International Dental Journal 2015; 65: 71–76

SCIENTIFIC RESEARCH REPORT

doi: 10.1111/idj.12143

Relationship between apical periodontitis and marginal

bone loss at individual level from a general population
Leif Jansson1,2
1
Departments of Periodontology, Public Dental Service at Kista and Skanstull, Stockholm County Council, Stockholm, Sweden; 2Division of
Periodontology, Department of Dental Medicine, Karolinska Institutet, Huddinge, Sweden.

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 radio-
graphic 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 peri-
odontitis 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 peri-
odontitis was significantly higher in subjects with more MBL, irrespective of age, number of remaining teeth, relative fre-
quency 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.

Key words: Apical periodontitis, bone loss, epidemiology, marginal periodontitis

region of the tooth. The host response consists of

INTRODUCTION
Marginal periodontitis is an infectious disease caused
by bacteria in the dental plaque. The disease is initi-
ated by a microbial biofilm-induced host response,
which results in bone and soft-tissue destruction. The
tendency to develop the disease varies and is depen-
dent on background factors, such as genetic predispo-
sition, 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 per-
centage 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 dis-
ease 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
© 2014 FDI World Dental Federation
hyperaemia, vascular congestion and migration of
polymorphonuclear leucocytes towards the site of
infection. The most common cause of apical periodon-
titis is the presence of a root filling, particularly if the
quality of the root filling is inadequate3. Coronal res-
torations, primary carious lesions and reduced mar-
ginal bone level have been reported as other risk
factors of apical periodontitis3. The prevalence of api-
cal 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 peri-
odontitis 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.
71
Jansson
The magnitude of the periodontitis progression rate
was enhanced in teeth with a persisting apical peri-
odontitis7. Other studies found that endodontic treat-
ment was impaired by marginal bone loss (MBL)8 and
that the prevalence of apical periodontitis was signifi-
cantly 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 pres-
ence of coronal restorations, primary carious lesions
and MBL were found to be associated with the devel-
opment 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 fac-
tors for marginal periodontitis. However, the potential
influence of plaque as a confounder in the relationship
between apical and marginal periodontitis in indivi-
dual 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 epidemio-
logical investigation, which was performed in 1970–
197110. The baseline investigation was approved by
the Research Ethics Committee at Karolinska Institu-
tet. The current research was conducted in full accor-
dance 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 individu-
als, 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 radio-
graphs 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
72
• The quality of the root filling, which was consid-
ered 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 regis-
tered if the periodontal space was widened and the
lamina dura could not be seen
• The MBL, which was measured mesially and dis-
tally at all (buccal wherever applicable) roots in per
cent (10% scale) of the apex–cementoenamel junc-
tion 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.
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 agree-
ments.
Statistical analysis
Statistical analyses were performed using the statisti-
cal package IBM SPSS Statistics 19.0 (IBM Corpora-
tion, Armonk, NY, USA). Correlation analyses were
performed by calculating the Pearson0 s correlation
coefficients (r). Differences among the mean values
were analysed using the unpaired Student0 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 sig-
nificant at P < 0.05.
RESULTS
The distribution according to the MBL index is pre-
sented 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
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
>4.0
13
3
© 2014 FDI World Dental Federation
 Apical periodontitis and marginal bone loss

