Abstract
Background/purpose
Previous studies have shown the relationship between individual oral health conditions and mortality; however, the relationship between mortality and multiple oral health conditions has not been examined. This study investigates the link between individual oral health problems and oral comorbidity and mortality risk.
Materials and methods
Data are derived from the National Health and Nutrition Examination Survey 1999–2004, which is linked to the National Death Index for mortality follow-up through 2006. We estimated the risk of mortality among people with three individual oral health conditions—tooth loss, root caries, and periodontitis as well as with oral comorbidity—or having all three conditions.
Results
Significant tooth loss, root caries, and periodontal disease were associated with increased odds of dying. The relationship between oral health conditions and mortality disappeared when controlling for sociodemographic, health, and/or health behavioral indicators. Having multiple oral health problems was associated with an even higher rate of mortality.
Conclusion
Individual oral health conditions—tooth loss, root caries, and periodontal disease—were not related to mortality when sociodemographic, health, and/or health behavioral factors were considered, and there was no differential pattern between the three conditions. Multiple oral health problems were associated with a higher risk of dying.
Keywords: comorbidity, mortality, oral health conditions
Introduction
Although oral health conditions are not viewed by the general population as life-threatening conditions, poor oral health has been shown to be strongly associated with subsequent mortality.1–7 Tooth loss is thought to be indirectly related to higher mortality by causing poor nutrition and poor eating behavior.8 Dental caries and periodontitis are hypothesized to contribute to a proinflammatory state, which accelerates the atherosclerotic process and leads to coronary heart disease.9 Some researchers propose that poor oral health is related to mortality because oral health problems and cardiovascular diseases often share a commonality of risk factors, such as age, low socioeconomic status, and smoking10; thus, the relationship is, in fact, spurious. Other possible explanations that support the relationship between poor oral health and mortality include neglect of oral hygiene, less use of dental care services/treatment among people who are sick or disabled,11,12 and adverse effects of certain diseases or treatments such as cancer and chemotherapy on oral health.13
Although various explanations have been proposed to substantiate the relationship between oral health and mortality, previous studies have focused on examining the relationship between a single indicator of oral health or a composite indicator of oral health and mortality. Although in some cases oral health conditions may share underlying causes such as poor oral hygiene and poor oral habits (i.e., tooth loss generally starts with dental caries or periodontal disease), oral health conditions may vary in their etiology. Thus, different oral health conditions may be linked to mortality differently. Hence, it is important to understand whether individual oral health conditions are differentially related to mortality.
The association of multiple oral health conditions with mortality may be greater than the sum of the individual conditions, or multiple conditions may interact with each other in a manner that is multiplicative. The influence on mortality, of having multiple oral health conditions or oral comorbidity has not been examined. Comorbidity of health conditions is common in the aging population, and many studies have shown the effect of increased levels of comorbidity on adverse health outcomes, including mortality. 14 It is possible that there is a similar “comorbidity” effect for oral health conditions and mortality; however, to date, there is no existing research on this subject.
Race/ethnicity, education, chronic health conditions, and health behaviors, such as obesity and smoking, have been identified as confounders in the relationship between oral health conditions and mortality15–20; therefore, they were included in this study. This research sought to examine the relationship between three different oral health conditions (tooth loss, tooth decay, and periodontitis) and mortality to determine how oral health conditions were individually and jointly related to mortality in the U.S. population.
Materials and methods
Data were taken from the National Health and Nutrition Examination Survey (NHANES) (1999–2004). This contrasts with many prior studies linking oral health and mortality, in which an unrepresentative group, such as cardiovascular patients or individuals with diabetes, formed the analytic sample.1,5,21 NHANES is a series of cross-sectional studies representative of the civilian, noninstitutionalized population of the United States. NHANES is an ongoing study that collects and releases data for 2-year periods. To have sufficient sample size for analysis, we pooled the data from the periods 1999–2000, 2001–2002, and 2003–2004. The data are well suited to the current study because they contain information from a detailed dental examination and are linked to the National Death Index for mortality follow-up through 2006. Data from this period are used for three additional reasons: the oral health measures of interest are available in these years, subsequent waves do not contain information on periodontitis, and later data are not yet linked to mortality data. The analytic sample included 5588 persons aged 40 years and older with information on all three oral health outcomes. Mortality was traced up to 7 years from the date of examination through 2006. Those who died from accidents or violence were excluded from the sample, as we would not expect this mortality to be related. About 6.0% (N = 334) of sample persons died during this period.
