International Journal of Medical Dentistry111 [613860]

International Journal of Medical Dentistry111
Oral Pathology DENTAL INFECTIONS AND THE ATHEROSCLEROSIS RISK IN A
SUBPOPULATION OF SOUTH ROMANIA
Alexandru Andrei ILIESCU1, Paula PERLEA2, Ruxandra Diana SINESCU3, Delia VOICULESCU4,
Laura DÂRȚU5, Georgiana ILIESCU6, Anca TORCĂTORU7, Irina GHEORGHIU8, Bogdan VLĂDILĂ9,
Oana Andreea DIACONU10, Cristian PETCU11, Andrei ILIESCU12, Ion Bogdan CODOREAN13
1Senior lecturer, DMD, DDS, PhD, Faculty of Dental Medicine, University of Craiova, Romania
2Senior lecturer, DMD, PhD, Faculty of Dental Medicine, “Carol Davila” University of Bucharest, Romania
3Assoc. Prof., MD, PhD, ”Elias” Emergency Teaching Hospital, “Carol Davila” University of Bucharest, Romania
4MD, PhD student: [anonimizat], SCUBA, Bucharest, Romania
5Senior lecturer, PhD, Faculty of Medical Dentistry, “Apollonia” University of Ia și, Romania
6DMD, PhD student: [anonimizat],“Carol Davila” University of Bucharest, Romania
7Univ. Assist., DMD, PhD, Faculty of Dental Medicine, University of T ârgu Mureș, Romania
8Senior lecturer, DMD, PhD, Faculty of Dental Medicine, “Carol Davila” University of Bucharest, Romania
9DMD, PhD student: [anonimizat], Bucharest, Romania
10Senior lecturer, DMD, PhD, Faculty of Dental Medicine, University of Craiova, Romania
11Univ. Assist., DMD, PhD, Faculty of Dental Medicine, University of Craiova,Romania
12Profesor, DMD, PhD, Faculty of Medical Dentistry, “Apollonia” University of Ia și, Romania
13Univ.Assist., MD, PhD, Universitary Emergency Military Central Hospital, “Carol Davila” University of Bucharest, Romania
Corresponding author: [anonimizat]
Abstract
Periodontal disease and chronic apical periodontitis are
considered risk factors for cardiovascular diseases. This
cross-sectional study, performed in a subpopulation living
in the South area of Romania, investigated the association
between the afore-mentioned oral lesions and
atherosclerosis. The research was focused on common
carotid artery intima-media wall thickness IMT and
dislipidemia, in a batch of 30 hypertensive subjects, age
41-50. Over 40% of the patients diagnosed with periodontal
disease and/or chronic apical periodontitis developed
subclinical atherosclerosis. Associated dyslipidemia to an
increased IMT over 0.9 mm in subjects affected by
periodontal disease or combined lesions with chronic
apical periodontitis might be considered a strong predictor
of future cardiovascular events.
Keywords : periodontal disease, chronic apical periodontitis,
atherosclerosis, dislipidemia, IMT
1. INTRODUCTION
The concept linking the oral pathology and
systemic diseases is not a new one. Over the past
century, the “focal infection” theory resulted in
millions of tooth extractions, claiming that
periodontal and apical lesions represent the main
risk for systemic inflammatory and infectious
complications [1].Even if, initially, this undiscriminating
therapeutic attitude was not supported by
rigorous scientific evidence, current epidemiologic
studies relate an increasing relationship between
oral diseases and systemic pathology, such as
atherosclerosis, cardiovascular diseases, diabetes,
adverse pregnancy outcome or lung diseases [1,2].
Along with age, hypertension, diabetes,
smoking, total cholesterol, high triglycerides,
CRP (C-reactive protein), to date chronic
periodontal and apical inflammations are also
considered risk factors for cardiovascular
diseases [1-4].
This issue is of paramount importance, as
anaerobic gram-negative bacteria from
periodontal deep pockets or infected tooth root
canals, such as Porphyromonas gingivalis ,
Prevotella intermedia , Tannerella forsythia,
appeared as involved in multiple pathogenic
mechanisms, including the direct invasion of
endothelial cells [5].
Considering the above-mentioned pathogenic
hypothesis, the objective of the present cross-
sectional study was to illustrate the possible
association between periodontal disease and
chronic apical periodontitis and atherosclerosis,