of the sample was 24.6 [standard deviation (SD) = Table 3 Relative frequencies of root-filled teeth, root-
7.86]. The age distribution of the dentate subjects is filled teeth with apical periodontitis, teeth with caries
presented in Table 2 and the range was 18–65 years. and teeth with restorations, according to the marginal
Forty-nine per cent of the sample was male. A signifi- bone loss (MBL) index
cant and positive correlation was found between age
MBL Root-filled Root-filled Teeth Teeth with
and MBL (Table 2). The percentage of smokers was index teeth teeth with with restorations
50%. apical periodontitis caries
The prevalence of root-filled teeth was found to be 1.0 3.1 21 14 53
13%. The subjects with an MBL index of 1.0 had 1.1–2.0 10 29 20 68
3.1% root-filled teeth, whereas the corresponding 2.1–3.0 18 41 21 72
3.1–4.0 17 80 25 73
value for subjects with an MBL index of >4.0 was >4.0 25 67 37 59
25% (Table 3). More than 75% of the root-filled
teeth in individuals with an MBL index of >3.0 had Values are given as per cent.
the diagnosis apical periodontitis (Table 3), whilst
this condition was registered for 34% of the whole
sample of root-filled teeth. MBL was significantly cor- Table 4 Relative frequencies of root-filled teeth, root-
related to the percentage of root-filled teeth (r = 0.27, filled teeth with apical periodontitis, teeth with caries
P < 0.01) and to the percentage of root-filled teeth and teeth with restorations, according to smoking
with apical periodontitis (r = 0.20, P < 0.01). Ninety- habits
two per cent of the subjects had ≥20% teeth with car- Smoking Root-filled Root-filled Teeth Teeth with
ies (Table 3) and the percentage of teeth with restora- habits teeth teeth with apical with restorations
tions was more than 50% within all strata, according periodontitis caries
to the MBL index (Table 3). The MBL was signifi- Non-smoker 13 37 19 68
cantly correlated to the percentage teeth with caries Smoker 13 41 23 69
(r = 0.19, P < 0.01) and to the percentage teeth with Values are given as per cent.
restorations (r = 0.16, P < 0.01).
The relative frequencies of root-filled teeth, root-
Table 5 Relative frequencies of root-filled teeth, root-
filled teeth with apical periodontitis, teeth with caries,
filled teeth with apical periodontitis, teeth with caries
or teeth with restorations did not differ significantly
and teeth with restorations, according to plaque index
between smokers and non-smokers (Table 4). The
mean percentage of root-filled teeth with apical peri- Plaque Root-filled Root-filled teeth Teeth with Teeth with
odontits was 38% for subjects with a plaque index of index teeth with apical caries restorations
periodontitis
<0.5, and the corresponding percentage for those with
a plaque index of ≥0.5 was 40% (Table 5). This dif- <0.5 11 38 19 66
≥0.5 15 40 22 69
ference was not statistically significant. However, the
plaque index was significantly and positively corre- Values are given as per cent.
lated 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 Table 6 Results of multiple regression analysis for
the diagnosis apical periodontitis, whilst the corre- dentate individuals using the marginal bone loss
sponding relative frequency for root-filled teeth with (MBL) index for teeth without apical periodontitis as
an inadequate root filling was 37%. The quality of the dependent variable (R2 = 0.43, n = 1,152)
the root filling was not significantly correlated to the Variable B SE P
MBL index.
Age (years) 0.03 0.003 <0.001
Smoking (0 = no, 1 = yes) 0.27 0.06 <0.001
Table 2 Age distribution and marginal bone loss Number of teeth 0.02 0.01 <0.01
(MBL) index for the subjects Plaque index 0.02 0.14 NS
Number of root-filled teeth/number 0.92 0.33 <0.01
Age(years) n MBL index of teeth
Number of teeth with apical 0.33 0.07 <0.001
18–20 4 1.1 (0.81) periodontitis/number of root-filled
21–30 286 1.2 (0.20) teeth
31–40 215 1.6 (0.60) Number of teeth with caries/ 0.03 0.22 NS
41–50 254 2.0 (0.82) number of teeth
51–60 321 2.3 (0.90) Number of teeth with restorations/ 0.05 0.18 NS
61–65 72 2.4 (0.69) number of teeth

MBL index values are given as mean (standard deviation). NS, not significant; SE, standard error.

