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Periodontal disease and systemic diseases in an older population
Archives of Gerontology and Geriatrics 59 (2014) 474–479
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Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Periodontal disease and systemic diseases in an older population ¨ zgu¨n O ¨ zc¸aka a,*, Sema Becerik a, Nurgu¨n Bıc¸akcı a, Asuman H. Kiyak b O a b
University of Ege, School of Dentistry, Department of Periodontology, I˙zmir, Turkey University of Washington, School of Dentistry, Department of Oral and Maxillofacial Surgery, Seattle, WA, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 15 February 2011 Received in revised form 26 May 2014 Accepted 28 May 2014 Available online 12 June 2014
Objective: To evaluate the relationship between older adults’ medical and oral conditions and their selfreports of periodontal conditions with clinically obtained data. Background: Concerns about oral health of elders and its association with systemic diseases have been gaining more attention. Methods: A total of 201 older subjects were interviewed about their previous medical and dental histories and were asked to complete a health questionnaire. Each subject received full mouth exam, including counting number of natural teeth remaining, gingival (GI) and plaque index (PI), CPITN and denture status. Results: Elders who completed health questionnaires had mean age of 62.5. Mean CPITN score was 1.62(1.12), PI was 1.57(1.48), and GI was 1.55(1.31). Women had higher prevalence of CVD and osteoporosis than men (p = 0.008, p = 0.0001, respectively). Subjects who reported bleeding upon brushing had higher PI and GI scores (p = 0.03, p = 0.05, respectively). Smokers were more likely to describe their periodontal tissues as unhealthy (72.3% vs. 27.7%, p = 0.01), whereas self-reports of healthy vs. unhealthy gums did not differ between non-smokers. Conclusion: These findings suggest that a number of systemic conditions are associated with indicators of periodontal disease, and self-reports of oral conditions are independent of systemic diseases. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Systemic diseases Smoking Periodontitis Self-reports Older adults
1. Introduction Concerns about the oral health status of older persons have been gaining attention in both developing and developed countries in the last decades as this population has increased, and as more elders retain their natural teeth. As with other countries, Turkey’s aging population is increasing and more of them are keeping their teeth. Older persons have more chronic conditions and use more medications than younger populations. On the other hand, economically and socially disadvantaged older adults and those with disabilities are more likely to experience tooth loss and have a greater risk for caries and periodontal diseases (Unluer, Gokalp, & Dogan, 2007). Inflammatory periodontal diseases exhibit an association with multiple systemic conditions. Although the evidence is correlational, patients who suffer from certain systemic diseases tend to be at greater risk for periodontal. Currently, there is
* Corresponding author at: Ege University, School of Dentistry, Department of Periodontology, 35100 Bornova, I˙zmir, Turkey. Tel.: +90 535 279 01 00; fax: +90 232 388 03 25. ¨. O ¨ zc¸aka). E-mail address: [email protected] (O http://dx.doi.org/10.1016/j.archger.2014.05.011 0167-4943/ß 2014 Elsevier Ireland Ltd. All rights reserved.
a lack of consensus among experts on the nature of these associations and confusion among health care providers and the public on how to interpret this rapidly growing body of science. The local and systemic effects of periodontal infections and inflammation are usually exerted for many years, typically among those who are middle-aged or older. Numerous epidemiological associations linking chronic periodontitis to age-associated and biologically complex conditions such as diabetes, cardiovascular disease, osteoporosis, respiratory diseases, rheumatoid arthritis, certain cancers, erectile dysfunction, kidney disease and dementia, have been reported (Otomo-Corgel, Pucher, Rethman, & Reynolds, 2012). The progression of periodontal disease is influenced by variety of factors like microorganisms, host response, systemic background, and genetic makeup of the host. Amongst them, diabetes mellitus tops the list. Diabetes and periodontitis influence the clinical outcome of each other and control of both influences the clinical improvement of each (Daniel, Gokulanathan, Shanmugasundaram, Lakshmigandhan, & Kavin, 2012). Subjects with diabetes mellitus are 2.8 times more likely to have destructive periodontal disease (Emrich, Schlossman, & Genco, 1991) and 4.2 times more likely to have significant alveolar bone loss (Taylor, Burt, Becker, Genco, & Shlossman, 1998) compared to systemically healthy subjects.
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Williams (2008) reviewed the literature that demonstrates a link between cardiovascular disease and periodontal disease, while Cronin (2009) concluded that periodontal disease is a risk factor for CVD. Pihlstrom (2001) includes osteoporosis among the diseases associated with periodontal disease. In fact, a longitudinal follow-up of community-dwelling older adults enrolled in a clinical trial found that decline in periodontal status over five years was best predicted by osteoporosis and ethnicity (greater among whites and African Americans, less among Asian Americans) (Swoboda, Kiyak, Darveau, et al., 2008). Early systematic reviews and a definitive controlled clinical trial indicate that intensive periodontal therapy can reduce systemic inflammation (Tonetti, 2009). Although the average lifespan in most western societies is increasing, both systemic and oral health deteriorates with aging, and can reduce quality of life, even while life span expands thanks to modern medicine (Crimmins & Beltra´n-Sa´nchez, 2011; Mombelli, 1998). Hence, it is not surprising that the leading cause of death has shifted from infectious to chronic diseases. It is therefore important to examine and identify risk factors; including age, gender, smoking and medical conditions, that may have an impact on oral health and treatment needs. The objectives of the present study were to assess: (a) the associations between systemic and oral conditions, and (b) older adults’ self-reports of periodontal conditions vs. clinically obtained data. The following hypotheses were tested: 1. Older males and females differ in their profile of systemic diseases and periodontal conditions. 2. Older adults with certain systemic diseases have signs of periodontal disease. 3. Older adults can accurately report periodontal conditions that are observable (i.e. healthy gums, bleeding upon brushing, teeth mobility). 4. Older adults with certain systemic diseases and who smoke are report more periodontal problems.
2. Materials and methods 2.1. Sample A total of 201 older subjects from western Turkey participated, completing oral health assessments and health histories, and providing information on their demographic backgrounds. They were identified from adults who were patients of record at Ege University School of Dentistry. Subjects older than 55 years were included to the study. Data were collected from these patients over a period of 15 months between March 2008 and May 2009. Edentulous subjects were excluded. Eligible subjects gave written informed consent in accordance with the Helsinki Declaration. The study protocol was approved by the Ethics Committee of the Medical Faculty of Ege University. 2.2. Health history All subjects were interviewed about their previous medical and dental histories, and were asked to complete a health questionnaire, which was then reviewed by project dentists. The validity of this information was confirmed by reviewing subjects’ national health insurance records, and correcting self-reports of systemic diseases and medications as needed.
