Correlation between the state of periodontal tissues and selected risk factors for periodontitis and myocardial infarction

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Introduction
The current level of knowledge indicates a relationship between periodontal disease and systemic diseases, including diabetes, cardiovascular diseases, stroke, premature birth and low birth weight, as well as Parkinson's disease, Alzheimer's disease and pancreatic cancer.Periodontitis can constitute not only a risk factor for these diseases, but also a condition modifying other primary risk factors associated with the occurrence of cardiovascular complications (lipid disorders, arterial hypertension, etc.) or diabetes. 1,2ardiovascular diseases are the main cause of premature death in most European countries.This situation is closely associated with lifestyle and the influence of risk factors on the occurrence and course of cardiovascular diseases.
Risk factors beyond our control include age, gender, genetic load.Those on which we have an influence include cigarette smoking, arterial hypertension, lipid disorders, diabetes and obesity, bad eating habits, stress.
The results of studies in recent years also suggest that in the future periodontal disease may be considered one of the many risk factors for cardiovascular diseases. 3esearch has shown that the same risk factors as well as the same pathophysiological processes are the underlying cause for the destabilization of atherosclerotic plaques and the destruction of periodontal tissues.Particular attention should be paid to the interactions that could potentially occur between periodontal diseases and other risk factors, i.e. the concentration of lipoproteins LDH and HDL, or arterial hypertension, due to their joint participation in the induction of oxidative stress in the circulatory system. 2,4xidative stress, generally coexisting with pathogens associated with periodontal disease, which are often detected in atherosclerotic plaque, accelerates apoptosis, and increases inflammation.This process can initiate the erosion of atherosclerotic plaque and raise its vulnerability to rupture, which is a high risk of thrombosis and acute coronary events. 5,6he prevalence of periodontal disease in our civilization and the positive results of periodontal therapy necessitate a deeper examination of the pathogenetic mechanisms linking periodontitis with atherosclerosis and consequently with the resulting cardiovascular diseases. 7,8herefore, the objective of this study was to assess the state of periodontal tissues and to analyze the correlation between the state of periodontal tissues and selected risk factors for myocardial infarction in patients after acute myocardial infarction.

Material and methods
The study was conducted in the Department of Periodontology and in the Clinic and Department of Cardiology of five medical universities in Poland (Warszawa, Szczecin, Wrocław, Lublin, Białystok) in 2010-2014.
The study included 417 patients hospitalized with recent acute myocardial infarction (MI).The inclusion criteria were MI history and age below 70 years.The patients agreed to participate in the study by signing a declaration approved by the Bioethics Committee in Medical University of Warszawa (opinion: KB-145/2011).Patients diagnosed with cancer, rheumatic disease, autoimmune disease, chronic liver disease, chronic renal disease stages 4 and 5, stroke history and individuals receiving periodontal treatment or systemic antibiotic therapy in the preceding 6 months were excluded from the study.

Social enquiry and general medical history
All participants of the study were interviewed, which included a collection of the following data: • General patient data: first name, family name, gender, date of birth, phone number, place of residence; • Education, defined as primary, secondary and higher education; • Socio-economic status, determined on the basis of income per family member per month: < 800 PLN, 800--1500 PLN, > 1500 PLN; • Cigarette smoking, defined as: current (smoking of 10 or more cigarettes a day continuously for at least 5 years), smoking in the past and never; • Identification of risk factors for cardiovascular disease: arterial hypertension, diabetes, as well as BMI and WHR.

Physical examination
Physical measurements were performed in accordance with applicable guidelines.All the study participants were evaluated for: • Weight [kg], height [cm], waist circumference [cm] and hip circumference [cm], which allowed for the calculation of each patient's body mass index (BMI was calculated by dividing the body weight [kg] by the square of the body height [m 2 ]) and WHR (WHR was calculated by dividing the waist circumference by the hip circumference).BMI 25-29.9kg/m 2 was defined as overweight, and BMI ≥ 30 kg/m 2 was defined as obesity.Abdominal obesity was diagnosed when waist circumference (WC) was ≥ 80 cm in women and ≥ 94 cm in men.
• Blood pressure, which was measured in a sitting position after several minutes' rest, using a sphygmomanometer.Arterial hypertension was defined as systolic blood pressure ≥ 140 mm Hg or diastolic blood pressure ≥ 90 0mm Hg or use of antihypertensive drugs.

