Public Awareness of the Association between Periodontal Disease and Systemic Disease

Periodontal disease is associated with other non-communicable diseases including diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, and respiratory tract infections. This association merits careful study of the general population’s awareness level in order to leverage the current state of science to improve general health and quality of life. This study included 502 residents of Saudi Arabia who received computer-assisted interviews to fill up the survey. Results indicated a low level of awareness among the study population regarding the association of periodontal disease to diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, and respiratory tract infections. A higher level of awareness was noticed with individuals with periodontal disease, themselves or a member of their family having a systemic disease, and who have a specialized person or scientific article as their source of information. This observed low level of awareness deserves the attention of public health authorities to prioritize programs that increase the awareness, improve health, and reduce burden of systemic diseases of high prevalence, morbidity, and mortality.


Introduction
Periodontal disease is a chronic inflammatory infection that results in the progressive destruction of supporting tissues of the teeth, with continuing loss of connective tissue attachment and resorption of the bone [1]. According to the World Health Organization (WHO), severe periodontal disease affects over one billion individuals, constituting about fourteen percent of the world population [2]. Different risk factors are associated with periodontal disease, the strongest being cigarette smoking and diabetes mellitus [3]. If left untreated, periodontal disease can result in patients with missing teeth, affecting their well-being and quality of life [4][5][6].
Periodontal disease appears to be associated with other non-communicable systemic diseases. Not only is periodontitis a risk for difficult glycemic control, but it is also a complication of diabetes mellitus, resulting in a "bidirectional association" between them [7]. Periodontal disease affects glycemic control and increases the risk of developing hyperglycemia, which increases with periodontal disease severity [8][9][10][11]. Some evidence suggests that the treatment of periodontal disease would result in better glycemic control [12]. For coronary heart disease and atherosclerosis, patients with periodontal disease are at an increased risk for these diseases, including acute myocardial infarctions [13]. In addition, oral bacteria have been detected in atherosclerotic plaques [5,14]. Periodontal disease has been reported to affect hypertension, causing increased systolic and diastolic blood pressure [15]. Moreover, other reports have demonstrated systolic and diastolic blood

Survey Design and Outcome Measures
The survey instrument consisted of a five-point Likert scale (strongly disagree, disagree, I do not know, agree, and strongly agree) to assess awareness of the general public regarding the association of having periodontal disease with four systemic diseases, namely diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, and respiratory tract infections. In addition, demographic information of the participants, including sex, age, region, education level, and frequency of dental visits, was collected. Furthermore, self-perceived/reported affliction by dental disease (untreated dental caries or periodontal disease) or systemic diseases of interest in this study for self or family members and the source of their stated selection regarding the association between periodontal disease and systemic disease, has been collected. The survey had ten close-ended questions.
We conducted several rounds of linguistic validation to ensure clarity and understanding of the survey questions via focus groups. In addition, group members were asked to review and discuss survey questions and answers. Based on the outcomes of linguistic validation procedures, the survey was further edited, and the final version was approved.

Data Analysis
Descriptive analysis was used to describe the variables. In addition, awareness about the association of periodontal disease with systemic disease was described as frequencies and percentages within each demographic item, self-reported dental and health condition, and source of information.
Inferential statistical analysis was performed to evaluate the relationship between various socio-demographic factors and the perceived association of periodontal disease with systemic disease. The relationship between various socio-demographic factors and the perceived association of periodontal disease with systemic disease were examined using a chi-square test or Fisher's Exact test, depending on data frequency. The perceived association data were analyzed using a dichotomized version of the Likert scale (agree and strongly agree combined). Significant factors from bivariate analysis were further explored with multivariate analysis using binary logistic regression models.
Level of significance 0.05 was used for all inferential analysis, with p-values < 0.05 reported as statistically significant. Both descriptive and inferential analysis was performed using SPSS Statistics software (IBM Corp, Version 28.0. Armonk, NY, USA).

