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Radiographic Assessment of Dental Health in Middle-aged Men Following Sudden Cardiac Death
1 Medical School, University of Tampere and Research Unit of Clinical Chemistry, Tampere University Hospital, Finland; Correspondence: * corresponding author, Päivionkatu 21, FIN-74100 Iisalmi, Europe; vesa.karhunen{at}fimnet.fi
Poor oral health has been suggested to be a risk factor for myocardial infarction. To study if dental pathology might predispose to pre-hospital sudden cardiac death, and using a sum index of panoramic tomography findings, we compared the oral health of middle-aged (33–69 yrs) male victims (Helsinki Sudden Death Study) of sudden cardiac death (n = 117) with that of controls, who died of non-cardiac diseases (n = 63) or suffered unnatural sudden death (n = 120). The mean number of teeth was 15.2, and 17.4% of the men were edentulous. Frequent age-associated findings in dentate victims were fillings (79.9%), horizontal bone loss (72.1%), periapical lesions (45.6%), residual roots (38.2%), and vertical pockets (30.9%). In multivariate analysis with coronary heart disease risk factors and number of teeth as covariates, poor oral health was associated (p = 0.053) with the risk of sudden cardiac death along with age, smoking, and body mass index. This association was especially strong (p = 0.009) among victims < 50 yrs.
Key Words: dental • panoramic tomography • sudden cardiac death • myocardial infarction • coronary heart disease • middle-aged • male • autopsy
Previous studies have suggested an association among dental infections, clinical myocardial infarction, and coronary heart disease. However, the results have been contradictory—both positive and negative findings have been reported (Mattila et al., 1989; DeStefano et al., 1993; Paunio et al., 1993; Joshipura et al., 1996; Morrison et al., 1999; Hujoel et al., 2000; Tuominen et al., 2003). According to a recent meta-analysis, individuals with periodontal disease are at a higher risk of future coronary events, the risk being greater in those  65 yrs (Janket et al., 2003). Today, most (> 50%) cardiovascular deaths are sudden, and take place out-of-hospital. Among men aged < 50–55 yrs, as many as 90% of deaths due to coronary heart disease belong in this category (Huikuri et al., 2001; Mikkelsson et al., 2001). The risk factors of pre-hospital sudden cardiac death are mainly unresolved, because sudden death is often the first manifestation of coronary heart disease, and most victims have not been examined by a physician prior to death. Knowledge about risk factors is difficult to obtain after death, and laboratory values or dental records are rarely available. This background explains why the possible association between pre-hospital sudden cardiac death and dental infections has not been studied. The dental data used in the earlier epidemiological studies on the association between dental infections and cardiovascular disease were obtained from questionnaires (Joshipura et al., 1996; Howell et al., 2001) or clinical examinations (DeStefano et al., 1993; Paunio et al., 1993; Beck et al., 1996; Hujoel et al., 2000; Wu et al., 2000; Tuominen et al., 2003). Panoramic tomography supported by clinical examination has seldom been applied (Mattila et al., 1989, 2000), although it gives a more comprehensive view of oral health. Post mortem panoramic tomography has previously been used for the assessment of marginal bone loss in a small series of cadavers (Soikkonen et al., 1990). In this paper, we report on our use of panoramic tomography to study the dental health of middle-aged males who died suddenly out-of-hospital, to test the hypothesis that poor oral health may be a risk factor for sudden cardiac death.
Autopsy Series The prospective autopsy series was comprised of 300 middle-aged men, aged 33–69 yrs, who were subjected to medico-legal autopsy at the Department of Forensic Medicine, University of Helsinki (The Helsinki Sudden Death Study), in a period of 12 mos between January, 1991, and January, 1992. The purpose of the Helsinki Sudden Death Study was to examine the epidemiology, pathogenesis, and also acquired and genetic risk factors of sudden cardiac death (Ilveskoski et al., 1999; Mikkelsson et al., 2001). Indications for autopsy were sudden out-of-hospital death, accidental death, suspected intoxication, or suicide. In the Helsinki area, a medico-legal autopsy is performed in 42% of all those who die before the age of 65 yrs. In our study, the cause of death was of cardiac origin in 39% of cases, other disease (non-cardiac natural death) in 21% of cases, and unnatural sudden death due to intoxication or violence (self-inflicted or accidental) in 40% of cases.
Methods
Panoramic Tomography Following the autopsy, the cadavers were taken on a transportable table to the x-ray room, located in the autopsy facilities. The panoramic tomography apparatus (Zonarc, Palomex Oy, Finland) was placed in a horizontal position on the wall. The table with the cadaver was elevated into the correct position to obtain panoramic tomography of the jaws. Panoramic x-rays taken by the autopsy technicians were available for 247 (82.3%) of the series of 300 cases. There were no statistically significant differences in any of the above characteristics between the whole study population (n = 300) and men with panoramic tomographies available (data not shown).