Dental and periodontal examination
The dental examination took place within 6 weeks after the myocardial infarction.This examination was carried out in an artificial light, using a dental mirror and a peri-odontal probe (Hu-Friedy PCPUNC 15).The number of teeth, the number of roots with pulp necrosis present in the mouth and edentulousness rate were determined.The examination did not include third molars.The periodontal examination covered: • Dichotomous Plaque Index (PI) by O'Leary 9 on 4 surfaces of the tooth (mesial, distal, lingual and buccal); the presence or absence of plaque was determined; • Bleeding on Probing (BoP) index by Ainamo and Bay 10 where the examination was conducted at 4 sites around the tooth: mesial buccal (MB), buccal (B), distal buccal (DB) and lingual (L), only the presence or absence of bleeding from gingiva while probing the pocket was determined; • Pocket depth (PD) at 4 sites around the tooth: MB, B, DB, L, which was defined as the distance from the gingival margin to the bottom of the pocket determined by the probe; • The number of active (bleeding) pockets above 4 mm in depth; • Clinical attachment loss (CAL) at 4 sites around the tooth: MB, B, DB, L, which is defined as the distance between the bottom of the pocket determined by the probe and the cemento-enamel junction.
The periodontal status of each patient was determined on the basis of the CPI index definition 11 , with the following categories: • CPI-0 -no inflammatory symptoms, • CPI-1 -presence of bleeding on probing, • CPI-2 -presence of supra-and/or subgingival calculus or filling overhangs, • CPI-3 -presence of pathological periodontal pockets from 3.5 to 5.5 mm deep, • CPI-4 -the presence of pathological periodontal pockets 5.5 mm and deeper.

Statistical analysis
Statistical analysis was performed using PQStat v. 1.4.4 software.The Mann-Whitney and Kruskal-Wallis tests were used to assess the significance of differences between 2 and more groups.The χ 2 test was used to search significant differences between the frequencies of the analyzed data.Correlation between variables were measured by the Spearman rank correlation.P-value lower than 0.05 was decided as significant differences.

Characteristics of the study group
The age of patients ranged from 25 to 69 years, with the median at 57 years, and with significantly more men than women (77.9% vs 22.1%).
Most of the patients came from large cities (223 individuals, 56.9%), the least -69 patients (17.6%) -lived in the country outside urban areas.
Within the study group the largest subgroup were individuals with a secondary education 53.9%, the least numerous -with incomplete university education or full university education (15.7%).
Analyzing the income per family member it was observed that more than half had an income ranging from 800 to 1500 PLN per family member (Table 1).
The results of the periodontal examination showed an average of 12 preserved teeth in women and 18 in men (total median: 16 preserved teeth).Mean values of plaque index (PI) were high in both females and males (76.9% and 78.2% respectively).Also the BOP index was high, regardless of gender (44.6%).The number of pockets > 4 mm was significantly higher in men (Table 2).

Characteristic of risk factors and correlations between variables
Analyzing risk factors for heart diseases, overweight (BMI 25-30 kg/m 2 ) or obesity (BMI ≥ 30 kg/m 2 ) were observed in almost 80% of patients.Most of the patients were current or past smokers of tobacco (almost 80%), arterial hypertension was present in 90.1% of individuals in the study group, diabetes in almost 25%, dyslipidemia in more than half of the patients with myocardial infarction (Table 3).

Number of patients 417
Percentage of the study group 100.0%An analysis of the relationship between periodontal status and sociological parameters demonstrated a statistically significant correlation between the number of lost teeth, and age, gender, education and income, a similar association was observed between CPI median and education and income of patients.
An inverse correlation between BOP and PI on one hand and education and income on the other hand was also observed (Table 4).
The conducted study showed a correlation between age, place of residence, education and income on one hand and average pocket depth, number and percentage of pockets above 4 mm and mean CAL on the other one (Table 5).
No correlation was observed between BMI and activity and severity of periodontitis or the state of oral hygiene and CPI median.
The number of lost teeth, BOP and CPI correlated with smoking.The number of lost teeth and the plaque index showed a statistically significant positive correlation with the cumulative effects of tobacco and its combustion products in the form of the number of pack-years (Table 6).
An analysis of the results showed no relationship between the depth, number and percentage of periodontal pockets and the clinical attachment level on one hand and BMI on the other hand, whereas a certain correlation was observed between tobacco smoking on one hand and the average depth of pockets, the number and percentage pockets > 4 mm and the average clinical attachment loss on the other hand.
Own research also shows that a great majority, 97% of individuals with heart attack history, are past or present cigarette smokers.Actually smokers had significantly deeper periodontal pockets and clinical attachment loss.There was significant correlation between CAL and body weight measured only by WHR (Table 7).
The number of teeth in patients with diabetes was significantly lower than among non-diabetic group (Table 8).

