10.1 Introduction

Periodontitis is a multifactorial inflammatory disease that destroys the supporting tissues of the teeth. The disease is induced by bacteria and the progression and the severity depends on the immune response of the host to the bacterial invasion1. Epidemiological studies have indicated that periodontitis affects only a part of the general population and that only a small proportion is diagnosed with the severe form of the disease. Environmental risk factors, such as smoking and diabetes mellitus, as well as genetic-related factors modify the interactions between the pathogenic bacteria and the host and hence the extent, severity and progression of the disease. Among these factors, psychological conditions such as stress and depression have been identified as potential modifiers of periodontal health2. The mechanisms by which those conditions may influence the periodontal status are complex.

Hans Selye was the first to describe stress in 19363. According to psychologists we have two types of stress, eustress and distress, and the latter is commonly called stress. Eustress or ‘good stress’ is considered to be a positive kind of stress that is short term, motivates, improves performance and has beneficial effects on the brain, body and health. In contrast, distress or negative stress, ‘bad stress’, can be short term, lasting for a period of minutes or hours; or chronic, persisting for several hours per day during several weeks or months. Chronic stress is unpleasant, decreases performance and can lead to mental and physical problems, the intensity of which depends on the perception, processing and coping behaviour of the individual. Stress should not be confused with anxiety, which is an emotion characterised by an unpleasant state of inner turmoil. Anxious individuals have a feeling of uneasiness or worry and overreact to situations that are only subjectively seen as menacing. Anxiety disorders can be caused by stress and they often occur with several mental disorders, particularly bipolar disorders and depression. Although the line between stress and anxiety is fine, most of the time stress can be dealt more easily and usually fades away when the stressor is gone; whereas anxiety might need professional psychological and medical treatment, medication and continual counselling.

Stressors, both negative and positive, are different agents and conditions that trigger the stress response and may be identified as: environmental (temperature, loud noises, crowds), daily events (delays, disputes, new hobby), life changes (relocation, redundancy, child), professional (high work load, deadlines, performance assessments, promotion), chemical (drugs, alcohol), social (divorce, bereavement, marriage) or psychological. Stress modifies the biological and the behaviour expression in people. Depending on whether the stressor acts as a short-term factor or whether it is chronic, the response of the organism is different. The inflammatory response (the body’s response to attack or stimuli) is regulated by hormones, and stress has been shown to affect the hormones’ ability to regulate that response. Dysregulation of the stress system caused by chronic stress can affect the body homeostasis and have clinical manifestations4. In chronic stress conditions, under the effect of stress hormones such as cortisol, there is simultaneous enhancement and suppression of the immune system via alterations on cytokine secretion by T-helper (Th) 1 and Th2 cells5. Suppression of protective immunity leads to increased susceptibility to viral and bacterial infections. Acute stress, in contrast, induces enhancement of both innate/primary and adaptive/secondary immunity as well as mental and physical performance.

Stress is the product of three elements: environment, the nature of the stressor and the susceptibility of the person to the stress6. A person cannot be in a continuous state of strain and emotional tension. People adopt different coping mechanisms in order to deal with a stressful situation, and these can be effective or ineffective. Matheny et al7 defined coping as “an effort, healthy or unhealthy, conscious or unconscious, to prevent, eliminate, or weaken stressors or to tolerate their effects in the least hurtful manner”. In psychology two main ways are identified in which a person can react to stress; either in a passive way, in that the individual suffers or denies the experienced stress; or in an active way, when the person decides to face and clarify the situation. Carver et al8 described three coping mechanisms:

● problem-focused coping that includes active coping, planning and restraint coping

● emotion-focused coping that includes seeking social support for emotional reasons, positive reinforcement and growth, acceptance and humour

● dysfunctional coping that focuses on emotions, behavioural disengagement, alcohol and drug use and denial.

Depression has been associated with both stress and periodontal disease. Depressive disorder is a very complex and multifactorial condition with genetic predisposition and non-genetic contributory factors9. It is one of the five major mental diseases, like autism, attention deficit hyperactivity disorder, bipolar disorder and schizophrenia. According to the World Health Organization (WHO), depression is the leading cause of disability worldwide, with an estimated 300 million people of all ages being affected10. It is characterised by low mood, low self-image, unwillingness to take part in normally enjoyable activities, low energy, disturbed sleep or appetite, poor concentration and physical complaints/pain with no apparent physical cause. The influence of depression in the pathogenesis of periodontitis and vice versa is discussed in this chapter.

