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Referência usada por mim na revisão de literatura nos tópicos: 2.1 DIABETES MELLITUS, 2.3.3 Tratamento para a melhora mútua das doenças

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Referência usada por mim na revisão de literatura nos tópicos: 2.1 DIABETES MELLITUS, 2.3.3 Tratamento para a melhora mútua das doenças

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SIMPSON, T. C. et al. Treatment of periodontitis for glycaemic control in people with diabetes mellitus. Cochrane database of systematic reviews, [s. l.], v. 4, p. 1-134, 2022. DOI:https://doi.org/10.1002/14651858.CD004714.pub4. Disponível em: https://www.cochranelibrary.com/cdsr/doi/10.1002/14651858.CD004714.pub4/full. Acesso em: 3 maio 2025.

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Treatment of periodontitis for glycaemic control in people with diabetes mellitus - Simpson, TC - 2022 | Cochrane Library

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Referência usada por mim na revisão de literatura nos tópicos: 2.1 DIABETES MELLITUS, 2.3 RELAÇÃO BIDIRECIONAL ENTRE A DIABETES MELLITUS E A PERIODONTITE, 2.3.1 Hiperglicemia, 
2.3.3 Tratamento para a melhora mútua das doenças

# data[].attributes.subject
Referência usada por mim na revisão de literatura nos tópicos: 2.1 DIABETES MELLITUS, 2.3 RELAÇÃO BIDIRECIONAL ENTRE A DIABETES MELLITUS E A PERIODONTITE, 2.3.1 Hiperglicemia, 
2.3.3 Tratamento para a melhora mútua das doenças

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GENCO, R. J; BORGNAKKE, W. S. Diabetes as a potential risk for periodontitis: association studies. Periodontology 2000, [s. l.], v. 83, n. 1, p. 59-63, June 2020. DOI: https://doi.org/10.1111/prd.12271. Disponível em: https://onlinelibrary.wiley.com/doi/10.1111/prd.12271. Acesso em: 1 maio 2025.

# data[].attributes.headline
Referência usada por mim na revisão de literatura nos tópicos: 2.1 DIABETES MELLITUS, 2.3 RELAÇÃO BIDIRECIONAL ENTRE A DIABETES MELLITUS E A PERIODONTITE, 2.3.2 Microbiota oral, 2.3.3 Tratamento para a melhora mútua das doenças

# data[].attributes.subject
Referência usada por mim na revisão de literatura nos tópicos: 2.1 DIABETES MELLITUS, 2.3 RELAÇÃO BIDIRECIONAL ENTRE A DIABETES MELLITUS E A PERIODONTITE, 2.3.2 Microbiota oral, 2.3.3 Tratamento para a melhora mútua das doenças

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TAN, L. et al. Association between periodontitis and the prevalence and prognosis of prediabetes: a population-based study. Journal of Translational Medicine, [s. l.], v. 21, n. 484, p. 1-10, July 2023. DOI: https://doi.org/10.1186/s12967-023-04340-y. Disponível em: https://translational-medicine.biomedcentral.com/articles/10.1186/s12967-023-04340-y#citeas. Acesso em: 1 maio 2025.

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Abstract

Background

Diagnosis and intervention of prediabetes is an emerging method for preventing diabetic progression and complications. Periodontitis has been reported to strongly correlate with the dysregulation of glucose metabolism. Nonetheless, the relationship between periodontal status and the prevalence of prediabetes as well as its prognosis remains elusive. This study aimed to investigate the association of periodontitis with the prevalence of prediabetes and furtherly explore the all-cause mortality of different periodontal status among patients with prediabetes.

Methods

The dateset from the National Health and Nutrition Examination Survey (NHANES) was utilized for our study. Participants were divided into two groups (with or without periodontitis) and further assigned into subgroups by different grades of periodontitis to analyze the association between periodontitis and prevalence of prediabetes. Then we analyzed the association between all-cause mortality and periodontitis among patients with prediabetes. Weighted multivariate logistic/Cox regression models were adopted in our study.

Results

A total of 15390 participants were included and divided into a periodontitis group (n = 5033) and a nonperiodontitis group (n = 10357). The results showed that participants with periodontitis had a higher risk of prediabetes. After adjusting for covariables, more severe periodontitis was positively related to prediabetes (moderate vs. no periodontitis: OR = 1.46, 95% CI: 1.29-1.65; severe vs. no periodontitis: OR = 1.62, 95% CI 1.31-2.01). Furtherly, we explored the association between all-cause mortality and periodontal status among patients diagnosed with prediabetes (n = 4518) and found that severe (HR = 1.806, 95% CI 1.19-2.74) and moderate periodontitis (HR = 2.42, 95% CI 1.95-3.01) were associated with elevated all-cause mortality among patients with prediabetes.

Conclusions

In general, the results suggest that periodontitis is positively associated with the prevalence and mortality of prediabetes. These results suggest that good management of periodontal status could be a potential strategy to reduce the occurrence and development of prediabetes.

Introduction

Prediabetes is the stage of intermediate hyperglycemia characterized by particular parameters, including impaired fasting glucose (IFG), impaired glucose tolerance (IGT) and specific scope of hemoglobin A1c (HbA1c) by The American Diabetes Association (ADA) [ 1]. Over the past few decades, the prevalence of prediabetes has been continuously increasing, with rates reaching as high as 43.5% in America [ 2]. Studies have shown that prediabetes patients have a higher risk of developing diabetes, cardiovascular complications and even death [ 3]. A recent study demonstrated that early management of prediabetes can alleviate the risk of progression to diabetes [ 4]. Despite this, attention and research toward prediabetes remains inadequate when compared to diabetes. Therefore, it is essential to identify more early interventions to prevent the progression of prediabetes to diabetes and cardiovascular complications.

As is commonly understood, individuals experiencing oral diseases are predisposed to metabolic dysregulation [ 5]. Periodontitis, a gradual and symptomless ailment, is a prevalent oral disease that results in tooth destruction and is generally irreversible [ 6]. The effects of periodontitis have been reported to be associated with cardiovascular complications in patients with dysglycemia, adversely impacting glycemic control [ 7]. A two-year follow-up study on the Indian population revealed that periodontitis was associated with an increased risk of poor glycemic control [ 8]. In addition, studies investigating the impact of periodontal treatment on glycemic control reported that a reduction in HbA1c of approximately 0.4% was found in diabetic patients with periodontal treatment [ 9]. Nevertheless, whether patients afflicted with periodontitis have a high risk of developing prediabetes and death has yet to be ascertained.