Results
Out of 808 potential participants contacted, 502 accepted to participate and completed the interview (response rate 62.1%). The condition was satisfied regarding equal sex and region distribution of the sample (Table 1). Almost half of the sample (48%) believe that they are free of dental caries and periodontal disease, while 74.8% believe that they are free of the systemic diseases studied, and 37.6% have no family member affected by diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, or respiratory tract infection (Table 2). In the overall sample, most participants chose "I do not know" in the association between periodontal disease and systemic disease (Table 3). Diabetes mellitus was the disease with the least "I do not know" response (47.2%), hypertension and respiratory tract infection were the most with 54.0% each, and coronary heart disease and atherosclerosis was 51.1% (Table 3). The highest percentage of respondents that believe there is an association between periodontal disease and systemic disease (agree and strongly agree) was for diabetes mellitus (35.7%), followed by hypertension (28.1%). Most participants (59.8%) selected the association between periodontal disease and systemic disease based on their opinion (Table 4). * The total of percentage is more than 100% due to individuals having more than one source of information.

Periodontal Disease and Diabetes Mellitus
The general population's awareness regarding the association of periodontal disease and diabetes mellitus was demonstrated as the response to the association of periodontal disease with diabetes mellitus, categorized according to demographic, dental and health status, and source of information. Descriptive analysis using frequencies and percentages is presented in Table 5. The totals of percentages are more than 100% due to individuals having more than one condition simultaneously. Per-centages are calculated for each row.
The strength of the association between periodontal disease and diabetes mellitus was examined between levels of various factors, and results are presented in Table 6. The analysis was performed using a chi-square test or Fisher's Exact test.
The analysis of the perceived strength of the association of periodontal disease with diabetes showed several statistically significant predictors. These factors result in an increased proportion of responses who agree or strongly agree with the statement of awareness of periodontal disease and diabetes mellitus association. Here are the factors that are statistically significant: Member(s) of participant's family having coronary heart disease and atherosclerosis (p = 0.031) • Participant having an information source as a specialized person in media or on social media (p = 0.002 and p < 0.001, respectively) • Having an information source as scientific article (p < 0.001) The significant predictors from bivariate analysis were entered into multivariate analysis-binary logistic regression model ( Table 7). The dependent variable was the perceived association between periodontal disease and diabetes mellitus, with two levels: strongly agree/agree vs. strongly disagree/disagree/neutral. The results of multi-variate analysis suggest that only three factors remain statistically significant: Having an information source as a specialized person on social media (OR = 2.34, Having an information source as scientific article (OR = 2.98, p = 0.008)

Periodontal Disease and Coronary Heart Disease and Atherosclerosis
The general population's awareness regarding the association of periodontal disease and coronary heart disease and atherosclerosis was demonstrated as the response to the association of periodontal disease with coronary heart disease and atherosclerosis, categorized according to demographic, dental and health status, and source of information. Descriptive analysis using frequencies and percentages is presented in Table 8. The totals of percentages are more than 100% due to individuals having more than one condition simultaneously. Per-centages are calculated for each row.
The strength of the association between periodontal disease and coronary heart disease and atherosclerosis was examined between levels of various factors, and results are presented in Table 9. The analysis was performed using a chi-square test or Fisher's Exact test.
The analysis of the perceived strength of the association of periodontal disease with coronary heart disease and atherosclerosis showed several statistically significant predictors. Here are the significant factors that result in an increased proportion of responses who agree or strongly agree with the statement of awareness of periodontal disease and coronary heart disease and atherosclerosis association: Having an information source as a specialized person in media or on social media (p < 0.001) • Having an information source as general accounts on social media (p < 0.001) • Having an information source as scientific article (p < 0.001) The significant predictors from bivariate analysis were entered into multivariate analysis-binary logistic regression model (Table 10). The dependent variable was the perceived association between periodontal disease and coronary heart disease and atherosclerosis, with two levels: strongly agree/agree vs. strongly disagree/disagree/neutral. The results of multivariate analysis suggest that only seven factors remain statistically significant: Having an information source as scientific article (OR = 6.43, p < 0.001)

