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Clinical

Oral Health and Mortality Risk from Pneumonia in the Elderly

S. Awano1,*, T. Ansai1, Y. Takata2, I. Soh1, S. Akifusa3, T. Hamasaki1, A. Yoshida1, K. Sonoki2, K. Fujisawa2 and T. Takehara1

1 Division of Community Oral Health Science and
2 Division of General Internal Medicine, Department of Health Promotion, Kyushu Dental College, 2-6-1 Manazuru, Kokurakita-ku, Kitakyushu 803-8580, Japan; and
3 Department of Preventive Dentistry, Kyushu University Faculty of Dental Science, 3-1-1 Maidashi, Higashi-ku, Fukuoka, Japan

Correspondence: * corresponding author, awa-shu{at}kyu-dent.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although poor oral health influences the occurrence of pulmonary infection in elderly people, it is unclear how the degree of oral health is linked to mortality from pulmonary infection. Therefore, we evaluated the relationship between oral health and four-year mortality from pneumonia in an elderly Japanese population. The study population consisted of 697 (277 males, 420 females) of the 1282 individuals who were 80 years old in 1997. Data on oral and systemic health were obtained by means of questionnaires, physical examinations, and laboratory blood tests. One hundred eight of the study persons died between 1998 and 2002. Of these, 22 deaths were due to pneumonia. The adjusted mortality due to pneumonia was 3.9 times higher in persons with 10 or more teeth with a probing depth exceeding 4 mm (periodontal pocket) than in those without periodontal pockets. Therefore, the increase in teeth with periodontal pockets in the elderly may be associated with increased mortality from pneumonia.

Key Words: aspiration pneumonia • elderly person • mortality from pneumonia • oral health • periodontal disease


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Aspiration pneumonia is recognized as a major health problem that is linked to mortality in elderly people. Several studies have documented that the oral cavity might be a reservoir for the respiratory pathogens that are responsible for aspiration pneumonia in high-risk elderly adults living in nursing homes (Scannapieco et al., 1992; Fourrier et al., 1998; Russell et al., 1999).

Oral anaerobic bacteria, such as periodontal bacteria, have been isolated from the expectorated specimens of aspiration pneumonia in elderly people (Bartlett et al., 1974; Bartlett and Gorbach, 1975a,b; Bartlett, 1987). Periodontal bacteria possess an array of virulence factors that cause infectious diseases, and these bacteria may be more capable of causing aspiration pneumonia, as well as periodontitis, compared with other oral bacteria (Papapanou et al., 1997; Russell et al., 1999; Scannapieco, 1999; Okuda et al., 2005). Furthermore, differences in the prevalence of oral bacteria reflect the state of the oral cavity, such as the number of teeth, level of oral hygiene, and degree of periodontal health (Stoltenberg et al., 1993; Lucas et al., 2002). It has recently been found that the quantity of periodontal bacteria coating the tongue in 85-year-old persons increases in relation to the number of teeth (Tachibana et al., 2006). Therefore, in elderly people, a high number of teeth may be linked to the prevalence of periodontal bacteria in the oral cavity, and may be a risk factor for occurrence of aspiration pneumonia.

Furthermore, recent studies also showed that the reduction in the number of teeth in elderly people might influence mortality (Hamalainen et al., 2003; Shimazaki et al., 2003). However, these reports evaluated mortality from all causes; they did not show a relationship between the dental state and mortality associated with aspiration pneumonia.

Therefore, we focused on the infectious agents associated with aspiration pneumonia to evaluate the relationship between oral status and the four-year mortality rate from pneumonia in elderly people.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Population
The study population consisted of 80-year-old persons (born in 1917) who lived in Fukuoka Prefecture, Japan. All persons who fit the age requirement and resided in the 9 districts that were selected at random were invited to participate in the survey. Of the 1282 individuals contacted, 697 (277 males, 420 females) agreed to participate.

The survey was conducted according to the principles expressed in the Helsinki Declaration and was approved by the Human Investigations Committee of Kyushu Dental College. The details of the study protocol were explained to all participants, and written informed consent was obtained prior to participation.