Currently, there are no effective methods to avert the onset of prediabetes. Hence, we attempted to find an early marker for prediabetes and intervene accordingly. Based on the findings of the association between periodontitis and glycemic control, we hypothesize that periodontitis is associated with a greater prevalence of prediabetes and its poor prognosis. Consequently, the purpose of this investigation is to ascertain whether periodontitis serves as a risk factor for the incidence and adverse outcomes of prediabetes, utilizing data from the National Health and Nutrition Examination Survey (NHANES).

Methods and participants

Study population

The NHANES (RRID:SCR_013201) is continuous survey research that provides population estimates related to the nutrition and health of adults and children in America. The survey employs a stratified, multistage probability design to recruit a representative sample of the American population. Data were obtained via personal structured interviews at home, health examinations at a mobile examination center, and specimen analyses in the laboratory. NHANES 1999-2004 and 2009-2014 were approved by The National Center for Health Statistics (NCHS) Ethics Review Board and conducted in accordance with the Helsinki Declaration of 1975, as revised in 2013. Informed consent was obtained from all participants. The acquisition and analysis of data was consistent with NHANES research requirements.

Identification of prediabetes and periodontitis

Prediabetes was diagnosed by one of the following four principles: (1) Self-reported prediabetes: participants answer "Yes" to the question "Have you ever been told prediabetes/IGT/IFG/borderline diabetes/blood sugar higher than normal but not high enough to be called diabetes in diabetes questionnaire". (2) HbA1c: 5.7%-7.0%. (3) Fasting plasma glucose: 5.6-7.0 mmol/L. (4) oral glucose tolerance test: 7.8-11.0 mmol/L [ 10].

Periodontitis was defined as clinical attachment loss (CAL; the difference between pocket depth and gingival recession) ≥ 3 mm. This has been recommended for epidemiological studies as an extent measure of periodontitis and is henceforth referred to as CAL extent. The severity of periodontitis was defined by following Centers for Disease Control and Prevention in partnership with the American Academy of Periodontology (CDC-AAP) case definitions for surveillance of periodontitis [ 11].

Inclusion and exclusion process

We used the data from the NHANES 1999-2004 and 2009-2014 cycles. First, 15390 patients with clear periodontal, prediabetes and other covariable data were included to explore the association between periodontitis status and the risk of prediabetes. Furthermore, we enrolled 4518 participants with prediabetes of 15390 sample to further explore the association between periodontitis status and all-cause mortality (Fig. 1).

Outcomes

The outcome of association analysis was diagnosed with prediabetes. The outcome of survival analysis was all-cause mortality with periodontitis or not among patients diagnosed with prediabetes. All-cause mortality was ascertained by linkage to National Death Index records through 2018. ICD-10 was used to determine the causes of death.

Assessment of covariates

Standardized questionnaires obtained information on sociodemographic characteristics, smoking status, and alcohol consumption. Never smokers were classified as those who reported smoking < 100 cigarettes during their lifetime. Those who smoked > 100 cigarettes in their lifetime were considered current smokers, and those who smoked > 100 cigarettes and had quit smoking were considered former smokers. Nondrinkers were defined as consuming no drinks per year. Heavy alcohol use was defined as ≥ 3 drinks per day for females, ≥ 4 drinks per day for males, or binge drinking [≥ 4 drinks on the same occasion for females, ≥ 5 drinks on the same occasion for males] on 5 or more days per month. Moderate alcohol use was defined as ≥ 2 drinks per day for females, ≥ 3 drinks per day for males, or binge drinking ≥ 2 days per month. Other frequencies of alcohol consumption were defined as mild alcohol use. Body mass index (BMI) was calculated from weight/height ² (kg/m ²). Diabetes was defined as follows: (1) doctor diagnosed you as having diabetes; (2) HbA1c > 7%; (3) fasting glucose ≥ 7.0 mmol/L; (4) random blood glucose ≥ 11.1 mmol/L, (5) two-hour oral glucose tolerance test (OGTT) blood glucose ≥ 11.1 mmol/L; and (5) use of diabetes medication or insulin. Hyperlipidemia was defined as follows: (1) triglyceride ≥ 150 mg/dL, (2) cholesterol ≥ 200 mg/dL, (3) low-density lipoprotein (LDL)-cholesterol ≥ 130 mg/dL, (4) high-density lipoprotein (HDL)-cholesterol < 40 mg/dL (male); 50 mg/dL (female), and (5) use of hyperlipidemia medication. Coronary heart disease (CHD) was defined as self-reported CHD. Homeostasis model assessment-insulin resistance (HOMA-IR) was calculated by the following formula: HOMA-IR = [fasting plasma glucose (mU/L) × fasting plasma glucose (mmol/L)]/22.5. Homeostasis model assessment-insulin sensitivity (HOMA-IS) was estimated by the following formula: HOMA-IS = 22.5/[fasting plasma glucose (mU/L) × fasting plasma glucose (mmol/L)]. In addition, strict laboratory analyses were performed, including the assessment of glucose, insulin, HbA1c, triglyceride, HDL, LDL, and C-reactive protein (CRP) levels at baseline. Further details of these measurements were documented in the NHANES Laboratory Medical Technologists Procedures Manual.

Statistical analysis

All analyses incorporated sample weights, strata, and primary sampling units to produce accurate national estimates. Sample characteristics are reported as the means (SEs) for normally distributed continuous variables, medians (interquartile ranges) for nonnormally distributed continuous variables, and percentages for categorical variables. Weighted multivariate logistic regression models were performed to estimate the OR and 95% confidence interval associated with periodontitis status and prediabetes with the first group as a reference. Weighted Cox proportional hazards regression was used to estimate hazard ratios (HRs) and 95% CIs of all-cause mortality in relation to periodontitis. Person-time was calculated as the interval between the NHANES interview date and the date of death or the end of the follow-up (31-December-2018), whichever occurred first. We constructed three statistical models. Model 1: no covariates were adjusted. Model 2: Age (continuous), gender (male or female), race/ethnicity (Mexican American, other Hispanic, non-Hispanic white, non-Hispanic black, or other Race), and education level (less than high school, high school, more than high school) were adjusted. Model 3: age (continuous), gender (male or female) and race/ethnicity (Mexican American, other Hispanic, non-Hispanic white, non-Hispanic black, or other Race), education level (less than high school, high school, more than high school), smoking status (never, former, or current), alcohol use (never, former, mild, moderate. severe), BMI (continuous), hypertension (no or yes), hyperlipidemia (yes or no), and CHD (yes or no) were adjusted. Any individuals with missing covariate data were not included in the analyses in Model 2 and Model 3 (listwise deletion). Furthermore, stratified analyses were conducted to examine whether the detected association differed by age, sex, and body mass index. All analyses were performed using R software (4.1.0). Two-sided P < 0.05 was considered statistically significant. The Bonferroni correction threshold was used to account for multiple comparisons.

