extension of
generalized chronic periodontitis are higher in T2DM patients with
poor glycemic control compared to patients with good glycemic
control.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
Data of the patients are registered at the Clinical
County Emergency Hospital of Oradea, Bihor, Romania and at the two
private dental clinics, Oradea, Romania. Any further information
concerning the study is available from the corresponding author
upon reasonable request.
Authors' contributions
MS, HC, AT and IT made the interventions and
collected, analyzed and interpreted the patient data regarding
pre-intervention and post-intervention evolution. SN, AP, CB and
IIR made substantial contributions to the conception of the work
and interpretation of data; also, they drafted the manuscript and
were major contributors in writing the manuscript. All authors read
and approved the final manuscript to be published. All the authors
agreed to be accountable for all aspects of the work in ensuring
that questions related to the accuracy or integrity of any part of
the work are appropriately investigated and resolved.
Ethics approval and consent to
participate
This research was authorized by the Ethics
Commission of the Emergency Clinical County Hospital of Oradea,
Oradea, Romania, and conducted respecting the World Medical
Association (WMA) Code of Ethics (Declaration of Helsinki
1967).
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing
interests.
References
|
1
|
Singh M, Bains VK, Jhingran R, Srivastava
R, Madan R, Maurya SC and Rizvi I: Prevalence of periodontal
disease in type 2 diabetes mellitus patients: A cross-sectional
study. Contemp Clin Dent. 10:349–357. 2019.PubMed/NCBI View Article : Google Scholar
|
|
2
|
Vesa CM, Popa L, Popa AR, Rus M, Zaha AA,
Bungau S, Tit DM, Corb Aron RA and Zaha DC: Current data regarding
the relationship between type 2 diabetes mellitus and
cardiovascular risk factors. Diagnostics. 10(314)2020.PubMed/NCBI View Article : Google Scholar
|
|
3
|
Simpson TC, Weldon JC, Worthington HV,
Needleman I, Wild SH, Moles DR, Stevenson B, Furness S and
Iheozor-Ejiofor Z: Treatment of periodontal disease for glycaemic
control in people with diabetes mellitus. Cochrane Database Syst
Rev: Nov 6, 2015 (Epub ahead of print). doi:
10.1002/14651858.CD004714.pub3.
|
|
4
|
Grant RW and Kirkman MS: Trends in the
evidence level for the American Diabetes Association's ‘Standards
of Medical Care in Diabetes’ from 2005 to 2014. Diabetes Care.
38:6–8. 2015.PubMed/NCBI View Article : Google Scholar
|
|
5
|
Dobrică EC, Găman MA, Cozma MA, Bratu OG,
Pantea Stoian A and Diaconu CC: Polypharmacy in type 2 diabetes
mellitus: Insights from an internal medicine department. Medicina
(Kaunas). 55(436)2019.PubMed/NCBI View Article : Google Scholar
|
|
6
|
Iorga RA, Bacalbasa N, Carsote M, Bratu
OG, Stanescu AM, Bungau S, Pantis C and Diaconu CC: Metabolic and
cardiovascular benefits of GLP-1 agonists, besides the hypoglycemic
effect (Review). Exp Ther Med. 20:2396–400. 2020.PubMed/NCBI View Article : Google Scholar
|
|
7
|
Diaconu C, Salmen T, Găman MA, Bratu OG,
Mischianu D, Marcu RD, Suceveanu AI, Costache RS and Pantea Stoian
A: SGLT2 inhibition in patients with type 2 diabetes and
cardiovascular diseases: Which are the benefits? Rom J Mil Med.
122:16–21. 2019.
|
|
8
|
Zaha CD, Vesa C, Uivarosan D, Bratu O,
Fratila O, Tit DM, Pantis C, Diaconu CC and Bungau S: Influence of
inflammation and adipocyte biochemical markers on the components of
metabolic syndrome. Exp Ther Med. 20:121–128. 2020.PubMed/NCBI View Article : Google Scholar
|
|
9
|
Popa AR, Fratila O, Rus M, Aron RA, Vesa
CM, Pantis C, Diaconu CC, Bungau S and Nemeth S: Risk factors for
adiposity in the urban population and influence on the prevalence
of overweight and obesity. Exp Ther Med. 20:129–133.