Baseline Data
The baseline survey was performed in March, 1998, and included a standardized oral examination, a medical examination, and laboratory blood tests (Takata et al., 2001). Of the 697 individuals who agreed to participate, oral examinations were performed on 694 persons, and 672 of these completed a questionnaire regarding lifestyle and oral and systemic health, and also underwent the physical examination and laboratory blood tests. The participants included 35 persons with a history of cerebrovascular disease (stroke), 120 persons with a history of cardiovascular disease (CVD), 18 persons with a history of pneumonia, and three persons with a history of cancer.

Evaluation of Methyl Mercaptan Generated from the Tongue Coating
Following the oral examination, the tongue coating of each person was scraped twice by means of a sterile microspatula at different 1-cm areas on the rear dorsal surface of the tongue. The tongue-coating samples were immediately suspended in a sterile 15-mL polypropylene tube with 2.5 mL of Todd-Hewitt Broth (DIFCO, Detroit, MI, USA) and 0.05% L-methionine, and the sample tubes were stored at 4°C in a dark box and transported by air to the Lion Science Research Center (Odawara, Japan). After nearly 24 hrs, the gas in each tube was replaced with a gas composed of 80% N2, 10% CO2, and 10% H2; the tubes were then incubated in this anaerobic condition for 24 hrs at 37°C. Following the incubation, the tongue-coating samples were agitated for 30 sec, and a 0.5-mL sample of the headspace volatile gases was withdrawn by means of a gas-tight syringe. The samples were then injected into a gas chromatography system equipped with a flame photometric detector specific for sulfur compounds. We used the resulting data to evaluate the level of methyl mercaptan (CH3SH) generated from anaerobic bacteria in the tongue coating (Persson et al., 1990; Yaegaki and Sanada, 1992).

Evaluation of Candida Species on the Lingual Surface
In addition to the above-mentioned scraping, 1-cm areas on the rear dorsal surface of the tongue of each person were scraped 2 more times with a sterile cotton swab. The swab samples were immediately applied to a special medium for detecting Candida species (Dentocult-CA, Orion Diagnostica, Espoo, Finland), and the number of different Candida species present was estimated according to the manufacturer’s instructions.

Repetitive Saliva-swallowing Test
We conducted a repetitive saliva-swallowing test to screen for dysphagia, as reported elsewhere (Tamura et al., 2002). The number of times that the participants could swallow saliva during a 30-second period was recorded. If the person could not swallow saliva because there was no saliva in the mouth, the test was performed with 1 mL of water instead of saliva.

Follow-up Survey
The date and cause of all deaths among the 697 participants of this study were followed for 4 yrs after their baseline examinations. This follow-up survey was performed at the end of March, 2002, based on resident registration cards and official death certificates available in the registers of the Public Health Centers of each district included in the study. Deaths were classified by trained physicians according to the International Classification of Diseases, 10th revision (WHO, 2002).

Statistical Analysis
Based on the results of the follow-up survey, the participants were categorized into the following three groups: the survival group (n = 589; participants still alive after 4 yrs); pneumonia-death group (n = 22; participants who died of pneumonia during the four-year follow-up); and ‘other-death’ group (n = 86; participants who died of causes other than pneumonia during the four-year follow-up). The statistical significance of the baseline data of the three groups was determined by one-way ANOVA with post hoc tests, or by chi-square tests.

We evaluated the parameters related to mortality caused by pneumonia using univariate and multivariate Cox regression models. The quantitative variables were converted into categorical variables for the Cox model according to the following parameters: (1) number of teeth (four groups) — edentulous, 1–9 teeth, 10–19 teeth, or 20 or more teeth; (2) number of teeth with a probing depth exceeding 4 mm (periodontal pocket) (three groups) — no teeth with periodontal pockets, 1–9 teeth with periodontal pockets, or 10 or more teeth with periodontal pockets; and (3) results of medical examination (three groups for each diagnostic standard) — low, normal, or high. The variables entering into the univariate and multivariate Cox models were determined by the statistical significance (p < 0.05) in one-way ANOVA with post hoc tests or chi-square tests, and in the univariate models, respectively.

