Stress and periodontitis : a litterature review

Introduction

Susceptibility for periodontitis can be explained on the one hand by genetic factors : genetic polymorphisms or gene mutations may alter for example certain functions of the immunesystem (^{Korman et al., 1997}). On the other hand acquired environmental factors may convert a periodontitis resistent subject to a susceptible subject (^{Seymour, 1991}). This includes not only the acquisiton of systemic diseases, but also infection with a particular pathogenic bacterial strain or a depression of the immune response due to smoking or stress. The role of stress as factor that may influence the susceptibility to destructive periodontal disease is challenging and intriguing ; it has been speculated for years that stress may increase the susceptibility to periodontitis (reviewed by ^{Ballieux, 1991} ; ^{Monteira da Silva et al., 1995} ; ^{Breivik et al., 1996}).

The term stress serves as a common used descriptor for very complex and incompletely understood psychological, psychosocial and physiological factors. Stress is in fact the psychophysiological response of an organism to perceived challenge or threat (^{Breivik et al., 1996}). The intensity of the stress response to a given situation is determined by the perception of the organism and its perceived ability to handle the situation (coping) (^{Breivik et al., 1996}). Further it needs to be understood that stress in relation to periodontal diseases is chronic in nature, and not the one-time stressful event without lasting psychological or emotional effects.

It is now well accepted that stress due to certain personality traits and psychological states or due to major (negative) life events, may influence the host defense system (^{Ballieux, 1991} ; ^{Monteira da Silva et al., 1995} ; ^{Breivik et al., 1996}). It is intriguing that the chemical messenger substances such as neurotransmitters and neuropeptides from the nervous system, hormones from the endocrine glands, and immune mediators like cytokines and prostaglandins, may lead to interaction between brain and the immune system. This area of research is called psycho-neuro-endocrine-immunology, and the effects of various psychosocial stressors on the immune system have been studied in recent years. Stress has been shown to increase the release of hormones such as cortisol, adrenocorticotrophic hormone (ACTH), endorphin, epinephrine (adrenalin) and norepinephrine (noradrenalin). These hormones can have a variety of effects on the immune system. For example, cortisol has been shown to inhibit :

- the proliferative response of T-cells to mitogens ;

- lymphokine production ;

- monocyte function ;

- T suppressor cells ;

- cytotoxic response ;

- serum immunoglobulin production.

Some hormones suppress NK cell activity, while others increase the activity of these cells. However, one should realise that many studies have been in vitro assessments using pharmacological doses of specific hormones.

Thus it is generally believed that chronic stress may have a net negative effect on the efficacy of the immune response (^{Ballieux, 1991} ; ^{Monteira da Silva et al., 1995} ; ^{Breivik et al., 1996}). Most studies indicate that psychological stress affects primarily the cellular immune system, and has little impact on plasma cell antibody production (^{Workman and La Via, 1991}). For example, subjects under examination stress have decreased responsiveness of T cells. A similar observation was made for individuals with bereavement stress, who were examined before and after spousal death due to breast cancer. Separated/divorced men exhibited a decreased cellular control of latent virusses, and in another study separated/divorced women demonstrated to have reduced lymphocyte responsiveness ; it is concluded that stress from marital discord results in decreased cellular incompetence (^{Workman and La Via, 1991}). Although it has been stated that stress may have very little effect on immunoglobulin producing plasma cells, it is interesting to note that subjects with high levels of stress appeared to have increased frequencies of upper respiratory infections, in conjunction with low levels of salivary IgA ; stress-induced changes in sIgA levels are the result of an increased output of the neurotransmitters (nor)epinephrine (^{Ballieux, 1991}).

In line with the above, it has been postulated that subjects with psychological and/or emotional stress, have an increased susceptibility for periodontitis ; this can result in an episode of progressive periodontal destruction (^{Seymour, 1991} ; ^{Ballieux, 1991} ; ^{Monteira da Silva et al., 1995} ; ^{Breivik et al., 1996}). Increasing evidence for the association between stress and periodontitis is emerging.

Stress and disease in general

There have been many reports linking psychosocial factors to (infectious) disease (^{Silver et al., 1986} ; ^{Kiecolt-Glaser et al., 1988}, ¹⁹⁹¹ ; ^{Cohen et al., 1991} ; ^{Cohen and Williamson, 1991} ; ^{Sheridan et al., 1994} ; ^{Kiecolt-Glaser and Glaser, 1995}). However, the majority of studies regarding stress and host defence lack solid evidence of a causal relationship between the stress-induced alterations in immune functions and the development of immune-mediated disease (^{Hillhouse et al., 1991} ; ^{Kellner, 1991}). In the following, some of these studies are briefly reviewed.