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Based on the literature review presented above, diseases of interest in this study are: CVD, hypertension, diabetes, osteoporosis, high cholesterol, and kidney diseases. For each of these conditions, if the subject reported the condition, they were asked if they were currently using a medication for that condition. 2.3. Smoking habits Because smoking habits have been associated with periodontal disease, all enrolled subjects were questioned about this behavior. They were asked if they had (1) never smoked, (2) quit smoking and when, or (3) if they were still smoking. Also, for current and former smokers, we asked the duration of smoking and number of cigarettes smoked per day. 2.4. Oral assessments The oral examinations were performed by two experienced ¨ .O ¨ . and S.B.). The inter-examiner agreement for periodontists (O the measurement of clinical periodontal status showed good reliability, with an inter-examiner reliability coefficient alpha of 0.81. Each subject received a full mouth intraoral examination. Examiners also recorded the number of remaining teeth and dentures. Six sites per tooth were assessed in the mesiobuccal (MB), midbuccal (B), distobuccal (DB), distolingual (DL), midlingual (L), and mesiolingual (ML) sites. Measurements of GI (Silness & Lo¨e, 1964) and PI (Lo¨e & Silness, 1963) scores on six Ramfjord teeth (right maxillary first molar, left maxillary central incisor, left maxillary first premolar, left mandibular first molar, right mandibular central incisor and right mandibular first premolar) were recorded. If any of these six teeth was missing, we assessed the opposing tooth, or if that tooth was also missing we examined one of the adjacent teeth. The full mouth recordings of probing depth (six sites per tooth) were also made and used for the assignment of sextant-based CPITN scores (Ainamo & Ainamo, 1985). 2.5. Self-reports of oral health In addition to the clinical indicators of periodontal disease and missing teeth, we asked subjects if they had the following observable conditions: 1. Do your gums bleed when you brush? Yes/No 2. Are your teeth mobile? Yes/No 3. Are your gums healthy? Yes/No
3. Statistical analysis The relevant data from patient surveys were collected and recorded on a pre-established spreadsheet using a code book with specific diseases, medications and oral conditions listed. A frequency distribution was created for each of the systemic diseases and medications. Descriptive statistics including frequencies, means, standard deviations, and ranges were conducted, using the SAS statistical program (SAS statistic software, version 8.2 (SAS Institute, Cary, NC). In order to test the four hypotheses proposed above, we conducted a series of t-tests, chi square tests and Mann–Whitney U tests. To test the first hypothesis, chi square tests were conducted to assess the association between gender and systemic diseases to determine not just associations between and rates of disease, but also the direction of any observed differences. T-tests were used to compare men and women on their clinical oral health status, and
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chi square tests to assess the association between gender and self-reports of periodontal status. In testing the second hypothesis, we compared the oral health of elders with and without the systemic diseases listed above, and those who used or did not use medications for these diseases. Ranges and standard deviations of clinical periodontal parameters were analyzed by Mann–Whitney U test and logistic regression analyses to adjust for age, sex and smoking using presence/ absence of disease were performed. The third hypothesis was intended to test the validity of self-reports of observable oral health. A series of t-tests were conducted to determine if subjects with bleeding upon brushing, with mobile teeth and with self-perceived healthy periodontal tissue differed on GI, PI, CPITN scores and on missing teeth from their counterparts who reported no bleeding, no mobile teeth and whose self-reported periodontal health was poor. The fourth hypothesis focused on the link between smoking, systemic diseases and self-reported periodontal disease. Chi square tests were used to test the association between this latter variable, systemic diseases and smoking. 4. Results Table 1 illustrates the demographic, periodontal and systemic disease status of all 201 subjects. Note that some subjects had missing data, particularly on the clinical periodontal measures. As shown, the sample ranged from age 55–83, with a mean age of 62.5. The majority (64.7%) were men. Although CPITN, PI and GI scores ranged up to 3.5, mean scores on those clinical periodontal parameters were in the lower range (mean = 1.62, 1.57, 1.55, respectively), indicating relatively low periodontal disease rates, but with considerable variance across patients). On average, this sample was missing 7.38 teeth, ranging from 0 to 25. The prevalence of systemic diseases in this sample was relatively low.
Table 2 Gender differences in disease frequencies.
CVD (%) Diabetes mellitus (%) Hypertension (%) Cholesterol (%) Osteoporosis (%) Kidney disease (%) a
% Total with disease
Females N = 71
Males N = 130
P value
24.4 13.9 43.8 26.4 16.4 6
35.21 11.26 47.88 30.98 36.61 1.40
18.46 15.38 41.53 23.85 5.38 8.46
0.008a 0.42 0.39 1.27 <0.0001a 0.06
Significant difference.
Men and women also were compared on clinical indicators of oral health. Their CPITN scores were significantly different (p = 0.01), with higher scores for men. Men were almost twice as likely to use dentures as did women (66% vs. 34%, p = 0.001). Men had slightly more missing teeth on average (6.87 vs. 7.68), but this difference was non significant. Not surprisingly, women were far more likely to report never having smoked (60.6%), whereas men were more likely to be current or past smokers (59.2%), resulting in a significant association between smoking and gender (p = 0.025). 4.2. Hypothesis 2 The second hypothesis posited that older adults with certain systemic diseases will have more objective signs of periodontal disease and tooth loss than adults without these diseases. The Odds Ratio and 95% CI of the CVD, hypertension, osteoporosis and diabetes mellitus shown in Table 4. CPITN and number of missing teeth were unrelated to any systemic disease. The only class of drugs associated with oral status was antihypertensives; subjects who used these medications had slightly more missing teeth (p = 0.05).
4.1. Hypothesis 1 4.3. Hypothesis 3 This hypothesis stated that older males and females differ in their profile of systemic diseases and periodontal conditions, such that older men were expected to have higher rates of CVD and hypertension, whereas older women were more likely to have osteoporosis. Women were also expected to have fewer teeth (i.e. more missing teeth) than men. Tests of this hypothesis revealed some associations between gender and systemic diseases. As shown in Table 2, women had a higher prevalence of CVD (p = 0.008), contrary to the hypothesis. They also had higher rates of osteoporosis, as hypothesized (p = 0.0001). Men had six times the rate of kidney disease as women, but because of low prevalence rates overall, this difference only approached significance (p = 0.06) (Table 3).
The third hypothesis focused on the association between selfreports and clinical indicators of periodontal disease. Older adults were expected to accurately report periodontal conditions that are observable (i.e. healthy gums, bleeding upon. brushing, loose teeth). As shown in Table 5, observed differences were in the predicted direction. Subjects who reported bleeding upon brushing had higher PI and GI scores (p = 0.03, 0.05 respectively). Those who reported mobility had worse PI scores (p = 0.02) but did not differ on GI scores. However, self-reports of healthy vs. unhealthy gums were unrelated to clinical periodontal measures. CPITN was unrelated to any of the self-reported measures.
Table 1 Descriptive data.
Table 3 Sex differences on clinical periodontal measurements (mean SD).
