Abstract
Objectives
This investigation, based on a 3-year epidemiological surveillance open cohort study, aimed to provide an insight of the prevalence of periodontitis, dental caries and peri-implant pathology and to compare inferentially between healthy and systemic compromised patients.
Methods
A total of 22009 patients were observed consisting in 9035 men (41.1%) and 12974 women (58.9%) with an average age of 48.5 years (standard deviation of 15.6 years). The prevalence of the 3 chronical oral diseases was calculated. The comparison between healthy and systemic compromised patients for each oral disease was performed through multivariate logistic regression: Odds ratios (OR) with 95% confidence intervals (95%CI) were estimated in one general model and one systemic condition specific model adjusted for age and gender. Attributable fractions were estimated for systemic conditions (both models). The level of significance was set at 5%.
Results
The prevalence rate of periodontitis, dental caries and peri-implant pathology was 17.6%, 36.6% and 13.9%, respectively. The systemic compromised status was associated with the prevalence of the three chronical oral diseases on the general models. The systemic condition specific models yielded Diabetes [OR = 1.49, 95%CI (1.24;1.79)] and HIV+ [OR = 4.37, 95%CI (1.05;18.24)] as risk indicators for Periodontitis; cardiovascular conditions [OR = 1.10, 95%CI (1.01;1.20)], Diabetes [OR = 1.24, 95%CI (1.05;1.46)] and neurologic conditions [OR = 1.84, 95%CI (1.32;2.57)] as risk indicators for dental caries; and smoking habits as a risk indicator for all three oral diseases [OR = 1.90, 95%CI (1.74;2.07) for Periodontitis; OR = 1.18, 95%CI (1.09;1.27) for dental caries; OR = 1.84, 95%CI (1.64;2.07) for peri-implant pathology]. Attributable fractions estimated a potential reduction of 12.2% of Periodontitis, and 4.3% of dental caries cases if the exposure to systemic conditions was prevented; while the prevention of exposure to smoking alone would result in a potential reduction of 37%, 7%, and 39% of Periodontitis, dental caries, and peri-implant pathology cases, respectively.
Clinical significance
The present study describes an epidemiological approach to the distribution and determinants of the three principal chronical oral diseases. The association of systemic conditions and smoking habits with oral disease prevalence highlight the importance of a narrow monitoring system.
Conclusions
The present study reported a high prevalence for oral disease and a potential association of a systemic compromised status and smoking habits with the three chronical oral diseases.
1
Introduction
Oral diseases represent a public health problem that has assumed increasing importance in the social consciousness. This is due, in addition to the decreased quality of life due to loss of dental pieces , to growing evidence of the potential effect in terms of overall health, with the exposure to periodontitis as the most significant : this particular disease, has been recognized for its potential participation and influence on the general health processes, a feedback mechanism proposed for instance in the relationship between periodontitis and uncontrolled diabetes with both diseases feeding on each other deregulation . A recent systematic review highlighted this fact, pointing to necessity of adopting measures in the dental environment at the level of smoking cessation, reducing the consumption of sugar, and weight control in patients at risk for a disease or combination of the following diseases: periodontal disease, tooth decay, diabetes, cardiovascular disease and some cancers . A recent cohort study registered a synergistic effect between periodontal disease and tobacco use in the increased risk of lung cancer, to an extent beyond the sum of the independent effects . A recent review of the literature pointed periodontal disease and tobacco consumption as risk indicators for the development of rheumatoid arthritis , while another literature review suggested a link between periodontal disease and coronary heart disease with chronical kidney disease .
Nevertheless, the confirmation of the causal relation between systemic conditions and chronical oral diseases warrants more research beyond biologically plausible mechanisms that despite abundant , fail to demonstrate this causality as in the relation between Diabetes and Periodontitis for example. Given the complexity of oral and systemic chronical diseases, there is still a limitation on the ability to identify specific environmental causes and host susceptibility to adverse health outcomes, especially if they are dependent on multiple factors, if occurring after a long exposure time or if they correspond to subtle disturbances and sub-clinical stages of disease. In order to overcome this problem, epidemiological surveillance is assumed as current public health practice, highlighting the attention to the hazards, sources and corresponding routes of exposure and the health outcomes .
The aim of this study was to provide an insight of the prevalence for periodontitis, caries and peri-implant pathology and to compare their prevalence inferentially between healthy and systemic compromised patients using an epidemiological surveillance system established on a private oral rehabilitation group.
