Graphical abstract

Introduction

Periodontal disease is an infectious condition that includes both gingivitis and periodontitis. Gingivitis, characterized by inflammation of the gums and subsequent bleeding, is considered an early stage of the disease. Over time, periodontitis can develop, with changes including the accumulation of plaque and calculus, bacterial dysbiosis, the formation of periodontal pockets, gingival recession, tissue destruction, and alveolar bone loss, all of which may result in tooth loss [1]. The progression of periodontitis involves an intricate interplay between the oral microbiome and the host. This complexity is due in part to the extensive bacterial diversity found within the subgingival space, as well as the host’s immune response [2]. Additionally, periodontal inflammation can have systemic consequences by promoting low-grade inflammation throughout the body, adversely affecting various organs [3].

In the 1990s, the term “periodontal medicine” was introduced by Offenbacher et al. [4]. In the early 21st century, dentists began to alert their patients to the potential link between periodontal disease and various systemic conditions. However, during this time, the relationship was often described in a unidirectional manner, suggesting that periodontal disease could contribute to the development of systemic diseases. Currently, the interaction between periodontal disease and systemic diseases is understood to be bidirectional, with each condition having the potential to influence the other [5]. Notably, periodontitis is garnering substantial attention as a possible risk factor for cardiovascular disease and type 2 diabetes. It has also been shown to be associated with adverse pregnancy outcomes, respiratory diseases, kidney diseases, certain cancers, and even Alzheimer’s disease [6].

Recent evidence from intervention studies suggests that local treatment of periodontitis can improve markers of comorbidity, including blood pressure, glycemic index, and C-reactive protein (CRP) levels. Understanding the impact of disseminated periodontal pathogens on certain extraoral pathologies and examining the systemic inflammation associated with periodontitis, including the adaptation of bone marrow hematopoietic progenitors, may offer new therapeutic strategies to mitigate the risk of comorbidities linked to periodontitis. In this context, Fischer et al. [7] reported a decrease in systemic inflammation markers related to cardiovascular disease (including interleukin 1, interleukin 6, and fibrinogen), along with improvements in CRP, total cholesterol, and triglyceride levels, following 6 months of non-surgical periodontal therapy. A contributing factor to this independent association may be the capacity of periodontitis to induce low-grade systemic inflammation, which can influence the development of comorbidities. This may occur through mechanisms such as the ulcerated epithelium of periodontal pockets allowing bacteria and their products (e.g., lipopolysaccharide or proteases) to enter the bloodstream, leading to bacteremia [8]. Additionally, the innate immune system—including mature innate immune cells, their progenitor populations, and the inflammatory mediators they secrete—may represent a link between periodontitis and systemic diseases [9].

The objective of this exploratory-descriptive study was to evaluate the hypothesis that periodontal disease is positively associated with several chronic non-communicable diseases with substantial prevalence in the population. Additionally, we aimed to determine whether a greater severity of periodontal disease strengthens this association.

Materials and Methods

Design

This exploratory-descriptive study employed a cross-sectional design to investigate the periodontal health status, number of missing teeth, and systemic health conditions among residents of 3 Family Health Strategy units in the municipality of Vila Velha, ES (Ataíde, Jardim Colorado, and Divino Espírito Santo), from 2021 to 2023. Exclusion criteria encompassed an age of under 18 years and the absence of more than 14 teeth, as the latter condition would render the assessment of periodontal health conditions unfeasible.

Variables

Two professional evaluators were calibrated to minimize bias in diagnosing oral health conditions, achieving a kappa index of 0.87 [10,11]. Periodontal health status was assessed using the community periodontal index (CPI), as proposed by the World Health Organization (WHO). The CPI is used to evaluate the presence of bleeding, calculus, and shallow and deep periodontal pockets, referencing a sextant examination. Probing was performed with a WHO-recommended model 621 periodontal probe featuring a 0.5-mm spherical tip, which is considered atraumatic and comparatively reliable for detecting gingival bleeding. Additionally, a colored band indicated measurements from 3.5 to 5.5 mm. The scores from each sextant were summed to yield a total score, which was regarded as a measure of the individual’s periodontal health. General health data were sourced from the citizen’s electronic medical record, eSus (managed by the Ministry of Health), supplemented by a thorough anamnesis that included measurements of blood pressure and capillary blood glucose. We evaluated variables such as arterial hypertension, diabetes, ischemic events (acute myocardial infarction and stroke), arthritis, neurological issues (dementia, Parkinson disease, Alzheimer disease, and cognitive impairment), and cancer. Potential confounding factors, including smoking, overweight, age, and sex, were also considered.