© 2014 FDI World Dental Federation 73

Jansson
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 signifi-
cantly correlated to the MBL index or to the plaque
index (Table 6).
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
studies14–17 and shows high reproducibility of mea-
surements.
The prevalence of root-filled teeth was found to be
13%. In another Swedish epidemiological study, per-
€
formed by Odesj€ o 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 Odesj€ € o and the periodontal tissues. The accessory canals con-
18
et al. 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 mar-
ginal bone level, potential confounding variables have
to be included in the stepwise multiple regression analy-
ses. 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 smok-
ing, even without compensating for degree of MBL.
The presence of root fillings of inadequate quality
was found to be correlated with the prevalence of api-
cal 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 con-
founder in the analyses.
As earlier studies have demonstrated a significant
relationship between the presence of an apical radiolu-
cency and MBL at the tooth level3–6, the mean MBL of
teeth without apical periodontitis was used as the
dependent variable in regression analyses to eliminate
74
the risk of the influence of these teeth on the studied
relationship at individual level. The present study indi-
cates a strong relationship between apical and marginal
periodontitis. The correlation is of the same magnitude
as age and smoking, which are well-established predic-
tors of marginal periodontitis14,20–23. The results are in
agreement with those of two earlier studies3,9. In these
studies, apical periodontitis was stratified into a dichot-
omous 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 associa-
tion exists between the percentage of root-filled teeth
with apical periodontitis and the degree of MBL. How-
ever, a cross-sectional study does not allow conclusions
about causality. Advanced MBL may hypothetically be
a predictor of an increasing risk to develop apical peri-
odontitis in root-filled teeth. On the other hand, the
presence of apical periodontitis may increase an indi-
vidual’s risk for periodontitis progression. In addition,
spread of microorganisms and their products through
anatomical pathways in both directions has been dis-
cussed (for review, see Sunitha et al.24). Apical fora-
men, accessory canals and dentinal tubules are possible
pathways of communication between the root canal
nect the root canal with the periodontal ligament. The
dentinal tubules are possible pathways for microorgan-
isms 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 infec-
tions25. 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 path-
ways between the root canal and the periodontal liga-
ment. 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 simi-
larity between apical and marginal periodontitis con-
cerning 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 mar-
ginal 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
© 2014 FDI World Dental Federation

associations between these diseases are unknown.
However, there is increasing evidence that these condi-
tions manifest as a result of an imbalance between pro-
inflammatory and anti-inflammatory cytokines29. An
association between periodontal disease and Alzhei-
mer0 s disease has been suggested owing to similar poly-
morphisms 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 dis-
eases, 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 con-
founders defined as variables significantly correlated
with the presence of apical periodontitis and marginal
periodontitis. A multivariable analysis has been per-
formed by using potential known confounders, such
as the presence of restorations, age, plaque and smok-
ing, 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 demon-
strated a strong, significant association between the
presence of apical and marginal periodontitis at indi-
vidual level. The presence of plaque did not have a
significant influence on this relationship. The mecha-
nisms 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.
REFERENCES
1. Hugoson A, Norderyd O. Has the prevalence of periodontitis
changed during the last 30 years? J Clin Periodontol 2008 35
(Suppl 8): 338–345.
© 2014 FDI World Dental Federation
Apical periodontitis and marginal bone loss
2. Nair PNR. Pathogenesis of apical periodontitis and the causes of
endodontic failures. Crit Rev Oral Biol Med 2004 15: 348–381.
3. Kirkevang LL, Vaeth M, H€ orsted-Bindslev P et al. A. Risk fac-
tors for developing apical periodontitis in a general population.
Int Endod J 2007 40: 290–299.
4. Kirkevang LL, H€ orsted-Bindslev P, Ørstavik D et al. Frequency
and distribution of endodontically treated teeth and apical peri-
odontitis in an urban Danish population. Int Endod J 2001 34:
198–205.
5. Jansson L, Ehnevid H, Lindskog S et al. Relationship between
periapical and periodontal status. A clinical retrospective study.
J Clin Periodontol 1993 20: 117–123.
6. Stassen IGK, Hommez GMG, De Bruyn H et al. The relation
between apical periodontitis and root-filled teeth in patients with
periodontal treatment need. Int Endod J 2006 39: 299–308.
7. Jansson L, Ehnevid H, Lindskog S et al. The influence of end-
odontic infection on progression of marginal bone loss in peri-
odontitis. J Clin Periodontol 1995 22: 729–734.
8. Ørstavik D, Qvist V, Stoltze K. A multivariate analysis on the
outcome of endodontic treatment. Eur J Oral Sci 2004 112:
224–230.
9. Bahrami G, Wenzel A, Kirkevang LL et al. Risk indicators for a
reduced marginal bone level in the individual. Oral Health Prev
Dent 2006 4: 215–222.
10. Lavstedt S. A methodological-roentgenological investigation on
marginal alveolar bone loss, Thesis. Acta Odontol Scand 1975
33(Suppl): 67.
11. Ainamo J, Bay I. Problems and proposals for recording gingivi-
tis and plaque. Int Dent J 1975 25: 229–235.
12. Schei O, Waerhaug J, L€ ovdal A et al. Alveolar bone loss as
related to oral hygiene and age. J Periodontol 1959 30: 7–16.
13. Henrikson CO, Lavstedt S. Precision and accuracy in intraoral
roentgenological determination of proximal marginal bone loss.
Acta Odontol Scand 1975 33(Suppl 67): 50–89.
14. Lavstedt S, Bolin A, Henriksson CO. Proximal alveolar bone
loss in a longitudinal radiographic investigation (II). A 10-year
follow-up study of an epidemiological material. Acta Odontol
Scand 1986 44: 199–205.
15. Salonen L, Frithiof L, Wouters F et al. Marginal alveolar bone
height in an adult Swedish population. J Clin Periodontol 1991
18: 223–232.
16. Eliasson S, Bergstr€
om J. Minimum periodontal bone loss in
dentally-aware adults. A 10-year prospective study. J Clin Peri-
odontol 1997 24: 34–38.
17. Hugoson A, Laurell L. A prospective longitudinal study on peri-
odontal bone height changes in a Swedish population. J Clin
Periodontol 2000 27: 665–674.
€
18. Odesj€o B, Hellden L, Salonen L et al. Prevalence of previous
endodontic treatment, technical standard and occurrence of
periapical lesions in a randomly selected adult, general popula-
tion. Dent Traumatol 1990 6: 265–272.
19. Kirkevang LL, Wenzel A. Risk indicators for apical periodonti-
tis. Community Dent Oral Epidemiol 2003 31: 59–67.
20. Bergstr€
om J. Influence of tobacco smoking on periodontal bone
height. Long-term observations and a hypothesis. J Clin Period-
ontol 2004 31: 260–266.
21. Grossi SG, Genco RJ, Machtei EE et al. Assessment of risk for
periodontal disease. II. Risk indicators of alveolar bone loss. J
Periodontol 1995 66: 23–29.
22. Hugoson A, Laurell L, Lundgren D. Frequency distribution of
individuals aged 20-70 years according to severity of periodon-
tal disease experience in 1973 and 1983. J Clin Periodontol
1992 19: 227–232.
23. Jansson L, Lavstedt S. Influence of smoking on marginal bone
loss and tooth loss – a prospective study over 20 years. J Clin
Periodontol 2002 29: 750–756.
75
Jansson