Results

Participant characteristics

In this study, 15390 participants were enrolled in our analysis. There were 5033 participants with periodontitis and 10357 participants without periodontitis. Compared to participants without periodontitis, participants with periodontitis were more likely to be female, older, have a higher education level, hypertension, hyperlipidemia, CHD, be former alcohol user, smoke, have a higher BMI and glucose/insulin/HbA1c/HOMA-IR, have prediabetes, and have diabetes (Table 1).

Table 1 Baseline characteristics of included participants in NHANES 1999-2004 and 2009-2014

Logistic regression between periodontitis and prediabetes

We conducted weighted multivariate logistic regression models to explore the association between periodontitis status and prediabetes (Table 2). Compared to nonperiodontitis, periodontitis was positively associated with prediabetes in all models (OR = 2.37, 95% CI 2.16-2.60; 1.45, 95% CI 1.30-1.61; 1.47, 95% CI 1.31-1.63). The p value of all models was < 0.001. We further stratified periodontitis into three statuses according to the CDC-AAP case definitions. In Model 1, all periodontitis statuses were significantly associated with prediabetes (OR = 1.42, 95% CI 1.15-1.77; 2.39, 95% CI 2.15-2.66; 2.74, 95% CI 2.26-3.32). The p value of all periodontitis statuses equaled 0.001. After adjusting for covariables, moderate and severe periodontitis were positively associated with prediabetes in Model 2 (OR = 1.46, 95% CI 1.30-1.65, 1.57, 95% CI 1.27-1.94) and Model 3 (OR = 1.46, 95% CI 1.29-1.65; 1.62, 95% CI 1.31-2.01). The p value of moderate and severe periodontitis was < 0.001 in Models 2 and 3. Furthermore, a significant association remained between periodontitis and prediabetes in most subgroups (Additional file 1: Table S1).

Table 2 Association between the pre-diabetes and periodontitis among participants in NHANES 1999-2014

Cox regression between periodontitis and mortality of patients with prediabetes

A total of 4518 participants with prediabetes were included to further explore the correlation between periodontitis status and diabetes mortality by weighted Cox proportional hazards regression. The characteristics of these participants are shown in Additional file 1: Table S2. The average follow-up time was 128.41 ± 1.67 months (Additional file 1: Table S2). Compared to the nonperiodontitis group, participants with periodontitis were pivotally correlated with mortality of prediabetes in all models (HR = 2.41, 95% Cl 1.98-2.94, p < 0.001; 1.47, 95% Cl 1.20-1.80, p < 0.001; 1.28, 95% Cl 1.04-1.57, p = 0.02). After stratifying the status of periodontitis, moderate and severe periodontitis were positively correlated with mortality of prediabetes (HR = 2.42, 95% Cl 1.95-3.01, p < 0.001; 1.806, 95% Cl 1.19-2.74, p = 0.005). After further adjustments for age, sex, race, education level, alcohol use, BMI, hypertension, CHD, moderate periodontitis was significantly associated with mortality of prediabetes in Model 2 (HR = 1.45, 95% CI 1.17-1.80, p < 0.001) and Model 3 (HR = 1.25, 95% CI 1.00-1.55, p = 0.047) (Table 3). The Kaplan-Meier survival curve presented similar results (Fig. 2). In the subgroup analysis, older age, female sex, high education level, mild alcohol use, former smoking, hypertension, hyperlipidemia, and higher BMI were positively correlated with all-cause mortality of prediabetes (Additional file 1: Table S3).

Table 3 All-cause mortality of patients with pre-diabetes during different periodontal status in NHANES 1999-2004 and 2009-2014

Kaplan‒Meier survival curve of prediabetic patients with/without periodontitis. A. Kaplan‒Meier survival curve of the prediabetes patients with/without periodontitis; B. Kaplan‒Meier survival curve of the prediabetes patients with different statuses of periodontitis

Discussion

With the discovery of pathophysiological processes, periodontitis is regarded as a chronic inflammatory disease that is associated with other noninfected systemic diseases, including cardiovascular and metabolic diseases, rheumatic arthritis, and Alzheimer's disease [ 12]. Chiu [ 13], Demmer [ 14], and Saito [ 15] et al. reported that periodontitis was significantly associated with the elevation of HbA1c and the development of insulin tolerance. To further explore this relationship, our study aimed to investigate the association between periodontitis and prediabetes.

The findings of this study indicate a significant association between moderate and severe periodontitis and the occurrence of prediabetes. Similarly, Desvarieux [ 16] and Shiva [ 17] et al. reported that periodontal infection and inflammation were associated with insulin resistance and impaired glucose tolerance in the nationally representative American and Iranian sample. Nonetheless, Pérez [ 18] et al. established a 3-year oral health status cohort enrolled overweight adults and no association between periodontitis and the risk of prediabetes/diabetes were reported. But the median follow-up time of this longitudinal study was 2.96 years which may be too short to influence the results of the prevalence risk of prediabetes/diabetes. And in this study, patients with moderate or severe periodontitis had a significant improvement in periodontal health during follow-up, which could have a great influence on the results. Simultaneously, Amar [ 19] and Loos [ 20] et al. demonstrate that severe periodontitis was associated with the elevation of HbA1c and HOMA-IR. We found that moderate periodontitis was also positively associated with prediabetes. On the one hand, this may be due to the uniform quality control of periodontal examinations in the NHANES study. On the other hand, we utilized the CDC-AAP criterion to define the status of periodontitis. This criterion can effectively promote the clinical periodontal condition. But it excluded buccal and/or lingual sites which can impact periodontal condition. Therefore, large-scale prospective studies are still needed to investigate the impact of periodontitis on the development and prognosis of prediabetes.

