The Journal of the American Dental Association
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J Am Dent Assoc, Vol 134, No 12, 1591-1596.
© 2003 American Dental Association

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RESEARCH

JADA Continuing Education

A prospective study of social support, anger expression and risk of periodontitis in men



ANWAR T. MERCHANT, D.M.D., Sc.D., WARANUCH PITIPHAT, D.D.S., M.S., BILAL AHMED, B.D.S., ICHIRO KAWACHI, M.D., Ph.D. and KAUMUDI JOSHIPURA, B.D.S., Sc.D.


   ABSTRACT
 TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background. Stress is associated with poor oral hygiene, increased glucocorticoid secretion that can depress immune function, increased insulin resistance and potentially increased risk of periodontitis.

Methods. The authors examined the association between social support, anger expression and periodontitis in 42,523 male, U.S.-based, health professionals. Subjects were aged 40 to 75 years in 1986, and more than half were dentists. The men were free of a diagnosis of periodontitis at the start of follow-up in 1996.

Results. Subjects who reported having at least one close friend had a 30 percent lower risk of developing periodontitis compared with those who did not have a close friend (relative risk, or RR = 0.70; 95 percent confidence interval, or CI, 0.51–0.96). Men who participated in religious meetings or services had a 27 percent lower risk of developing periodontitis compared with men who did not participate in religious meetings (RR = 0.73; 95 percent CI, 0.64–0.83). After the authors adjusted for potential confounding variables, men whose anger scores were in the top quintile were 72 percent more likely to report having periodontitis compared with men whose scores were in the lowest quintile (RR = 1.72; 95 percent CI, 1.39–2.12). Men who reported being angry on a daily basis had a 43 percent higher risk of developing periodontitis compared with men who reported being angry seldom.

Conclusion. Reduced social isolation and anger expression may play an important role in maintaining oral health, as well as general health and well-being.

Clinical Implications. When treating patients with periodontitis, clinicians should be cognizant of the social and behavioral factors that may affect oral health.

Stress has been associated with poor oral hygiene,1 increased secretion of glucocorticoids that can depress immune function2 and increased insulin resistance.3 All of these mechanisms potentially can increase the risk of developing periodontitis.46 Cross-sectional and case-control studies have shown positive associations between periodontitis and depression,7 loneliness,8 financial stress9 and traumatic life events,1013 but there have been no prospective studies evaluating these associations. Social support may counter the effects of stress on the neuroendocrine system.14 Anger expression is positively associated with stress.15 We conducted this study to prospectively evaluate the role of anger expression and social support in periodontitis risk in a large cohort of middle-aged to older men.

Reduced social isolation and anger expression may play an important role in maintaining oral health.


   SUBJECTS, MATERIALS AND METHODS
 TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Study population. The Health Professionals Follow-up Study is an ongoing, questionnaire-based, prospective, cohort investigation designed to examine the association between lifestyle and nutritional factors, as well as the occurrence of major diseases. Subjects are 51,529 male health professionals who were aged 40 to 75 years and living in the United States when they responded to a baseline questionnaire mailed in 1986. The cohort consisted of dentists (57.6 percent), veterinarians (19.6 percent), pharmacists (8.1 percent), optometrists (7.3 percent), osteopathic physicians (4.3 percent) and podiatrists (3.1 percent). We send follow-up questionnaires biennially to update information about potential risk factors and to ascertain newly diagnosed diseases, including periodontitis. Information about social support and psychological states was collected in 1996.

Periodontitis assessment. We considered men who reported having had periodontitis for the first time from 1996 to 2000 to be case subjects (they responded "yes" to the question, "Have you had professionally diagnosed periodontal disease with bone loss?"). Validation studies among dentists16 and other health professionals17 have demonstrated that self-reported periodontitis is a good measure in this population.

Social support. We used a questionnaire to assess subjects’ perceived social support from people in their close network of family, friends and community groups. The questionnaire included items about marital status, number of close friends and relatives, frequency of contact with friends and relatives, religious group affiliation and participation in community organizations.

Anger expression. We assessed subjects’ anger expression by inquiring about their arguments with others, striking out when infuriated, saying nasty things, losing their temper and, if annoyed, expressing their feelings. For each item, the subjects rated themselves on a 4-point ordinal scale: 1 = almost never, 2 = sometimes, 3 = often, 4 = almost always. The anger expression, or AX, score is the sum of all the ratings for the items. The method used is similar to that described by Spielberger and colleagues.18

Statistical methods. Of the 51,529 men in the study in 1986, 3,717 were excluded because they died before 1996 (when social support was assessed), and another 5,289 were excluded because they reported having had periodontal disease before 1996; this left 42,523 men in our analysis.