2020.PubMed/NCBI View Article : Google Scholar
|
|
10
|
Kumar PS: Oral microbiota and systemic
disease. Anaerobe. 24:90–93. 2013.PubMed/NCBI View Article : Google Scholar
|
|
11
|
Zaha DC, Bungau S, Aleya S, Tit DM, Vesa
CM, Popa AR, Pantis C, Maghiar OA, Bratu OG, Furau C, et al: What
antibiotics for what pathogens? The sensitivity spectrum of
isolated strains in an intensive care unit. Sci Total Environ.
687:118–127. 2019.PubMed/NCBI View Article : Google Scholar
|
|
12
|
Zaha DC, Bungau S, Uivarosan D, Tit DM,
Maghiar TA, Maghiar O, Pantis C, Fratila O, Rus M and Vesa CM:
Antibiotic consumption and microbiological epidemiology in surgery
departments: Results from a single study center. Antibiotics Basel.
9(81)2020.PubMed/NCBI View Article : Google Scholar
|
|
13
|
Joshipura KJ, Muñoz-Torres FJ, Dye BA,
Leroux BG, Ramírez-Vick M and Pérez CM: Longitudinal association
between periodontitis and development of diabetes. Diabetes Res
Clin Pract. 141:284–293. 2018.PubMed/NCBI View Article : Google Scholar
|
|
14
|
Mealey BL and Oates TW: Diabetes mellitus
and periodontal diseases. J Periodontol. 77:1289–1303.
2006.PubMed/NCBI View Article : Google Scholar
|
|
15
|
Löe H: Periodontal disease. The sixth
complication of diabetes mellitus. Diabetes Care. 16:329–334.
1993.PubMed/NCBI
|
|
16
|
Jimenez M, Hu FB, Marino M, Li Y and
Joshipura KJ: Type 2 diabetes mellitus and 20 year incidence of
periodontitis and tooth loss. Diabetes Res Clin Pract. 98:494–500.
2012.PubMed/NCBI View Article : Google Scholar
|
|
17
|
Katagiri S, Nitta H, Nagasawa T, Izumi Y,
Kanazawa M, Matsuo A, Chiba H, Fukui M, Nakamura N, Oseko F, et al:
Effect of glycemic control on periodontitis in type 2 diabetic
patients with periodontal disease. J Diabetes Investig. 4:320–325.
2013.PubMed/NCBI View Article : Google Scholar
|
|
18
|
Goyal L, Gupta ND and Bey A: Periodontal
therapy: A useful adjunct to improve glycemic control. J Pharm
Bioallied Sci. 4:173–174. 2012.PubMed/NCBI View Article : Google Scholar
|
|
19
|
World Medical Association declaration of
Helsinki. Recommendations guiding physicians in biomedical research
involving human subjects. JAMA. 277:925–926. 1997.PubMed/NCBI
|
|
20
|
Preshaw PM, Alba AL, Herrera D, Jepsen S,
Konstantinidis A, Makrilakis K and Taylor R: Periodontitis and
diabetes: A two-way relationship. Diabetologia. 55:21–31.
2012.PubMed/NCBI View Article : Google Scholar
|
|
21
|
Winning L, Patterson CC, Neville CE, Kee F
and Linden GJ: Periodontitis and incident type 2 diabetes: A
prospective cohort study. J Clin Periodontol. 44:266–274.
2017.PubMed/NCBI View Article : Google Scholar
|
|
22
|
Miyawaki A, Toyokawa S, Inoue K, Miyoshi Y
and Kobayashi Y: Self-reported periodontitis and incident type 2
diabetes among male workers from a 5-year follow-up to MY Health Up
Study. PLoS One. 11(e0153464)2016.PubMed/NCBI View Article : Google Scholar
|
|
23
|
Chiu SY, Lai H, Yen AM, Fann JC, Chen LS
and Chen HH: Temporal sequence of the bidirectional relationship
between hyperglycemia and periodontal disease: A community-based
study of 5,885 Taiwanese aged 35-44 years (KCIS No. 32). Acta
Diabetol. 52:123–131. 2015.PubMed/NCBI View Article : Google Scholar
|
|
24
|
Demmer RT, Jacobs DR Jr and Desvarieux M:
Periodontal disease and incident type 2 diabetes: Results from the
First National Health and Nutrition Examination Survey and its
epidemiologic follow-up study. Diabetes Care. 31:1373–1379.
2008.PubMed/NCBI View Article : Google Scholar
|
|
25
|
Kebede TG, Pink C, Rathmann W, Kowall B,
Völzke H, Petersmann A, Meisel P, Dietrich T, Kocher T and
Holtfreter B: Does periodontitis affect diabetes incidence and
haemoglobin A1c change? An 11-year follow-up study. Diabetes Metab.
