Periodontitis and Metabolic Control of Adults with Type 1 Diabetes

Introduction

Chronic conditions such as periodontitis and type 1 diabetes mellitus (T1DM) have a significant impact on public health globally. Periodontitis is a chronic inflammatory disease of the periodontium and is hallmarked by loss of connective tissue and alveolar bone (Caton et al. 2018). T1DM is caused by the autoimmune destruction of the beta cells within the pancreas, leaving the sufferer chronically dependent on exogenous insulin (Magliano and Boyko 2021). There is ever-increasing knowledge that suggests a bidirectional relationship between periodontitis and type 2 diabetes mellitus (T2DM; Polak et al. 2020). Although the relationship between periodontitis and T1DM has been studied extensively, there is limited evidence in South Africa on the association of periodontitis with T1DM. The burden of noncommunicable diseases, such as diabetes mellitus, on the public health system in South Africa warrants this research in the attempt to define holistic management protocols for patients with this metabolic disease.

A systematic analysis of the association between T1DM and periodontitis showed that there was an association between the 2 diseases and that periodontitis severity was greater in T1DM than in healthy controls (Costa et al. 2023). Periodontitis was found to have a prevalence of 20% in patients with T1DM (Dicembrini et al. 2020). The same authors presented data confirming T1DM as a relative risk for the development of periodontitis as confirmed by clinical attachment loss (Dicembrini et al. 2020). Uncontrolled diabetes mellitus results in complications that harm mortality rates and the quality of life of affected patients. Periodontitis is associated with the development of diabetes mellitus–related complications in adults with T1DM (Oliveira et al. 2016). The prevalence of periodontitis was reportedly higher in patients with uncontrolled T1DM, a finding similar to that in individuals with T2DM (Dicembrini et al. 2020). The role of hyperglycemia and its effects on the periodontium in T1DM was confirmed elsewhere (Costa et al. 2023). Periodontitis can lead to tooth loss, and a longitudinal study observing oral health determinants in T1DM reported a statistically significant loss of teeth in T1DM with diabetic-induced peripheral neuropathies (Steigmann et al. 2022). There are limitations to studies that have been attributed to the heterogeneity in the diagnosis and evaluation of the periodontium as well as the variability of the genetic backgrounds of populations. The latter emphasizes the need for baseline data from variable geographic origins to globally define this relationship between periodontitis and T1DM.

Diabetes mellitus has been described as a “looming health crisis” in an already resource-constrained public health system in South Africa (Statistics South Africa 2023). The tertiary health care facility from where the sample population hailed services patients who represent the lower socioeconomic communities and those affected by the staggering unemployment rates of about one-third to 44% of the population (Coovadia 2023). South Africa has the highest global Gini index, reported to be 63 in 2021 (Sulla and Facundo 2022; Dyvik 2024). This inequality affects health care access, specifically when aiming to address diseases with a holistic approach. (Coovadia 2023; Statistics South Africa 2023). Studies like these are required to engage with the extent of all related comorbidities of diseases that burden the public health care system and to inform their strategic management in resource-constrained populations. Periodontitis is often not considered in the holistic care of patients with diabetes mellitus, especially in resource-poor settings.

This study aims to determine the association between periodontitis and metabolic control in adult patients with T1DM in an outpatient hospital setting in South Africa.

Methods

This cross-sectional study was conducted to determine the association between periodontitis and glycemic control of adults with T1DM.

Patients from the endocrinology outpatient clinic at Tygerberg Hospital, who also attended the periodontology clinic at Tygerberg Oral Health Centre, Faculty of Dentistry of the University of the Western Cape, were invited to participate in the study, which used convenient sampling. Patients were recruited between February and August 2021.

Patients with known T1DM who were 18 y or older were included in the study. Patients who were younger than 18 y, who had T2DM, were pregnant or lactating, and were taking medications that affect the periodontium were excluded from the study.

The diagnosis of periodontal disease was made according to the 2017 American Academy of Periodontology and the European Federation of Periodontology (EFP) classification of periodontal and peri-implant health diseases and conditions (Caton et al. 2018) and based on the following clinical indices collected by a single clinician (A.S.): bleeding on probing percentage, probing pocket depths, as well as associated radiographic assessment of alveolar bone loss. A Williams periodontal probe was used to conduct this periodontal examination.