The criteria for arterial hypertension were a measurement exceeding 140/90 mmHg or the use of antihypertensive drugs. For diabetes, the criterion was a fasting blood glucose level exceeding 125 mg/dL.

In terms of confounding factors, individuals who consumed 5 or more cigarettes per day were classified as smokers, whereas overweight was defined as having a body mass index exceeding 25 kg/m².

Data Analysis

The associations between periodontal disease and the presence of chronic non-communicable diseases were quantified using simple logistic regression, adjusted for confounding factors such as age, smoking, and overweight. This analysis enabled the association of comorbidity outcomes, including hypertension, diabetes, ischemic events, arthritis, neurological issues, and cancer, with the total periodontal index and the number of missing teeth.

Statistical Analysis

To classify the severity of periodontal disease and the extent of tooth loss, the study population was divided into quartiles based on the CPI. Using odds ratios (ORs), we could then assess whether a higher risk of these comorbidities was associated with a greater severity of periodontal disease and/or a higher number of missing teeth. Statistical analyses were conducted using IBM SPSS ver. 24.0 (IBM Corp.), with an alpha significance level set at 5% for all tests. Data were described in terms of observed frequency and percentage. The sample size was calculated based on the population of the municipality of Vila Velha, which is approximately 467,000 inhabitants according to the CENSO 2022 (administered by the Brazilian Institute of Geography and Statistics) [12]. With a margin of error of 5% and a confidence level of 95%, the minimum initial sample size was determined to be 246; however, we chose to expand our sample to obtain a more robust analysis.

Ethics Approval

This project received approval from the Ethics Committee of the Health Sciences Center (CCS-UFES), as documented in Opinion No. 5,048,518, dated October 20, 2021. Subsequently, the Vila Velha City Hall authorized its execution, under process No. 42,621/2021. All participating volunteers underwent a clinical and periodontal examination conducted by a trained and qualified professional, following the completion of an informed consent form.

Results

The study population consisted of 334 volunteer participants from 3 Family Health Units in the city of Vila Velha, ES (UESF Ataíde, UESF Jardim Colorado, and UESF Divino Espírito Santo), comprising 106 men and 228 women. The participants ranged in age from 19 to 81 years, with a median age of 45 years (Table 1). Table 2 summarizes the oral health condition of the study population, while Table 3 presents the data regarding systemic health conditions. In patients aged 45 years or older, significant associations were found between the total periodontal index and both hypertension and diabetes. Specifically, patients with a periodontal index of 9 to 13 exhibited about 3.5 times the odds of having hypertension as those with an index of 1 to 2, while those with an index of 14 or higher had an OR for hypertension of approximately 2.9. Furthermore, patients with a periodontal index of 9 to 13 were around 5.8 times as likely to have diabetes as those with an index of 1 to 2 (Table 4). In female patients, the total periodontal index was significantly associated with hypertension, diabetes, and cancer. Women with a periodontal index between 9 and 13 faced approximately 2.8 times the odds of having hypertension as those with an index of 1 to 2, while women with an index of 14 or higher exhibited an approximate OR of 5.5. Furthermore, relative to women with an index of 1 to 2, those with a periodontal index between 9 and 13 were 5.7 times as likely to have diabetes, and those with an index of 14 or higher were 8.7 times as likely to have cancer (Table 5). No significant association was observed between the total periodontal index and any comorbidity in male patients, suggesting that the presence of comorbidities in men is independent of this index. Similarly, no significant association was found between the total periodontal index and comorbidities among smokers and overweight patients, allowing us to eliminate the effects of these potential confounding factors. The number of missing teeth was significantly associated with hypertension and diabetes in female patients. Women with 1 to 2 missing teeth were 3.8 times as likely to have hypertension as those with all their teeth. The likelihood of hypertension was even greater for participants with more teeth absent, with an OR of around 10.5 for those with 3 to 5 missing teeth and 12.3 for those with 6 or more. Additionally, women with 6 or more missing teeth were 9.3 times as likely to have diabetes as those with a full set of teeth (Table 6). In male patients, a significant association was also found between the number of missing teeth and hypertension. Men with 6 or more missing teeth were 4.7 times as likely to have hypertension as those with all their teeth intact (Table 7). The number of missing teeth exhibited no statistically significant associations with the comorbidities of smokers and overweight patients, allowing us to rule out the influence of these potential confounding factors.