2
Materials and methods
This prospective open-cohort study was conducted in four clinical centers (Lisbon, Porto, Coimbra and Portimão; Portugal) with an increased demand for implant-supported fixed prosthetic rehabilitations. This study was approved by an independent ethical committee (Ethical Committee for Health, authorization no. 005/2012). The study population consisted of patients over 18 years of both genders. The study population, with an estimated higher social-economic status average was not representative of the Portuguese population.
Inclusion criteria were patients who had natural teeth or dental implants, followed at the four centers. Exclusion criteria were patients with less than 18 years of age and patients without natural teeth or dental implants, and patients with removable dentures.
Examinations were performed by 22 trained/calibrated clinicians. Reliability assessment of dental examinations was conducted with 30 patients for each pathology (periodontitis, caries and peri-implant pathology) annually. The overall inter-examiner reliability was estimated using a weighted average of the pairwise inter-examiner reliability estimates. Inter-examiner reliability results for weighted kappa scores during the three years of follow-up were 0.84, 0.83 and 0.84 for periodontitis; 0.88, 0.89 and 0.87 for caries; and 0.85, 0.84 and 0.83 for peri-implant pathology.
The epidemiologic surveillance study was performed with inclusion and follow-up of patients between July 1, 2012 and December 31, 2015. A total of 22009 patients were observed during the follow-up of the study, with each patient having varying lengths of follow-up and varying number of clinic visits.
In each clinical appointment, a digital form was filled and submitted to a database (Google forms; Google Inc., Mountain View, California, USA). The information filled consisted in the date of observation, clinicians’ identification and the patients’ information. The independent variables were: code, age (in years), gender, systemic problems (presence and identification or absence). This information was collected through an anamnesis questionnaire with collection of the patients’ medications or treatments that was updated on each clinical appointment as per protocol.
The dependent variables were: periodontitis (presence or absence), caries (presence or absence), peri-implant pathology (presence or absence), gingivitis (presence or absence), and mucositis (presence or absence) according to the following definitions:
Periodontitis was defined as inflammation of the gingiva and the adjacent attachment apparatus with loss of clinical attachment and loss of adjacent supporting bone according to the American Academy of Periodontology . Caries was defined as cavitated dentin carious lesions or the presence of a new restoration, according to WHO criteria ; Peri-implant pathology was defined as the presence of peri-implant pockets >/ = 5 mm, vertical bone loss and loss of attachment >/ = 2 mm in implants with at least one year of follow-up. Gingivitis was defined as inflammation of the gingiva in the absence of clinical attachment loss . Mucositis was defined as inflammation of the mucosa surrounding the dental implant without signs of vertical bone or attachment loss .
2.1
Statistical analysis
Descriptive and inferential analysis of the data was performed. The prevalence of each chronical or acute condition (dependent variables) was calculated; The prevalence of compromising conditions from the point of view of overall health was calculated, namely: hepatitis, cardiovascular conditions, thyroid conditions, diabetes, rheumatologic condition (Rheumatoid Arthritis, Arthrosis, fibromyalgia, osteoporosis), Oncologic condition, inflammatory condition (Crohn’s disease, multiple sclerosis), neurological disorders (Parkinson’s disease, Alzheimer’s disease, sclerosis, epilepsy), autoimmune conditions (lupus), HIV, renal conditions, genetic conditions (trisomy 21), syndromes (Sjogren syndrome, Ménière syndrome), and smoking habits (present or absent). The list of conditions was decided based on the probable influence of oral disease. Respiratory conditions were not accounted given the reported influence of cariogenic or periodontal pathogens on respiratory disease and not the opposite . The association between the systemic status and the prevalence of each oral disease was estimated through multivariate conditional regression models. For each oral disease, two models were estimated: one general model with the variables age (</ = 48 years, > 48 years), gender and systemic status (healthy, one systemic condition, more than one systemic condition) as potential predictors; and another model disease specific with age, gender, hepatitis, cardiovascular conditions, thyroid conditions, diabetes, rheumatologic conditions, HIV+, oncologic conditions, inflammatory conditions, neurologic conditions, autoimmune conditions, renal conditions, genetic conditions, syndromes and smoking habits as potential predictors. The introduction of the variables was performed at once (without stepwise). Crude and adjusted odds ratios (OR) with corresponding 95% confidence intervals (95% CI) were estimated in both models for each oral disease . Sensitivity analysis was performed in order to investigate the influence of the “length of follow-up” on the results, yielding no significant changes in the correlation matrix, or the risk indicators in direction and magnitude for any of the three chronical oral diseases after adjusting for “length of follow-up”. Model fit was assessed through the Hosmer and Lemeshow test. The level of significance was set at 5%.