Age CPITN PI GI
N
Range
Mean SD
201 186 185 186
55–83 0.43–3.47 0–3.33 0.08–3.0
62.5 3.8 1.62 1.12 1.57 1.48 1.55 1.31
Systemic diseases
N
% with disease
CVD Diabetes Hypertension Osteoporosis Cholesterol Kidney disease
49 28 88 33 53 12
24.4 13.9 43.3 16.4 26.4 6.0
Age (year) CPITN GI PI Missing teeth Dentures Yes (%) No (%) Smoking (%) Never Former Current
Females N = 71
Males N = 130
P value
62.23 4.86 1.49 0.56 1.54 0.53 1.62 0.71 6.87 6.41
62.65 5.31 1.69 0.51 1.56 0.54 1.54 0.60 7.68 6.26
0.57 0.01 0.88 0.43 0.40
34.15 65.85
63.86 36.14
0.001
60.56 18.31 21.13
40.77 30.00 29.23
0.025
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Table 4 Clinical assessment and systemic diseases (median SD).
CVD
With/without OR [%95 CI] With/without OR [%95 CI] With/without OR [%95 CI] With/without OR [%95 CI]
Hypertension Diabetes Mellitus Osteoporosis
CPITN
PI
GI
1.63 0.55/1.59 0.52 0.77 [0.41–1.46] 1.68 0.54/1.55 0.52 1.41 [0.81–2.45] 1.57 0.66/1.60 0.51 1.09 [0.48–2.48] 1.51 0.53/1.59 0.54 0.83 [0.41–1.71]
1.41 0.75/1.50 0.60 0.88 [0.52–1.49] 1.58 0.67/1.50 0.61 1.28 [0.81–2.02] 1.45 0.52/1.50 0.66 0.88 [0.45–1.76] 1.58 0.77/1.50 0.60 2.05 [1.11–3.78]
1.40 0.53/1.70 0.53 0.53 [0.28–1.01] 1.95 0.52/1.50 0.54 1.75 [0.99–3.09] 1.54 0.46/1.70 0.55 0.80 [0.36–1.79] 1.52 0.53/1.66 0.53 1.02 [0.50–2.08]
Corrected age, sex, smoking.
4.4. Hypothesis 4 Based on the previous literature, we hypothesized that older adults with certain systemic diseases and who smoke would be more likely to report periodontal problems. As shown in Table 6, we found the opposite results, suggesting that self-reports of oral conditions are independent of systemic diseases. Subjects with CVD, hypertension and high cholesterol were significantly less likely to report problems with tooth mobility. Self-reports of bleeding with brushing were related only to kidney diseases. Bleeding was reported by 75% of subjects with kidney diseases (p = 0.01), despite the fact that very few subjects in this sample had kidney diseases. In response to the question about healthy periodontal tissue, the majority again reported healthy gums, but only on hypertension and anti-hypertensive medications were these significant (p = 0.002 and p = 0.006 respectively). Elders with hypertension were more likely to report healthy gums (58%) than those without hypertension, as were those using antihypertensives (57%). This was in contrast to the objective assessments reported above; GI scores were higher among those with hypertension, and those using antihypertensives were missing more teeth. The same pattern emerged for smoking vs. tooth mobility. The majority of smokers were highly likely to report no mobility, at even higher rates than non-smokers (82% vs. 64%, respectively; p = 0.03). On the other hand, almost three times more elders who smoked reported unhealthy gums (72.3%, p = 0.01), whereas selfreports of healthy vs. unhealthy gums did not differ between nonsmokers. 5. Discussion Periodontitis is generally a chronic disorder characterized by the breakdown of the tooth supporting tissues and impaired host inflammatory immune response. This condition is due fundamentally to an ecological imbalance between the normal microbial biofilm on teeth and the host tissues (Newman, 1974). There is increasing evidence linking periodontitis to systemic diseases (Kuo, Polson, & Kang, 2008) such as diabetes (Graves, Liu, & Oates, 2007; Herring & Shah, 2006; Preshaw, Foster, & Taylor, 2007) and, especially CVD (Fardi & Papadimitriou, 2007; Ford, Yamazaki, & Seymour, 2007; Paquette, Brodala, & Nichols, 2007); hence the search for factors that may explain such relationships.
This clinical study proposed four hypotheses. First we hypothesized that older men and women differ in their profile of systemic disease and periodontal conditions. When we compared the clinical parameters of periodontal disease in older men and women, they differed only on CPITN scores. Gender differences in the association between number of teeth and hypertension were described in an earlier study (Vo¨lzke, Schwahn, Do¨rr, et al., 2006); our results were in line with another study in the same population showing elevated atherosclerotic risk in younger men with periodontal disease but not in women (Desvarieux, Schwahn, Vo¨lzke, et al., 2004). Likewise, the longitudinal NHANES II data (DeStefano, Anda, Kahn, et al., 1993) yielded a relation of periodontal disease with coronary artery disease and mortality, predominantly in men. In concordance with these findings, another study (Grau, Becher, Ziegler, et al., 2004) demonstrated periodontal disease as a risk factor for ischemic stroke only among males. Contrary to our hypothesis and the literature review above, women in the current study had a higher prevalence of CVD than men. In a recent study Perez et al. stated that women with more severe menopausal symptoms had a greater prevalence of osteoporosis and cardiovascular disease risk factors. In the present study most of women study participants (%56.3) were menopausal women. In this respect contrary to the literature thus they showed higher prevalence of CVD than the men participants (Pe´rez, Palacios, Chavida, & Pe´rez, 2012). Gender differences were also found in rates of osteoporosis, such that women are more likely to have this condition than men (Taguchi, Suei, Ohtsuka, et al., 1999) and therefore extraction may be required due to increased tooth mobility at an earlier stage of periodontitis. Hence, women might not reach a threshold of caries or periodontal disease necessary for the development of vascular consequences (Desvarieux et al., 2004). Table 6 Self-reports of oral conditions and their association with systemic diseases and smoking status.
Systemic disease CVD Hypertension Cholesterol Smoker status Still smoke Never smoke
Table 5 Clinical assessment and self-report (mean score). Self-report
Bleeding/no bleeding Mobility/no mobility NS: not significant.