In a longitudinal study, long-term spousal caregivers of dementia victims were compared to matched controls (^{Kiecolt-Glaser et al., 1991}). Not only showed the chronically stressed caregivers negative immunological changes, they reported also more days of infectious illness, primarily upper respiratory tract infections. Furthermore, caregivers had a much greater incidence of depressive disorders than controls. In a study examining the effects of marital discord in males, 32 separated/divorced men were compared to matched married controls (^{Kiecolt-Glaser et al., 1988}). Separated/divorced men appeared more psychologically distressed, lonelier, and reported more recent illnesses than married men. Separated/divorced men who had both initiated the separation and were separated within the last year, were less distressed and reported better health than the non-initiators. ^{Silver et al. (1986}) examined the relationship of psychological factors in recurrent herpes simplex virus-induced lesions. Herpes simplex lesion recurrences and pain were related to the level of pschyological distress. The most important variable in this study appeared to be coping strategies, as the greatest rates of recurrence were found in those subjects who took an emotional-focused, avoidant-coping approach. ^Cohen ) studied the relationship between stress and susceptibility to the common cold. A controlled inoculum of one of a number of viral agents was administered ; infection was documented by viral isolation and specific antibody responses. The severity was rated by both the study participants and the investigators. The results of this study indicated relations between stress and both viral infection and the rate of development of the clinical colds as a result of the viral challenge.

Stress and periodontal diseases

Stress assessment

Several psychosocial factors as measures of stress have been associated with periodontal diseases. These factors generally include on the one hand minor and major stressors, i.e. daily hassles and life events respectively, and the subjectively perceived impact of these stressors. On the other hand, psychological trait and state variables are often used to measure stress. The measurement tools for the various stress factors are often self administered questionaires which have been validated in the appropriate language ; older studies have used interviews as well as the medical and dental records for stress assessments. Some examples of these stress variables are described below. Minor stressors as a result of daily hassles include traffic jam, stolen property, lost keys, medical or dental treatment. Major stressors are often related to some of the following categories of life events : work, financial situation, health, family and friends, and marital circumstances. Psychological trait factors (personality characteristics) include hostility, neuroticism and extroversion/introversion, while psychological state variables include vital exhaustion and depression.

Stress and ANUG

Traditionally acute necrotizing ulcerative gingivitis (ANUG) is associated with emotional stress and impaired host resistance. It has even been suggested that recent emotional stress is one of the most common predisposing factors for this type of periodontal disease. Diagnosis, etiology, and the role of stress as secundary etiological factor of ANUG has excellently been reviewed by ^{Johnson and Engel (1986}). Just one study will be reviewed here to illustrate the relationship between stress and ANUG.

^{Cohen-Cole et al. (1983)} published a study in which they assessed psychiatric, psychosocial and endocrine data during and 2 weeks after symptomatic illness of ANUG patients. A group of 35 ANUG patients, originating from a university periodontal clinic, was compared to a group of 35 healthy controls, matched for age, sex, and dental hygiene. Psychiatric screening was performed and a number of self-reported inventories were employed to measure stressful life events. Blood and urine samples were collected of each subject for tests of immune and endocrine functions at different time intervals. ANUG patients reported significantly more negative life events during the previous year and a greater impact of these events on their lives. In addition, psychiatric screening revealed significantly more psychopathology (trait anxiety, depression and psychopathic deviance), not only during the acute disease, but also after complete resolution of the disease, at two-week follow-up. Furthermore, patients showed :

- elevated serum cortisol levels before ANUG resolution ;

- elevated cortisol levels in overnight urine, before and after disease resolution ;

- depressed lymphocyte proliferation ;

- depressed PMN leukotaxis and phagocytosis.

The findings in this study suggest that certain psychiatric and psychosocial variables may be etiologically significant in the pathogenesis of ANUG through endocrine and/or immune mechanisms.