We used a pooled logistic regression model, which is asymptotically equivalent to the Cox proportional hazards model,19 to estimate the relative risks of periodontitis according to each item in the social support and anger level measures, as well as the AX scale, for each quintile. We updated time-varying covariates (such as smoking status) every two years. We adjusted for age (five categories from 50–54 years to 70 years and older), smoking (five categories), body mass index (five categories), diabetes (dichotomous), marital status (married, divorced, widowed, never married, missing information) and alcohol use (five categories) for all of the analyses.


   RESULTS
 TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Of 42,523 men who were free of periodontitis in 1996, 1,122 (2.6 percent) reported having received a professional diagnosis of periodontitis within the next four years. Men with periodontitis were heavier and more likely to smoke, consume alcohol and be diabetic than were men without periodontitis (Table 1Go). Sixteen percent did not report their marital status. Among those who reported their marital status, 90 percent were married, 5 percent were divorced, 3 percent were widowed and 2 percent were never married.


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TABLE 1 CHARACTERISTICS OF SUBJECTS WITH AND WITHOUT PERIODONTITIS.

 
Thirty-two percent of the men reported that they almost never felt angry, 31 percent reported that they felt angry one to two times a month, 18 percent once a week, 13 percent three to four times a week, 5 percent daily and 1 percent twice or more daily. Ninety-seven percent of the subjects responded that they had at least one close friend, 52 percent participated in community activities, 65 percent participated in religious meetings or services, 83 percent received visits from their children and 72 percent received visits from close relatives at least once a month. The risk of developing periodontitis was slightly higher for divorced, widowed and never-married men than it was for married men, but the difference was not statistically significant (Table 2Go). When we compared men who had no children with men who had at least one living child, we found no difference in the risk of developing periodontitis. Men whose children visited them at least once a month had a 13 percent lower risk of developing periodontitis than did those whose children visited them less often (Table 2Go)


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TABLE 2 MULTIVARIATE ASSOCIATION BETWEEN SOCIAL SUPPORT AND RISK OF PERIODONTITIS.*

 
Men who reported having at least one close friend were at a 30 percent lower risk of developing periodontitis compared with men who did not have a close friend (Table 2Go). Men who participated in religious meetings were at a 27 percent lower risk of developing periodontitis compared with men who did not participate in religious meetings (Table 2Go).

The risk of developing periodontitis increased with higher anger expression scores on the AX scale. After adjusting for confounding variables, we found that men whose anger scores were in the top quintile were 72 percent more likely to report having received a diagnosis of periodontitis compared with those whose scores were in the lowest quintile (Table 3Go). In addition, men who responded that they felt angry one to two times per month or more often were at an increased risk of developing periodontitis compared with those who responded that they almost never felt angry (Table 3Go). These results were materially similar when we restricted the analysis to whites, men who never smoked and dentists, as well as after further multivariate adjustment for profession.


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TABLE 3 MULTIVARIATE ASSOCIATION BETWEEN ANGER EXPRESSION AND RISK OF PERIODONTITIS.*

 

   DISCUSSION
 TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Social support. After adjusting for potential confounding variables, we found that men who had more social support were less likely to develop periodontitis, and men who expressed anger more frequently were more likely to develop periodontitis compared with men who had low social support and less anger expression, respectively. Men who reported having at least one close friend and those who participated in religious services were at a reduced risk of developing periodontitis. Divorced, widowed and never-married men were at a slightly higher risk of developing periodontitis compared with married men, although the difference was not statistically significant. A high proportion of the men in our study were married (90 percent versus 54 percent20 in the U.S. population).

Anger expression. All of the statistically significant (P < .05) responses to questions regarding anger expression were positively associated with periodontitis risk. The responses to questions about slamming doors, striking out at others, saying nasty things and expressing feelings if annoyed were not statistically significant by themselves. However, the anger expression score (AX scale), in which all of the questions are taken together, was positively associated with periodontitis risk and was statistically significant. Moreover, we saw a dose-response relationship between rising risk of periodontitis and increasing anger expression score.

Because this was a prospective study with a high follow-up rate, the chance of bias was reduced. We adjusted finely for smoking, dividing current smokers into three categories according to the number of cigarettes smoked, and separated former smokers from men who never smoked. We also restricted the analysis to men who never smoked, whites and dentists, and found similar results. Further adjustment for profession (dentist or nondentist) did not alter the findings. Our analysis was asymptotically equivalent to the Cox proportional hazards model, and because we had biennially updated histories of the men, we could update the results according to time-dependent covariates, including smoking history and diabetes.