Previous studies just suggested severe periodontitis was significantly associated with mortality of type 2 diabetes mellitus [ 21]. In our study, we found that moderate periodontitis was found to be positively correlated with all-cause mortality in individuals with prediabetes. We assumed that chronic systemic inflammation aroused by periodontitis and blood sugar dysregulation promotes the progression of various systemic diseases, including cardiovascular diseases, resulting in increased mortality [ 22].

Although abundant research has revolved around periodontitis and IGT/insulin resistance, the mechanism remains unclear. A recent study demonstrated that the oral microbiota contained approximately 500-700 prevalent taxa [ 23]. Among them, Porphyromonas gingivalis (P. gingivalis) and Aggregatibacter actinomycetemcomitans ( A. actinomycetemcomitans) were shown to be classical pathogens of periodontitis [ 24]. These pathogens activate the innate immune system in situ and secrete inflammatory factors [ 25]. Several studies have demonstrated that gingival crevicular fluid (GCF) and serum of patients with periodontitis contain high levels of TNF-α, IL-1β, IL-6, and other proinflammatory factors that play a pivotal role in the development of insulin secretion and resistance [ 26, 27]. Izumi [ 28] et al. built a periodontitis animal model affected by A. actinomycetemcomitans and performed an insulin/glucose tolerance test. The level of insulin resistance was significantly elevated. Furthermore, Luan et al. utilized P. gingivalis to establish an animal model [ 29]. They revealed that the levels of TNF-α and IL-6 were increased and the expression of PPARa, Irs1, and sitr1 was decreased, which suggested that glucose metabolism was dysregulated. Regarding clinical trials, Kocher [ 30] et al. conducted a multiple-center randomized study to explore the influence of nonsurgical periodontal treatment on prediabetes status. They revealed that treatment of periodontitis decreased the levels of HbA1c and CRP, which was consistent with our results. Kowall [ 31] et al. implied that periodontitis was only associated with poorly controlled diabetes, not prediabetes. The reason for the different conclusions may be the different races of the included participants and the different definitions of periodontitis. Therefore, further long-term follow-up is needed to clarify the role of root canal treatment of severe periodontitis in improving prediabetes.

In addition, these pathogens produce abundant virulence factors directly and via outer membrane vesicles (OMVs). These virulence factors, which activate macrophages and induce systemic inflammation, included lipopolysaccharide (LPS), protein, lipid, muramic acid, RNA, and DNA [ 32, 33, 34]. Subcutaneous chronic infusion of P. gingivalis LPS into high-fat diet-fed mouse enhanced insulin resistance of mouse [ 35]. Moreover, Ruiz [ 36] and Ivanovski [ 37] et al. noticed that GCF of patients with periodontitis had elevated concentrations of extracellular vesicles, especially OMV. OMV is a 50-250 nm particle derived from gram-negative bacteria [ 38]. OMV from P. gingivalis increased the expression of Toll-like receptors and nod-like receptors, which mediated insulin resistance signaling [ 38, 39]. Nonetheless, animal experiments and clinical trials to clarify the mechanism of virulence factors of these key pathogens in prediabetes are still lacking.

Clinical implication

The early diagnosis and intervention of prediabetes are important for preventing diabetic conversion and complications. Currently, the first-line therapy for prediabetes was lifestyle modification or metformin. Intensive lifestyle modification was more beneficial than metformin, such as diet, exercise, and weight loss [ 40]. However, there are no effective methods to decrease the morbidity of prediabetes. Our findings offer valuable insights into elucidating the association between periodontitis and prediabetes. As periodontitis is a common disease in the adult population, our findings provide a novel insight into the risk and treatment of prediabetes from the perspective of oral health status. Endocrinologists should pay attention to the oral condition of patients with prediabetes rather than only diabetes patients. Endocrinologists should also focus not only on oral health during the treatment of diabetes but also pay attention to the prevention of the development and deterioration of prediabetes through oral health management. Future studies are necessary to investigate whether therapeutic interventions aimed at addressing periodontitis can reverse or impede the progression of prediabetes to diabetes and thereby prevent subsequent negative health outcomes.

Limitations

This study explored the association between periodontitis and prediabetes. We conducted a large-scale sample retrospective study and adjusted for potential covariables to guarantee validity. However, some limitations remain. First, we only enrolled American adults in our study, which does not represent the population of another region. Second, although we considered every confounding variable, some variables still affected the prevalence and mortality of prediabetes. Third, the accuracy of periodontal pocket detection is limited by the type of probe. Therefore, the classification of periodontitis severity should be further demonstrated. We will conduct a further multicenter study and animal experiment to further validate our findings.

Conclusion

In summary, moderate and severe periodontitis were significantly associated with the risk of prediabetes. Moderate periodontitis was positively correlated with mortality in prediabetes patients. This suggests that periodontitis may be a new and valuable risk indicator of prediabetes. Early treatment of periodontitis may improve the prognosis of prediabetes.

Availability of data and materials

The data used in this study are from a public database at https://www.cdc.gov/nchs/nhanes/index.htm, which can be accessed by everyone through the links provided in the paper.

Abbreviations

DM:

Diabetes mellitus

NHANES:

National Health and Nutrition Examination Survey

NCHS:

National Center for Health Statistics

CAL:

Clinical Attachment Loss

CDC-AAP:

Centers for Disease Control and Prevention in partnership with the American Academy of Periodontology

BMI:

Body Mass Index

OGTT:

Oral glucose tolerance test

LDL:

Low-Density Lipoprotein

HDL:

High-Density Lipoprotein

CHD:

Coronary Heart Disease

HOMA-IR:

Homeostasis Model Assessment-Insulin Resistance

HOMA-IS:

Homeostasis Model Assessment-Insulin Sensitivity

CRP:

C-Reactive Protein

HR:

Hazard Ratio

P. gingivalis:

Porphyromonas gingivalis

A. actinomycetemcomitans:

Aggregatibacter actinomycetemcomitans

GCF:

Gingival Crevicular Fluid

OMV:

Outer membrane vesicles

LPS:

Lipopolysaccharide

References

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Acknowledgements

The authors thank all the staff and participants in NHANES 1999-2004 and 2009-2014 for their contribution to the donation, collection, and sharing of data.

Funding

The work was supported by grants from the National Natural Science Foundation of China (Nos. 82000301 to L.Z. Y), Natural Science Foundation of Hunan Province, China (Nos. 2021JJ40938 to L.Z.Y).

