Relationship between apical periodontitis and marginal bone loss at individual level from a general population

Abstract

Aim: To study the relationship between the presence of apical periodontitis in root-filled teeth and marginal bone loss (MBL) in individual subjects from a general population. Materials and methods: The study was conducted on a sample of 1,152 dentate individuals (participants in an epdemiological investigation) who were subjected to clinical and radiographic investigations. The presence of root fillings and apical periodontitis were registered. MBL was measured mesially and distally at all roots. The MBL index of the subject was defined as the mean MBL value at all measurable points in the same individual. Multiple regression analysis was adopted to calculate the influence of the presence of apical periodontitis and potential confounders on the dependent variable, MBL index. Results: There was a significant correlation between MBL and the percentage of root-filled teeth and the percentage of root-filled teeth with apical periodontitis. The results of the multiple regression analysis showed that the relative frequency of root-filled teeth with apical periodontitis was significantly higher in subjects with more MBL, irrespective of age, number of remaining teeth, relative frequency of root-filled teeth and smoking habits. Conclusions: A significant association between the presence of apical and marginal periodontitis in individual subjects was found. The mechanisms behind the associations between these diseases are unknown and this cross-sectional observational study did not permit distinction between cause and effect. It is hoped that future cohort studies may provide more knowledge about the biological actions behind the relationship between apical and marginal disease.

INTRODUCTION

Marginal periodontitis is an infectious disease caused by bacteria in the dental plaque. The disease is initiated by a microbial biofilm-induced host response, which results in bone and soft-tissue destruction. The tendency to develop the disease varies and is dependent on background factors, such as genetic predisposition, and risk factors, such as smoking and diabetes. The prevalence of advanced periodontal disease has been found to be 6–7% in Scandinavia and the percentage of the population in this group does not seem to have changed over the last 30 years; in contrast, a trend for a decreasing number of individuals with mild or moderate periodontitis has been observed (for review, see Hugoson and Norderyd¹).

Apical periodontitis is a chronic inflammatory disease caused by infection in the pulp canal system (for review, see Nair²). The microbes or their products invade the root canal and may spread into the apical region of the tooth. The host response consists of hyperaemia, vascular congestion and migration of polymorphonuclear leucocytes towards the site of infection. The most common cause of apical periodontitis is the presence of a root filling, particularly if the quality of the root filling is inadequate³. Coronal restorations, primary carious lesions and reduced marginal bone level have been reported as other risk factors of apical periodontitis³. The prevalence of apical periodontitis at the tooth level has been reported to vary between 1.5% and 10%, whilst the prevalence of apical periodontitis in root-filled teeth varies between 16% and 52%⁴.

The association between apical and marginal periodontitis has been investigated in several studies on individual subjects as well as at the tooth level. A positive correlation between the presence of apical periodontitis and marginal periodontitis at the tooth level has been found in periodontitis-prone individuals5., 6. as well as in a general population³. The magnitude of the periodontitis progression rate was enhanced in teeth with a persisting apical periodontitis⁷. Other studies found that endodontic treatment was impaired by marginal bone loss (MBL)⁸ and that the prevalence of apical periodontitis was significantly lower for periodontally treated teeth⁶.

After adjustment for confounders, multivariable analyses have shown that the number of teeth with apical periodontitis is increased in individuals with a reduced marginal bone level3., 9.. A longitudinal study over 6 years demonstrated that the presence of root fillings was the most important risk factor for the development of apical lesions³. In addition, the presence of coronal restorations, primary carious lesions and MBL were found to be associated with the development of apical periodontitis at individual level. In these studies, marginal bone level was divided into strata depending on the magnitude of MBL3., 9.. Plaque and smoking are two of the most important risk factors for marginal periodontitis. However, the potential influence of plaque as a confounder in the relationship between apical and marginal periodontitis in individual subjects has so far not been studied. The aim of the present study was to investigate the relationship between the presence of apical periodontitis in root-filled teeth and MBL at individual level in a general population using MBL as a continuous variable in the analyses, with plaque index and smoking being included as potential confounders in this relationship.