Discussion

Atherosclerotic cardiovascular disease (ACD) refers to a group of conditions affecting the heart and blood vessels, including coronary heart disease (manifesting as angina or acute myocardial infarction), cerebrovascular disease (such as stroke or transient ischemic attacks), and peripheral arterial disease. Sharma [13] identified a consistent link between periodontitis and new ACD cases, noting that this association was especially pronounced in adults under 65 years old and in men. Our findings support these observations, as we detected a significant association with arterial hypertension in individuals over 45 years old and in those with a CPI between 9 and 13 (p=0.011) or a CPI of 14 or higher (p=0.022). A meta-analysis by Bahekar et al. [14], which synthesized data from 5 cohort studies encompassing 86,092 patients, indicated that people with periodontal disease are 1.14 times as likely to develop coronary heart disease compared to periodontally healthy individuals, even when accounting for common risk factors such as smoking. In case-control studies involving 1,423 patients, these researchers observed an even stronger association (OR, 2.22). Our research aligns with these findings, demonstrating a significant link between periodontal disease and high blood pressure, independent of shared risk factors like smoking and overweight. However, our study did not establish a significant connection with ischemic events. Upon calculating the ORs, we found that participants with more advanced periodontal disease (specifically, those with a CPI between 9 and 13 and those with a CPI greater than 14) had ORs of 3.53 and 2.91, respectively—figures exceeding those reported by Bahekar et al. [14]. Zhao et al. [15] reported similar findings in a cohort of university students, with a positive association between periodontal disease and hypertension (OR, 1.28). Although this value is lower than our result, it can be attributed to the younger age of the population studied.

Another cross-sectional study that supports our findings was conducted by Machado et al. [16] and included 1,064 patients. The findings indicated that individuals with moderate and severe periodontitis were more likely to be diagnosed with high blood pressure, with ORs of 2.60 and 2.20, respectively, relative to those without the condition. The data underscore the concept that patients with periodontitis, especially those with more severe gingival inflammation and deeper periodontal pockets, face a higher risk of changes in systolic and diastolic blood pressure. Similarly, our study revealed that the upper quartiles of the CPI exhibited stronger associations with arterial hypertension (OR, 3.53 for the 3rd quartile and OR, 2.91 for the 4th quartile) than the lower quartiles, which included patients with better periodontal health.

A study conducted by De Angelis et al. [17], employing a methodological design very similar to the present research, also yielded results that align with our findings. They enrolled 533 volunteers over the age of 65 years, with both male and female participants. The authors concluded that both high CPI values and significant tooth loss were positively associated with the likelihood of developing cardiovascular disease. These associations persisted after adjusting for other comorbidities and lifestyle factors such as alcohol consumption and smoking. In a study of postmenopausal North American women, Gordon et al. [18] identified a positive and statistically significant correlation between blood pressure levels and periodontal health. They determined that more severe periodontal disease was associated with higher blood pressure. Additionally, they found a positive correlation between tooth loss and hypertensive disease, with an OR of 1.14 for those missing more than 5 teeth. Our findings corroborate the link between arterial hypertension and periodontal index in the 3rd (p=0.029; OR, 2.82) and 4th (p<0.001; OR, 5.50) quartiles of CPI among women. Concerning tooth loss, our data indicate comparatively high odds of hypertension in the groups missing 1 to 2 teeth (p=0.012; OR, 3.79), 3 to 5 teeth (p<0.001; OR, 10.44), and 6 or more teeth (p<0.001; OR, 12.31). Byun et al. [19] also analyzed the association between periodontal disease and cardiovascular diseases, conducting a large study with approximately 170,000 participants. They concluded that periodontal disease is a significant risk factor for acute myocardial infarction (OR, 1.34) and stroke (OR, 1.35). Alhadainy et al. [20] assessed the link between oral diseases and self-reported history of stroke in an elderly US population. Of all oral health variables examined, only the number of missing teeth was significantly associated with stroke history. Compared to patients missing 0 to 3 teeth, individuals missing 4 to 10 teeth had an OR of 1.72 (95% confidence interval [CI], 1.36–2.29), while those missing 11 to 27 teeth had an OR of 2.40 (95% CI, 2.24–2.69) and exhibited a significantly higher likelihood of reporting a stroke. The OR was highest for edentulous patients, who had 28 missing teeth (OR, 3.09; 95% CI, 2.97–3.12). Our results did not show a significant relationship between ischemic events (stroke and acute myocardial infarction) and periodontal disease. Regarding hypertension, Mendes et al. [21] previously demonstrated an association between high blood pressure and tooth loss. Their cross-sectional study of 10,576 patients revealed a positive and statistically significant link between extensive tooth loss (defined as the absence of more than 10 teeth) and systemic arterial hypertension, even after adjusting for common risk factors such as smoking. Similarly, our findings indicated a positive association between tooth loss and high blood pressure in both women and men. Additionally, we noted an association between tooth loss and diabetes exclusively in female participants; women with 6 or more missing teeth had a significantly increased risk of diabetes (OR, 9.32; p=0.005). The significance of this indicator underscores the concept that advanced periodontal disease can lead to the loss of many teeth, and the absence of teeth may thus be indicative of the chronicity of the condition.

