Periodontal disease and quality of life in patients with circulatory diseases

Abstract Introduction Circulatory system diseases are one of the leading causes of death. Periodontal health is a component of oral and general health that contributes to quality of life. Objective To analyze periodontal conditions and quality of life in patients with circulatory diseases. Material and method Cross-sectional study, with patients with circulatory diseases (n=125). The clinical periodontal examination was performed considering: biofilm, bleeding on probing, suppuration, probing depth, gingival recession, and clinical attachment level. Quality of life was assessed with the Medical Outcomes Study 36 – Item Short-Form Health Survey (SF-36) and Oral Health Impact Profile – short form (OHIP-14). Data were analyzed with parametric and nonparametric tests (α=5%). Result Elderly and men had a greater severity of periodontal disease. The Elderly had lower values in the domains of "Functional capacity" and "Physical aspects" (SF-36). The domain "Pain" had lower values in subjects with health/gingivitis. OHIP-14 did not show differences in the comparisons. There was no correlation between quality of life and the severity of periodontal disease. Conclusion Among patients with circulatory diseases, the elderly and men had greater severity of periodontal disease. The elderly had a poorer quality of life (functional capacity and physical aspects). There was no correlation between the severity of periodontal disease and quality of life.


INTRODUCTION
Circulatory diseases are one of the leading causes of death worldwide.In 2020, approximately 19.1 million deaths were attributed to cardiovascular diseases.The age-adjusted mortality rate per 100,000 population was 239.8 and the age-adjusted prevalence rate was 7,354.1 per 100,000 population.The highest mortality rates due to cardiovascular diseases in 2020 were in eastern Europe and Central Asia, while the rates were lower in North America (the highest-income region), Asia-Pacific, Latin America, and Western Europe 1 .In Brazil, circulatory diseases caused 10.8 million deaths between 1980 and 2019 2,3 .However, the trend of deaths from circulatory diseases has decreased during this period, but this decrease was uneven between Brazilian states, with greater reductions in the southern and southeastern regions, which have better socioeconomic indicators 2,4 .Regions with higher development and lower social inequality had the lowest mortality rates from circulatory diseases 1,2,5 .
Periodontal disease is a multifactorial inflammatory condition induced by the presence of dental biofilm, which affects the gums and supporting tissues and can lead to bone resorption and tooth loss [6][7][8][9] .Periodontal health is a component of an individual's oral and general health that contributes to their well-being and quality of life [6][7][8] .Periodontitis can be observed in more than 50% of the adult population, and its severe form affects 11% of people, making it the sixth most prevalent disease in humanity 7,8 .Several studies have shown that periodontitis is associated with several systemic conditions including diabetes, circulatory diseases, and premature birth 7,8,10,11 .Individuals with periodontal disease are at increased risk of tooth loss, edentulism, and masticatory dysfunction, which can have a negative impact on their nutrition, quality of life, and self-esteem 12 .Improvement in periodontal conditions contributes to the improvement of systemic health and well-being 7,8 .
Quality of life has been related to the degree of satisfaction with family, romantic, social, and environmental life, and existential aesthetics.It is a dynamic and complex phenomenon, not only a consequence of objective indicators but also of subjective aspects 4,13 .One of the validated generic instruments for evaluating quality of life is the short form health survey (SF-36), which has been applied to patients with systemic involvement and is easy to administer and understand 14 .Quality of life related to oral health is a multidimensional concept determined by a variety of conditions that affect the individual's perception, encompassing issues of physical, psychological, and social health.Therefore, the concepts of quality of life and health are inseparable 13,[15][16][17] .Dental problems can affect eating, sleeping, speaking, communication, social interaction, and self-esteem, leading to difficulties in daily activities and resulting in decreased quality of life 6,12,18,19 .The oral health impact profile short form (OHIP-14) is a validated instrument that allows for the detection of associations between social impact and perceived treatment needs and quantifies the levels of impact with good reliability 6,12,14,[19][20][21] .It also has a diversity of domains, and is of rapid administration and interpretation of results, allowing to evaluate of the severity, extent, and prevalence of negative impacts in a single session [13][14][15][16][17][18] .
Therefore, this study aimed to analyze periodontal conditions and quality of life in patients with circulatory system diseases.