MATERIALS AND METHODS

The study was conducted on subjects in an epidemiological investigation, which was performed in 1970–1971¹⁰. The baseline investigation was approved by the Research Ethics Committee at Karolinska Institutet. The current research was conducted in full accordance with the World Medical Association Declaration of Helsinki. Written informed consent was obtained from all participants involved in the study. A stratified sample of 1,152 dentate individuals, 18–66 years of age, from the population in the County of Stockholm, was subjected to clinical and radiographic investigations as well as to an interview. In the intra-oral, radiographic investigation, 18 radiographs were used per person in fully dentate persons.

The following variables in dentate individuals were extracted from the database (Lavstedt¹⁰):

• •Age
• •Gender
• •Smoking habits
• •Plaque index¹¹
• •Number of remaining teeth
• •Presence of caries
• •Presence of restorations
• •Presence of root fillings
• •The quality of the root filling, which was considered to be adequate if the root filling ended 2 mm or less from the apex and if a hermetic seal of the root canal was seen
• •Presence of apical periodontitis, which was registered if the periodontal space was widened and the lamina dura could not be seen
• •The MBL, which was measured mesially and distally at all (buccal wherever applicable) roots in per cent (10% scale) of the apex–cementoenamel junction distance¹². If the ratio was less than 10%, it was given the variable value of 1, in the 10–20% interval it was given the value of 2, and so forth (Table 1)
• •The MBL index of the subject was defined as the mean of the MBL values at all measurable points in the same individual.

Table 1.

Relative frequency distribution of subjects according to the marginal bone loss (MBL) index

MBL index	Relative frequencydistribution(%)
1.0	8
1.1–2.0	52
2.1–3.0	24
3.1–4.0	13
>4.0	3

The clinical examinations and the radiographic assessments of alveolar bone level were performed by one examiner and the intra-examiner evaluation of radiographic assessments resulted in a reproducibility of 92%¹³. An oral radiologist evaluated the quality of the root fillings and apical conditions, and the Kappa value was found to be 0.83 for intra-observer agreements.

Statistical analysis

Statistical analyses were performed using the statistical package IBM SPSS Statistics 19.0 (IBM Corporation, Armonk, NY, USA). Correlation analyses were performed by calculating the Pearson′s correlation coefficients (r). Differences among the mean values were analysed using the unpaired Student′s t-test. Multiple regression analysis was adopted to calculate the influence of the presence of apical periodontitis and potential confounders on the dependent variable, MBL index. Results were considered statistically significant at P < 0.05.

RESULTS

The distribution according to the MBL index is presented in Table 1. For 60% of the subjects, the MBL index was found to be ≤2.0, while for 16% the MBL index was >3.0. The mean number of remaining teeth of the sample was 24.6 [standard deviation (SD) = 7.86]. The age distribution of the dentate subjects is presented in Table 2 and the range was 18–65 years. Forty-nine per cent of the sample was male. A significant and positive correlation was found between age and MBL (Table 2). The percentage of smokers was 50%.

Table 2.

Age distribution and marginal bone loss (MBL) index for the subjects

Age(years)	n	MBL index
18–20	4	1.1 (0.81)
21–30	286	1.2 (0.20)
31–40	215	1.6 (0.60)
41–50	254	2.0 (0.82)
51–60	321	2.3 (0.90)
61–65	72	2.4 (0.69)

MBL index values are given as mean (standard deviation).

The prevalence of root-filled teeth was found to be 13%. The subjects with an MBL index of 1.0 had 3.1% root-filled teeth, whereas the corresponding value for subjects with an MBL index of >4.0 was 25% (Table 3). More than 75% of the root-filled teeth in individuals with an MBL index of >3.0 had the diagnosis apical periodontitis (Table 3), whilst this condition was registered for 34% of the whole sample of root-filled teeth. MBL was significantly correlated to the percentage of root-filled teeth (r = 0.27, P < 0.01) and to the percentage of root-filled teeth with apical periodontitis (r = 0.20, P < 0.01). Ninety-two per cent of the subjects had ≥20% teeth with caries (Table 3) and the percentage of teeth with restorations was more than 50% within all strata, according to the MBL index (Table 3). The MBL was significantly correlated to the percentage teeth with caries (r = 0.19, P < 0.01) and to the percentage teeth with restorations (r = 0.16, P < 0.01).

Table 3.