Scoring of Dental Status The number of teeth was recorded (including third molars), and edentulous cases (no visible sign of teeth or residual roots) were identified. Dental osseous lesions (periapical lesions Ø 1–4 mm and cysts Ø > 4 mm) and signs of caries (caries lesions and residual roots) were assessed, and pericoronal lesions and impacted teeth recorded. Moreover, signs of dental care, e.g., number of fillings and root canal treatments, were recorded. We assessed periodontal health by measuring horizontal bone loss (with a ruler with a millimeter scale, the distance between the dentin-enamel junction and marginal alveolar bone at the root surface), as well as by scoring vertical bony pockets (> 3 mm) and furcation lesions (III grade). After the assessment procedure was completed, the observers (VK, HF) held a consensus meeting in which the x-ray pictures with scores that differed between the observers were jointly assessed. The original inter-observer accordance was 95.4%, and 135 values (4.6%) were reviewed. To be able to describe the overall oral health status of dentate victims in one figure to be used in statistical analyses, we formed a "Panoramic Tomography Index" by summing the number of residual roots, vertical bony pockets, periapical, cystic, furcation, caries, and pericoronitis lesions. A similar approach has been used in previous studies (Mattila et al., 1989; Janket et al., 2004). There were no significant differences in the number of teeth, the panoramic tomography index, or individual dental parameters between men with and men without interview data, with the exception of slightly more caries lesions (p = 0.058) and horizontal bone loss (p = 0.032) in men without interview data.
Data Analysis
Frequencies of Dental Pathological Findings The majority of the men had some pathological lesions (Table 2  ). Most victims (98.4%) had lost one or more teeth, and the number of remaining teeth varied from edentulous (17.4%) to a full dentition (32 teeth, 1.6%). The mean number of teeth was 15.2 (SD 10.6, median 16, range 32).
Frequently occurring findings in dentate victims were fillings (79.9%) and horizontal bone loss (72.1%), followed by periapical lesions (45.6%), residual roots (38.2%), and root canal treatments (33.8%). Other findings were vertical bony pockets (30.9%), caries lesions (28.4%), and furcation lesions (23%). Impacted teeth (15.5%), pericoronal lesions (5.9%), and cysts (4.9%) were less common. Of all teeth (n = 3759), 34.7% (n = 1306) had fillings, the mean number being 6.4 (SD 5.7) per subject. Signs of severe periodontal infection—vertical bony pockets or furcation lesions—were found in 36.8% of dentate victims (n = 75).
Age-dependency of Dental Pathological Findings
Oral Health in Victims of Sudden Cardiac Death In the Mann-Whitney test, dentate victims of sudden cardiac death had significantly poorer oral health status, as measured by the panoramic tomography index (Table 4 ) (mean 5.1 vs. 3.5, median 4 vs. 2, p = 0.015), compared with controls (unnatural sudden deaths and non-cardiac natural deaths). In binary logistic regression analysis with age, body mass index, smoking, hypertension, diabetes, education level, number of teeth, and the panoramic tomography index as covariates, body mass index (p = 0.005), age (p = 0.010), smoking (p = 0.016), and the panoramic tomography index (p = 0.053) remained in the model as the most significant explanatory factors for sudden cardiac death.
When we repeated the analyses in the subgroups formed by dividing the series into three age groups used previously to test for age-dependency, victims of sudden cardiac death < 50 yrs tended to have panoramic tomography scores higher than those of controls (mean 4.6 vs. 2.5, median 2.5 vs. 1, p = 0.077) in the univariate test (Mann-Whitney). In binary logistic regression analysis with covariates as above, the panoramic tomography index (p = 0.009, OR 1.244, 95% CI 1.057 to 1.463), along with smoking (p = 0.005), hypertension (p = 0.016), and number of teeth (p = 0.061), remained in the model as significant explanatory factors for sudden cardiac death among men aged < 50 yrs. In age groups 50–59 yrs and > 60 yrs, the panoramic tomography index was no longer a significant risk factor (p = 0.941 and p = 0.177, respectively).