Clinical assessment: CPITN
PI
P value
NS NS
1.69/1.49 1.76/1.51
0.03 0.02
GI
P value
1.64/1.49 NS
0.05 NS
Systemic disease Hypertension Uses antihypertensive meds Smoker status Still smoke Never smoke
Self-reports: mobility (%)
No mobility (%)
P value
10.2% 16 11.3
89.8% 84.0 88.7
0.01 0.04 0.02
17.7 35.9
82.3 64.2
0.03
Gums healthy (%)
Unhealthy (%)
P value
58 57
42 43
0.002 0.006
27.7 49
72.3 51
0.01
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Possible reasons for non-significant associations between systemic disease and gender may be the relatively small sample size of this survey. In fact, large nationwide epidemiological studies can give the most reliable picture of systemic disease and periodontal diseases in a country; such data are not available in Turkey. The other reason may be the small percentage of older adults with systemic disease; most of the subjects in this study were systemically healthy. This may suggest that the population seeking care at a dental school in Turkey is generally healthier than their peers in the community who do not seek dental care or seek it from private providers. Another possibility is that the mean age of subjects in this study was relatively young and heterogeneous study population. The variation in age is from 55 to 83 years with a mean age of 62.5. They were classified as ‘‘young-old’’ adults and younger old persons differ markedly about persons older old and over, who are more likely geriatric patients. The second hypothesis posited that older adults with systemic disease have more clinical signs of periodontal disease and tooth loss than adults without systemic disease. Although the relationship between periodontal disease and some systemic diseases such as diabetes, CVD and hypertension were stated in the literature, in our results the odds ratios not support the association of these disease. One reason may be the low rates of these diseases Both periodontal disease and hypertension share common social and lifestyle risk factors that influence utilization of dental and medical care services. Recent analyses of a birth cohort demonstrated that low social status predicted both poor oral health and high blood pressure (Poulton, Caspi, Milne, et al., 2002). Besides possible biological mechanisms, differences in pain perception between hypertensive and normotensive adults may further link hypertension to tooth loss. In our results CPITN and number of missing teeth were unrelated to any systemic diseases, including hypertension, but adults who used antihypertensive drugs had slightly more missing teeth. Our third hypothesis focused on the association between selfreports and clinical parameters of periodontal disease. Adults who reported bleeding upon brushing had higher PI and GI scores. Subjects who reported any tooth mobility had worse PI scores but their GI scores were unrelated to tooth mobility. We also hypothesized that adults with systemic diseases and who smoke would report more periodontal problems. Our results supported this hypothesis when periodontal status was defined as ‘‘unhealthy gums’’ but not when elders were asked about the mobility of their teeth. The majority of smokers reported unhealthy gums, but an even larger proportion stated that they had no mobility. This suggests that patients use different criteria to define poor oral health, and that tooth mobility may not be as good an indicator of poor periodontal health as a generalized perception of unhealthy gums. Thompson, Yonke, Rapley, et al. (1999) compared patients’ selfreported medical history responses with their laboratory data, and found that many patients may be unaware of their current and correct medical conditions. In our study, the validity of medical history and drug usage was confirmed by reviewing subjects’ national health insurance records, and correcting self-reports of systemic diseases and medications as needed. It should be noted that this was unnecessary in most cases, with only 2% of subjects omitting information, and 1% erroneously including a disease in their health history. Recognition of the mounting evidence of relationships between oral and systemic health will require future cohorts of dental hygienists, dentists, physicians, nurses, and other healthcare providers to work together. Nowhere is this more important than in the early identification of individuals with systemic diseases such as undiagnosed diabetes and the co-management of the oral and overall health of these patients.
6. Conclusion Determining cause-and-effect mechanisms of periodontal and systemic diseases are more complicated. Although there is a lack of consensus among experts on the nature of these associations and confusion among health care providers. The current evidence regarding the role of periodontal disease in increasing systemic inflammation to suggest that nondental care providers should screen patients for periodontal disease. For both dental and nondental practitioners who embrace the opportunity to become more actively involved in this important arena of healthcare, this new and exciting level of clinical practice is certain to benefit patients and to be professionally rewarding. Source of funding This study has been funded solely by the institutions of the authors. Conflict of interest The authors declare that they have no conflict of interests. Acknowledgement We would like to thank Lingmei Zhou at the University of Washington for conducting all statistical analyses. References Ainamo, J., & Ainamo, A. (1985). Partial indices as indicators of the severity and prevalence of periodontal disease. International Dental Journal, 35, 322–326. Crimmins, E. M., & Beltra´n-Sa´nchez, H. (2011). Mortality and morbidity trends: Is there compression of morbidity? Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 66, 75–86 Review. Cronin, A. (2009). Periodontal disease is a risk marker for coronary heart disease? Evidence-Based Dentistry, 10, 22–25. Daniel, R., Gokulanathan, S., Shanmugasundaram, N., Lakshmigandhan, M., & Kavin, T. (2012). Diabetes and periodontal disease. Journal of Pharmacy and Bioallied Sciences, 4(Suppl. 2), S280–S282. DeStefano, F., Anda, R. F., Kahn, H. S., Williamson, D. F., & Russell, CM. (1993). Dental disease and risk of coronary heart disease and mortality. British Medical Journal, 306, 688–691. Desvarieux, M., Schwahn, C., V—lzke, H., Demmer, R. T., Ldemann, J., Kessler, C., et al. (2004). Gender differences in the relationship between periodontal disease, tooth loss and atherosclerosis. Stroke, 35, 2029–2035. Emrich, L. J., Schlossman, M., & Genco, R. J. (1991). Periodontal disease in non-insulin dependent diabetes mellitus. Journal of Periodontology, 62, 123–131. Fardi, A., & Papadimitriou, D. (2007). Periodontal and atherosclerosis-induced diseases. International Angiology, 26, 197–205. Ford, P. J., Yamazaki, K., & Seymour, G. J. (2007). Cardiovascular and oral disease interactions: What is the evidence? Primary Dental Care, 14, 59–66. Grau, A. J., Becher, H., Ziegler, C. M., et al. (2004). Periodontal disease as a risk factor for ischemic stroke. Stroke, 35, 496–501. Graves, D. T., Liu, R., & Oates, T. W. (2007). Diabetes-enhanced inflammation and apoptosis: Impact on periodontal pathosis. Periodontology 2000, 45, 128–137. Herring, M. E., & Shah, S. K. (2006). Periodontal disease and control of diabetes mellitus. Journal of the American Osteopathic Association, 106, 416–421. Kuo, L. C., Polson, A. M., & Kang, T. (2008). Associations between periodontal diseases and systemic diseases: A review of the inter-relationships and interactions with diabetes, respiratory diseases, cardiovascular diseases and osteoporosis. Public Health, 122, 417–433. Lo¨e, H., & Silness, J. (1963). Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontologica Scandinavica, 21, 533–551. Mombelli, A. (1998). Aging and the periodontal and peri-implant microbiota. Periodontology 2000, 16, 44–52 Review. Newman, H. N. (1974). Diet, attrition, plaque and dental disease. British Dental Journal, 136, 491–497. Otomo-Corgel, J., Pucher, J. J., Rethman, M. P., & Reynolds, M. A. (2012). State of the science: Chronic periodontitis and systemic health. Journal of Evidence-Based Dental Practice, 12(3 Suppl.), 20–28. Paquette, D. W., Brodala, N., & Nichols, T. C. (2007). Cardiovascular disease, inflammation, and periodontal infection. Periodontology 2000, 44, 113–126. Pe´rez, J. A., Palacios, S., Chavida, F., & Pe´rez, M. (2012). Severity of menopausal symptoms and cardiovascular and osteoporosis risk factors. Climacteric, 8 http://dx.doi.org/10.3109/13697137.2012.688077