We measured oral health using three separate dichotomous indicators: (1) significant loss of permanent teeth, (2) presence of root caries, and (3) presence of periodontitis. We classified people into two groups based on the number of permanent teeth: 0–15 teeth or 16 or more teeth. Presence of root caries was defined as having root caries on any surface examined. Periodontitis in this study was measured using the case definition for periodontitis developed by the CDC Periodontal Disease Surveillance Work-group.22 Respondents with severe (≥2 interproximal sites with loss of attachment ≥6 mm and ≥1 interproximal sites with pocket depth ≥5 mm) or moderate (≥2 interproximal sites with loss of attachment ≥4 mm or ≥2 interproximal sites with pocket depth ≥5 mm) periodontitis were coded as having periodontitis.
We first showed the descriptive statistics indicating the extent of oral health problems and other characteristics of the sample. Then, we estimated the risk of dying within 7 years for those with different oral health conditions using multiple logistic regression models. The first model regressed mortality on each oral health measure and age and gender (Model 1), then a series of variables that were likely to be linked to both mortality and oral health conditions were introduced in subsequent models (Models 2–4) as follows: fewer years of formal education (≤11 years) and race/ethnicity (non-Hispanic black and Hispanic, with non-Hispanic white as the reference group) (Model 2); other health conditions that might be related to oral health, including the prevalence of four chronic conditions [heart disease, diabetes, stroke, and cancer (except skin cancer)] (Model 3); health behaviors that might be linked to oral health, including being obese (body mass index greater than or equal to 30), and being a current smoker (Model 4). In the final model (Model 5), all variables were entered together. Adding these variables sequentially into the model allows us to determine how much of the difference in mortality by oral health status was independent of inclusion of these other known risk factors for mortality.
Using the results of the equations to predict mortality by oral health status, we plotted the mortality curves by age to illustrate the extent to which specific oral health conditions and a combination of these conditions are associated with mortality.
Results
Table 1 shows the weighted sample characteristics. About half of the study population was female (50.9%), and about 3.81% of the sample died between 1999 and 2006. About 2% had heart disease or stroke, whereas about 9% and 10% had diabetes and cancer, respectively.
Table 1.
Sample characteristics for demographic and oral and other health measures in NHANES 1999–2004 (N = 5588): weighted percent and mean presented.
| Mean age (y) | 53.92 (SD = 16.61) |
|---|---|
| % Female | 50.93% |
| % Died | 3.81% |
| % Fewer teeth (≤15) | 13.35% |
| % Root caries | 11.68% |
| % Periodontal disease | 12.67% |
| Mean number of oral conditions (0–3) | 0.47 (SD = 0.73) |
| % Heart disease | 2.44% |
| % Stroke | 2.14% |
| % Diabetes | 8.55% |
| % Cancer | 10.08% |
SD = standard deviation.
The prevalence of each of the oral health conditions was fairly similar: 13.35% had significant tooth loss, 11.7% had the presence of root caries, and periodontal disease was present in 12.7% of the sample.
The results of logistic regression models to predict the relationship between oral health conditions and mortality are shown in Tables 2–4. Each oral health indicator is shown in a separate table. The odds ratios (ORs) indicate the relative likelihood of dying. We first looked at how having lost a significant number of teeth was related to mortality (Table 2). Having fewer teeth was linked to increased odds of dying when controlling for only age and gender (OR = 1.74) (Model 1). When variables including sociodemographic, health indicators, and health behavior variables were added to the models (Models 2–4), the effect of having fewer teeth on mortality remained significant but was reduced. In the final model, with all potential explanatory variables included, the effect was no longer significant.
Table 2.
Odds ratios (95% confidence intervals) for the association between having missing teeth and mortality: NHANES 1999–2004.
| Model 1 | Model 2 | Model 3 | Model 4 | Model 5 | |
|---|---|---|---|---|---|
| Age | 1.09* (1.08–1.10) | 1.09* (1.08–1.10) | 1.08* (1.07–1.09) | 1.10* (1.09–1.12) | 1.09* (1.08–1.11) |
| Female | 0.53* (0.40–0.70) | 0.53* (0.40–0.70) | 0.57* (0.43–0.76) | 0.56* (0.42–0.75) | 0.61* (0.46–0.83) |
| Fewer teeth | 1.74* (1.28–2.37) | 1.54* (1.12–2.12) | 1.68* (1.23–2.31) | 1.52* (1.10–2.09) | 1.34 (0.96–1.88) |
| Low education | 1.58* (1.13–2.19) | 1.50* (1.06–2.11) | |||
| Black | 1.61* (1.04–2.50) | 1.62* (1.03–2.55) | |||
| Hispanic | 0.97 (0.58–1.61) | 0.97 (0.56–1.68) | |||
| Heart disease | 1.80* (1.07–3.02) | 2.02* (1.19–3.44) | |||
| Diabetes | 1.90* (1.32–2.73) | 1.65* (1.12–2.45) | |||
| Stroke | 1.88* (1.06–3.34) | 1.79 (0.98–3.26) | |||
| Cancer | 1.65* (1.17–2.32) | 1.80* (1.26–2.58) | |||
| Obese | 1.32* (0.97–1.80) | 1.22 (0.88–1.68) | |||
| Smoking | 3.27* (2.29–4.66) | 3.24* (2.26–4.65) | |||
| N | 5588 | 5581 | 5588 | 5492 | 5456 |
| −2 Log likelihood | 1649.96 | 1632.78 | 1603.07 | 1534.88 | 1475.13 |
P < 0.05
NHANES = National Health and Nutrition Examination Survey.