112
Volume 5 • Issue 2 April / June 2015 • Alexandru Andrei ILIESCU, Paula PERLEA, Ruxandra Diana SINESCU, Delia VOICULESCU, Laura DÂRȚU, Georgiana ILIESCU, Anca
TORCĂTORU, Irina GHEORGHIU, Bogdan VLĂDILĂ, Oana Andreea DIACONU, Cristian PETCU, Andrei ILIESCU, Ion Bogdan CODOREANin a subpopulation living in the South area of
Romania.
2. MATERIALS AND METHOD
30 consecutive cardiac patients with confirmed
hypertension (systolic blood pressure ≥ 140 mm
Hg or diastolic blood pressure ≥ 90 mm Hg),
with ages between 41-50 years and no history of
myocardial infarction or stroke, were recruited.
A similar (as to age, gender, smoking habits, and
residence) number of 30 matched clinically
healthy patients were enrolled as controls.
Patients with other chronic infections than
dental disease were excluded. The same
exclusion and inclusion criteria were applied to
both groups of subjects who underwent a
comprehensive oral examination to diagnose
periodontitis, defined by an attachement loss ≥
3 mm, and apical periodontitis.
A calibration exercise was previously
performed to obtain acceptable intra-examiner reproducibility for probing depth and recession
of the gingival margin. Panoramic radiographs
of the jaws were taken and, in case of apical
radiolucensis, additional isolated periapical
radiographs for irrespective tooth. A single
specialist performed all radiographic
examinations.
Blood samples were collected to evaluate
serum total cholesterol and triglycerides, and
common carotid artery intima-media wall
thickness (cIMT) was measured in each patient,
using a high-resolution B-mode ultrasound
carotid scan KI-lM200HDPE ( Siemens ), at a
frequency of 50-60Hz.
3. RESULTS
As general characteristics, women and men
were present in equal ratios in both groups, but
women were younger (45.2 vs 46.06) so that,
according to age, the distribution is unequal
(Fig.1).
3
2 23 3
24 4
34
23
23
23 36
3 3
41y 42y 43y 44y 45y 46y 47y 48y 49y 50ypacients number
men women
Fig.1. Distribution of subjects according to age
As expected, average plaque thickness
registered higher average values in hypertensive
subjects, comparatively with the healthy group
(0.92 mm vs 0.87 mm). However, the average plaque thickness size had close values in both
men and women (Fig.2), with discretely higher
records in men (0.88 mm vs 0.87 mm in healthy,
respectively 0.93 vs 0.92 in hypertensive ones).

International Journal of Medical Dentistry113
DENTAL INFECTIONS AND THE ATHEROSCLEROSIS RISK IN A SUBPOPULATION OF SOUTH ROMANIAIn healthy subjects, 13 out of 30 (43.33%) had IMT
≥ 0.9 mm, as compared to the hypertensive ones, where 19 out of 30 (63.33%) recorded similar
values.
0,880,93
0,870,92
healthy hypertensiveaverage IMT
men women
Fig.2. Average IMT values in healthy and hypertensive subjects
Combined lesions (periodontitis and chronic
apical periodontitis) and periodontitis are prevalent in hypertensive subjects, comparatively
with the healthy ones (Fig.3).
8
59
6
5
1
012345678910
Periodontitis Chronic apical periodontitis Combined
hypertensive healthy
Fig.3. Distribution of periodontitis and chronic apical periodontitis

114
Volume 5 • Issue 2 April / June 2015 • Alexandru Andrei ILIESCU, Paula PERLEA, Ruxandra Diana SINESCU, Delia VOICULESCU, Laura DÂRȚU, Georgiana ILIESCU, Anca
TORCĂTORU, Irina GHEORGHIU, Bogdan VLĂDILĂ, Oana Andreea DIACONU, Cristian PETCU, Andrei ILIESCU, Ion Bogdan CODOREANDislipidemia was considered when serum
total cholesterol increased > 200 mg/dl, serum
triglycerides were > 150 mg/dl or both were increased. The occurrence of dislipidemia is
illustrated in relation with oral pathology (Fig.4)
and IMT (Fig.5).