24. Sunitha VR, Emmadi P, Namasivayam A et al. The periodontal 30. Jeftha A, Holmes H. Periodontitis and cardiovascular disease.
– endontic continuum: a review. J Conserv Dent 2008 11: SADJ 2013 68: 60–63.
54–62. 31. Mrak RE, Griffin WST. Interleukin-1, neuroinflammation, and
25. Kobayashi T, Hayashi A, Yoshikawa R et al. The microbial Alzheimer’s disease. Neurobiol Aging 2001 22: 903–908.
flora from root canals and periodontal pockets of non-vital 32. Li X, Kolltveit KM, Tronstad L et al. Systemic diseases caused
teeth associated with advanced periodontitis. Int Endod J 1990 by oral infections. Clin Microbiol Rev 2000 13: 547–558.
2: 100–106.
26. Nair PNR. Apical periodontitis: a dynamic encounter between
root canal infection and host response. Periodontol 2000 1997 Correspondence to:
13: 121–148. Leif Jansson,
27. Kerekes K, Olsen I. Similarities in the microfloras of root canals Department of Periodontology
and deep periodontal pockets. Dent Traumatol 2006 6: 1–5. Folktandv
arden Skanstull,
28. Saklatvala J, Dean J, Clark A. Control of the expression G€otgatan 100,
of inflammatory response genes. Biochem Soc Symp 2003 70:
95–106.
S-118 62 Stockholm,
29. Barthold PM, Marshall RI, Haynes DR. Rheumatoid arthritis:
Sweden.
a review. J Periodontol 2005 76: 2066–2074. Email: leif.jansson@ftv.sll.se

76 © 2014 FDI World Dental Federation