The sample size was determined to be 120, based on a 5% significance level and a power of 80% with a guestimate odds ratio of 1.8 when assessing whether there was an association between periodontal diagnosis and opposing subjects with healthy gingiva in participants with poor metabolic control.

The patients provided informed consent for participation. The informed consent was conducted in writing in a language that the patient understood (Afrikaans, English, and isiXhosa). The patients could withdraw from the study at any time with no prejudice. The data-capturing sheet for each participating patient was coded to aid data anonymity. The study was reviewed and approved by the Biomedical Research and Ethics Committee of the University of the Western Cape and the following registration number was granted: BM18/9/14. Additional permission was granted from the dean of dentistry to access the patients. All participating patients who required intervention were referred for treatment at the faculty of dentistry. All periodontal treatment required was conducted by the author (A.S.).

Results

There were 120 adult participants, of whom 61.67% (n = 74), were female and 38.33 % (n = 46) were male. Most were nonsmokers and younger than 44 y. There were 78 (65%) participants with uncontrolled blood glucose (BG) and 42 (35%) with good control in this sample, based on HbA1c ≤ 7%. The median HbA1c level was 8.75 (interquartile range: 6.1 to 12.2).

Table 1 depicts that 97% of the participants with periodontitis had uncontrolled BG. There were 40 (35.4%), 28 (24.8%), and 45 (39.8%) participants who were classified as mild periodontitis (stage I/II), moderate periodontitis (stage III), and severe periodontitis (stage IV). Of the participants classified as mild periodontitis, 21 (52.5%) were uncontrolled. In the moderate and severe stages, 18 (64.3%) and 37 (82.2%) were classified as having uncontrolled diabetes (P = 0.013). The bleeding score was higher in uncontrolled (94, IQR: 83 to 100) compared with controlled persons with T1DM (73 IQR: 63 to 82) (P < 0.001). More females with periodontitis had uncontrolled BG than those with better metabolic control, but this was not statistically significant (P = 0.248) (Figure 1).

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Table 1.

Relation between Periodontitis and Demographics with Blood Glucose (Metabolic) Control in the Participants.

	Total, n (%)	Metabolic Control		P Value
		Controlled, n (%)	Uncontrolled, n (%)
Periodontitis
No	7 (5.8)	5 (11.9)	2 (2.6)
Yes	113 (94.17)	37 (88.1)	76 (97.4)	0.05 a
Sex
Female	74 (61.7)	31 (73.8)	43 (55.1)
Male	46 (38.33)	11 (26.2)	35 (44.9)	0.248
Age
<25	31 (25.8)	11 (26.2)	20 (25.6)
25 to 34	38 (31.7)	13 (31)	25 (32.1)
35 to 44	31 (25.8)	10 (23.8)	21 (26.9)
45 to 54	12 (10.0)	6 (14.3)	6 (7.7)
≥55	8 (6.7)	2 (4.8)	6 (7.7)	0.741 a
Smoking
No	79 (65.8)	33 (78.6)	46 (59)
Yes	41 (34.2)	9 (21.4)	32 (41)	0.094
Periodontal staging
Mild (stage I/II)	40 (35.4)	19 (47.5)	21 (52.5)
Moderate (stage III)	28 (24.8)	10 (35.7)	18 (64.3)
Severe (stage IV)	45 (39.8)	8 (17.8)	37 (82.2)	0.013*
Bleeding score percentage, median [IQR]	84 [73 to 100]	73 [63 to 82]	94 [83 to 100]	<0.001*

IQR, interquartile range.

a

Fisher’s exact test.

*

Statistically significant.

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Figure 1.

Metabolic control by sex and periodontal state.

Figure 2 depicts the role of smoking in the sample. All smokers had periodontitis, and there was no significant difference between BG in smokers and nonsmokers.

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Figure 2.

Metabolic control by smoking and periodontal state.

In the simple logistic regression, severe periodontitis compared with mild/moderate periodontitis had a 4.18 (1.56 to 11.2) odds of lack of metabolic control. However, when taking into consideration sex and bleeding score as a percentage, periodontal severity was no longer statistically significant. Males had a 2.66 (0.968 to 7.29) times likelihood of experiencing a lack of metabolic control, but this was not statistically significant. However, bleeding score percentage remained statistically significant in the simple and multiple logistic regressions (Table 2).

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Table 2.