We discovered that dental pathological lesions were common among victims who died suddenly out-of-hospital, and most lesions showed strong age-dependency. Among men aged < 50 yrs, poor oral health seemed to be an especially significant risk factor for pre-hospital sudden cardiac death. The Mini-Finland survey, a nationwide comprehensive study on general and dental health in the adult population in 1980, provided epidemiological data on the oral health of Finnish adults (Vehkalahti et al., 1991). According to the survey, the mean number of teeth remaining in males aged 30 to 69 yrs from this area (including the Helsinki area) was 17.7, and 15% of the men were edentulous. These numbers do not greatly deviate from those in our study, in which the mean number of teeth was 15.2, and 17.4% of the men were edentulous. In the Mini-Finland study, the mean number of teeth with fillings was 8.8, and 42% of teeth in dentate males had fillings. Corresponding numbers from our study are 6.4 and 34.7%, respectively. Similarly, 38% of males in the survey had severe destruction of the periodontium (pockets > 6 mm), compared with 36.8% (vertical pockets or furcation lesions) in our study. For other dental pathological findings, no comparable data are available for Finland or other countries. Analysis of these data suggests that the dental health in our study sample does not deviate much from that observed in the general male population living in Southern Finland at the time of the collection of the autopsy series. In our study, younger victims of sudden cardiac death (< 50 yrs) had more oral pathology compared with men in the control group, measured by the panoramic tomography index, after adjustment for the conventional coronary heart disease risk factors. Our results are in line with those from another Finnish study (Mattila et al., 1989), where pantomography indices were also used as a measure of total oral infection load. In that study, patients with acute myocardial infarction had poorer dental health than controls matched for age and sex. The mechanisms behind the association between dental pathological findings and different phenotypes of coronary heart disease are not known at present and should be the focus of further research. The main phenotypes of coronary heart disease are angina pectoris, myocardial infarction, and sudden cardiac death. Our results support the hypothesis that ongoing dental infections might play a role as one of the triggering factors of sudden cardiac death, possibly leading to activation of thrombogenic factors or contributing to the inflammatory process within the unstable coronary plaque. The use of panoramic tomography has been advocated in some studies (Walsh et al., 1997), whereas other studies have preferred periapical radiographs (Pepelassi et al., 2000). The reliability of panoramic tomography in the assessment of marginal alveolar bone loss has previously been studied in cadaver material (Soikkonen et al., 1990). Those investigators concluded that the method is sufficiently reliable, but that radiographic bone loss values were found to be about 27% less than clinical values. Other reports on clinical patients have agreed with this and have suggested that underestimation of bone loss ranges from 13 to 32% (Akesson et al., 1992). Thus, except for slight underestimation, the assessment of periodontal pathology can be made with sufficient confidence by the use of panoramic tomography in dentate areas. From edentulous areas, the measurement of bone loss would be too uncertain, because of lack of a reference point (dentin-enamel junction). The main problem in the scoring of the radiographs was that, in many cases, the quality of the routinely taken x-rays was not as good as that of x-rays taken in normal dental practice. Because the subjects were cadavers with rigor mortis, the chin might be tipped up or down, and the head turned toward either side, both resulting in distorted x-rays. However, the number of teeth, periapical lesions, horizontal bone loss, and number of fillings showed age associations typical of those reported in many previous studies (Kelly, 1967; Pilot et al., 1992; Holm, 1994; Kirkevang et al., 2001). This speaks for the validity of the post mortem panoramic tomography method. The main weakness of the present study is the lack of information on coronary heart disease risk factors for 45% of the sample. Sudden death is often the first symptom of heart disease, especially among middle-aged men (Huikuri et al., 2001; Mikkelsson et al., 2001). Since, in most cases, no hospital records were available, the only way to gather data on risk factors was by interviewing spouses, children, and other close relatives and, in some cases, a close friend of the deceased. For many cases, there was nobody to provide detailed information. Although there were no significant differences in the demographic characteristics or in the severity of coronary stenosis, number of teeth, or the panoramic tomography index between deceased with and those without interview data, our results should be interpreted with caution. Although the dental health of our cases does not differ from that observed in the general male population living in Southern Finland, our victims may not be representative of the general middle-aged male population as such. In conclusion, the present results indicate that men who suffer sudden cardiac death in early middle age seem to exhibit greater dental pathology compared with men who die of other causes. This suggests that infections of dental origin may be among the risk factors for sudden cardiac death. Post mortem panoramic tomography seems to be a valid method for the assessment of dental health in victims of sudden cardiac death, giving a comprehensive view of dental pathology. Since the victims of sudden cardiac death show heterogeneous cardiac pathology, more detailed studies on the contributions of different dental pathological processes are needed.
We thank Miira Vehkalahti, DDS, PhD, Department of Oral Public Health, Institute of Dentistry, University of Helsinki, for suggestions concerning the manuscript. This work was supported by the Yrjö Jahnsson Foundation, the Finnish Foundation of Alcohol Research, the Elli and Elvi Oksanen Fund of the Pirkanmaa Fund under the auspices of the Finnish Cultural Foundation, the Medical Research Fund of Tampere University Hospital, the Finnish Medical Foundation, and the Finnish Foundation for Cardiovascular Research. No fees have been paid to, or other financial arrangements made with, the investigators. Received for publication June 15, 2004. Revision received September 14, 2005. Accepted for publication September 29, 2005.
Journal of Dental Research, Vol. 85, No. 1,
89-93 (2006)
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ABSTRACT
INTRODUCTION
1 findings in panoramic tomography]