Table 4.
Odds ratios (95% confidence intervals) for the association between periodontal disease and mortality: NHANES 1999–2004.
| Model 1 | Model 2 | Model 3 | Model 4 | Model 5 | |
|---|---|---|---|---|---|
| Age | 1.09* (1.08–1.10) | 1.09* (1.08–1.10) | 1.08* (1.07–1.09) | 1.10* (1.09–1.12) | 1.09* (1.08–1.11) |
| Female | 0.55* (0.42–0.73) | 0.55* (0.41–0.73) | 0.60* (0.45–0.81) | 0.58* (0.43–0.78) | 0.63* (0.47–0.85) |
| Periodontal disease | 1.57* (1.14–2.17) | 1.41* (1.01–1.95) | 1.64* (1.18–2.27) | 1.36 (0.97–1.90) | 1.30 (0.92–1.84) |
| Low education | 1.60* (1.15–2.23) | 1.51* (1.07–2.13) | |||
| Black | 1.66* (1.07–2.57) | 1.63* (1.04–2.58) | |||
| Hispanic | 0.96 (0.58–1.60) | 0.96 (0.56–1.67) | |||
| Heart disease | 1.73* (1.03–2.91) | 2.01* (1.18–3.42) | |||
| Diabetes | 1.99* (1.39–2.86) | 1.70* (1.15–2.51) | |||
| Stroke | 1.96* (1.10–3.48) | 1.80 (0.99–3.30) | |||
| Cancer | 1.68* (1.19–2.37) | 1.83* (1.28–2.62) | |||
| Obese | 1.34 (0.98–1.83) | 1.24 (0.90–1.71) | |||
| Smoking | 3.33* (2.34–4.76) | 3.24* (2.25–4.66) | |||
| N | 5588 | 5581 | 5558 | 5492 | 5456 |
| −2 Log likelihood | 1654.58 | 1635.72 | 1604.69 | 1537.99 | 1475.82 |
P < 0.05.
NHANES = National Health and Nutrition Examination Survey.
Next, we examined the association between root caries and mortality (Table 3); those with root caries were more likely to die than those with no decay (OR = 1.75) (Model 1, Table 3). The effect remained, albeit reduced, with the inclusion of sociodemographic variables (Model 2). When indicators of other health states were included (Model 3), the effect increased; when smoking was considered, the effect was no longer significant (Models 4 and 5).
Table 3.
Odds ratios (95% confidence intervals) for the association between root caries and mortality: NHANES 1999–2004.
| Model 1 | Model 2 | Model 3 | Model 4 | Model 5 | |
|---|---|---|---|---|---|
| Age | 1.09* (1.08–1.10) | 1.09* (1.08–1.10) | 1.08* (1.07–1.09) | 1.11* (1.09–1.12) | 1.09* (1.08–1.11) |
| Female | 0.55* (0.41–0.72) | 0.54* (0.41–0.72) | 0.60* (0.45–0.79) | 0.58* (0.43–0.77) | 0.63* (0.46–0.84) |
| Root caries | 1.75* (1.23–2.49) | 1.51* (1.05–2.18) | 1.77* (1.24–2.53) | 1.41 (0.98–2.04) | 1.29 (0.88–1.89) |
| Low education | 1.60* (1.15–2.23) | 1.52* (1.08–2.15) | |||
| Black | 1.60* (1.03–2.50) | 1.61* (1.02–2.54) | |||
| Hispanic | 0.97 (0.58–1.61) | 0.96 (0.56–1.67) | |||
| Heart disease | 1.79* (1.07–3.02) | 2.05* (1.20–3.48) | |||
| Diabetes | 1.98* (1.38–2.84) | 1.70* (1.15–2.51) | |||
| Stroke | 1.91* (1.07–3.41) | 1.78 (0.97–3.25) | |||
| Cancer | 1.67* (1.19–2.36) | 1.82* (1.27–2.61) | |||
| Obese | 1.32 (0.97–1.80) | 1.22 (0.89–1.69) | |||
| Smoking | 3.36* (2.36–4.79) | 3.28* (2.28–4.71) | |||
| N | 5588 | 5581 | 5558 | 5492 | 5456 |
| −2 Log Likelihood | 1652.90 | 1634.95 | 1603.89 | 1537.92 | 1476.43 |
P < 0.05.