Survival curves in relation to numbers of teeth with periodontal pockets in 3 categories were analyzed by the Kaplan-Meier method, followed by the log-rank test.

All statistical analyses were performed with SPSS 14.0 for Windows (SPSS, Chicago, IL, USA).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The baseline characteristics of the participants were compared among the Survival, Pneumonia-death, and Other-death groups (Table 1Go, Appendix Table). In the four-year period from March, 1998, to March, 2002, 108 persons (58 males, 50 females) died. Of these deaths, 22 were due to pneumonia (Pneumonia-death group: 16 males, six females), and 86 were due to other causes, such as cancer and cardiovascular disease (Other-death group: 42 males, 44 females). The gender ratios differed significantly among the three groups (chi-square test, p < 0.001). The mean number of teeth in the Other-death group was significantly less than that in the Survival or Pneumonia-death group. There were significant differences in the ratios of the three groups between persons not using dentures (No denture group) and those who used a partial set of dentures (Partial denture group), or who used a full set of dentures (Full denture group) (chi-square test, p < 0.001). The mean number of teeth with periodontal pockets was significantly greater in the Pneumonia-death group than in other groups (Fisher’s LSD test, p < 0.05). Among the medical histories, there was a significant difference in ratios of persons with/without a history of stroke among the three groups (chi-square test, p < 0.05); the ratio of persons with a history of stroke in the Pneumonia-death group was greater than those without such a history. In the medical examination, the levels of serum total cholesterol and serum albumin were significantly lower in the Pneumonia-death and Other-death groups than in the Survival group, whereas the fasting serum glucose level was significantly greater in the Pneumonia-death group than in the other groups (Fisher’s LSD test, p < 0.05). The body mass index was significantly lower in the Pneumonia-death group than in the other groups. Furthermore, the proportion of smokers among the three groups was significantly different from that of non-smokers (chi-square test, p < 0.001).


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  		Table 1. Baseline Characteristics of 80-year-old Persons Who Survived or Died Due to Pneumonia or Other Causes during the Four-year Follow-up [total number of persons in each group (n), mean (standard deviation) or number of persons (%)]
 
Univariate Cox regression analyses of the four-year mortality rates from all causes, from pneumonia, and from causes other than pneumonia were performed with variables found to differ significantly among the groups (Table 2Go). The significant predictors of pneumonia mortality were being male, the presence of 10 or more teeth with periodontal pockets, a positive history of stroke, low cholesterol, and a low body mass index. Furthermore, being male, the use of a full denture, low albumin, low cholesterol, high glucose, a low body mass index, and smoking were significant predictors of mortality from all causes, while the use of a full denture and the presence of no teeth with periodontal pockets, low albumin, low cholesterol, high glucose, and smoking were the significant predictors of mortality from causes other than pneumonia.


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  		Table 2. Predictors of the Four-year Mortality from All Causes, from Pneumonia, and from Causes Other Than Pneumonia, According to Univariate Cox Regressions [Hazard ratio (95% confidence interval)]
 
The survival curves (Fig.Go) showed that persons with 10 or more teeth with periodontal pockets had a significantly increased mortality from pneumonia compared with the others, and that persons with no teeth with periodontal pockets had a significantly increased mortality from causes other than pneumonia compared with those with 1–9 teeth with periodontal pockets (log-rank test, p < 0.05).


Figure 1
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  		Figure. Survival curves for mortality from pneumonia (A) and causes other than pneumonia (B) in relation to numbers of teeth with periodontal pockets exceeding 4 mm (PD) in 3 categories.

 
The multivariate-adjusted hazard ratios (HRs) of the four-year mortality from all causes, from pneumonia, and from causes other than pneumonia were evaluated by the Cox multivariate regression model, with the variables found to be predictors of mortality in the univariate analysis (Table 3Go). The adjusted HR for mortality from pneumonia was significantly greater (by 3.9-fold) in persons with 10 or more teeth with periodontal pockets than in persons with no teeth with periodontal pockets. Moreover, the adjusted mortality due to pneumonia was significantly higher in males, persons with low cholesterol, and those with a low body mass index. Furthermore, the adjusted all-cause mortality risk was significantly higher in individuals with low albumin or low cholesterol, in addition to smokers, and significantly lower in individuals with a high body mass index. The adjusted mortality due to causes other than pneumonia was higher in persons with low albumin, and in smokers.