Characterization of the Study and Research Subjects
This is a descriptive, quantitative, cross-sectional study with a convenience sample composed of patients with circulatory diseases under regular outpatient care at a university hospital in the state of Paraná, southern Brazil.The research followed the principles and recommendations of the STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) initiative 22 and was approved by the local research ethics committee (Process: 3.028.211;CAAE: 01591118.7.0000.0105),and all volunteers signed the informed consent form.
The sample size was based on the prevalence of cardiovascular diseases in the Brazilian population 3 .Therefore, the calculated minimum sample size was 123 volunteers with a confidence level of 95% and a margin of error of 5%.The inclusion criteria comprised both genders, over 18 years old, with a minimum of 6 teeth, diagnosed with cardiovascular disease (ICD-10) 23 , and no change in medication for at least 2 months.Exclusion criteria included: patients with acute oral conditions (ulcerative lesions, abscesses, and acute infections), uncontrolled chronic systemic disease, those who were unable, for any reason, to answer the questionnaires; lactating or pregnant women; and individuals who underwent periodontal or orthodontic treatment in the last 3 months.Data collection was carried out consecutively and non-probabilistically from November 2018 to November 2019.During this period, 125 patients who met the study inclusion criteria were evaluated.

Evaluation of Periodontal Conditions
The examination of periodontal conditions involved the counting of tooth loss, sites with biofilm presence, bleeding on probing, marginal suppuration, probing depth, gingival recession, and clinical attachment level.Periodontal evaluation was performed using a manual periodontal probe (North Carolina CP-15, Millennium Plus-Golgran Ind. Com.Instr.Odontológicos, São Caetano do Sul, São Paulo, Brazil) at six sites per tooth, with third molars excluded.Taking into account the classification of periodontal diseases and conditions 9 , we assign scores according to the severity of the periodontal disease.Score 1. Periodontal health and gingivitis (gingivitis defined as bleeding on probing ≥10% of sites, absence of attachment loss, and probing depth up to 3mm); Score 2. Periodontitis stages 1 and 2 (clinical attachment level ≤4mm and probing depth ≤5mm); Score 3. Periodontitis stages 3 and 4 (clinical attachment level ≥5mm and probing depth ≥6mm) 24 .

Training and Calibration
Two trained examiners (LZL and LTN) performed periodontal examinations on a group of patients to assess the inter-examiner reproducibility of measurements of gingival recession, probing depth, and clinical attachment level.Before the study, the investigators discussed and trained on the clinical parameters of dental biofilm, bleeding on probing, and marginal suppuration during the clinical examination of patients in a preliminary phase.Thirteen patients were examined to evaluate reproducibility but were not included in the final study sample.Each examiner made measurements in duplicate, with a 40-minute interval between exams.The Weighted Kappa test was used to assess inter-examiner agreement, which was substantial for gingival recession (0.74), probing depth (0.92), and clinical attachment level (0.85).

Quality of Life Assessment
Quality of life was assessed using the Medical Outcomes Study 36-Item Short-Form Health Survey (SF-36), an eight-domain questionnaire related to health: social functioning, physical functioning, general health, vitality, mental health, emotional well-being, pain, and role limitations due to physical health.Each domain has a score of 0-100, and the total is a simple average of the domains, with higher values representing a better quality of life 14 .Quality of life-related to oral health was measured using the reduced version of the Oral Health Impact Profile (OHIP-14), consisting of 14 questions divided into 7 dimensions, all related hierarchically 15 .This is an internationally used instrument to evaluate the quality of life-related to oral health, as it has good psychometric qualities and measures selfperception of the specific consequences of oral conditions 13 .
The SF-36 and OHIP-14 questionnaires were answered in the presence of the interviewer (LT) before the periodontal examination, in the health institution where the subjects were waiting for health appointments.