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Archives of Gerontology and Geriatrics journal homepage: www.elsevier.com/locate/archger
Periodontal disease and systemic diseases in an older population ¨ zgu¨n O ¨ zc¸aka a,*, Sema Becerik a, Nurgu¨n Bıc¸akcı a, Asuman H. Kiyak b O a b
University of Ege, School of Dentistry, Department of Periodontology, I˙zmir, Turkey University of Washington, School of Dentistry, Department of Oral and Maxillofacial Surgery, Seattle, WA, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 15 February 2011 Received in revised form 26 May 2014 Accepted 28 May 2014 Available online 12 June 2014
Objective: To evaluate the relationship between older adults’ medical and oral conditions and their selfreports of periodontal conditions with clinically obtained data. Background: Concerns about oral health of elders and its association with systemic diseases have been gaining more attention. Methods: A total of 201 older subjects were interviewed about their previous medical and dental histories and were asked to complete a health questionnaire. Each subject received full mouth exam, including counting number of natural teeth remaining, gingival (GI) and plaque index (PI), CPITN and denture status. Results: Elders who completed health questionnaires had mean age of 62.5. Mean CPITN score was 1.62(1.12), PI was 1.57(1.48), and GI was 1.55(1.31). Women had higher prevalence of CVD and osteoporosis than men (p = 0.008, p = 0.0001, respectively). Subjects who reported bleeding upon brushing had higher PI and GI scores (p = 0.03, p = 0.05, respectively). Smokers were more likely to describe their periodontal tissues as unhealthy (72.3% vs. 27.7%, p = 0.01), whereas self-reports of healthy vs. unhealthy gums did not differ between non-smokers. Conclusion: These findings suggest that a number of systemic conditions are associated with indicators of periodontal disease, and self-reports of oral conditions are independent of systemic diseases. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Systemic diseases Smoking Periodontitis Self-reports Older adults
1. Introduction Concerns about the oral health status of older persons have been gaining attention in both developing and developed countries in the last decades as this population has increased, and as more elders retain their natural teeth. As with other countries, Turkey’s aging population is increasing and more of them are keeping their teeth. Older persons have more chronic conditions and use more medications than younger populations. On the other hand, economically and socially disadvantaged older adults and those with disabilities are more likely to experience tooth loss and have a greater risk for caries and periodontal diseases (Unluer, Gokalp, & Dogan, 2007). Inflammatory periodontal diseases exhibit an association with multiple systemic conditions. Although the evidence is correlational, patients who suffer from certain systemic diseases tend to be at greater risk for periodontal. Currently, there is
* Corresponding author at: Ege University, School of Dentistry, Department of Periodontology, 35100 Bornova, I˙zmir, Turkey. Tel.: +90 535 279 01 00; fax: +90 232 388 03 25. ¨. O ¨ zc¸aka). E-mail address: [email protected] (O http://dx.doi.org/10.1016/j.archger.2014.05.011 0167-4943/ß 2014 Elsevier Ireland Ltd. All rights reserved.
a lack of consensus among experts on the nature of these associations and confusion among health care providers and the public on how to interpret this rapidly growing body of science. The local and systemic effects of periodontal infections and inflammation are usually exerted for many years, typically among those who are middle-aged or older. Numerous epidemiological associations linking chronic periodontitis to age-associated and biologically complex conditions such as diabetes, cardiovascular disease, osteoporosis, respiratory diseases, rheumatoid arthritis, certain cancers, erectile dysfunction, kidney disease and dementia, have been reported (Otomo-Corgel, Pucher, Rethman, & Reynolds, 2012). The progression of periodontal disease is influenced by variety of factors like microorganisms, host response, systemic background, and genetic makeup of the host. Amongst them, diabetes mellitus tops the list. Diabetes and periodontitis influence the clinical outcome of each other and control of both influences the clinical improvement of each (Daniel, Gokulanathan, Shanmugasundaram, Lakshmigandhan, & Kavin, 2012). Subjects with diabetes mellitus are 2.8 times more likely to have destructive periodontal disease (Emrich, Schlossman, & Genco, 1991) and 4.2 times more likely to have significant alveolar bone loss (Taylor, Burt, Becker, Genco, & Shlossman, 1998) compared to systemically healthy subjects.
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Williams (2008) reviewed the literature that demonstrates a link between cardiovascular disease and periodontal disease, while Cronin (2009) concluded that periodontal disease is a risk factor for CVD. Pihlstrom (2001) includes osteoporosis among the diseases associated with periodontal disease. In fact, a longitudinal follow-up of community-dwelling older adults enrolled in a clinical trial found that decline in periodontal status over five years was best predicted by osteoporosis and ethnicity (greater among whites and African Americans, less among Asian Americans) (Swoboda, Kiyak, Darveau, et al., 2008). Early systematic reviews and a definitive controlled clinical trial indicate that intensive periodontal therapy can reduce systemic inflammation (Tonetti, 2009). Although the average lifespan in most western societies is increasing, both systemic and oral health deteriorates with aging, and can reduce quality of life, even while life span expands thanks to modern medicine (Crimmins & Beltra´n-Sa´nchez, 2011; Mombelli, 1998). Hence, it is not surprising that the leading cause of death has shifted from infectious to chronic diseases. It is therefore important to examine and identify risk factors; including age, gender, smoking and medical conditions, that may have an impact on oral health and treatment needs. The objectives of the present study were to assess: (a) the associations between systemic and oral conditions, and (b) older adults’ self-reports of periodontal conditions vs. clinically obtained data. The following hypotheses were tested: 1. Older males and females differ in their profile of systemic diseases and periodontal conditions. 2. Older adults with certain systemic diseases have signs of periodontal disease. 3. Older adults can accurately report periodontal conditions that are observable (i.e. healthy gums, bleeding upon brushing, teeth mobility). 4. Older adults with certain systemic diseases and who smoke are report more periodontal problems.
2. Materials and methods 2.1. Sample A total of 201 older subjects from western Turkey participated, completing oral health assessments and health histories, and providing information on their demographic backgrounds. They were identified from adults who were patients of record at Ege University School of Dentistry. Subjects older than 55 years were included to the study. Data were collected from these patients over a period of 15 months between March 2008 and May 2009. Edentulous subjects were excluded. Eligible subjects gave written informed consent in accordance with the Helsinki Declaration. The study protocol was approved by the Ethics Committee of the Medical Faculty of Ege University. 2.2. Health history All subjects were interviewed about their previous medical and dental histories, and were asked to complete a health questionnaire, which was then reviewed by project dentists. The validity of this information was confirmed by reviewing subjects’ national health insurance records, and correcting self-reports of systemic diseases and medications as needed.