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  		Table 3. Hazard Ratios of the Four-year Mortality from All Causes, from Pneumonia, and from Causes Other Than Pneumonia, According to Multivariate Cox Regression [Hazard ratio (95% confidence interval)]
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In addition to poor oral hygiene, periodontal disease has been shown to be a risk factor for pulmonary infection (Scannapieco and Mylotte, 1996; Scannapieco and Ho, 2001; Scannapieco and Rethman, 2003; Okuda et al., 2005; Terpenning, 2005). To our knowledge, the present study is the first to provide evidence that periodontal disease in elderly people is associated with mortality from pneumonia.

An increased number of teeth with periodontal pockets might enhance the risk of mortality from aspiration pneumonia in elderly people. The incidence of periodontal pockets influences the prevalence of periodontal bacteria in the oral cavity (Riviere et al., 1995; Ashimoto et al., 1996; Papapanou et al., 1997; Paster et al., 2001). Generally, aspiration pneumonia in elderly people is caused almost entirely by anaerobic Gram-negative bacteria, such as periodontal bacteria, and several well-known periodontal pathogens are regarded as the most important pathogens of aspiration pneumonia (Preston et al., 1999; Terpenning et al., 2001; Shay, 2002). Also, anaerobic Gram-negative bacteria, including periodontal bacteria, produce high levels of CH3SH, one of the main causes of bad breath (Persson et al., 1990). Previous reports have suggested that the production of CH3SH by the tongue-coating bacteria reflects the prevalence of anaerobic bacteria in the oral cavity (Yaegaki and Sanada, 1992; Faveri et al., 2006). In the present study, the level of CH3SH generated from the tongue coating tended to be greater in the group of participants who died of pneumonia than in the other groups. Therefore, the prevalence of anaerobic bacteria might influence the incidence and prognosis of aspiration pneumonia.

The number of Candida species on the lingual surface tended to be higher in those who died of pneumonia than in other participants in this study. Generally, Candida species in the oral cavity increase in number when the immuno-competence of the host is weak (Dreizen, 1984); therefore, the higher numbers of Candida species in those who died of pneumonia might have been associated with reduced host immunocompetence, which influences resistance against virulent bacteria.

Aspiration pneumonia tends to recur and is related to cerebral infarction, which may disrupt swallowing function (Yamaya et al., 2001). In our study, a history of cerebrovascular disease was significantly correlated with pneumonia mortality, but it was not an independent predictor of pneumonia mortality risk in the multivariate Cox model. Furthermore, neither pneumonia history nor swallowing function was significantly related to pneumonia mortality in this study, possibly because the participants may have been in better health than the high-risk elderly population living in nursing homes. Most individuals were capable of participating in the examinations independently.

In conclusion, a higher number of teeth with a probing pocket depth exceeding 4 mm was an independent predictor of mortality from pneumonia in a Japanese population of 80-year-olds. Therefore, pneumonia mortality in the elderly may be related to poor oral health, with a prevalence of periodontal diseases.


   ACKNOWLEDGMENTS
 
This work was supported by a research grant from the 8020 Promotion Foundation (T.T.) and by Grants-in-Aid (B) 15390655 (Y.T.) and (C) 16592029 (M.F.) from the Ministry of Education, Culture, Sports, and Technology of Japan.


   FOOTNOTES
 
A supplemental appendix to this article is published electronically only at http://jdr.iadrjournals.org/cgi/content/full/87/4/334/DC1.

Received for publication March 12, 2007. Revision received November 6, 2007. Accepted for publication January 14, 2008.


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 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Journal of Dental Research, Vol. 87, No. 4, 334-339 (2008)
DOI: 10.1177/154405910808700418
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