Attributable fractions (AF) represent an impact measure of effect to illustrate the percentage of cases potentially prevented if the exposure to the risk factor was suppressed . The AF’s are based on the assumptions that there are no bias and that the removal of exposure to a risk factor would not affect other competitor factors. The AF’s of the cases exposed to risk indicators were estimated through the following equation according to the odds ratio of exposure: AF = (A1+/M1 + )(OR-1/OR), where A1 + =number of disease among exposed patients; M1 + = number of diseased; OR = odds ratio .
2
Materials and methods
This prospective open-cohort study was conducted in four clinical centers (Lisbon, Porto, Coimbra and Portimão; Portugal) with an increased demand for implant-supported fixed prosthetic rehabilitations. This study was approved by an independent ethical committee (Ethical Committee for Health, authorization no. 005/2012). The study population consisted of patients over 18 years of both genders. The study population, with an estimated higher social-economic status average was not representative of the Portuguese population.
Inclusion criteria were patients who had natural teeth or dental implants, followed at the four centers. Exclusion criteria were patients with less than 18 years of age and patients without natural teeth or dental implants, and patients with removable dentures.
Examinations were performed by 22 trained/calibrated clinicians. Reliability assessment of dental examinations was conducted with 30 patients for each pathology (periodontitis, caries and peri-implant pathology) annually. The overall inter-examiner reliability was estimated using a weighted average of the pairwise inter-examiner reliability estimates. Inter-examiner reliability results for weighted kappa scores during the three years of follow-up were 0.84, 0.83 and 0.84 for periodontitis; 0.88, 0.89 and 0.87 for caries; and 0.85, 0.84 and 0.83 for peri-implant pathology.
The epidemiologic surveillance study was performed with inclusion and follow-up of patients between July 1, 2012 and December 31, 2015. A total of 22009 patients were observed during the follow-up of the study, with each patient having varying lengths of follow-up and varying number of clinic visits.
In each clinical appointment, a digital form was filled and submitted to a database (Google forms; Google Inc., Mountain View, California, USA). The information filled consisted in the date of observation, clinicians’ identification and the patients’ information. The independent variables were: code, age (in years), gender, systemic problems (presence and identification or absence). This information was collected through an anamnesis questionnaire with collection of the patients’ medications or treatments that was updated on each clinical appointment as per protocol.
The dependent variables were: periodontitis (presence or absence), caries (presence or absence), peri-implant pathology (presence or absence), gingivitis (presence or absence), and mucositis (presence or absence) according to the following definitions:
Periodontitis was defined as inflammation of the gingiva and the adjacent attachment apparatus with loss of clinical attachment and loss of adjacent supporting bone according to the American Academy of Periodontology . Caries was defined as cavitated dentin carious lesions or the presence of a new restoration, according to WHO criteria ; Peri-implant pathology was defined as the presence of peri-implant pockets >/ = 5 mm, vertical bone loss and loss of attachment >/ = 2 mm in implants with at least one year of follow-up. Gingivitis was defined as inflammation of the gingiva in the absence of clinical attachment loss . Mucositis was defined as inflammation of the mucosa surrounding the dental implant without signs of vertical bone or attachment loss .