Periodontal Disease and Hypertension
The general population's awareness regarding the association of periodontal disease and hypertension was demonstrated as the response to the association of periodontal disease with hypertension, categorized according to demographic, dental and health status, and source of information. Descriptive analysis using frequencies and percentages is presented in Table 11. The totals of percentages are more than 100% due to individuals having more than one condition simultaneously. Per-centages are calculated for each row.
The strength of the association between periodontal disease and hypertension was examined between levels of various factors, and results are presented in Table 12. The analysis was performed using a chi-square test or Fisher's Exact test.
The analysis of the perceived strength of the association of periodontal disease with hypertension showed several statistically significant predictors. Here are the significant factors that result in an increased proportion of responses who agree or strongly agree with the statement of awareness of periodontal disease and hypertension association: Having an information source as a specialized person in media or on social media (p = 0.004 and p < 0.001, respectively) • Having an information source as general accounts on social media (p < 0.001) • Having an information source as scientific article (p < 0.001) The following factors significantly decrease the proportion of responses who agree or strongly agree with the statement of awareness of periodontal disease and hypertension association: • Member(s) of participant's family having diabetes mellitus (p = 0.045) • Having respondent's own opinion as an information source (p = 0.023) The significant predictors from bivariate analysis were entered into multivariate analysis-binary logistic regression model (Table 13). The dependent variable was the perceived association between periodontal disease and hypertension, with two levels: strongly agree/agree vs. strongly disagree/disagree/neutral. The results of multivariate analysis suggest that only six factors remain statistically significant:

Periodontal Disease and Respiratory Tract Infections
The general population's awareness regarding the association of periodontal disease and respiratory tract infections was demonstrated as the response to the association of periodontal disease with respiratory tract infections, categorized according to demographic, dental and health status, and source of information. Descriptive analysis using frequencies and percentages is presented in Table 14. The totals of percentages are more than 100% due to individuals having more than one condition simultaneously. Percentages are calculated for each row.
The strength of the association between periodontal disease and respiratory tract infections was examined between levels of various factors, and results are presented in Table 15. The analysis was performed using a chi-square test or Fisher's Exact test.  The significant predictors from bivariate analysis were entered into multivariate analysis-binary logistic regression model (Table 16). The dependent variable was the perceived association between periodontal disease and respiratory tract infections, with two levels: strongly agree/agree vs. strongly disagree/disagree/neutral. The results of multivariate analysis suggest that only four factors remain statistically significant:

Discussion
This study investigated the general public's awareness regarding the association of periodontal disease with four systemic diseases: diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, and respiratory tract infection. The overall results indicated a low level of awareness, where about 50% of individuals did not know about the association. However, when the data were analyzed according to various demographic, dental and medical health, and source of information variables, differences among the groups started to emerge. In general, people affected with periodontal disease, affected with the same systemic disease, have a family member with coronary heart disease and atherosclerosis, or use scientific articles or specialized individuals as a source of information will tend to be more aware of the association between having periodontal disease and the incidence or severity of diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, and respiratory tract infection.
The low level of awareness about the association between periodontal disease and systemic disease reported herein agrees with previous studies [24]. For example, the level of awareness about the effect of periodontal disease on diabetes mellitus in this study (35.7%) is similar to the average of the previously reported 21.8% for Saudi diabetic patients [27], and 44% for German patients [28]. In addition, the low level of awareness for the association between periodontal disease and coronary heart disease and atherosclerosis in this study (21.9%) agrees with a study that showed it to be less than 10% [29]. Despite the limitations of this study, namely being a cross-sectional study, self-reporting of dental and medical conditions by participants, and involving only Saudi residents, the general trend of this work's findings is similar to other studies. However, the variability in the extent of awareness between the current study and the other studies could be attributed to the differences in study samples and study methodology, as well as to the difference in the time of study conduction, where the reported association between periodontal disease and systemic disease increases with time, thereby increasing the level of awareness is expected.
The results revealed that individuals with periodontal and systemic diseases had increased awareness of their association. It is reasonable to hypothesize that such awareness had come from their healthcare providers, who have a high level of awareness regarding the association between periodontal disease and systemic disease [21,22]. In addition, findings of this study (Tables 5-16) shows that participants' information from specialized individuals contributed to the increased awareness and may reflect a change in society's learning behavior, where active members increasingly influence the general public on conventional and social media. Furthermore, higher awareness of the association demonstrated by subjects in this study who gained information from scientific articles may reflect a shift in knowledge dissemination norms brought by the ease of reach to open access journals on the internet.
The association of periodontal disease and systemic disease is an active area of research, with evidence suggesting a unidirectional, only one disease affecting the other, or bidirectional relationship. Each disease will adversely affect the other in this relationship. Periodontal disease association with diabetes mellitus is probably the most established bidirectional relationship, with periodontal disease affecting glycemic control [8], and individuals with periodontal disease have 19-33% more risk of developing hyperglycemia [9,10], which is increased with periodontal disease severity [11]. On the other hand, having diabetes mellitus is associated with three-times increased risk of having periodontal disease [30]. Individuals with severe periodontal disease have 11% higher risk of acute myocardial infarction [13]. In addition, tooth loss, a common end-stage result of periodontal disease, is associated with a 3% increased risk of coronary heart disease [31]. Periodontal disease-affected individuals have an increased mean systolic (3.36 mm Hg) and diastolic (2.16 mm Hg) blood pressure compared to healthy controls [15]. In addition, periodontal disease was associated with increased odds (2.3) of being diagnosed with hyper-tension (systolic blood pressure > 140 mm Hg) [15]. Interestingly, six months after periodontal disease treatment, there was a reduction in the mean systolic and diastolic blood pressure by 12.57 mm Hg and 9.65 mm Hg, respectively [16]. However, the evidence supporting blood pressure reduction following periodontal disease therapy is inconclusive [32]. Periodontal disease increases the risk of pneumonia, with an odds ratio of up to 4.4 reported in one study [17,18]. This association between periodontal disease and systemic disease merits efforts concerted at improving the periodontal health of the general public, both afflicted with systemic diseases and healthy individuals. In addition to the improved quality of life associated with having healthy teeth [6], it could also contribute to preventing or reducing the severity of some systemic diseases [5,19].
Improving oral health requires multi-level actions, starting with increasing the awareness of the general public regarding the association of periodontal disease and systemic disease utilizing the most effective means. Although members of medical and dental health teams have a high level of awareness regarding periodontal disease association with systemic diseases [20][21][22], this knowledge is yet to be transferred effectively to patients, as demonstrated in this and previous studies [24]. It seems that a lack of time, inadequate knowledge and training in oral health, as well as a lack of interaction with oral health care providers are the main barriers to providing patient education about the association between oral and systemic disease [21]. Therefore, efforts should be made to integrate patient education regarding the association between periodontal and systemic disease within care delivery; perhaps a support medical staff can be dedicated to such a task. In addition, medical care should include dental examination and treatment as part of systemic disease care through communication and collaboration with oral health care professionals [33,34]. Finally, the most effective venue to increase awareness for the general public should be utilized. The findings of this study show that specialized individuals, in various traditional and new social media outlets, as the source of high-awareness responses might be a good starting point.

Conclusions
Awareness of the general public regarding the association between periodontal disease and systemic disease is low. However, individuals having periodontal disease, being affected with the same systemic disease, having a family member with coronary heart disease and atherosclerosis, or using scientific articles or specialized individuals as a source of information were more aware of the association between having periodontal disease and the incidence or severity of diabetes mellitus, coronary heart disease and atherosclerosis, hypertension, and respiratory tract infection. This increased awareness of certain segments of the study population about the association of periodontal disease and systemic disease should form a basis to carefully understand the effect of various factors and then implement mechanisms to augment the awareness of the general population.