Stress and other periodontal diseases

Studies on trait and/or state

From the early 50's through the 70's, most literature deals with cross sectional studies or case reports, relating trait and/or state variables to the periodontal condition of subjects or veterans, with or without psychiatric conditions, who were not particularly selected on the basis of periodontitis (^{Manhold, 1953} ; ^{Belting and Gupta, 1961} ; ^{Davis and Jenkins, 1962} ; ^{Vogel et al., 1977}). For example, in a study among 50 US Navy subjects, two personality traits, i.e. neuroticism and extroversion/introversion, correlated significantly with periodontal pathology (^{Manhold, 1953}). ^{Belting and Gupta (1961}) compared a group of 104 veterans treated for psychiatric problems with a group of 122 veterans, receiving other medical therapies. The severity of periodontal disease was significantly greater among the psychiatric patients ; psychiatric patients with the same brushing frequency as the control patients showed higher periodontal disease scores. In another study in psychiatric patients, ^{Davis and Jenkins (1962}) reported a significant relationship existed between state anxiety and periodontal disease. The relationship of neuroticism and extroversion/introversion to periodontal disease and plaque scores were evaluated in a normal population of subjects, registrating for treatment at a dental school clinic (^{Vogel et al., 1977}). These latter investigators found significant correlations between introversion and plaque, between introversion and radiographic evidence of periodontal bone loss, and between introversion and the periodontal condition. Also, a significant relationship was found between neuroticism and radiograpic evidence of periodontal disease, although not at all age levels.

Two early studies have used periodontal patients to determining trait and/or state stress factors (^{Moulton et al., 1952} ; ^{Miller et al., 1956}). A total of 22 cases with periodontal disease were presented by ^{Moulton et al. (1952}). All subjects were studied by a psychiatrist, a dentist and a periodontist. The prevalence of one personality trait, i.e. (oral) dependency, was the most striking life problem of the group having either ANUG or chronic adult periodontitis (oral dependent subjects in this study were described as those subjects who tended to have excessive concern about their mouth, as insecurity made them hold on to childish forms of oral pleasure and they showed evidence of excessive dependence on parents or marital partner). ^{Miller et al. (1956}) reported a positive correlation between the state anxiety and periodontal disease, in a study with 50 adult periodontitis patients and two reference groups (2 000 students and 100 psychiatric patients).

Studies on life events

In the 70's, 80's and 90's, research into the possible association of stress with periodontal disease, was focussed on measurement of major stressors, i.e. life events. For example, aircraft noise as major stressor seems associated with periodontal disease in aircrew members (^{Haskell, 1975}). In a cross-sectional study, three groups of 25 men each were compared :

- jet fighter pilots (wearing helmets with ear protectors ; mean age 34) ;

- pilots and crew of a four-engine propeller driven aircraft (no protective headgear ; mean age 33) ;

- enlisted ground personel not exposed to aircraft noise (controls ; mean age 26).

The greatest amount of bone loss was found in the propeller driven aircraft group. Also, more bone loss was reported for pilots with the most flying hours. The " Periodontal Emotional Stress Syndrome " was described by ^{De Marco (1976}). In this report, 11 cases (mean age 27 years, range 22-32) with severe periodontal bone loss, were presented and could not be explained by the " normal " etiologic factors. The only common denominator in all cases was severe emotional stress associated with active duty in Vietnam. ^{Krasner (1978}) reported 7 cases with periodontitis, who had experienced stressfull episodes in recent years ; however these cases were regular periodontal patients, and they were no war-veterans or military personel.

One of the first studies systematically investigating the relationship between stressful life events and periodontitis, was published by ^{Green et al. (1986}). The study group consisted of 50 male veterans. Stressful life events were quantified with a self-reported questionnaire, concerning events in the preceding 12 months. The degree of periodontal disease was rated and the number of present physical signs and symptoms of gingivitis and periodontitis were counted. Measurements of life stress were found to be significantly associated with measures of periodontal disease. Furthermore periodontal disease was more widespread as stressors increased. This was particularly true when a subgroup of 10 veterans with low somatization scores were excluded in the analyses.

A study investigating the possible association between life events and oral health status was published by ^{Marcenes and Sheiham (1992}). The psychosocial variables included work-related mental demand, work control and work variety ; further marital quality was assessed, and the socio-economic status. Periodontal disease was classified as number of teeth with periodontal sites which bled on probing or with pockets. The proportion of teeth with bleeding sites after probing, and the proportion of teeth with pockets were calculated per subject. A significant relationship between periodontal health status and work-related demand, marital quality and socio-economic status was found. However, it should be noted that the vast majority of subjects had gingivitis or mild periodontitis. In another study by ^{Marcenes et al. (1993}), they investigated the relationship between self reported oral symptoms and life events among 3 861 subjects. The results of the study suggested that self reported life events and chronic and acute oral symptoms are associated. Interestingly, marital problems and family problems other than divorce were found to be the most important life event reported.