10.2 Clinical evidence

Several epidemiological and clinical observational studies have been conducted in order to investigate the association of psychological factors like stress and depression with the periodontal status of patients.

10.2.1 Periodontitis and stress

Periodontitis does not affect everyone in the general population in the same way. Numerous case-control, cross-sectional and prospective studies have attempted to investigate stress as a risk factor of periodontal disease. The effect of stress on the periodontium can be direct or indirect. The direct effect through the central and autonomic nervous system leads to immunosuppression. The indirect effect is mediated through lifestyle changes such as poor oral hygiene, poor dietary intake, no or infrequent dental visits, and smoking or alcohol habits11^,12.

The first reports on the role of psychological stress as a predisposing factor for periodontal disease come from the early 1950s when emotional stress was found to be associated with necrotising ulcerative gingivitis13^–15. For periodontitis, a cause–effect relationship with stress was less substantive. Although a great number of studies have been conducted, different and contradictory results have been reported. The population included in the majority of these studies are patients of hospitals, universities and private practices. In most of the studies, standard clinical periodontal measures were evaluated, such as the clinical attachment level (CAL), pocket probing depth (PPD) and bleeding on probing (BOP). In few studies the number of missing teeth or tooth loss was used as a surrogate measure of periodontal disease. In several investigations, the level of antibodies against specific bacteria related to periodontal disease, cytokine levels in gingival crevicular fluid (GCF) and cortisol levels in saliva and urine were also analysed. Finally, the effect of stress on periodontal treatment outcomes was evaluated in a number of studies.

In the late 1990s, Genco et al16, in a cross-sectional study, reported that stress associated with financial difficulties and poor coping mechanisms, is a significant risk indicator for more severe periodontitis – although not defined clearly – expressed as advanced clinical attachment loss. The impact of personal resilience as protective factor has been shown either in relation to periodontal disease risk17 or in relation to response to a standardised periodontal treatment18. A 24-month prospective study conducted by Wimmer et al19 aimed to examine the influence of different coping behaviours on the results of non-surgical periodontal therapy. The authors reported that patients with passive coping behaviour presented more severe disease (based on clinical attachment measures) and showed poorer response to therapy in comparison with patients with active coping strategies; the latter presented milder disease and responded favourably to treatment19.

Two systematic reviews on the role of stress as possible risk factor for periodontal disease reported, based on 14 and 26 articles, a positive association between stress and/or other psychological factors and periodontal disease11^,20. However, the different criteria used to determine periodontal disease or health, and the different methods used to evaluate stress in these studies, make comparisons difficult. Different scales and psychometric tests, either self-reported or filled by the examiner, were utilised and patients were classified based on various questionnaires for stress, anxiety, loneliness, depression and everyday strain. Psychometric tests are a standard and scientific instrument used to estimate a person’s mental capabilities and behavioural type. Psychometric tests examine the personality characteristics and aptitude or cognitive abilities. There are differences between the self-reporting and the observer’s scales. On the self-reporting ones, a good cooperation and understanding of the person is required. The answers can be influenced by the educational level and the cultural background of the person. On the observer’s evaluations the experience and the training of the person that conducts the test can influence the precision of the test21.

Furthermore, most of those tests are developed in the Occident, so when addressed to other populations they need re-adaptation and careful interpretation. Some examples of questionnaires are the self-reported psychiatric screening questionnaire-20, the Beck Depression Inventory, the Beck Anxiety Inventory (BAI), the State-Trait Anxiety Inventory (STAI), the Stress Symptoms Inventory (SSI), the Standard Stress Scale (SSS), the Perceived Stress Scale (PSS), the Zung Self-Rating Depression Scale and many others. Table 10-1 shows one of the most frequently used research measures of anxiety, the BAI, which is designed for individuals who are above the age of 1622. It is a 21-question multiple-choice self-reported test for anxiety. The questions are about common symptoms of anxiety that the person perceived in the last 7 days, and it takes 5 to 10 minutes to complete.