Statistical Analysis
Data were tabulated, processed, and analyzed using statistical software (IBM-SPSS Statistical Package for the Social Sciences® for Windows version 20.0, IBM, NY, USA), using descriptive and inferential statistics techniques.Quantitative and ordinal qualitative variables related to periodontal parameters were analyzed according to age and gender.The instruments used to measure quality of life were tested considering age, gender, and severity of periodontal disease.The normality of the data distribution was verified using the Kolmogorov-Smirnov test.After confirming a normal data distribution, comparisons of means between variables were made using independent samples t-tests and one-way ANOVA (with Tukey's post-test).Data that did not present normal distribution and the ordinal qualitative variable (severity scores of periodontal disease) were evaluated with nonparametric tests of Mann-Whitney and Kruskal-Wallis (with Dwass-Steel-Critcholw-Fligner posttest).To test the correlation between quality-of-life variables and the severity of periodontal disease, the Spearman correlation test was performed.The level of significance adopted was 5%.

RESULT
The final sample consisted of 125 participants with circulatory system diseases.The age ranged from 18 to 77 years, with a mean of 51.6±13.1 years, and 30% were over 60 years old.The majority were women (61%) and 66% reported being married/living together.Regarding monthly family income, 91% reported receiving up to 3 minimum wages per month.In terms of educational level, 58% completed elementary school.Obesity was observed in 46% of the individuals.The most prevalent circulatory diseases were lower limb varicose veins (ICD: I83 -43%) and primary essential hypertension (ICD: I10 -18%).A total of the 77% of volunteers controlled their systemic alteration with at least one medication.Most volunteers were nonsmokers (61%) and non-alcoholic (95%).Data are presented in Table 1.Regarding the severity of periodontal disease, 9% of the participants had a healthy or gingivitis status (score 1), 50% had stages 1 and 2 periodontitis (score 2), and 41% had stages 3 and 4 periodontitis (score 3).Elderly individuals and men had higher scores of periodontal disease severity (p<0.05).The population had an average of 9.2±7.5 missing teeth (33%), with individuals with score 1 (healthy/gingivitis) having a significant difference (p=0.038) in dental loss of 14.4±7.6 compared to those with stages 1 and 2 periodontitis (7.9±7.5), which was not significant for patients with stages 3 and 4 periodontitis (9.8±7.1).The probing depth ≥4mm was observed in 14% of sites, and the clinical attachment level ≥3mm was present in 19% of the sites.Considering age, the elderly (≥60 years) had greater dental loss and sites with clinical attachment level than those younger (p<0.001).Men had a higher percentage of sites with clinical attachment loss than women (Table 2).Quality of life measured with SF-36 had the domain "Social Functioning" with the highest score (70.1±30.2) and the lowest was observed in the "Physical Functioning" domain (40.8±44.6).Considering age, significant differences were observed in the "Physical Functioning" and "Role-Physical" domains, where older adults had lower scores (p<0.05).Women and men had similar results in all SF-36 domains.According to the severity of periodontal disease, the "Pain" domain had a lower score in individuals with score 1 (Health/Gingivitis) compared to patients with scores 2 (Stage 1 and 2 Periodontitis) and 3 (Stage 3 and 4 Periodontitis) (Table 3).The impact of oral conditions on quality of life measured by the OHIP-14 instrument had the lowest value in the domain of "Functional Limitation" and the highest in the domain of "Psychological Discomfort."The results of the OHIP-14 domains were similar considering the age, gender, and severity of periodontal disease (Table 3).