Discussion
Age and gender are an important, non-modifiable risk factor for both periodontal disease and cardiovascular disease.Numerous epidemiological studies confirm a higher incidence of periodontitis in the elderly. 12,13tudies conducted by Persson et al. 14 showed that both of these diseases may occur simultaneously, particularly in individuals over 60 years of age.The occurrence of periodontal disease was observed in about 50% of those aged over 60 years, and 55% were overweight or with an episode of stroke or acute coronary syndrome. 14ur study also showed a higher incidence of myocardial infarction, as well as periodontal disease in men.Male predilection for the occurrence of periodontal disease and cardiovascular disease was also observed by other authors. 13,15,16n analysis of modifiable factors, which depend on us, included, among other things, education and the degree of wealth.Our study showed a lower number of individuals with higher education and higher income among patients after myocardial infarction.Zhang et al. 17 demonstrated that education lasting at least 6 years significantly affects the decreased incidence of advanced periodontal disease and impacts the course of treatment and survival of patients after ACS.Individuals with higher education usually have a permanent job, which is associated with a regular income and frequent access to dental care.They also have higher health awareness.
Our results are also confirmed by other authors, indicating that the level of wealth is an important modifiable risk factor for periodontal disease. 13These results can also indicate that individuals with a low income lose their own teeth earlier, due to the limited possibility of receiving treatment.These results also showed a high proportion of toothlessness, which occurred earlier in individuals with a lower income after myocardial infarction. 12,18Studies by Bertoldi et al. 15 indicated that a higher income correlated with a lower number of lost teeth, but also with a better condition of periodontal tissues.People with a lower socio-economic status had fewer teeth, most likely due to the fact that tooth extractions are less expensive and less time consuming, and persons with higher status had more teeth, perhaps because they more often opted for conservative treatment.Analyzing the group of patients after myocardial infarction, it clear that the number of preserved teeth and the condition of periodontal tissues is much worse compared to epidemiological studies on randomly selected Poles of the same age group. 13Indeed, the average number of preserved teeth in the group after myocardial infarction was 12 in women and 18 in men (mean 16).
Studies by Górski et al. 19 showed an average of 24 teeth in the control group of the same age.In the group of patients after myocardial infarction also the percentage of edentulous individuals was high at 16.3% in women and 9.2% in men (mean 10.8%), in the control group examined by the above-mentioned author the number of edentulous patients was 2.5%.
A research by Desvarieux et al. 20 on the relation between the number of teeth and progression of atherosclerosis and risk of myocardial infarction showed plaque in carotid arteries in 46% of individuals who had lost from 0 to 9 teeth and in 60% of individuals who had lost more than 10 teeth.Also studies by Schillinger et al. 21indicated that toothless patients had more advanced atherosclerotic lesions in carotid arteries.
Holmlund et al. 22 reported that individuals with more than 10 teeth demonstrated a 7-fold increase in the risk of mortality from heart attacks compared to persons with more than 25 teeth, as well as more advanced atherosclerotic lesions in carotid arteries in individuals with fewer teeth.

Conclusions
Summing up, it must be said that in the light of modern research the role of risk factors for the occurrence and course of periodontal diseases and cardiovascular diseases is unquestionable, but whether the list of known risk factors for CVD will be supplemented by periodontitis is a matter of time and research.
Our own studies have confirmed that periodontitis and the degree of its severity have an impact on hypertension and diabetes, WHR, which potentially could influence the occurrence of cardiovascular diseases, which could lead to myocardial infarction.

Table 1 .
Characteristics of the study group

Table 2 .
Full-mouth dental and periodontal status

Table 3 .
Values medical risk factors for periodontitis

Table 4 .
Relations between sociodemographic variables and periodontal status (number of teeth, PI, BoP and CPI indices)

Table 5 .
Relations between sociodemographic variables and periodontal status (PD, CAL)