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Based on the literature review presented above, diseases of interest in this study are: CVD, hypertension, diabetes, osteoporosis, high cholesterol, and kidney diseases. For each of these conditions, if the subject reported the condition, they were asked if they were currently using a medication for that condition. 2.3. Smoking habits Because smoking habits have been associated with periodontal disease, all enrolled subjects were questioned about this behavior. They were asked if they had (1) never smoked, (2) quit smoking and when, or (3) if they were still smoking. Also, for current and former smokers, we asked the duration of smoking and number of cigarettes smoked per day. 2.4. Oral assessments The oral examinations were performed by two experienced ¨ .O ¨ . and S.B.). The inter-examiner agreement for periodontists (O the measurement of clinical periodontal status showed good reliability, with an inter-examiner reliability coefficient alpha of 0.81. Each subject received a full mouth intraoral examination. Examiners also recorded the number of remaining teeth and dentures. Six sites per tooth were assessed in the mesiobuccal (MB), midbuccal (B), distobuccal (DB), distolingual (DL), midlingual (L), and mesiolingual (ML) sites. Measurements of GI (Silness & Lo¨e, 1964) and PI (Lo¨e & Silness, 1963) scores on six Ramfjord teeth (right maxillary first molar, left maxillary central incisor, left maxillary first premolar, left mandibular first molar, right mandibular central incisor and right mandibular first premolar) were recorded. If any of these six teeth was missing, we assessed the opposing tooth, or if that tooth was also missing we examined one of the adjacent teeth. The full mouth recordings of probing depth (six sites per tooth) were also made and used for the assignment of sextant-based CPITN scores (Ainamo & Ainamo, 1985). 2.5. Self-reports of oral health In addition to the clinical indicators of periodontal disease and missing teeth, we asked subjects if they had the following observable conditions: 1. Do your gums bleed when you brush? Yes/No 2. Are your teeth mobile? Yes/No 3. Are your gums healthy? Yes/No
3. Statistical analysis The relevant data from patient surveys were collected and recorded on a pre-established spreadsheet using a code book with specific diseases, medications and oral conditions listed. A frequency distribution was created for each of the systemic diseases and medications. Descriptive statistics including frequencies, means, standard deviations, and ranges were conducted, using the SAS statistical program (SAS statistic software, version 8.2 (SAS Institute, Cary, NC). In order to test the four hypotheses proposed above, we conducted a series of t-tests, chi square tests and Mann–Whitney U tests. To test the first hypothesis, chi square tests were conducted to assess the association between gender and systemic diseases to determine not just associations between and rates of disease, but also the direction of any observed differences. T-tests were used to compare men and women on their clinical oral health status, and
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chi square tests to assess the association between gender and self-reports of periodontal status. In testing the second hypothesis, we compared the oral health of elders with and without the systemic diseases listed above, and those who used or did not use medications for these diseases. Ranges and standard deviations of clinical periodontal parameters were analyzed by Mann–Whitney U test and logistic regression analyses to adjust for age, sex and smoking using presence/ absence of disease were performed. The third hypothesis was intended to test the validity of self-reports of observable oral health. A series of t-tests were conducted to determine if subjects with bleeding upon brushing, with mobile teeth and with self-perceived healthy periodontal tissue differed on GI, PI, CPITN scores and on missing teeth from their counterparts who reported no bleeding, no mobile teeth and whose self-reported periodontal health was poor. The fourth hypothesis focused on the link between smoking, systemic diseases and self-reported periodontal disease. Chi square tests were used to test the association between this latter variable, systemic diseases and smoking. 4. Results Table 1 illustrates the demographic, periodontal and systemic disease status of all 201 subjects. Note that some subjects had missing data, particularly on the clinical periodontal measures. As shown, the sample ranged from age 55–83, with a mean age of 62.5. The majority (64.7%) were men. Although CPITN, PI and GI scores ranged up to 3.5, mean scores on those clinical periodontal parameters were in the lower range (mean = 1.62, 1.57, 1.55, respectively), indicating relatively low periodontal disease rates, but with considerable variance across patients). On average, this sample was missing 7.38 teeth, ranging from 0 to 25. The prevalence of systemic diseases in this sample was relatively low.
Table 2 Gender differences in disease frequencies.
CVD (%) Diabetes mellitus (%) Hypertension (%) Cholesterol (%) Osteoporosis (%) Kidney disease (%) a
% Total with disease
Females N = 71
Males N = 130
P value
24.4 13.9 43.8 26.4 16.4 6
35.21 11.26 47.88 30.98 36.61 1.40
18.46 15.38 41.53 23.85 5.38 8.46
0.008a 0.42 0.39 1.27 <0.0001a 0.06
Significant difference.
Men and women also were compared on clinical indicators of oral health. Their CPITN scores were significantly different (p = 0.01), with higher scores for men. Men were almost twice as likely to use dentures as did women (66% vs. 34%, p = 0.001). Men had slightly more missing teeth on average (6.87 vs. 7.68), but this difference was non significant. Not surprisingly, women were far more likely to report never having smoked (60.6%), whereas men were more likely to be current or past smokers (59.2%), resulting in a significant association between smoking and gender (p = 0.025). 4.2. Hypothesis 2 The second hypothesis posited that older adults with certain systemic diseases will have more objective signs of periodontal disease and tooth loss than adults without these diseases. The Odds Ratio and 95% CI of the CVD, hypertension, osteoporosis and diabetes mellitus shown in Table 4. CPITN and number of missing teeth were unrelated to any systemic disease. The only class of drugs associated with oral status was antihypertensives; subjects who used these medications had slightly more missing teeth (p = 0.05).
4.1. Hypothesis 1 4.3. Hypothesis 3 This hypothesis stated that older males and females differ in their profile of systemic diseases and periodontal conditions, such that older men were expected to have higher rates of CVD and hypertension, whereas older women were more likely to have osteoporosis. Women were also expected to have fewer teeth (i.e. more missing teeth) than men. Tests of this hypothesis revealed some associations between gender and systemic diseases. As shown in Table 2, women had a higher prevalence of CVD (p = 0.008), contrary to the hypothesis. They also had higher rates of osteoporosis, as hypothesized (p = 0.0001). Men had six times the rate of kidney disease as women, but because of low prevalence rates overall, this difference only approached significance (p = 0.06) (Table 3).
The third hypothesis focused on the association between selfreports and clinical indicators of periodontal disease. Older adults were expected to accurately report periodontal conditions that are observable (i.e. healthy gums, bleeding upon. brushing, loose teeth). As shown in Table 5, observed differences were in the predicted direction. Subjects who reported bleeding upon brushing had higher PI and GI scores (p = 0.03, 0.05 respectively). Those who reported mobility had worse PI scores (p = 0.02) but did not differ on GI scores. However, self-reports of healthy vs. unhealthy gums were unrelated to clinical periodontal measures. CPITN was unrelated to any of the self-reported measures.
Table 1 Descriptive data.
Table 3 Sex differences on clinical periodontal measurements (mean SD).