Simple and Adjusted Multiple Logistic Regression.

Simple Logistic Regression (Metabolic Control)	Odds Ratio (95% CI)	P Value	Multiple Logistic Regression (Metabolic Control)Odds Ratio (9%% CI)	P Value
Periodontitis stage
Mild (stage I/II)
Moderate PD (stage III)	1.63 (0.604 to 4.39)	0.335	0.85 (0.23 to 2.8)	0.789
Severe PD (stage IV)	4.18 (1.564 to 11.2)	0.004*	1.79 (0.6 to 5.8)	0.328
None	36 (0.063 to 2.09)	0.256	1.34 (0.2 to 10.8)	0.778
Age category, y
<25
25 to 34	1.06 (0.391 to 2.86)	0.912
35 to 44	1.16 (0.403 to 3.31)	0.788
45 to 54	.55 (0.143 to 2.12)	0.385
≥55	1.65 (0.283 to 9.6)	0.577
Gender
Female
Male	2.29 (1.01 to 5.21)	0.047*	2.76 (0.9 to 7.8)	0.054
Smoking status
No
Yes	2.55 (1.075 to 6.05)	0.034*
Bleeding percentage	1.09 (1.055 to 1.13)	<0.001*	1.09 (1.05 to 1.13)	<0.001*

*

Statistically significant.

Discussion

In this study, we aimed to explore the relationship between periodontitis and metabolic control in patients with T1DM. The findings of this study will add to the growing body of knowledge trying to identify and understand the associations between periodontal health severity and metabolic control, especially in a South African setting. This is important since South Africa has one of the highest global burdens of diabetes mellitus (Cho et al. 2018). Knowledge about diabetes and its comorbidities is limited in the African setting, and thus there is a need for policy makers to be made aware of the severe implications of this disease (Moodley and Rambiritch 2014).

The prevalence of uncontrolled BG as well as periodontitis in the study sample was 65% and 94%, respectively. These findings underscore the importance of addressing periodontal health in individuals with T1DM, particularly in regions with a high prevalence of both conditions. The control of BG in patients with T1DM and periodontitis is also strongly recommended as an inclusion for wholistic patient management, regardless of the stage of periodontitis diagnosed (Sanz et al. 2020; Herrera et al. 2022).

The reason for the high prevalence of BG can be explained by patient recruitment, which was from a tertiary endocrinology outpatient facility, thus creating a study sample in which there was a potential for bias. The prevalence of periodontitis in this sample population was higher than reported values found in other T1DM populations, where the range of periodontitis prevalence was reported to be 82% to 4% (Dicembrini et al. 2020). This variability can be attributed to the different diagnostic criteria used for the diagnosis of periodontal diseases across publications (Dicembrini et al. 2020). Geographic diversity is another plausible reason for the variation of periodontitis prevalence presented among T1DM. The current study diagnosed each patient according to the latest classification of periodontal and peri-implant diseases (Caton et al. 2018), and the severity of periodontitis, as defined by staging, was not significantly associated with metabolic control in this sample (P = 0.013). The periodontal disease classification has included diabetes mellitus as a modifying factor when diagnosing periodontitis (Caton et al. 2018). This is the first periodontal disease classification system that recognizes the role of diabetes mellitus in the pathogenesis of periodontitis and its prognostic value with respect to its severity and management. Periodontitis has been known as a complication of diabetes mellitus; however, these diseases are now considered to be comorbid diseases (Polak et al. 2020).

Several possible factors may have contributed to the lack of association between periodontitis and its severity in our study; confounding factors such as plaque index were not collected, and this is a limitation in the present study. The autoimmune nature of T1DM may have a different interaction with periodontitis than T2DM and also could account for this outcome; however, this may be negated by a later discussion on the role of hyperglycemia in the relationship between T1DM and periodontitis. Our small sample size may have had an impact on the statistical power to detect associations.