Author information

Authors and Affiliations

1. Department of the Geriatrics, The Third Xiangya Hospital, Central South University, Changsha, 410013, Hunan, China

Liao Tan & Zhaoya Liu

2. Department of Cardiology, The Third Xiangya Hospital, Central South University, Changsha, Hunan, China

Liao Tan

3. Department of Cardiovascular Medicine, Xiangya Hospital, Central South University, Changsha, Hunan, China

Jie Liu

Contributions

LT analyzed the data and drafted the manuscript. JL drafted the manuscript. ZL ensured that the descriptions were accurate and agreed upon by all the authors. All authors made substantial contributions to the interpretation of the data and provided critical revisions to the manuscript.

Corresponding author

Correspondence to Zhaoya Liu.

Ethics declarations

Ethics approval and consent to participate

This study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2013. NHANES 1999-2004 and 2009-2014 were approved by The NCHS Ethics Review Board (Protocol #98-12, Continuation of protocol #2005-06, Protocol #2011-17, and Continuation of protocol #2011-07), and informed consent was obtained from all participants. This study was based on publicly available data. The acquisition and analysis of data were consistent with NHANES research requirements.

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this article.

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Tan, L., Liu, J. & Liu, Z. Association between periodontitis and the prevalence and prognosis of prediabetes: a population-based study. J Transl Med 21, 484 (2023). https://doi.org/10.1186/s12967-023-04340-y
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# data[].attributes.attachment_link.title
Association between periodontitis and the prevalence and prognosis of prediabetes: a population-based study - Journal of Translational Medicine

# data[].attributes.attachment_link.description
Background Diagnosis and intervention of prediabetes is an emerging method for preventing diabetic progression and complications. Periodontitis has been reported to strongly correlate with the dysregulation of glucose metabolism. Nonetheless, the relationship between periodontal status and the prevalence of prediabetes as well as its prognosis remains elusive.

# data[].attributes.headline
Referência usada por mim na revisão de literatura nos tópicos: 2.3.1 Hiperglicemia, 2.3.2 Microbiota Oral, 2.3.3 Tratamento para a melhora mútua das doenças

# data[].attributes.subject
Referência usada por mim na revisão de literatura nos tópicos: 2.3.1 Hiperglicemia, 2.3.2 Microbiota Oral, 2.3.3 Tratamento para a melhora mútua das doenças

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OLIVEIRA, L. M. L.; BARBOSA, L. M. The relationship between periodontite and diabetes mellitus type ii facing the new classification of periodontal diseases: literature review. Rev Gaúch. Odontol., [s. l.], v. 68, p. 1-6, 2020. DOI: https://doi.org/10.1590/1981-863720200005920190060. Disponível em: https://www.scielo.br/j/rgo/a/zGYhKHjjsQcctvqncswkTdq/?lang=en. Acesso em: 2 maio 2025.

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ABSTRACT

Periodontal disease and type 2 diabetes mellitus are considered chronic diseases that at their core have a deep relationship with inflammation. It is assumed that there is a bidirectional relationship between periodontal disease and type 2 diabetes mellitus. It is estimated that approximately 10% of the world's population is affected by periodontal disease, in its most severe form, almost the same percentage estimated for people with diabetes, which is considered a 21st century emergency. The World Workshop for the Classification of Periodontal and Peri-implant Diseases and Conditions took place from September 9-11, 2017. The aim of this study is to analyze the results of this workshop with regard to the relationship between periodontal diseases/conditions and diabetes mellitus, in addition to conducting an integrative review on the topic. A literature review was conducted, using the Medline electronic databases via Pubmed, Scientific Electronic Library Online, Scientific and Technical Literature of Latin America and the Caribbean and Virtual Health Library. A new classification of periodontal disease included tools for individual assessment of the patient and recognizing risk factors that might negatively interfere in response to treatment. The occurrence of metabolic lack of control in periodontal patients with type 2 diabetes mellitus is now considered a factor of great importance for the assessment of individual susceptibility to the progression of periodontitis. Diabetes is believed to promote a hyper inflammatory response to bacterial challenge by modifying the tissue response of periodontal tissues.

Indexing terms
Classification; Diabetes mellitus; Diabetes mellitus, type 2; Periodontal diseases

RESUMO

A doença periodontal e o diabetes mellitus tipo 2 são consideradas doenças crônicas que tem em seu cerne um profundo relacionamento com mecanismos inflamatórios, pressupõe-se que haja uma relação bidirecional entre doença periodontal e diabetes mellitus tipo 2. Estima-se que aproximadamente 10% da população do mundo seja afetada pela doença periodontal, na sua forma mais severa, quase o mesmo percentual estimado para portadores de diabetes, que é considerada uma emergência do século XXI. Entre 9 e 11 de setembro de 2017, ocorreu o World Workshop para a Classificação das Doenças e Condições Periodontais e Peri-implantares. O objetivo deste estudo é analisar o que está colocado por esta classificação sobre a relação entre doenças/condições periodontais e diabetes mellitus, além de fazer uma revisão integrativa a respeito do tema. Foi realizada uma revisão de literatura, a partir das bases de dados eletrônicas Medline via Pubmed, Scientific Electronic Library Online, Literatura Científica e Técnica da América Latina e Caribe, Biblioteca Virtual em Saúde. A nova classificação das doenças periodontais incluiu ferramentas para uma avaliação individual do paciente, reconhecendo fatores de risco que possam interferir negativamente na resposta ao tratamento. A ocorrência de descontrole metabólico em pacientes periodontais com diabetes mellitus tipo 2, passa a ser considerada, então, um fator de grande importância para a avaliação da susceptibilidade individual para a progressão da periodontite. Acredita-se que o diabetes promova uma resposta hiperinflamatória ao desafio bacteriano, modificando a resposta tecidual dos tecidos periodontais.

Termos de indexação
Classificação; Diabetes mellitus; Diabetes mellitus tipo 2; Doenças periodontais

INTRODUCTION

It is assumed that there is a bi-directional relationship between DP and DM2 [,]. Longitudinal studies [,] positively associated DM2 with increased risk in developing periodontitis, accelerating its evolution. This association can be explained by the release of hormonal and inflammatory signs related to the pathogenesis of diabetes [] that can also contribute to tissue destruction, a characteristic of periodontitis.

Between September 9 and 11, 2017, the World Workshop for the Classification of Periodontal and Periimplant Diseases and Conditions took place. A committee, organized by the American Academy of Periodontics and the European Federation of Periodontics, updated the 1999 Classification and developed a similar scheme for peri-implant diseases and conditions.