^{Croucher et al. (1997}) have performed a nice case-control study on 100 periodontal patients (at least one site with 5.5 mm ; mean age 42 years) and 100 control subjects (no periodontal pockets > 3 mm ; mean age 42). For all subjects the number of life events which had occurred in the preceding 12 months as well as their impact was recorded. The total number of life events was not different between both groups, however the periodontal patients tended to report more negative life events with a greater impact, and were likely to report less positive life events compared to the controls. There was a highly significant association between the impact of life-events and periodontitis. In this study it was also found that after adjustment for tobacco smoking as co-variate in the analyses, the significant associations between periodontitis and the impact of life events remained. The results from this study provide evidence that psychosocial factors are of etiological importance in periodontitis.

Another approach towards the possible relationship between stress and periodontitis, was used by ^{Ludenia and Donham (1983}). They recorded in 101 veterans (mean age 53 years) not only the life events in relation the health, but they also investigated the « health locus of control » and degree of periodontal disease. Health locus of control is a measure how the experimental subjects appraise and cope with life events associated with health matters ; two ways of control are possible :

1) « internal control » or « internality » is defined as the degree to which individuals perceive the health related life events in their lives as being a consequence of their own actions and thereby controllable ;

2) « external control » or « externality » is defined as the degree to which individuals perceive events in their lives as being the result of forces beyond their control, and therefore due to chance, fate, or powerful others. However, contrary to the experimental hypothesis, the status of oral hygiene and the degree of periodontal disease were not correlated to « health internality » or to « health externality ».

Studies on life events and trait and/or state

One study from the early 60's (^{Baker et al., 1961}) and 2 very recent studies (^{Monteira da Silva et al., 1996} ; ^{Hamming et al., 1998}) have included both life events and trait and/or state psychosocial factors in their investigations. ^{Baker et al. (1961}) found a positive relationship between periodontal pathology and marital (un) happiness, broken home and hysteria scores in 62 psychological patients ; this was not observed in 40 control subjects. In a very nice study by ^{Monteira da Silva} ), 50 subjects with rapidly progressive periodontitis (RPP ; mean age 38 years), 50 subjects with routine chronic adult periodontitis (RCAP ; mean age 45 years), and 50 control subjects (mean age 39 years) without significant periodontal destruction, were analysed for a number of psychosocial factors. The combined psychosocial factors were significantly related to the periodontal diagnosis of RPP, RCAP and no significant periodontal destruction. Further it was shown that the RPP group presented with significantly increased depression scores when compared to the RCAP and control groups ; in addition the RPP group reported more loneliness than the other two groups.

In our department we also conducted a cross-sectional controlled study, to investigate whether the psychosocial factors major and minor life events, and the psychological trait and state factors « hostility » and « vital exhaustion », could be associated with periodontitis (^{Hamming et al., 1998}). We used questionnaires to investigate differences in psychosocial parameters between a group of periodontitis patients recruited in our periodontal clinic and a control group without periodontal breakdown recruited in general practices. Stressors were divided into minor life events, i.e. daily hassles, and major life events experienced over the last 12 months. While no association existed between daily hassles and periodontitis, it was observed that certain life events were more frequently associated with periodontitis : life events related to work, but also to a lesser degree, events related to health, were associated with periodontitis. Furthermore, we observed that, among periodontitis patients only, individuals with advanced periodontal breakdown reported more financial stress compared to those with mild periodontal destruction.

Longitudinal studies

In a preliminary communication, ^{Freeman and Goss (1993}) reported the results of a longitudinal prospective study among 18 subjects. The first molars and all incisors were examined over a 12-month period for plaque, bleeding, calculus and pocket depth. Occupational stress was assessed retrospectively at the first visit and at each subsequent visit ; time-intervals were not reported. Mean plaque score and mean probing depth increased significantly between week 0 and 52. However, the bleeding score in week 52 was significant lower. An increase in probing depth was significantly predicted by occupational stress. In a longitudinal study in 23 employed regular dental attenders, ^Linden ) reported that an increase in loss of periodontal attachment was predicted by increasing age, lower socio-economic status, lower job satisfaction and type A personality. But the subjects had also higher levels of plaque, calculus and bleeding on gentle probing. It is interesting to speculate whether the reported occupational stress problems are an secundary etiological factor for the loss of clinical attachment, or that the stress has resulted in behavioral changes, i.e. poor oral hygiene habits (see below).