NHANES = National Health and Nutrition Examination Survey.
Periodontal disease was also related to mortality (OR = 1.57) (Model 1, Table 4). As in the case for root caries, the effect of periodontal disease on mortality was reduced but remained significant with the inclusion of education and race/ethnicity. However, the effect of periodontal disease became insignificant with the inclusion of health behaviors (Models 4 and 5). Smoking was the most significant factor mediating the relationship between periodontal disease and death.
The results show that the strength of the association of oral health status and mortality differs by oral condition and is differently affected by controls for other variables. Although all oral health conditions examined here were related to mortality when only age and gender were controlled, the effect disappeared for root caries and periodontal disease when other sociodemographic variables and health behavior were included, respectively; the effect disappeared for tooth loss when all factors were considered. The relationship between root caries or periodontal disease to mortality appeared to be mainly through their joint links to smoking as a confounder.
Next, we examined the estimated probability of dying within the 7-year follow-up period by using the equations generated from the logistic regression equations that characterized people with each indicator of poor oral health (Fig. 1). Having fewer teeth was linked to higher mortality as compared to the other two oral conditions. Given that periodontal disease and root caries often result in loss of teeth, it was expected that having fewer teeth would be related to higher mortality than the other two oral health conditions. However, when an individual had all three oral health conditions, the mortality curve dramatically increased as he/she aged, whereas the mortality curves increased more slowly with age for those with no oral health problems. The shape of the mortality curve was similar for males and females, with a much lower overall mortality rate for females. Our analysis demonstrated a higher rate of mortality among people with multiple oral health conditions.
Figure 1.
Probability of dying in 7 years among those with oral health conditions.
Discussion
This study demonstrated that poorer oral health conditions were associated with higher mortality, but they were not associated with mortality when sociodemographic, health, and health behavior factors were considered. This means that the association of oral health and mortality largely arises from the association of oral health with these other factors.
The results showed that contrary to expectations, the association with mortality was similar for the three measures of oral health. It is possible that the three oral health conditions share underlying causes such as poor oral hygiene and poor oral care habits that may override any differential effects on mortality. The presence of one problem may lead directly or indirectly to another, thus relating to mortality in similar ways. At the same time, the lack of significant relationships between oral health problems and mortality with additional control variables may indicate that poor oral health is a marker or indicator of overall poor health status and/or poor health behaviors.
This study demonstrated that the presence of multiple oral health conditions was linked to even higher likelihood of mortality. Although we used cross-sectional data in a synthetic cohort limiting the interpretation of our results on age differences, the results nevertheless imply that the effect of having multiple oral health conditions may be more than the sum of the effect of each oral health condition. Further study of the role of comorbid oral conditions, for example, using severity measures for oral conditions by combining them into comorbidity indices, may provide us with a clearer understanding of the link between multiple oral conditions and mortality. It is critical to understand how having multiple oral health conditions may be another indicator of how certain groups of underprivileged or “dental care service inaccessible” people are at higher risk of mortality.
Because our focus was on the relationship between oral health conditions and mortality, we determined that the variables we examined could, in fact, explain the relationship between oral health conditions and mortality as confounders. Having heart disease, diabetes, and cancer appeared to be linked to both oral health conditions and death, as the literature has shown. The association with cancer was expected, given previous studies linking periodontal disease and cancer.23 All oral health conditions examined here are associated with inflammatory and infectious mechanisms, as well as with cardiovascular disease. It is possible that if severe dental caries are not treated, they can result in bacteria and blood infections, which can cause periodontitis, tooth loss, and/or death.24 Although further clinical research is needed to fully describe the mechanisms linking oral health conditions to mortality, we note that oral health conditions at the beginning can be easily prevented or treated with appropriate individual dental habits and public practice. The value of improving personal oral hygiene can be addressed through educational interventions.
In our study, smoking was found to explain a good part of the link between mortality and oral health conditions, particularly between mortality and root caries and periodontal disease. This makes sense given the previously reported effects of smoking on oral health, such as increased susceptibility to periodontitis25 and higher risk for oral cancer.26,27 Although our study focused on examining the relationship between mortality and different types of oral health conditions and oral comorbidity, further study on the role of specific mechanisms relating different oral health conditions and mortality is needed, particularly longitudinal work that can address the mediating influence of these mechanisms. This is crucial because the differential etiologies behind specific oral health conditions indicate different strategies for treatment and prevention.
Acknowledgments
This work was supported by the National Institutes of Health, National Institute of Dental & Craniofacial Research (1 R21 DE019950-02).
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