The aim of this study is to analyze the relationship between periodontal diseases/conditions and diabetes mellitus, as indicated by this new classification, in addition to promoting a literature review on the subject.

An integrative literature review was carried out, using Medline electronic databases via Pubmed, Scientific Electronic Library Online (Scielo), Scientific and Technical Literature of Latin America and the Caribbean (LILACS) and Virtual Health Library (VHL) between January and February 2019. The terms "Type 2 Diabetes Mellitus," "Periodontal Diseases," and "Periodontitis" were searched, combining Boolean AND/OR operators. Controlled clinical studies, literature reviews and consensus available in English, Portuguese or Spanish were considered as inclusion criteria.

DISCUSSION

DP and DM2 have a close relationship. This correlation has been studied for more than six decades, once it was perceived that periodontal tissues of diabetic patients are less resistant to local irritants; it was unknown at that time that high reactivity of periodontal tissues to these irritants attributes to this fact [].

The new classification of PD included tools for individual assessment of patients, recognizing risk factors that may interfere negatively in treatment response. The occurrence of metabolic lack of control in periodontal patients with DM2 is considered an important factor for evaluation in disease progression rate [], which, as seen, tends to be more accelerated in uncontrolled diabetic individuals.

Algorithm is a tool that systematizes the patient's individual clinical data, with the purpose of grouping them into categories which indicate the severity/complexity and rate of disease progression through well-defined criteria ( chart 1) [,].

The new classification system defines a kind of staging of periodontitis at various points in time, aiming to facilitate communication between professionals and assist in the definition of the prognosis for improving personalized care. It is understood that individuals have different severity/extension, rates of disease progression and/or associated risk factors [,].

According to the new classification [], the information derived from this staging should be complemented by data about the biological level of the disease (risk or current evidence of progression) for each patient. The purpose of this gradation is to consider the patient's susceptibility to periodontitis, taking into account his clinical history, manifested by the bone loss/year ratio, and risk determinants that acted together to cause bone loss throughout his life [].

The occurrence of recognized modifying risk factors, such as smoking and diabetes mellitus, has the power to increase the degree value, regardless of the primary criterion, represented by the rate of progression. For example, a stage II case, characterized by moderate loss of insertion, would assume a moderate rate of progression (Grade B). The detection of DM2, with poor metabolic control, could change the classification of the grade to C [].

CONCLUSION

The metabolic lack of control in diabetics, under the new classification, gains a more prominent position, since it is considered as an individual classification tool of the disease, in its staging and gradation. The diagnostic description will be periodontitis associated with diabetes mellitus, defining the stage and evaluating the degree of the disease, by its rate of progression over time. The degree, however, can be modified by the patient's metabolic control factors.

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The relationship between periodontite and diabetes mellitus type ii facing the new classification of periodontal diseases: literature review

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ABSTRACT Periodontal disease and type 2 diabetes mellitus are considered chronic diseases that...

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Referência usada por mim na revisão de literatura nos tópicos: 2.3.2 Microbiota Oral, 2.3.3 Tratamento para a melhora mútua das doenças

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Referência usada por mim na revisão de literatura nos tópicos: 2.3.2 Microbiota Oral, 2.3.3 Tratamento para a melhora mútua das doenças

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STEFFENS, J. P. et al. Clinical management of the interrelationship between diabetes and periodontitis: joint guidelines by the Brazilian Society of Periodontology (SOBRAPE) and the Brazilian Society of Endocrinology and Metabolism (SBEM). Brazilian Journal of Periodontology, [s. l.], v. 32, n. 1, p. 90–113, Jan./Apr. 2022. DOI: https://doi.org/10.14436/0103-9393.32.1.090-113.oar. Disponível em: https://www.brazilianperiodontology.com/artigo/688/Periodontology-2022-v32n1/9073. Acesso em 1 maio 2025.

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Artigo: Manejo clínico da inter-relação diabetes e periodontite: diretrizes conjuntas da Sociedade Brasileira de Periodontologia (SOBRAPE) e da Sociedade Brasileira de Endocrinologia e Metabologia (SBEM) - Periodontology 2022 v32n1 - Clinical Orthodontics

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Bem vindo ao DentalGO a plataforma online dos melhores dentistas

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Referência usada por mim na revisão de literatura no tópico: 2.3.1 Hiperglicemia.

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Referência usada por mim na revisão de literatura no tópico: 2.3.1 Hiperglicemia.

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MATOS, L. O. et al. Periodontitis and identification of undiagnosed hyperglycemia. Rev. Odontol. UNESP, [s. l.], v. 50, p. 1-9, 2021. DOI: https://doi.org/10.1590/1807-2577.03921 Disponível em: https://www.scielo.br/j/rounesp/a/7NmNRTxM4S84NncmyhbGgyM/?lang=en. Acesso em: 2 maio 2025.

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Abstract

Introduction Individuals with pre-diabetes have altered glycemic levels, are generally asymptomatic, and are at increased risk for developing type 2 diabetes mellitus.

Objective Identify the prevalence of periodontal individuals with undiagnosed hyperglycemia and associated impact factors.

Material and method Fifty-six patients with periodontitis and without diabetes self-report, users of dental clinic services at Federal University of Juiz de Fora were included in this research, during one year and a half of experimental evaluation. Socioeconomic and demographic data, anthropometric patterns, fasting capillary blood glucose, and complete periodontal examination (six sites per tooth) were evaluated.

Result The sample consisted of 58.9% female, mean age 53 years old, 58.9% obese/overweight and 45.3% had a low level of education. A total of 28.6% (n=16) participants had undiagnosed hyperglycemia (between 100 to 160 mm / dL), of which 81.3% were obese/overweight, 25% were smokers, 56.3% reported having a history of diabetes in the family, 93.8% had a family income up to 2 brazilian´s minimum wages. BMI values ​​were higher in the group of patients with hyperglycemia (29.8 ± 5.7, p = 0.03) compared to the group without hyperglycemia (26.6 ± 5.6). Patients with hyperglycemia had a greater number of sites with clinical attachment loss (CAL) between 4 and 6 mm (p = 0.04) when compared with the normoglycemic group.

Conclusion Undiagnosed CAL attachment loss between 4 and 6 mm due to periodontitis than normoglycemic individuals.

Descriptors:
Hyperglycemia; prediabetic state; diabetes mellitus; periodontitis; risk factors

Resumo

Introdução Indivíduos com pré-diabetes apresentam níveis glicêmicos alterados, geralmente são assintomáticos e apresentam risco aumentado para desenvolver diabetes mellitus tipo 2.