It is possible that an unmeasured factor (residual confounding) could have affected the results because this was an observational study; however, we adjusted for a number of known potential confounding variables and the associations did not change. For an unknown confounder to alter the results substantially, it would need to be a strong risk factor for periodontitis and be prevalent in the general population.21 We are unaware of any such factor.

We did not adjust for oral hygiene, but its association with periodontitis is not clear4; moreover, we found that oral hygiene in this group was good and was not associated with risk of periodontitis.22 Therefore, it is unlikely that oral hygiene or other factors could explain these associations. Because this group was homogenous in terms of socioeconomic status, residual confounding by this factor is less likely. For the same reason, caution must be exercised when extrapolating these findings to less privileged populations, in which social ties may play a more critical role than they do in this population of health professionals.

Study limitation. One limitation of this study is that we did not obtain clinical periodontal measurements, and relied on self-reports of professionally diagnosed periodontitis. However, because half of the subjects were dentists and the remainder were other health professionals, it seems likely that they were able to answer this question accurately. In subsamples of men for whom we had radiographs, we found good correlations between self-reports of professionally diagnosed periodontitis and clinically diagnosed disease in dentists16 and nondentists.17

Empirically, we found that the associations between oral hygiene and self-reports of professionally diagnosed periodontitis and radiographically diagnosed disease were almost identical in this population.22 Some misclassification of the outcome still is possible because of the self-reported data, but the effect of this most likely would be to attenuate any association,23 and is unlikely to explain the positive findings. The questions regarding social support and anger expression (that is, the AX scale) have been validated in previous studies, and have been found to reasonably measure these constructs.24

Proposed models. Genco and colleagues25 demonstrated an increased concentration of cortisol in the saliva of people with periodontitis compared with the concentration in people without the disease, and proposed two models through which stress can affect the risk of periodontitis. In the first model, they postulated that stress is associated with activation of the hypothalamic-pituitary-adrenal axis.25 Stress induces the hypothalamus to release corticotrophic-releasing hormone, which acts on the pituitary gland to secrete adrenocotropic hormone; this, in turn, stimulates the adrenal cortex to release glucocorticoids (reflected in the increased salivary cortisol concentration).25 Glucocorticoids can depress immune function by inhibiting macrophage antigen in neutrophils,26 lymphocyte differentiation27 and eicosanoid production28; in this way, they increase the risk of periodontal infection.

In the second model, Genco and colleagues25 proposed that stress may be associated with increased smoking, poor diet and ineffective oral hygiene, resulting in an increased risk of developing periodontitis.25

Glucocorticoids increase blood glucose levels and induce insulin resistance.3 Diabetes and the insulin resistance state are associated with the accumulation of advanced glycation end products in periodontal tissues, which induces inflammation and periodontitis.29 It is plausible, therefore, that stress could result in an increased risk of periodontitis through glucocorticoid secretion and consequent insulin resistance.


   CONCLUSION
 TOP
 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Case series,11 cross-sectional studies8,9,12 and case-control studies7,10 have reported consistent findings with regard to the association between increased stress and periodontitis. There are plausible mechanisms to explain this association.25,30 Our findings from a prospective cohort study confirm the results of these studies. Reduced social isolation, increased social support and reduced need to express anger (perhaps achieved through stress management programs) may play an important role in improving oral health, as well as general health and well-being.


   FOOTNOTES
 

Dr. Merchant is a research associate, Department of Nutrition, Harvard School of Public Health, and Department of Oral Health Policy and Epidemiology, and a clinical instructor, Harvard School of Dental Medicine, Boston. Address reprint requests to Dr. Merchant, 665 Huntington Ave., Boston, Mass. 02115, e-mail "amerchan{at}hsph.harvard.edu".


Dr. Pitiphat is a doctoral student, Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, and Department of Epidemiology, Harvard School of Public Health, Boston. She also is an assistant professor, Department of Community Dentistry, Khon Kaen University, Khon Kaen, Thailand.


Dr. Ahmed is a research assistant, Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, Boston.


Dr. Kawachi is a professor, Department of Society, Human Development and Health, Harvard School of Public Health, Boston. He also is a professor, The Channing Laboratory, Department of Medicine, Harvard Medical School, and Brigham and Women’s Hospital, Boston.


Dr. Joshipura is an associate professor, Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, and Department of Epidemiology, Harvard School of Public Health, Boston.


This study was supported by National Institutes of Health research grants CA55075, HL35464 and DE12102.


Dr. Pitiphat received the support of the Royal Thai Government while she conducted this study.


The authors thank the participants in the Health Professionals Follow-up Study for their cooperation and participation.


   REFERENCES
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 ABSTRACT
 SUBJECTS, MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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