Table 10-1 Beck anxiety inventory (BAI)22. The BAI contains of 21 questions, each answer being scored on a scale of 0 to 3: 0–9, normal to minimal anxiety; 10–18, mild to moderate anxiety; 19–29, moderate to severe anxiety; 30–63, severe anxiety.

In Table 10-2, after a review of the existing literature, 40 studies were included: 21 case-control, 17 cross-sectional, 2 prospective cohort studies and 1 longitudinal study. Most of the included studies (n = 24) report clinical findings, whereas the remaining studies (n = 14) report, in addition, biochemical and/or microbiological data. Already in 1986, Green et al44 found in a cohort of a private clinic that the severity of periodontal disease augments with the presence of stressors measured with a somatisation scale. In 1996, Linden et al53, in a longitudinal study, concluded that occupational stress is correlated to the progression of periodontitis, as increasing periodontal attachment loss could be predicted by lower job satisfaction and type A personality. In a case-control study, Moss et al39 investigated the association of psychological factors like stress, daily strain and depression, as documented in a self-reported questionnaire, and adult periodontitis. They concluded that elevated depression influences immune response in periods of stress and that depression is associated with more extensive periodontal disease39. When compared to a group of periodontitis patients or a periodontally healthy group, rapidly progressive periodontitis (representing Grade C periodontitis according to the current classification) was significantly more correlated with loneliness and depression in the cross-sectional study of Monteiro da Silva et al25. In a group of participants in battles of the Croatian War of Independence with post-traumatic stress disorder, rapidly progressive periodontitis (Grade C periodontitis) was also frequently diagnosed23. The disease was associated with higher concentrations of interleukin (IL)-6 in saliva and more frequently isolated Aggregatibacter actinomycetemcomitans strains, when compared to a group of patients with other forms of periodontitis23. The authors suggested that stress should be considered as an important factor in the causation of Grade C periodontitis23.

Table 10-2 Clinical studies investigating the association of stress and periodontitis or gingival inflammation

The studies of Genco et al16^,43 evaluating the role of stress on periodontal disease pathogenesis reported that psychological stress associated with financial strain and distress is a significant risk factor for more severe periodontal disease. Based on three psychological questionnaires and on radiographic measurements of bone loss for evaluation of periodontal destruction, Dolic et al42 found a positive correlation between bone loss and 10 psychological factors including chemical odour sensitivity, general environmental sensitivity I and II, physical sensitivity, general respiratory sensitivity, allergic sensitivity, skin sensitivity, gastrointestinal sensitivity, environmental sensitivity and somatisation, after adjusting for confounding factors such as age, sex and smoking. They used several questionnaires to evaluate the psychological factors and PPD, CAL and radiographic bone loss for periodontal evaluation. Moreover, in an Indian population, 180 workers were assessed in order to study the relationship between work-related stress and periodontitis: a high prevalence of job stress was found to be related with periodontitis49. In a prospective case-control study, in which only gingival inflammation was evaluated, Deinzer et al32 found that students participating in a major exam presented more inflammation as compared to a group not participating in the exam. The authors concluded that psychological stress affects periodontal conditions via neglect of oral hygiene32. Several other clinical studies reported that stressful life events like everyday stress, family changes, loss of a spouse and personality traits are correlated with an unfavourable effect in the course of chronic periodontitis31^,36^,38^,46.

A number of investigations aimed to explore the mechanisms by which stress is associated with periodontal disease. It was suggested that stress contributes to the disruption of the homeostatic regulation between bacteria and the host’s immune system by altering the production of cytokines16^,59^,60. When samples of GCF were analysed in periodontally healthy and diseased individuals, stress was found to be associated with higher levels of IL-1β, IL-6 and IL-8, which reflect periodontal destruction activity34. Moreover, the salivary cortisol levels were found to be positively associated with the extent and severity of periodontitis45 as well as with both stress and periodontitis30. A recent study investigated a cohort of 70 inmates of a central prison in Kerala, India60. These were grouped according to their PPD, and other clinical periodontal parameters as well as stress levels were recorded. Attachment loss, stress score and salivary cortisol were highest in the group presenting the deepest periodontal pockets. Interestingly, there was also a positive correlation between salivary cortisol level and prison time served by the inmates. However, this study did not include a control group and despite the large age range of participants, no age adjustment was performed60. Additionally, a recent meta-analysis investigating whether periodontitis has an effect on salivary cortisol, as a reflection of free blood cortisol levels, confirmed that aggressive forms of periodontitis (Grade C periodontitis) are associated with higher salivary cortisol levels compared to healthy controls (ratio of means: 1.53, 95% confidence interval [CI] 1.11 to 2.12)61. However, this meta-analysis was underpowered, having included only six cross-sectional studies and reported several methodological shortcomings of the included studies, such as different case definitions, limited adjustment for confounders and no blinded examiners61.