2.1
Statistical analysis
Descriptive and inferential analysis of the data was performed. The prevalence of each chronical or acute condition (dependent variables) was calculated; The prevalence of compromising conditions from the point of view of overall health was calculated, namely: hepatitis, cardiovascular conditions, thyroid conditions, diabetes, rheumatologic condition (Rheumatoid Arthritis, Arthrosis, fibromyalgia, osteoporosis), Oncologic condition, inflammatory condition (Crohn’s disease, multiple sclerosis), neurological disorders (Parkinson’s disease, Alzheimer’s disease, sclerosis, epilepsy), autoimmune conditions (lupus), HIV, renal conditions, genetic conditions (trisomy 21), syndromes (Sjogren syndrome, Ménière syndrome), and smoking habits (present or absent). The list of conditions was decided based on the probable influence of oral disease. Respiratory conditions were not accounted given the reported influence of cariogenic or periodontal pathogens on respiratory disease and not the opposite . The association between the systemic status and the prevalence of each oral disease was estimated through multivariate conditional regression models. For each oral disease, two models were estimated: one general model with the variables age (</ = 48 years, > 48 years), gender and systemic status (healthy, one systemic condition, more than one systemic condition) as potential predictors; and another model disease specific with age, gender, hepatitis, cardiovascular conditions, thyroid conditions, diabetes, rheumatologic conditions, HIV+, oncologic conditions, inflammatory conditions, neurologic conditions, autoimmune conditions, renal conditions, genetic conditions, syndromes and smoking habits as potential predictors. The introduction of the variables was performed at once (without stepwise). Crude and adjusted odds ratios (OR) with corresponding 95% confidence intervals (95% CI) were estimated in both models for each oral disease . Sensitivity analysis was performed in order to investigate the influence of the “length of follow-up” on the results, yielding no significant changes in the correlation matrix, or the risk indicators in direction and magnitude for any of the three chronical oral diseases after adjusting for “length of follow-up”. Model fit was assessed through the Hosmer and Lemeshow test. The level of significance was set at 5%.
Attributable fractions (AF) represent an impact measure of effect to illustrate the percentage of cases potentially prevented if the exposure to the risk factor was suppressed . The AF’s are based on the assumptions that there are no bias and that the removal of exposure to a risk factor would not affect other competitor factors. The AF’s of the cases exposed to risk indicators were estimated through the following equation according to the odds ratio of exposure: AF = (A1+/M1 + )(OR-1/OR), where A1 + =number of disease among exposed patients; M1 + = number of diseased; OR = odds ratio .
3
Results
A total of 22009 patients were observed during the follow-up period between July 2012 and July 2015 (average: 24 months; standard deviation: 11 months; median: 25 months), consisting in 9035 men (41.1%) and 12974 women (58.9%) with an average age of 48.5 years (standard deviation of 15.6 years). The total number of patients with natural teeth accounted for 90.3% (n = 19868), whereas all patients with implants represented 53.9% (n = 11863) ( Table 1 ).
| Total patients (%) | Male patients (%) | Female patients (%) | |
|---|---|---|---|
| Demographics | |||
| Number of patients | 22009 (100%) | 9035 (100%) | 12974 (100%) |
| Average age (standard deviation) | 48.5 (15.6) | 48.0 (15.9) | 48.9 (15.4) |
| Presence of natural teeth | 19868 (90.3%) | 8282 (91.7%) | 11586 (89.3%) |
| Presence of dental implants | 11863 (53.9%) | 4478 (49.6%) | 7385 (56.9%) |
| Oral status | |||
| Presence of Gingivitis | 10663 (48.5%) | 4592 (55.5%) | 6071 (52.4%) |
| Presence of Mucositis | 6594 (55.6%) | 2455 (54.8%) | 4139 (56.1%) |
| Presence of Periodontitis | 3497 (17.6%) | 1717 (20.7%) | 1780 (15.4%) |
| Presence of Caries | 7263 (36.6%) | 3118 (37.7%) | 4145 (35.8%) |
| Presence of Peri-implant pathology | 1652 (13.9%) | 638 (14.2%) | 1014 (13.7%) |
| Systemic status | |||
| Healthy patients | 12821 (58.2%) | 5229 (57.9%) | 7592 (58.5%) |
| Patients with Systemic conditions | 9188 (41.8%) | 3806 (42.1%) | 5382 (41.5%) |
| Hepatitis | 171 (0.8%) | 92 (1.0%) | 79 (0.6%) |
| Cardiovascular conditions | 3776 (17.2%) | 1606 (17.8%) | 2170 (16.7%) |
| Thyroid conditions | 758 (3.4%) | 60 (0.7%) | 698 (5.4%) |
| Diabetes | 781 (3.6%) | 425 (4.7%) | 356 (2.7%) |
| Rheumatologic conditions | 852 (3.9%) | 64 (0.7%) | 788 (6.1%) |
| HIV + | 31 (0.1%) | 25 (0.3%) | 6 (0.004%) |
| Oncologic conditions | 429 (2.0%) | 113 (1.3%) | 316 (2.4%) |
| Inflammatory conditions | 81 (0.4%) | 24 (0.3%) | 57 (0.4%) |
| Neurologic conditions | 175 (0.8%) | 68 (0.8%) | 107 (0.8%) |
| Autoimmune conditions | 66 (0.3%) | 10 (0.1%) | 56 (84.8%) |
| Renal conditions | 25 (0.1%) | 14 (0.2%) | 11 (0.008%) |
| Genetic conditions | 12 (0.05%) | 4 (0.004%) | 8 (0.006%) |
| Syndromes | 15 (0.05%) | 1 (0.0005%) | 14 (0.01%) |
| More than one systemic condition | 1923 (8.7%) | 677 (7.5%) | 1246 (9.6%) |
| Smoking habits | 4387 (19.9%) | 2101 (23.3%) | 2286 (17.6%) |
Considering the acute conditions, the prevalence of gingivitis was 53.7% (n = 10663); whereas for mucositis, a prevalence of 55.6% (n = 6594) was calculated. About 14462 patients (65.6%) had at least one acute oral condition.