01234567
Periodontitis Chronic apical periodontitis Combined No lesion
hypertensive healthy
Fig.4. Dislipidemia vs dental and periodontal pathology
124
23 3
0 03 3 3
1
0,7mm 0,8mm 0,9mm 1mm 1,1mm 1,2mmsubjects number
hypertensive healthy
Fig.5. Dislipidemia vs IMT

International Journal of Medical Dentistry115
DENTAL INFECTIONS AND THE ATHEROSCLEROSIS RISK IN A SUBPOPULATION OF SOUTH ROMANIA4. DISCUSSION
Atherosclerosis is a multifactorial disease and
its conventional risk factors, such as age, sex,
smoking, diabetes, obesity, systolic blood
pressure, low- and high-density lipoprotein
cholesterol, triglycerides, are well understood
[6]. Unfortunately, they can justify only 50-70%
of the clinical events [7]. Among other putative
factors in the biological background of
atherosclerosis, a pivotal pathogenic role is
played low-grade chronic inflammation and
infection [8,9].
Dental infections, periodontal disease and
apical periodontitis are favorable candidates as
trigger factors of atherosclerosis and
cardiovascular diseases [10-16]. It was proved
that, in patients with periodontal disease,
atherosclerotic complications – such as coronary
artery disease, myocardial infarction and stroke
– are strongly associated. Moreover, they depend
on the severity of gingival inflammation and
bone resorption [7 ,17].
As to the connection between chronic apical
periodontitis and the subsequent in time
occurring cardiovascular events, current reports
are still confusing. Though the pathogenic
mechanisms of periodontal disease and chronic
apical periodontitis and their link to cardiovascular
diseases might be similar, clinical evidence does
not support an association between chronic
apical inflammatory lesions and cardiovascular
diseases [8].
Apparently, the association between chronic
apical periodontitis and cardiovascular diseases
is more obvious in young people. It is assumed
that, in older subjects, some other mechanisms
might prevail in developing a cardiovascular
disease [4,8, 14].
The purpose of this cross-sectional study was
to determine to what extent the periodontal
disease and chronic apical periodontitis are
associated with carotid artery intima-media wall
thickness (IMT), a widely adopted surrogate for
predicting rates of cardiovascular events
[3,18,19].
The control group had no cardiovascular
events or current clinical heart disturbances.
However, in 43.33% of the healthy subjects, the IMT value was ≥ 0.9 mm, which means that they
had already developed subclinical atherosclerosis.
As expected, the average IMT counts were higher
in hypertensive subjects, compared to the healthy
ones.
The present study also revealed a higher
prevalence of dislipidemia in periodontal disease
and combined lesions. In periodontal disease, no
differences were observed between healthy and
hypertensive subjects. Surprisingly, in chronic
apical periodontitis, the values of dislipidemia
were higher in healthy subjects, as compared to
hypertensive ones. Probably, our results converge
to the above-mentioned reports on the association
of chronic apical periodontitis with heart diseases,
as the participants in our group of study were
not exactly young (between 40 and 50 years).
Moreover, some dislipidemic subjects were not
affected by any inflammatory or infective oral
disease prone to initiate a cardiovascular disease.
It has also to be highlighted that, when IMT
exceeds 0.9 mm, which is an overt signal of
atherosclerosis, the prevalence of dislipidemia in
healthy subjects shows a strong trend to equalize
the similar IMT value in hypertensive ones.
While the pathogenic link of gingival
inflammation with cardiovascular diseases is
already accepted, the role of chronic apical
periodontitis is still confusing and controversial.
According to our results, it seems that root canal
infection might be only a cumulative contributor
to developing a cardiovascular disease, associated
to a previous or simultaneous periodontal
disease.
However, it has to be considered that, in
patients affected by periodontal disease and/or
chronic apical periodontitis, association of
dislipidemia with an increased IMT are strong
predictors of future cardiovascular events.
5. CONCLUSIONS
1. Over 40% of the patients (age 40-50)
diagnosed with periodontal disease and/or
chronic apical periodontitis developed subclinical
atherosclerosis.
2. Associated dislipidemia to an increased
IMT over 0.9 mm in patients affected by
periodontal disease or combined lesions with