Age CPITN PI GI
N
Range
Mean SD
201 186 185 186
55–83 0.43–3.47 0–3.33 0.08–3.0
62.5 3.8 1.62 1.12 1.57 1.48 1.55 1.31
Systemic diseases
N
% with disease
CVD Diabetes Hypertension Osteoporosis Cholesterol Kidney disease
49 28 88 33 53 12
24.4 13.9 43.3 16.4 26.4 6.0
Age (year) CPITN GI PI Missing teeth Dentures Yes (%) No (%) Smoking (%) Never Former Current
Females N = 71
Males N = 130
P value
62.23 4.86 1.49 0.56 1.54 0.53 1.62 0.71 6.87 6.41
62.65 5.31 1.69 0.51 1.56 0.54 1.54 0.60 7.68 6.26
0.57 0.01 0.88 0.43 0.40
34.15 65.85
63.86 36.14
0.001
60.56 18.31 21.13
40.77 30.00 29.23
0.025
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Table 4 Clinical assessment and systemic diseases (median SD).
CVD
With/without OR [%95 CI] With/without OR [%95 CI] With/without OR [%95 CI] With/without OR [%95 CI]
Hypertension Diabetes Mellitus Osteoporosis
CPITN
PI
GI
1.63 0.55/1.59 0.52 0.77 [0.41–1.46] 1.68 0.54/1.55 0.52 1.41 [0.81–2.45] 1.57 0.66/1.60 0.51 1.09 [0.48–2.48] 1.51 0.53/1.59 0.54 0.83 [0.41–1.71]
1.41 0.75/1.50 0.60 0.88 [0.52–1.49] 1.58 0.67/1.50 0.61 1.28 [0.81–2.02] 1.45 0.52/1.50 0.66 0.88 [0.45–1.76] 1.58 0.77/1.50 0.60 2.05 [1.11–3.78]
1.40 0.53/1.70 0.53 0.53 [0.28–1.01] 1.95 0.52/1.50 0.54 1.75 [0.99–3.09] 1.54 0.46/1.70 0.55 0.80 [0.36–1.79] 1.52 0.53/1.66 0.53 1.02 [0.50–2.08]
Corrected age, sex, smoking.
4.4. Hypothesis 4 Based on the previous literature, we hypothesized that older adults with certain systemic diseases and who smoke would be more likely to report periodontal problems. As shown in Table 6, we found the opposite results, suggesting that self-reports of oral conditions are independent of systemic diseases. Subjects with CVD, hypertension and high cholesterol were significantly less likely to report problems with tooth mobility. Self-reports of bleeding with brushing were related only to kidney diseases. Bleeding was reported by 75% of subjects with kidney diseases (p = 0.01), despite the fact that very few subjects in this sample had kidney diseases. In response to the question about healthy periodontal tissue, the majority again reported healthy gums, but only on hypertension and anti-hypertensive medications were these significant (p = 0.002 and p = 0.006 respectively). Elders with hypertension were more likely to report healthy gums (58%) than those without hypertension, as were those using antihypertensives (57%). This was in contrast to the objective assessments reported above; GI scores were higher among those with hypertension, and those using antihypertensives were missing more teeth. The same pattern emerged for smoking vs. tooth mobility. The majority of smokers were highly likely to report no mobility, at even higher rates than non-smokers (82% vs. 64%, respectively; p = 0.03). On the other hand, almost three times more elders who smoked reported unhealthy gums (72.3%, p = 0.01), whereas selfreports of healthy vs. unhealthy gums did not differ between nonsmokers. 5. Discussion Periodontitis is generally a chronic disorder characterized by the breakdown of the tooth supporting tissues and impaired host inflammatory immune response. This condition is due fundamentally to an ecological imbalance between the normal microbial biofilm on teeth and the host tissues (Newman, 1974). There is increasing evidence linking periodontitis to systemic diseases (Kuo, Polson, & Kang, 2008) such as diabetes (Graves, Liu, & Oates, 2007; Herring & Shah, 2006; Preshaw, Foster, & Taylor, 2007) and, especially CVD (Fardi & Papadimitriou, 2007; Ford, Yamazaki, & Seymour, 2007; Paquette, Brodala, & Nichols, 2007); hence the search for factors that may explain such relationships.
This clinical study proposed four hypotheses. First we hypothesized that older men and women differ in their profile of systemic disease and periodontal conditions. When we compared the clinical parameters of periodontal disease in older men and women, they differed only on CPITN scores. Gender differences in the association between number of teeth and hypertension were described in an earlier study (Vo¨lzke, Schwahn, Do¨rr, et al., 2006); our results were in line with another study in the same population showing elevated atherosclerotic risk in younger men with periodontal disease but not in women (Desvarieux, Schwahn, Vo¨lzke, et al., 2004). Likewise, the longitudinal NHANES II data (DeStefano, Anda, Kahn, et al., 1993) yielded a relation of periodontal disease with coronary artery disease and mortality, predominantly in men. In concordance with these findings, another study (Grau, Becher, Ziegler, et al., 2004) demonstrated periodontal disease as a risk factor for ischemic stroke only among males. Contrary to our hypothesis and the literature review above, women in the current study had a higher prevalence of CVD than men. In a recent study Perez et al. stated that women with more severe menopausal symptoms had a greater prevalence of osteoporosis and cardiovascular disease risk factors. In the present study most of women study participants (%56.3) were menopausal women. In this respect contrary to the literature thus they showed higher prevalence of CVD than the men participants (Pe´rez, Palacios, Chavida, & Pe´rez, 2012). Gender differences were also found in rates of osteoporosis, such that women are more likely to have this condition than men (Taguchi, Suei, Ohtsuka, et al., 1999) and therefore extraction may be required due to increased tooth mobility at an earlier stage of periodontitis. Hence, women might not reach a threshold of caries or periodontal disease necessary for the development of vascular consequences (Desvarieux et al., 2004). Table 6 Self-reports of oral conditions and their association with systemic diseases and smoking status.
Systemic disease CVD Hypertension Cholesterol Smoker status Still smoke Never smoke
Table 5 Clinical assessment and self-report (mean score). Self-report
Bleeding/no bleeding Mobility/no mobility NS: not significant.