The association between tooth loss and blood pressure measurements was investigated in a study by Hosadurga et al. [22]. In this cross-sectional study involving 270 volunteers, the authors identified a significant positive association between the absence of more than 10 teeth and elevated systolic blood pressure. In contrast, a study by Almoznino et al. [23], which included approximately 132,000 individuals aged 18 to 50 years, did not find a significant link between periodontal disease and high blood pressure. However, when analyzing CRP levels resulting from periodontal inflammation, the authors noted a marginally positive association with hypertension (OR, 1.01). These findings diverge from those of our study and most of the literature, as previously mentioned. A potential reason for this discrepancy could be the age range of the population in their study, which consisted mainly of young adults. In contrast, our results align with most evidence published on this topic. The diversity and broad age range of our study population underscore the importance of our findings. The robustness of the data—gathered through clinical evaluations, self-reports, and medical record reviews—lends considerable credibility and allows for comparison, as these methods are commonly employed in various studies addressing this issue.

Diabetes mellitus is a clinical syndrome characterized by hyperglycemia due to a hereditary and/or acquired deficiency in insulin production, action, or both. The association between this disease and periodontitis has been documented since the 1960s. However, the specific mechanism linking diabetes mellitus and periodontal disease remains to be fully elucidated [24]. To clarify the relationship between these conditions, Stohr et al. [25] conducted a systematic review with meta-analysis, which revealed a positive prospective bidirectional association between periodontal disease and diabetes mellitus. Our study identified a significant correlation between periodontal disease and diabetes only in those with a periodontal index between 9 and 13 (the 3rd quartile). This group was 5.8 times as likely to develop diabetes (p=0.029) as those in the first quartile. Another recent systematic review examined the epidemiological link between periodontitis and type 2 diabetes mellitus across 4 electronic databases, identifying 53 observational studies. The results showed that the adjusted prevalence of type 2 diabetes mellitus was significantly higher in patients with periodontitis (OR, 4.04; p<0.001) and vice versa (OR, 1.58; p<0.001). Severe periodontitis was associated with a 53% higher incidence of type 2 diabetes mellitus (p<0.001), a finding that was generally consistent. In contrast, the impact of mild periodontitis was less pronounced (relative risk, 1.28; p=0.007). These findings led the authors to conclude a bidirectional relationship between diabetes and periodontitis [26]. In a randomized clinical trial, Rapone and colleagues [27] assessed the correlation between periodontal treatment and glycemic control in patients with type 2 diabetes. Following 6 months of follow-up among 187 patients, they concluded that non-surgical periodontal therapy reduces levels of glycated hemoglobin and CRP. Similar outcomes were reported by Qureshi et al. [28]. Furthermore, a cross-sectional study involving 11,429 participants by Ghanem and Nagy [29] found that self-perceived poor oral health was a risk factor for diabetes (OR, 1.35; 95% CI, 1.04–1.75). This study underscores the importance of incorporating oral health measures into comprehensive diabetes management approaches.