116
Volume 5 • Issue 2 April / June 2015 • Alexandru Andrei ILIESCU, Paula PERLEA, Ruxandra Diana SINESCU, Delia VOICULESCU, Laura DÂRȚU, Georgiana ILIESCU, Anca
TORCĂTORU, Irina GHEORGHIU, Bogdan VLĂDILĂ, Oana Andreea DIACONU, Cristian PETCU, Andrei ILIESCU, Ion Bogdan CODOREANchronic apical periodontitis might be considered
a strong predictor of future cardiovascular
events.
References
1. Lindhe J, Karring T, Lang NP. Clinical periodontology
and implant dentistry. 4th edition. Oxford: Blackwell
Munksgaard; 2003. Chapter 16, Williams RC,
Paquette D. Periodontitis as a risk for systemic
disease; p 366-386.
2. Marton, IJ. How does the periapical inflammatory
process compromise general health? Endod Topics.
2004; 8:3-14.
3. Baldassarre D, Veglia F, Hamsten A, Humphries SE,
Rauramaa R, de Faire U, Smit AJ, Giral P, Kurl S,
Mannarino E, Grossi E, Paoletti R, Tremoli E.
Progression of carotid intima-media thickness as
predictor of vascular events. Arterioscler Thromb
Vasc Biol. 2013; 33:2273-2279.
4. Caplan D. Epidemiologic issues in studies of
association between apical periodontitis and
systemic healt. Endod Topics. 2004; 8:15-35.
5. Reyes L, Herrera D, Kozarov E, Roldan S, Progulske-
Fox A. Periodontal bacterial invasion and infection:
contribution to atherosclerotic pathology. J Clin
Periodontol. 2013; 40:S30-S50.
6. Desvarieux M, Demmer RT, Rundek T, Boden-
Albala B, Jacobs DR, Papapanou PN, Sacco RL.
Relationship between periodontal disease, tooth
loss, and carotid artery plaque. The oral infections
and vascular disease epidemiology study (INVEST).
Stroke. 2003; 34:2120-2125.
7. Haynes WG, Stanford C. Periodontal disease and
atherosclerosis. From dental to arterial plaque.
Arterioscler Thromb Vasc Biol. 2003; 23:1309-1311.
8. Cotti E, Dessi C, Piras A, Mercuro G. Can chronic
dental infection be considered a cause of
cardiovascular diseases? A review of the literature.
Int J Cardiol. 2011; 148:4-10. 9. Yu YH, Chasman DI, Buring JE, Rose L, Ridker PM.
Cardiovascular risks associated with incident and
prevalent periodontal disease. J Clin Periodontol.
2015; 42:21-28.
10. Beck JD, Pankow J, Tyroler HA, Offenbacher S.
Dental infections and atherosclerosis. Am Heart J.
1999; 138:528-522.
11. Deshpande RG, Khan MB, Genco CA. Invasion of
aortic and heart endothelial cells by Porphyromonas
gingivalis . Infect Immun. 1998; 66:5337-5343.
12. Haraszthy V, Zambon J, Trevisan M. Identification
of periodontal pathogens in atheromatous plaques .
J Periodontol. 2000; 71:1554-1560.
13. Abbas M, Bignamini V, Corea F. Effects of chronic
microbial infection on atherosclerosi s.
Atherosclerosis. 2006; 187: 439-440.
14. Joshipura KJ, Pitiphat W, Hung H, Willett WC,
Colditz GA, Douglass CW. Pulpal inflammation and
incidence of coronary heart disease. J Endod. 2006;
32:99-103.
15. Niedzielska I, Janic T, Cierpka S, Swietochowska E.
The effect of chronic periodontitis on the
development of atherosclerosis: review of the
literature. Med Sci Monit. 2008; 14:103-106.
16. Willershausen B, Kasaj A, Willershausen I, Zahorka
D, Briseno B, Blettner M, Genth-Zotz S, Münzel T.
Association between chronic dental infection and
acute myocardial infarction. J Endod. 2009; 35:626-
630.
17. Söder PO, Söder B, Nowak J, Jogestrand T. Early
carotid atherosclerosis in subjects with periodontal
diseases. Stroke. 2005; 36:1195-1200.
18. Engebretson SP, Lamster IB, Elkind MSV, Rundek
T, Serman NJ, Demmer RT, Sacco RL, Papapanou
PN, Desvarieux M. Radiographic measures of
chronic periodontitis and carotid artery plaque.
Stroke. 2005; 36:561-566.
19. Finn AV, Kolodgie FD, Virmani R. Correlation
between carotid intimal/medial thickness and
atherosclerosis. A point of view from pathology.
Arterioscler Thromb Vasc Biol. 2010; 30:177-181.

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