Periodontal health may also be affected by academic stress. Two studies conducted by Deinzer et al32^,62 focused mainly on IL-1β and reported higher levels of this biomarker in the GCF of the group of medical students participating in an important exam, when compared to those not having the exam. Similarly, in 20 dental hygienists a clinical evaluation was performed during a major exam and 4 weeks after54. GCF samples and saliva samples were collected at these two time-points and a visual analogue scale was used to evaluate the perceived stress by the students. During the exam, the plaque score and gingival inflammation were significantly higher than that after the exams. The amounts of IL-6 and IL-10 in GCF were also significantly higher and the median level of salivary cortisol was significantly raised during the exam period. In contrast, the amount of IL-1β did not change between the two time-points. Although these results appear contradictory as both pro-inflammatory (IL-6) and anti-inflammatory (cortisol and IL-10) factors were enhanced along with the clinical inflammation, it should be kept in mind that these results reflected the local response to plaque accumulation, as data were only for GCF and not for serum.

These findings were further confirmed by recent studies reporting that stress influences the periodontal status by altering the production of a number of inflammatory markers, the cortisol levels and the catecholamine metabolites in urine35^,37. In a study of 75 periodontitis patients, the association of several periodontal pathogens and the level of serum cortisol was tested. Patients with severe periodontitis revealed significantly higher mean levels of cortisol (P < 0.05), which, in turn, were positively correlated to the presence of Porphyromonas gingivalis (P < 0.01). The authors suggested that high levels of cortisol contribute to the occurrence of P. gingivalis in the biofilm41. In addition to stress, the coping measures used by a person to reduce or overcome a stressful event seem to be highly important for his or her general health (mental and physical). In relation to periodontal disease, Wimmer et al17 showed that periodontitis patients with inadequate stress coping (evaluated by a questionnaire) had greater attachment loss, thus they were at greater risk for severe periodontal disease. The same group in another study demonstrated that the coping behaviour of an individual is of great importance for both the course of periodontal disease and the treatment outcomes: passive coping was related to more advanced disease and poorer response to therapy in comparison with to active coping19. In a large cohort of 1000 subjects in Hong Kong, chronic job and financial strains with combination of inadequate coping were found to be significant risk indicators for periodontal attachment loss. On the other hand, adequate coping was correlated with decrease of stress-related odds and periodontal disease47.

The negative influence of stress and anxiety on periodontal treatment outcomes has been reported by several other authors. In a case-control study on ‘resistant periodontitis’, the group that responded less favourably to treatment displayed more psychological stress factors and a passive–dependent personality, as defined through interviews and psychological testing27. Similarly, on the basis of both clinical changes and biological markers evaluated before and at 6 months after non-surgical periodontal therapy, stressed patients showed a poorer response to therapy compared to unstressed patients26^,26a. As previously mentioned, stress can negatively influence the periodontal status indirectly through behaviour changes and habits such as poor oral hygiene, infrequent dental visits or smoking. In the case-control clinical study of Deinzer et al33, in which 16 matched-pair medical students participated with only half having a major exam, the levels of plaque were evaluated at baseline and 6 weeks after the day of the exam. Exam students presented higher plaque scores and reported reduction in thoroughness of oral hygiene. The authors concluded that stress correlates with less meticulous oral hygiene, thus leading to more inflammation33. In a cross-sectional pilot study, 45 periodontal patients answered questions related to composite health (age, family history of periodontal disease, hygiene habits), chronic stress, depression and demographic aspects50. The salivary cortisol level was measured and periodontal parameters such as PPD, CAL and number of teeth lost were assessed. Periodontitis was correlated with stress, depression, and high cortisol levels; attachment loss and missing teeth were related to oral hygiene neglect during periods of stress and depression. The authors concluded that stress and depression are associated with periodontitis through behavioural mechanisms50. In another study in which a Japanese population was examined for insomnia and prevalence of periodontal disease after the traumatic experience of an earthquake, a significant association was revealed between insomnia and periodontal problems (odds ratio [OR] 2.16, 95% CI 1.43 to 3.26)48. On the other hand, patients with lower grades of periodontitis, when compared to Grade C periodontitis before treatment, did not differ on plaque levels but smoked significantly more40.