Clinical assessment: CPITN
PI
P value
NS NS
1.69/1.49 1.76/1.51
0.03 0.02
GI
P value
1.64/1.49 NS
0.05 NS
Systemic disease Hypertension Uses antihypertensive meds Smoker status Still smoke Never smoke
Self-reports: mobility (%)
No mobility (%)
P value
10.2% 16 11.3
89.8% 84.0 88.7
0.01 0.04 0.02
17.7 35.9
82.3 64.2
0.03
Gums healthy (%)
Unhealthy (%)
P value
58 57
42 43
0.002 0.006
27.7 49
72.3 51
0.01
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Possible reasons for non-significant associations between systemic disease and gender may be the relatively small sample size of this survey. In fact, large nationwide epidemiological studies can give the most reliable picture of systemic disease and periodontal diseases in a country; such data are not available in Turkey. The other reason may be the small percentage of older adults with systemic disease; most of the subjects in this study were systemically healthy. This may suggest that the population seeking care at a dental school in Turkey is generally healthier than their peers in the community who do not seek dental care or seek it from private providers. Another possibility is that the mean age of subjects in this study was relatively young and heterogeneous study population. The variation in age is from 55 to 83 years with a mean age of 62.5. They were classified as ‘‘young-old’’ adults and younger old persons differ markedly about persons older old and over, who are more likely geriatric patients. The second hypothesis posited that older adults with systemic disease have more clinical signs of periodontal disease and tooth loss than adults without systemic disease. Although the relationship between periodontal disease and some systemic diseases such as diabetes, CVD and hypertension were stated in the literature, in our results the odds ratios not support the association of these disease. One reason may be the low rates of these diseases Both periodontal disease and hypertension share common social and lifestyle risk factors that influence utilization of dental and medical care services. Recent analyses of a birth cohort demonstrated that low social status predicted both poor oral health and high blood pressure (Poulton, Caspi, Milne, et al., 2002). Besides possible biological mechanisms, differences in pain perception between hypertensive and normotensive adults may further link hypertension to tooth loss. In our results CPITN and number of missing teeth were unrelated to any systemic diseases, including hypertension, but adults who used antihypertensive drugs had slightly more missing teeth. Our third hypothesis focused on the association between selfreports and clinical parameters of periodontal disease. Adults who reported bleeding upon brushing had higher PI and GI scores. Subjects who reported any tooth mobility had worse PI scores but their GI scores were unrelated to tooth mobility. We also hypothesized that adults with systemic diseases and who smoke would report more periodontal problems. Our results supported this hypothesis when periodontal status was defined as ‘‘unhealthy gums’’ but not when elders were asked about the mobility of their teeth. The majority of smokers reported unhealthy gums, but an even larger proportion stated that they had no mobility. This suggests that patients use different criteria to define poor oral health, and that tooth mobility may not be as good an indicator of poor periodontal health as a generalized perception of unhealthy gums. Thompson, Yonke, Rapley, et al. (1999) compared patients’ selfreported medical history responses with their laboratory data, and found that many patients may be unaware of their current and correct medical conditions. In our study, the validity of medical history and drug usage was confirmed by reviewing subjects’ national health insurance records, and correcting self-reports of systemic diseases and medications as needed. It should be noted that this was unnecessary in most cases, with only 2% of subjects omitting information, and 1% erroneously including a disease in their health history. Recognition of the mounting evidence of relationships between oral and systemic health will require future cohorts of dental hygienists, dentists, physicians, nurses, and other healthcare providers to work together. Nowhere is this more important than in the early identification of individuals with systemic diseases such as undiagnosed diabetes and the co-management of the oral and overall health of these patients.
6. Conclusion Determining cause-and-effect mechanisms of periodontal and systemic diseases are more complicated. Although there is a lack of consensus among experts on the nature of these associations and confusion among health care providers. The current evidence regarding the role of periodontal disease in increasing systemic inflammation to suggest that nondental care providers should screen patients for periodontal disease. For both dental and nondental practitioners who embrace the opportunity to become more actively involved in this important arena of healthcare, this new and exciting level of clinical practice is certain to benefit patients and to be professionally rewarding. Source of funding This study has been funded solely by the institutions of the authors. Conflict of interest The authors declare that they have no conflict of interests. Acknowledgement We would like to thank Lingmei Zhou at the University of Washington for conducting all statistical analyses. References Ainamo, J., & Ainamo, A. (1985). Partial indices as indicators of the severity and prevalence of periodontal disease. International Dental Journal, 35, 322–326. Crimmins, E. M., & Beltra´n-Sa´nchez, H. (2011). Mortality and morbidity trends: Is there compression of morbidity? Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 66, 75–86 Review. Cronin, A. (2009). Periodontal disease is a risk marker for coronary heart disease? Evidence-Based Dentistry, 10, 22–25. Daniel, R., Gokulanathan, S., Shanmugasundaram, N., Lakshmigandhan, M., & Kavin, T. (2012). Diabetes and periodontal disease. Journal of Pharmacy and Bioallied Sciences, 4(Suppl. 2), S280–S282. DeStefano, F., Anda, R. F., Kahn, H. S., Williamson, D. F., & Russell, CM. (1993). Dental disease and risk of coronary heart disease and mortality. British Medical Journal, 306, 688–691. Desvarieux, M., Schwahn, C., V—lzke, H., Demmer, R. T., Ldemann, J., Kessler, C., et al. (2004). Gender differences in the relationship between periodontal disease, tooth loss and atherosclerosis. Stroke, 35, 2029–2035. Emrich, L. J., Schlossman, M., & Genco, R. J. (1991). Periodontal disease in non-insulin dependent diabetes mellitus. Journal of Periodontology, 62, 123–131. Fardi, A., & Papadimitriou, D. (2007). Periodontal and atherosclerosis-induced diseases. International Angiology, 26, 197–205. Ford, P. J., Yamazaki, K., & Seymour, G. J. (2007). Cardiovascular and oral disease interactions: What is the evidence? Primary Dental Care, 14, 59–66. Grau, A. J., Becher, H., Ziegler, C. M., et al. (2004). Periodontal disease as a risk factor for ischemic stroke. Stroke, 35, 496–501. Graves, D. T., Liu, R., & Oates, T. W. (2007). Diabetes-enhanced inflammation and apoptosis: Impact on periodontal pathosis. Periodontology 2000, 45, 128–137. Herring, M. E., & Shah, S. K. (2006). Periodontal disease and control of diabetes mellitus. Journal of the American Osteopathic Association, 106, 416–421. Kuo, L. C., Polson, A. M., & Kang, T. (2008). Associations between periodontal diseases and systemic diseases: A review of the inter-relationships and interactions with diabetes, respiratory diseases, cardiovascular diseases and osteoporosis. Public Health, 122, 417–433. Lo¨e, H., & Silness, J. (1963). Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontologica Scandinavica, 21, 533–551. Mombelli, A. (1998). Aging and the periodontal and peri-implant microbiota. Periodontology 2000, 16, 44–52 Review. Newman, H. N. (1974). Diet, attrition, plaque and dental disease. British Dental Journal, 136, 491–497. Otomo-Corgel, J., Pucher, J. J., Rethman, M. P., & Reynolds, M. A. (2012). State of the science: Chronic periodontitis and systemic health. Journal of Evidence-Based Dental Practice, 12(3 Suppl.), 20–28. Paquette, D. W., Brodala, N., & Nichols, T. C. (2007). Cardiovascular disease, inflammation, and periodontal infection. Periodontology 2000, 44, 113–126. Pe´rez, J. A., Palacios, S., Chavida, F., & Pe´rez, M. (2012). Severity of menopausal symptoms and cardiovascular and osteoporosis risk factors. Climacteric, 8 http://dx.doi.org/10.3109/13697137.2012.688077
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