Relative frequencies of root-filled teeth, root-filled teeth with apical periodontitis, teeth with caries and teeth with restorations, according to the marginal bone loss (MBL) index

MBL index	Root-filled teeth	Root-filled teeth with apical periodontitis	Teeth with caries	Teeth with restorations
1.0	3.1	21	14	53
1.1–2.0	10	29	20	68
2.1–3.0	18	41	21	72
3.1–4.0	17	80	25	73
>4.0	25	67	37	59

Values are given as per cent.

The relative frequencies of root-filled teeth, root-filled teeth with apical periodontitis, teeth with caries, or teeth with restorations did not differ significantly between smokers and non-smokers (Table 4). The mean percentage of root-filled teeth with apical periodontits was 38% for subjects with a plaque index of <0.5, and the corresponding percentage for those with a plaque index of ≥0.5 was 40% (Table 5). This difference was not statistically significant. However, the plaque index was significantly and positively correlated to the percentages of root-filled teeth and teeth with caries. The quality of the root filling could be evaluated for 60% of the sample. Eighteen per cent of the root-filled teeth with an adequate root filling had the diagnosis apical periodontitis, whilst the corresponding relative frequency for root-filled teeth with an inadequate root filling was 37%. The quality of the root filling was not significantly correlated to the MBL index.

Table 4.

Relative frequencies of root-filled teeth, root-filled teeth with apical periodontitis, teeth with caries and teeth with restorations, according to smoking habits

Smoking habits	Root-filled teeth	Root-filled teeth with apical periodontitis	Teeth with caries	Teeth with restorations
Non-smoker	13	37	19	68
Smoker	13	41	23	69

Values are given as per cent.

Table 5.

Relative frequencies of root-filled teeth, root-filled teeth with apical periodontitis, teeth with caries and teeth with restorations, according to plaque index

Plaque index	Root-filled teeth	Root-filled teeth with apical periodontitis	Teeth with caries	Teeth with restorations
<0.5	11	38	19	66
≥0.5	15	40	22	69

Values are given as per cent.

The results of the multiple regression analysis, using the MBL index as the dependent variable, showed that the relative frequency of root-filled teeth with apical periodontitis was significantly increased for subjects with more MBL, irrespective of age, number of remaining teeth, the relative frequency of root-filled teeth and smoking habits (Table 6). The percentages of teeth with caries or restorations were not significantly correlated to the MBL index or to the plaque index (Table 6).

Table 6.

Results of multiple regression analysis for dentate individuals using the marginal bone loss (MBL) index for teeth without apical periodontitis as the dependent variable (R² = 0.43, n = 1,152)

Variable	B	SE	P
Age (years)	0.03	0.003	<0.001
Smoking (0 = no, 1 = yes)	0.27	0.06	<0.001
Number of teeth	−0.02	0.01	<0.01
Plaque index	0.02	0.14	NS
Number of root-filled teeth/number of teeth	0.92	0.33	<0.01
Number of teeth with apical periodontitis/number of root-filled teeth	0.33	0.07	<0.001
Number of teeth with caries/number of teeth	0.03	0.22	NS
Number of teeth with restorations/number of teeth	−0.05	0.18	NS

NS, not significant; SE, standard error.

DISCUSSION

This investigation was an epidemiological study on 1,152 dentate subjects (18–65 years of age) from the County of Stockholm. Radiographic assessments on the intra-oral radiographs were performed by an oral radiologist using a projection-related measurement technique, which has been adopted in several earlier studies14., 15., 16., 17. and shows high reproducibility of measurements.

The prevalence of root-filled teeth was found to be 13%. In another Swedish epidemiological study, performed by Ödesjö et al. in 1990¹⁸, the frequency of endodontically treated teeth was 8.6%, 24.5% of which had apical radiolucencies compared with 39% in the present study. The investigation by Ödesjö et al.¹⁸ was performed in 1990, 20 years after the data were collected for the present study, and the caries frequency reported was lower compared with that in the present study.

In order to investigate the relationship between the presence of teeth with apical radiolucencies and marginal bone level, potential confounding variables have to be included in the stepwise multiple regression analyses. Smoking is a well-known risk factor of marginal periodontitis, and an earlier study¹⁹, investigating risk indicators for apical periodontitis, found that smoking was significantly associated with the presence of teeth with apical periodontitis. However, the marginal bone level was not registered and was probably a confounder to this relationship. In the present study, the presence of apical periodontitis was not associated with smoking, even without compensating for degree of MBL.