Our study also assessed the bleeding score percentage and its effect on the metabolic control of participants with T1DM. We found that the odds of experiencing a higher bleeding percentage score resulted in an increased odds (odds ratio = 1.09) of experiencing a lack of metabolic control, which shows a clear relationship between the bleeding score percentage and the lack of metabolic control. A similar study from India also showed that bleeding was a significant factor for metabolic control in adults with T1DM, although their method of assessment was the bleeding index (Ajita et al. 2013). Clinically, this association between bleeding score percentage and lack of metabolic control emphasizes the inflammatory link (Polak et al. 2020) between these 2 diseases and the hyperinflammatory environment that periodontitis and diabetes mellitus elicit. These inflammatory changes have been substantiated by human and animal studies that have shown an increase in proinflammatory cytokines in serum, saliva, and gingival crevicular fluid. In the presence of inflammation, the ecology of the oral microbiome undergoes dysbiosis to favor the growth and development of more anaerobic gram-negative pathogenic species within the periodontium (Sanz et al. 2018; Polak et al. 2020). The action of hyperglycemia and the resultant host response act synergistically in many respects; one being the effect on innate immunity by the activation of toll-like receptors (2, 4, and 9), which in turn cascade a greater host inflammatory response (Polak et al. 2020). In vitro studies confirm the irreversible production of advanced glycation end products (AGE) in periodontal tissues within a hyperglycemic environment (Sanz et al. 2018). AGE serves to induce inflammation by its cellular effects as well as enhances oxidative stress (Chopra et al. 2022). Cells like gingival and periodontal ligament fibroblasts have been shown to secrete proinflammatory cytokines in response to AGE, thus having a direct effect on aggravating periodontitis in poorly controlled diabetes mellitus (Chopra et al. 2022). Blocking of AGE receptors in animal models with diabetes mellitus shows promising results as there is a decrease in the expression of proinflammatory cytokines and matrix metalloproteinases in periodontal tissues as well as a reduction of bone resorption, the hallmark of periodontitis. Increased oxidative stress in circulation creates an environment that favors the induction of osteoclastogenesis (Chopra et al. 2022). The receptor activator of nuclear factor kappa beta ligand (RANKL)/osteoprotegerin axis controls the resorption of bone. The former stimulates bone resorption by binding with RANK, which is expressed by preosteoclasts and osteoclasts. The latter antagonizes RANKL and inhibits osteoclastogenesis. Studies have shown that in diabetes mellitus, the axis is favored toward RANKL, specifically in poorly controlled diabetes mellitus. AGE also enhances the activity of osteoclasts and decreases the ability of mesenchymal stem cells to differentiate into osteoblasts. The above form part of the essential steps toward periodontitis in diabetes mellitus patients. Periodontal management of patients with T1DM is thus crucial to reduce this inflammatory insult. Patients with higher bleeding score percentages may be at an increased risk of uncontrolled metabolic disease, and this outcome is emphasizing the need for increased frequency of periodontal maintenance in T1DM patients and that oral health care workers should be included in the wholistic management of these patients.

The present study aimed to investigate the association between periodontitis and metabolic control in adults with T1DM within a South African setting. The findings contribute to the growing body of literature exploring the interplay between diabetes and periodontitis, shedding light on the unique characteristics of this association in the South African population.

This study’s findings are important for the future clinical and dental management of dentate patients with T1DM. Although not significant, the relationship between periodontal severity and metabolic control with the high prevalence of periodontitis underpins the importance of routine oral health assessments and preventative interventions. The integration of oral health care into diabetes management will promote interdisciplinary collaboration between diabetic health care providers and dental health professionals.

Future research should focus on studies with larger sample sizes in a more diverse setting using longitudinal study designs and examining a larger number of confounding factors. This could include examining shared inflammatory pathways or genetic factors that could provide a targeted focus on the pathophysiology of these conditions.

Conclusion

The presence of periodontitis alone does not have an impact on diabetes mellitus, but the staging of periodontitis, as determined by simple logistic regression and the percentage bleeding score, as determined by multiple logistic regression, have been shown to have an impact on metabolic control. Recognizing that advanced periodontitis can have an impact on lack of metabolic control emphasizes the need for a holistic approach toward integrated dental and diabetes management within this population. This study highlights the need for integrated tailor-made interventions that are aimed at patients with T1DM and periodontitis.

Author Contributions

A Jeftha, contributed to conception, design, and interpretation, drafted and critically revised the manuscript; A Suliman, contributed to data acquisition and interpretation, critically revised the manuscript; M. Conradie Smit, contributed to design, critically revised the manuscript; F. Kimmie-Dhansay, contributed to data analysis and interpretation, drafted and critically revised the manuscript. All authors gave their final approval and agree to be accountable for all aspects of work.