Overall, a total of 5057 patients (23%) were free from any acute or chronical condition.
The number of patients with at least one chronic oral disease corresponded to 10223 (46.5%), and 11776 patients (53.5%) were found free from chronic oral disease.
The total number of patients diagnosed with periodontitis was 3497, corresponding to a prevalence rate of 17.6%. Periodontitis occurred in 1840/7861 patients with systemic problems (23.4%) and 1657/12007 patients without systemic conditions (13.8%) ( Table 2 ). Concerning the multivariate regression analysis for periodontitis, the overall model disclosed, age > 48 years [OR = 2.64, 95% CI (2.44;2.87)], male gender [OR = 1.46, 95% CI (1.36;1.58)], presence of one systemic condition [OR = 1.25, 95% CI (1.14;1.37)] and smoking [OR = 1.90, 95% CI (1.74;2.07)] as risk indicators; while on the systemic status specific model, age > 48 years [OR = 2.67, 95% CI (2.46;2.91)], male gender [OR = 1.44, 95% CI (1.33;1.56)], diabetes [OR = 1.49, 95% CI (1.24;1.79)], HIV+ [OR = 4.37, 95% CI (1.05;18.24)] and smoking habits [OR = 1.90, 95% CI (1.74;2.07)] were disclosed as risk indicators ( Table 3 ). The presence of one systemic condition yielded an attributable fraction of 12.2%, while smoking habits, Diabetes and HIV+ attributable fractions were 37%, 5% and 1.2%, respectively ( Table 3 ).
| Periodontitis Prevalence | Caries prevalence | Peri-implant pathology prevalence | |
|---|---|---|---|
| Global sample | 3497/19868 = 17.6% | 7263/19868 = 36.6% | 1652/11863 = 13.9% |
| Healthy | 1657/12007 = 13.8% | 4255/12007 = 35.4% | 729/5875 = 12.4% |
| Systemic condition | 1840/7861 = 23.4% | 3008/7861 = 38.3% | 921/5988 = 15.3% |
| Hepatitis | 32/144 = 22% | 49/144 = 34% | 16/106 = 15.1% |
| Cardiovascular | 747/3061 = 24.4% | 1125/3061 = 36.8% | 394/2845 = 13.9% |
| Thyroid | 134/630 = 21.3% | 241/630 = 38.3% | 71/566 = 12.5% |
| Diabetes | 195/624 = 31.2% | 251/624 = 40.2% | 92/583 = 15.8% |
| Rheumatologic | 144/698 = 20.6% | 230/698 = 33% | 103/693 = 14.9% |
| HIV | 11/21 = 52.4% | 11/21 = 52.4% | 6/27 = 22.2% |
| Oncological | 77/343 = 22.4% | 130/343 = 37.9% | 46/321 = 14.3% |
| Inflammatory | 10/74 = 13.5% | 26/74 = 35.1% | 9/46 = 19.6% |
| Neurologic | 30/140 = 21.4% | 71/140 = 50.7% | 15/120 = 12.5% |
| Autoimmune | 8/58 = 13.8% | 20/58 = 34.5% | 4/43 = 9.3% |
| Renal | 2/21 = 9.5% | 8/21 = 38.1% | 1/17 = 5.9% |
| Genetic | 3/11 = 27.3% | 5/11 = 45.5% | 2/7 = 28.6% |
| Syndrome | 2/14 = 14.3% | 8/14 = 57.1% | 2/12 = 16.6% |
| More than one systemic condition | 398/1526 = 26.1% | 592/1526 = 38.8% | 259/1532 = 16.9% |
| Smoking habits | 951/3872 = 24.6% | 1548/3872 = 40% | 498/2536 = 19.6% |
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