DISCUSSION
Our results showed that 91% of patients with cardiovascular diseases had some stage of periodontitis.Elderly people and men showed higher severity of periodontal disease.Our data showed a high prevalence of periodontal disease (50% for stages 1 and 2 and 41% for stages 3 and 4) similar to other studies with populations that never received periodontal treatment 11 and with patients with cardiovascular diseases 6,11 .However, the prevalence of severe periodontal disease in the general population is lower (8 to 11%) 7,8 .
In our investigation, we confirmed results found in other studies in the literature that point to age, systemic condition, family income, and education level as possible factors associated with a higher prevalence of periodontal disease 4,7,8,18 .The dental loss found in our investigation was 33%, higher in the elderly group (45%).Other studies confirm this finding, indicating that the elderly are at increased risk of dental loss 5,11 , and factors such as hypertension also increase the risk of dental loss 10 .
Our findings showed that older adults had lower values for the domains "Physical functioning" and "Role-physical" in the SF-36 questionnaire.Other studies have shown that age can be a factor that influences quality of life, as well as chronic systemic diseases 4,6,21 .Considering individuals with different degrees of severity of periodontal disease, we observed differences in the "Pain" domain (SF-36), with patients with gingivitis/periodontal health having the worst results.We also observed that people diagnosed with gingivitis/periodontal health had a higher rate of tooth loss (52%).This result suggests that these patients had already lost their teeth under less favorable conditions, which could be responsible for the worse results in the "Pain" domain.
In stages 3 and 4 of periodontal disease, there is loss of attachment (≥5mm), dental mobility, and tooth loss, which can lead to masticatory dysfunction 9 , and negatively impact quality of life 6,12,14,16,20,21 .However, our results showed that the severity of periodontal disease did not influence most quality-of-life domains as measured by the instruments used.These findings were different from those of the literature, as our study included patients with circulatory system diseases who were under periodic control.Another aspect that may have been responsible for the differences between the results is the various methods used to classify periodontal diseases observed in other studies 6,14,16,20,21 .
The values obtained for the OHIP-14 domains were low, indicating that periodontal conditions had little influence on the quality of life of patients with circulatory diseases in our sample.The total scores for OHIP-14 for people with health/gingivitis, stage 1 and 2 periodontitis, and stage 3 and 4 periodontitis were 10.7, 6.4, and 7.3, respectively.These results were similar to other studies, where the total scores for OHIP-14 were low 21,24 .However, they differ from other studies that showed that the severity of periodontal disease may influence quality of life 6,14,16,21 .The differences found between our results and other studies may be related to population characteristics, where factors such as systemic conditions, family income, education level, and different methods of classifying periodontal diseases can influence the quality of life 16,24 .The correlation between the severity scores of periodontal diseases and the quality-of-life domains measured by the instruments SF-36 and OHIP-14 was weak, confirming that the severity of periodontal disease had little influence on the quality of life of patients with circulatory diseases under periodic control.Other studies have also shown a weak correlation between periodontal parameters (plaque index, gingival bleeding, probing depth, and periodontal condition) and quality of life indicators 17,19 .
As a limitation of the study, we can point out the variety of cardiovascular disorders (ICD-10) 23 , in our sample, in which we had 18 patients with different circulatory diseases, making the sample heterogeneous.Furthermore, 77% of the volunteers were taking medication to control their systemic condition, which can cause alterations in the oral cavity 25 .The experimental design (crosssectional study) does not allow the analysis of variable behavior over time or the determination of causal interrelationships.Despite the sample size obtained through a confidence interval calculation for a proportion, there was no balanced distribution considering age, gender, and severity of periodontal disease, which may have influenced the results of the statistical tests.
However, we can highlight several positive aspects of the methodology, as we used several clinical parameters to characterize a periodontal disease, and the evaluators were trained and calibrated, which favored the consistency of the data obtained.Although only two instruments were used to assess quality of life, both SF-36 and OHIP-14 are widely used with consistent results 6,12,17,[19][20][21]24 .
Our study provides additional information in the literature that contributes to understanding periodontal conditions and their influence on the quality of life of patients with chronic diseases.On the other hand, our results showed that the severity of periodontal disease interfered with the "Pain" domain.We also found that the domains "Functional Capacity" and "Physical Aspects" were influenced by age.These findings may help facilitate the development of strategies for dental treatment of patients with chronic diseases, aiming to improve their quality of life.

CONCLUSION
Among patients with circulatory system diseases, older adults and men had a higher severity of periodontal disease.
Older adults had a worse quality of life in the domains of functional capacity and physical aspects.There was no correlation between the severity of periodontal disease and indicators of quality of life.

Table 1 .
Characterization of patients with circulatory system diseases

Table 2 .
Periodontal parameters (Mean±SD) in patients with circulatory system diseases according to age and gender

Table 4 .
Correlation between the instruments used to measure quality of life (SF-36), oral health impact on quality of life (OHIP-14), and periodontal disease severity scores