Objetivo Identificar a prevalência de indivíduos periodontais com hiperglicemia não diagnosticada e os fatores de impacto associados.

Material e método Cinquenta e seis pacientes com periodontite e sem autorrelato de diabetes, usuários de serviços de clínica odontológica da Universidade Federal de Juiz de Fora foram incluídos nesta pesquisa, durante um ano e meio de avaliação experimental. Foram avaliados dados socioeconômicos e demográficos, padrões antropométricos, glicemia capilar de jejum e exame periodontal completo (seis sítios por dente).

Resultado A amostra foi composta por 58,9% do sexo feminino, média de idade de 53 anos, 58,9% obesidade / sobrepeso e 45,3% com baixa escolaridade. Um total de 28,6% (n=16) participantes tinham hiperglicemia não diagnosticada (entre 100 a 160 mm / dL), dos quais 81,3% eram obesos / com sobrepeso, 25% eram fumantes, 56,3% relataram ter histórico de diabetes na família, 93,8% tinham renda familiar de até 2 salários mínimos brasileiros. Os valores de IMC foram maiores no grupo de pacientes com hiperglicemia (29,8 ± 5,7, p = 0,03) em comparação ao grupo sem hiperglicemia (26,6 ± 5,6). Pacientes com hiperglicemia apresentaram maior número de sítios com perda clínica de inserção (CAL) entre 4 e 6 mm (p = 0,04) quando comparados ao grupo normoglicêmico.

Conclusão A perda de inserção de CAL não diagnosticada entre 4 e 6 mm devido à periodontite do que indivíduos normoglicêmicos.

Descritores:
Hiperglicemia; estado pré-diabético; diabetes mellitus; periodontite; fatores de risco

INTRODUCTION

Diabetes mellitus (DM) is a group of metabolic diseases characterized by hyperglycemia and considered a chronic disease that requires patient self-care and medical care to prevent acute complications. In Brazil, the prevalence of DM in adults was estimated at 7.6% in the most comprehensive epidemiological study carried out in the country. In this context, it is known that many diabetic patients remain undiagnosed and type 2 diabetes (DM2) is a serious public health problem, generally silent in its early stages, and as such, it often remains unrecognized for years. Data show that there are 463 million adults aged between 20 and 79 years with diabetes in the world and one in two individuals (232 million) have not been diagnosed.

Therefore, studies indicate that DM can increase the risk of developing periodontal disease by two or three times, affecting its prevalence, severity and progression. Additionally, the extent/severity of periodontitis can influence glycemic control and the development of complications in these patients.

The glucometer has been used in epidemiological research and, although, with limitations, it has become an alternative because it is an economical, accurate, fast, and portable method that contributes to the systemic assessment of the patient. The use of the glucose meter and the capillary blood glucose testing has been recommended in dental clinics, however, few professionals regularly use it in their offices.

Therefore, the aim of this study was to identify the prevalence of periodontal individuals with undiagnosed hyperglycemia and associated impact factors in periodontitis individuals seeking treatment in the dental clinics of the Federal University of Juiz de Fora, Governador Valadares, Brazil.

MATERIAL AND METHOD

Ethical Aspects

This study was approved by the Human Research Ethics Committee of the Federal University of Juiz de Fora (protocol number: 3.410.480) and was conducted according to the guidelines established by the Declaration of Helsinki. All volunteers were informed about the aims and method of this study, and gave their written consent to participate by signing a consent form.

Study Design, Setting, and Participants

Patients were recruited from the Dental Clinic of the Department of Dentistry, at Federal University of Juiz de Fora (UFJF), Brazil, between August 2018 and December 2019.

As inclusion criteria, all subjects who participated in this study had the diagnosis of periodontitis, presented a minimum of 12 natural teeth and aged 18 years or older. The following exclusion criteria were considered: self-reported individuals with DM, prediabetes, pregnant or lactating women and previous periodontal treatment in the last six months.

Risk Questions

The sample was subjected to a physical examination in which the following criteria were evaluated: waist circumference (WC), body mass (in kg), height, and the body mass index (BMI) recommended by the World Health Organ Tech Rep Ser (WHO). All completed an identification questionnaire that contained: name, age, gender, skin color self-report, smoking habit, family income, education level, family history and, self-report of diabetes, hypertension, high cholesterol, high triglyceride, and obesity. Average household income was categorized into five levels or social classes.

Periodontal Examination

The complete periodontal examination was performed on all teeth, except of the third molars, by three trained evaluators. Measurements were made at six sites per tooth using a Williams millimeter-periodontal probe. The evaluation considered: missing teeth, visible plaque index (VPI), gingival bleeding index (GBI), probing depth (PD), bleeding on probing (BOP), clinical attachment loss (CAL), suppuration, degree of furcation injury, and number of teeth with tooth mobility.

Capillary Blood Glucose Test

The fasting capillary blood glucose test was performed by a single previously trained examiner. Patients were instructed to fast from 8 hours to 10 hours until the appointment and a blood sample was obtained at the fingertip with disposable sterile lancets and applied to specific strips for reading on the monitor, (Accu-Chek Active ®, São Paulo, Brazil). All care was taken to minimize any risk of contamination during its assessment. Patients with identified hyperglycemia (≥ 100mg / dL) received instructions about the importance of seeking a doctor for systemic evaluation, practicing physical activity regularly, eating healthy diet, as well as the bidirectional relationship between periodontal disease and DM.

Data Processing and Statistical Analysis

Data analysis was performed using a specific program (Bioestat 5.3, Instituto Mamirauá, PA, Brazil), considering the null hypothesis based on the absence of difference between the groups, with a significance level of 5%. The unit of analysis was the patient. The data were submitted to the Shapiro-Wilk normality test. Continuous and ordinal data were analyzed using the t-test, in the case of the normal distribution; or by the Mann-Whitney test, when the distribution was non-normal. Nominal dichotomous data were analyzed using Fisher's Exact test, and the others using the Mann-Whitney test. The values were presented with mean and standard deviation.

RESULT

In the present study, 63 patients met the inclusion/exclusion criteria, however, a total of seven patients did not accept to participate in the research and, therefore, were not included in the analysis. The convenience sample, composed of 56 patients, had a mean age of 52.9 ± 9.3 years. A total of 28.6% (n = 16) participants had undiagnosed hyperglycemia (between 100 and 160 mm / dL) and in this group the BMI was, on average, 29.8 ± 5.7 (p = 0.03). In assessing the characterization of the groups, it was observed that the values of blood glucose, body mass, BMI were higher in the group of patients with hyperglycemia, compared to the group without hyperglycemia (p < 0.05) ( Table 1).