An exploratory case-control analysis of psychosocial factors in relation to adult periodontitis in a longitudinal study was published by ^Moss ). 79 individuals with recorded active periodontal destruction over a 1 year period (mean age 44 years) and 85 control subjects (mean age 44 years) were ask to fill out questionaires to assess daily strains, measures of psychologic distress, and coping style. Daily strains were addressed in five social domains (job, financial, spouse, being single, parenting children) and one global domain termed role strain. Results showed no differences for any of the psychosocial factors between cases and controls, although a trend was reported that subjects with periodontal destruction have somewhat more financial strain ; controls had somewhat higher strain on being single. Further exploration of the data by creating exposure thresholds, indicated that cases were more likely to have high scores for job strain, financial strain, and role strain, and less likely to have high scores for interpersonal sensitivity. The association between having a high score on financial strain and being a case was stronger among individuals reporting their annual income to be below $30,000. By creating several disease models using different variables to assess their impact on the association between role strain and adult periodontitis status, it was assured that this association was not completely explained by other factors modeled.

Behavioural changes related to stress

In the previous section more emphasis is put on the association psychological stress and periodontitis, supposedly resulting in a downregulation of the immunesystem. However, it needs also to be pointed out that mental stress may influence the lifestyle of individuals (reviewed by ^{Monteira da Silva et al., 1995}). Maybe the changing of lifestyle itself rather than a decrease in the host resistance contributes to periodontitis. Neglected oral hygiene might increase plaque scores in stressed subjects, and therefore making subjects more susceptible to periodontitis. ^Kurer ) for example, observed that subjects with higher depression scores also tended to have higher plaque scores. Furthermore, stress may have an influence on smoking habits ; more smoking may worsen periodontal disease (^{Haber et al., 1993} ; ^{Linden and Mullally, 1994} ; ^{Grossi et al., 1995}). And, although perhaps in the Western world not very common, extensive stressful life events may lead to poor nutrition, vitamin depletion and alcoholism.

^Sakki ) conducted a cross-sectional study among 527 55-year old citizens in which lifestyle and periodontal health were examined. For periodontal disease only pockets deeper than 3 mm were considerd. The following dental health behaviour and lifestyle variables were measured : tooth brushing frequency, dietary habits, alcohol consumption, tobacco smoking habits and physical activity. Furthermore, socioeconomic factors were measured. The percentage of teeth with pockets > 3 mm increased with diminishing toothbrushing frequency and an unhealthier lifestyle. In addition, it was suggested that there was an association between periodontal disease and socioeconomic status ; this may be explained by differences in lifestyle per socioeconomic group.

Conclusions

From this review on psychosocial factors and inflammatory periodontal disease, it can be concluded that (emotional) chronic stress may play a role as a cofactor/secondary etiological factor. For ANUG this seems more strongly evidenced. Since the beginning of the fifties a growing number of reports tried to correlate stress and periodontal disease. In most of these studies, periodontal indices were used, which included gingivitis and periodontitis features. Furthermore, many studies did not include control subjects. Until the mid 80's, studies investigated personality characteristics, often in psychiatric patients. When ^Green ) published their study, it was the first study to relate life events and periodontitis. In following studies growing attention was paid to life events. Although it has been suggested mainly from in vitro work, stress seems able to decrease the efficacy of the immunesystem and thereby the host response. But it is still unknown whether these influences are of clinical importance to disease in general and periodontitis in particular ; stress induced behavioral changes need to be taken into account as well. Reviewing the literature concerning the possible role of psychosocial factors in periodontitis, it seems justified to conclude that stress does have a relationship with destructive periodontal disease, however the magnitude of its contribution to the disease process is currently unknown.

Demande de tirés à part

Bruno G. LOOS, Department of Periodontology, Academic Center of Dentistry Amsterdam (ACTA), Louwesweg 1, 1066 EA AMSTERDAM - The NETHERLANDS.

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