44:243–249. 2008.PubMed/NCBI View Article : Google Scholar
|
|
26
|
Benguigui C, Bongard V, Ruidavets JB,
Chamontin B, Sixou M, Ferrières J and Amar J: Metabolic syndrome,
insulin resistance, and periodontitis: A cross-sectional study in a
middle-aged French population. J Clin Periodontol. 37:601–608.
2010.PubMed/NCBI View Article : Google Scholar
|
|
27
|
Demmer RT, Squillaro A, Papapanou PN,
Rosenbaum M, Friedewald WT, Jacobs DR Jr and Desvarieux M:
Periodontal infection, systemic inflammation, and insulin
resistance: Results from the continuous National Health and
Nutrition Examination Survey (NHANES) 1999-2004. Diabetes Care.
35:2235–2242. 2012.PubMed/NCBI View Article : Google Scholar
|
|
28
|
Islam SK, Seo M, Lee YS and Moon SS:
Association of periodontitis with insulin resistance, β-cell
function, and impaired fasting glucose before onset of diabetes.
Endocr J. 62:981–989. 2015.PubMed/NCBI View Article : Google Scholar
|
|
29
|
Song IS, Han K, Park YM, Ji S, Jun SH, Ryu
JJ and Park JB: Severe periodontitis is associated with insulin
resistance in non-abdominal obese adults. J Clin Endocrinol Metab.
101:4251–4259. 2016.PubMed/NCBI View Article : Google Scholar
|
|
30
|
Timonen P, Suominen-Taipale L, Jula A,
Niskanen M, Knuuttila M and Ylöstalo P: Insulin sensitivity and
periodontal infection in a non-diabetic, non-smoking adult
population. J Clin Periodontol. 38:17–24. 2011.PubMed/NCBI View Article : Google Scholar
|
|
31
|
Botero JE, Rodríguez C and Agudelo-Suarez
AA: Periodontal treatment and glycaemic control in patients with
diabetes and periodontitis: An umbrella review. Aust Dent J.
61:134–148. 2016.PubMed/NCBI View Article : Google Scholar
|
|
32
|
Genuth S, Eastman R, Kahn R, Klein R,
Lachin J, Lebovitz H, Nathan D and Vinicor F: American Diabetes
Association. Implications of the United Kingdom prospective
diabetes study. Diabetes Care. 26 (Suppl 1):S28–S32.
2003.PubMed/NCBI View Article : Google Scholar
|
|
33
|
DPTT study group. Engebretson S, Gelato M,
Hyman L, Michalowicz BS and Schoenfeld E: Design features of the
diabetes and periodontal therapy trial (DPTT): A multicenter
randomized single-masked clinical trial testing the effect of
nonsurgical periodontal therapy on glycosylated hemoglobin (HbA1c)
levels in subjects with type 2 diabetes and chronic periodontitis.
Contemp Clin Trials. 36:515–526. 2013.PubMed/NCBI View Article : Google Scholar
|
|
34
|
Ficara AJ, Levin MP, Grower MF and Kramer
GD: A comparison of the glucose and protein content of gingival
fluid from diabetics and nondiabetics. J Periodontal Res.
10:171–175. 1975.PubMed/NCBI View Article : Google Scholar
|
|
35
|
Iacopino AM: Periodontitis and diabetes
interrelationships: Role of inflammation. Ann Periodontol.
6:125–137. 2001.PubMed/NCBI View Article : Google Scholar
|
|
36
|
Taylor GW, Burt BA, Becker MP, Genco RJ,
Shlossman M, Knowler WC and Pettitt DJ: Severe periodontitis and
risk for poor glycemic control in patients with
non-insulin-dependent diabetes mellitus. J Periodontol.
67:1085–1093. 1996.PubMed/NCBI View Article : Google Scholar
|
|
37
|
Wu CZ, Yuan YH, Liu HH, Li SS, Zhang BW,
Chen W, An Z, Chen S, Wu Y, Han B, et al: Epidemiologic
relationship between periodontitis and type 2 diabetes mellitus.
BMC Oral Health. 20(204)2020.PubMed/NCBI View Article : Google Scholar
|
|
38
|
Tervonen T and Karjalainen K: Periodontal
disease related to diabetic status. A pilot study of the response
to periodontal therapy in type 1 diabetes. J Clin Periodontol.
24:505–510. 1997.PubMed/NCBI View Article : Google Scholar
|