Corbella et al. [30] hypothesized that periodontitis may be an independent risk factor for cancer development, both locally and at distant sites, due to the persistent chronic inflammation of periodontal tissues. These researchers observed a significant positive correlation between periodontal disease and various cancers, including those of the digestive tract, pancreas, prostate, breast, uterus, lung, and hematological system, as well as grouped esophagus/oropharynx cancer and non-Hodgkin lymphoma. Ma et al. [31] reported similar findings in a meta-analysis of epidemiological studies, lending support to the theory that periodontitis is linked to the development of esophageal cancer, prostate cancer, hematological cancer, and melanoma of the skin. These results underscore the importance of early prevention and treatment of periodontitis. Liu et al. [32] used a large database to demonstrate that individuals with periodontitis were at higher risk of developing gastric cancer compared to those with good oral health (OR, 1.13; 95% CI, 1.04–1.23; I²=0.00%; p<0.01). Additionally, Li et al. [33] sought to explore the bidirectional causal relationship between periodontitis and 4 types of urological tumors—kidney, prostate, bladder, and testicular cancers—using a Mendelian randomization approach. They found significant positive genetic correlations between periodontitis and kidney cancer (OR, 1.287; 95% CI, 1.04–1.594; p=0.020). We similarly identified a positive association between periodontal disease in the highest quartile, defined as a periodontal index of 14 or higher, and the incidence of cancer in study volunteers (p=0.045; OR, 8.71). However, we did not distinguish between cancer types.

The primary limitations of our study stem from its cross-sectional design, which precludes the ability to infer causality or assess the mechanisms underlying the relationship between periodontal disease and the chronic diseases under investigation. Another notable limitation is the potential for underdiagnosis of periodontitis resulting from our decision to employ the CPI methodology.

Conclusion

Our findings indicate that periodontal disease is positively and significantly associated with arterial hypertension and diabetes mellitus in those over 45 years old, independent of confounding factors such as smoking and overweight. Furthermore, greater severity of periodontal disease is associated with higher rates of hypertension and diabetes. Additionally, among women, severe periodontitis constitutes a risk factor for cancer, while tooth loss is implicated as a risk factor for high blood pressure and diabetes.

To further explore the topic and establish a causal link between oral health conditions and chronic non-communicable diseases, additional research is necessary. We propose a methodology that includes measuring inflammatory cytokines and detecting periodontal pathogens in atheroma plaques and neoplastic tissues using polymerase chain reaction. These studies could help elucidate the mechanisms underlying the association between periodontal disease and overall systemic health. Moreover, observational studies with long-term follow-up in specific populations could be conducted to evaluate the incidence of chronic diseases and correlate these findings with the oral health status of individuals.

Overall, our study underscores the importance of a multidisciplinary approach in the care of public health service users, considering the substantial interrelationship between oral health and systemic health. This approach is crucial for improving the effectiveness and efficiency of the therapies proposed.

HIGHLIGHTS

• Recent evidence from intervention studies suggests that local treatment of periodontitis can improve several markers of comorbidity, including blood pressure, glycemic index, and C-reactive protein levels.

• A positive association was observed between periodontal disease, hypertension, and diabetes among individuals over 45 years old, independent of potential confounding factors. Furthermore, a greater severity of periodontal disease was associated with higher rates of hypertension and diabetes.

• Our study underscores the importance of a multidisciplinary approach in the care of public health service users, highlighting the substantial interrelationship between oral health and systemic health.

Article information

Ethics Approval

This project received approval from the Ethics Committee of the Health Sciences Center (CCS-UFES), as documented in Opinion No. 5,048,518, dated October 20, 2021. Subsequently, the Vila Velha City Hall authorized its execution, under process No. 42,621/2021. All participating volunteers underwent a clinical and periodontal examination conducted by a trained and qualified professional, following the completion of an informed consent form.

Conflicts of Interest

The authors have no conflicts of interest to declare.

Funding

None.

Availability of Data

All data generated or analyzed during this study are included in the published article. Requests for additional data can be directed to the corresponding author.

Authors’ Contributions

Conceptualization: GVdM, ACRF, CCJ; Data curation: GVdM, BFSdM; Formal analysis: GVdM, CCJ; Investigation: GVdM, BFSdM; Methodology: GVdM, CCJ, ACRF; Project administration: GVdM; Resources: CCJ; Software: LHSP; Supervision: CCJ, ACRF; Validation: LHSP; Visualization: GVdM; Writing–original draft: GVdM; Writing–review & editing: all authors. All authors read and approved the final manuscript.

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Figure & Data

References

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