Most participants in the group with hyperglycemia had a family income of up to two minimum wages (93.8%) ( Table 2).

There were no significant differences regarding the behavioral data and systemic conditions of the sample ( Table 3).

Table 4 showed that patients with hyperglycemia had a greater number of sites with CAL between 4 and 6 mm (p = 0.04). It was also noted that the average number of missing teeth was 6.2 ± 4.1. Regarding periodontal diagnosis, there was no significant difference between the groups (data not shown).

DISCUSSION

Scientific data reveals that one out of every two individuals with DM in the world has not been diagnosed and that DM2 is generally silent in its early stages and often remains unrecognized for years. In patients with periodontitis, it is observed that the extent/severity of periodontitis can influence glycemic control and the development of complications in these individuals. In addition, DM can increase the risk of developing periodontal disease by two or three times, affecting its prevalence, severity, and progression. A sample of the present study found a prevalence of 28.6% of undiagnosed hyperglycemia among individuals with periodontitis.

Some studies that evaluated periodontal parameters, considering a population sample without a diagnosis of periodontitis, found prevalence values ​​higher than our study. In the study by Lalla et al., a prevalence of 36% of undiagnosed hyperglycemia was demonstrated in 506 individuals, aged over 30 years, who attended dental clinics in the United States, regardless of periodontal diagnosis. Other studies have found a prevalence equal or greater than 40% of unidentified hyperglycemia,. These studies showed differences in terms of sample size and patient selection criteria, in which individuals older than 40 years were included. However, some studies have evaluated patients with periodontitis and found results in agreement with the present study. Holm et al. identified a prevalence of 30.2% of undiagnosed hyperglycemia among 291 individuals in Denmark. On the other hand, the prevalence found by Mataftsi et al. in a sample of 139 individuals from Greece was 24.5%. Bossart et al. analyzed a sample with a similar size (n = 50) and the prevalence was 34%. Factors such as obesity, individuals' advanced age, smoking, and different locoregional habits of the samples might influence the different results about prevalence of undiagnosed hyperglycemia among the studies.

An important result of this study was the greater CAL between 4 and 6 mm found in hyperglycemic patients (p = 0.04). Similarly, Alasqah et al. evaluated a sample categorized according to HbA1c values as group 1 (pre-diabetes), group 2 (type 2 diabetes) and group 3 (control). The CAL were significantly higher in group 1 and 2 when compared to group 3. Mataftsi et al. identified that individuals with HbA1c ≥ 5.7% had significantly more sites with CAL > 5 mm. Likewise, a study with a representative sample of individuals with periodontitis identified that individuals with hyperglycemia had greater CAL when compared to those with normoglycemia.

Regarding the assessment of anthropometric patterns, body mass and BMI were significantly associated with hyperglycemia (p < 0.05). Since the sample was composed of periodontal individuals, this data is in agreement with previous reports that demonstrated that periodontitis is associated with obesity determined by BMI,. It is known that obesity increases insulin resistance and thus induces hyperglycemia, which may explain the fact that individuals with hyperglycemia had an average BMI of 29.8 ± 5.7, which represents advanced overweight/obesity. Several studies showed the association of BMI with hyperglycemia,,. Furthermore, Holm et al. analyzed a population with and without periodontitis and found that individuals with periodontitis and overweight have a higher risk factors of developing pre-diabetes and DM. In the study, they found a significant association between periodontitis, BMI and waist circumference (p < 0.05). Thus, periodontal patients with undiagnosed hyperglycemia in the present study may, in general, be at risk for developing diseases associated with obesity and diabetes.

Regarding periodontal diagnosis, there was no significant difference between the groups. It is noteworthy that the sample size when subdivided by categories of the classification is a limiting factor for statistical differences. However, a tendency was observed: 75% of the subgroup with hyperglycemia showed more advanced stages of periodontitis (stages III or IV) whereas in the normoglycemic subgroup this prevalence was 72.5% (no significant result, data not shown). In the literature, a greater proportion of patients with undiagnosed hyperglycemia exhibited Stage III periodontitis compared to periodontally healthy individuals.

The convenience sample, although representative of the number of periodontal patients seeking treatment at the dental clinics of the UFJF Campus Governador Valadares for a period of one and a half years, is a limiting factor of this study. Additionally, the use of the fasting capillary blood glucose test, and not the intravenous fasting blood glucose, represents a lower accuracy in the result, however, throughout the study care was taken to always guide the patient to be fasting between 8 to 10 hours.

Our result suggests that a simple screening approach in university dental clinics, involving a complete periodontal evaluation associated with a careful anamnesis for the assessment of risk factors and the fasting capillary blood glucose test using glucometers (simple, low-cost, and easy to handle) to identify patients with altered hyperglycemia without a diagnosis must be recommended. Thus, by identifying, guiding, and referring these patients for medical evaluation, the dentist may contribute to the early diagnosis of metabolic diseases. New research, more representative of the population, is necessary to allow more careful analysis of the impact factors of undiagnosed hyperglycemia in periodontal patients.

CONCLUSION

Within the limits of this study, it was possible to conclude that the prevalence of undiagnosed hyperglycemia among individuals with periodontitis was relevant, and that hyperglycemic individuals had higher body mass index and greater loss of insertion than normoglycemic individuals.

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Abstract Introduction Individuals with pre-diabetes have altered glycemic levels, are generally...

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Referência usada por mim na revisão de literatura no tópico: 2.3.1 Hiperglicemia

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Referência usada por mim na revisão de literatura no tópico: 2.3.1 Hiperglicemia

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FRANCO, M. M. et al. Glycemic control and the production of cytokines in diabetic patients with chronic periodontal disease.  Rev Gaúcha. Odontol., [s. l.], v. 65, n. 1, p. 37-43, Jan/mar. 2017. DOI: https://doi.org/10.1590/1981-863720170001000063063. Disponível em: https://www.scielo.br/j/rgo/a/M45sXLzjWfg5R4pMChV8JZx/?lang=en. Acesso em: 3 maio 2025.

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Glycemic control and the production of cytokines in diabetic patients with chronic periodontal disease

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ABSTRACT Objective: To evaluate the association of glycemic control and cytokine production in…