The presence of root fillings of inadequate quality was found to be correlated with the prevalence of apical periodontitis at the tooth level, in concordance with the study of Kirkevang et al.³. However, the quality of root fillings was not correlated with the degree of MBL and consequently was not a confounder in the analyses.

As earlier studies have demonstrated a significant relationship between the presence of an apical radiolucency and MBL at the tooth level3., 4., 5., 6., the mean MBL of teeth without apical periodontitis was used as the dependent variable in regression analyses to eliminate the risk of the influence of these teeth on the studied relationship at individual level. The present study indicates a strong relationship between apical and marginal periodontitis. The correlation is of the same magnitude as age and smoking, which are well-established predictors of marginal periodontitis14., 20., 21., 22., 23.. The results are in agreement with those of two earlier studies3., 9.. In these studies, apical periodontitis was stratified into a dichotomous variable, and marginal bone level was classified into three groups depending on the degree of bone loss, whilst these variables were analysed as continuous variables in the present study.

In the study population, a strong, significant association exists between the percentage of root-filled teeth with apical periodontitis and the degree of MBL. However, a cross-sectional study does not allow conclusions about causality. Advanced MBL may hypothetically be a predictor of an increasing risk to develop apical periodontitis in root-filled teeth. On the other hand, the presence of apical periodontitis may increase an individual’s risk for periodontitis progression. In addition, spread of microorganisms and their products through anatomical pathways in both directions has been discussed (for review, see Sunitha et al.²⁴). Apical foramen, accessory canals and dentinal tubules are possible pathways of communication between the root canal and the periodontal tissues. The accessory canals connect the root canal with the periodontal ligament. The dentinal tubules are possible pathways for microorganisms and their products when the dentinal tubules are exposed to the oral environment²⁴. An earlier study on caries-free teeth affected with advanced periodontitis found micro-organisms common to the root canal and the periodontal pocket, suggesting that the periodontal pocket may be a possible source of root-canal infections²⁵. In addition, a root-canal infection may serve as a reservoir of microorganisms and maintain apical inflammation as well as marginal destruction.

Consequently, the significant relationship between apical and marginal periodontitis at individual level might be explained by tooth-related factors, such as the spread of infectious products through patent pathways between the root canal and the periodontal ligament. Common host-related factors that increase the incidence of both oral diseases might be another model to explain the association between apical and marginal breakdown of periodontal tissue. There is great similarity between apical and marginal periodontitis concerning the inflammatory response and aetiology²⁶, as well as similarities in the microflora²⁷. Genetics is a significant factor for the host inflammatory response²⁸. Associations have been demonstrated between marginal periodontitis and other inflammatory diseases, such as rheumatoid arthritis (for review, see Barthold et al.²⁹) and cardiovascular disease (for review, see Jeftha and Holmes³⁰). The mechanisms behind the associations between these diseases are unknown. However, there is increasing evidence that these conditions manifest as a result of an imbalance between pro-inflammatory and anti-inflammatory cytokines²⁹. An association between periodontal disease and Alzheimer′s disease has been suggested owing to similar polymorphisms in the two genes for interleukin-1 being correlated to chronic inflammatory diseases³¹. Thus, associations between systemic diseases and marginal periodontitis have been found (for review, see Li et al.³²). Consequently, as apical periodontitis and marginal periodontitis have more characteristics in common compared with the similarities between oral inflammatory diseases and inflammatory systemic diseases, it is tempting to suggest that the individual inflammatory host response explains the association between apical and marginal periodontitis.

Finally, the association between the percentage of root-filled teeth with apical periodontitis and the degree of MBL may be explained by unknown confounders defined as variables significantly correlated with the presence of apical periodontitis and marginal periodontitis. A multivariable analysis has been performed by using potential known confounders, such as the presence of restorations, age, plaque and smoking, in order to eliminate the risk of confounding effects from these variables. However, the risk of uncontrolled confounding may be difficult to exclude in observational studies.

In conclusion, the present investigation has demonstrated a strong, significant association between the presence of apical and marginal periodontitis at individual level. The presence of plaque did not have a significant influence on this relationship. The mechanisms behind the associations between these diseases are unknown and a cross-sectional observational study does not permit distinction between cause and effect. It is hoped that future cohort studies may provide more knowledge on the biological actions behind the relationship between apical and marginal disease.

Acknowledgements

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest

None declared.