In addition to poor oral hygiene, several other stress-induced behavioural changes can indirectly affect periodontal health. Changes in dietary habits, such as excessive consumption of refined carbohydrates and soft drinks, increase plaque accumulation and gingival bleeding, thus the risk for periodontal disease51^,63^,64. Cigarette smoking is widely considered as the most important behavioural risk factor for periodontitis65^,66. In a study conducted in Lithuania aiming to test whether psychological stress and lifestyle are associated to periodontal status, a clear link between smoking and psychological stress was observed in men67. As has been previously suggested by Genco et al43, stress and smoking act as conditioning factors for periodontal disease. Until now, only few studies failed to show associations between stress and periodontitis21^,29. In a cross-sectional study including 160 participants, no association was found between psychiatric symptoms and established periodontitis. Similarly, in a case-control study based on a relatively small sample of participants with different forms of periodontitis, no correlation was found between stress evaluated by a non-standardised questionnaire and levels of IL-1β, IL-6 and cortisol in the blood24.

Association between stress and acute necrotising ulcerative gingivitis (ANUG) and periodontitis (ANUP) has been documented. This form of periodontitis is characterised by interproximal necrosis, presence of a grey pseudo-membrane that is easily removed, ulceration, soreness, bleeding of the affected tissues and with the papillae often having a crater-like appearance and a characteristic fetid odour. These symptoms have been correlated with stress68 and immunosuppression69 (Fig 10-1). Shannon et al14 in 1969 investigated the correlation between stress, measured by the urinary steroid excretion rate, and periodontal status in six groups; three groups presenting different degrees of gingivitis, one group with periodontitis, one with ANUG and one control. Although it was difficult to draw conclusions, the mean steroid level was higher in the ANUG group in comparison with the other groups14. Later, other cross-sectional and case-control studies reported that stress plays an important role in the pathogenesis of ANUG55^,57. The role of defective leucocyte function in ANUG patients compared to healthy controls was discussed by Cogen et al70, suggesting that the elevated rates of the stress hormone cortisol might be responsible.

To verify a direct association between stress and periodontitis requires a complete understanding of their mechanisms, and this is not yet acquired. In the present literature most of the studies evaluate one aspect of each modality and conclusions are drawn by observations and correlations without actually finding a causal relationship or defining the mechanism with which those correlations are created. Discrepancies in the literature are due to several methodological issues, and these should be kept in mind. Firstly, information is based exclusively on case series and cross-sectional studies that preclude an existing cause–effect relationship between stress and periodontitis. In the majority of studies, a small number of subjects is included (20 to 100 participants and only a few studies exceed 120 participants). Moreover, the definition of periodontitis and the inclusion criteria differ among studies; sometimes diagnosis is based on probing depths exclusively, on partial instead of full-mouth examination or on radiographic evidence of bone loss, and all these parameters have different thresholds, causing discrepancies in the definition and the severity of periodontitis.

Similarly, stress is evaluated by different methods and is usually self-reported. The lack of a uniform definition of stress and the difficulty in differentiating acute and chronic stress are also main shortcomings of the analysis and comparison of the different studies. Parameters such as coping behaviour, which is a key element of the individual’s response, are also not always evaluated. Last but not least, stress is commonly associated with comorbidities, such as diabetes mellitus, cardiovascular disease and rheumatoid arthritis, but this issue is also not sufficiently addressed in the literature. Moreover, not all the co-factors are taken into consideration. As mentioned previously, stress influences in different ways the host’s defence by acting on immune and neuroendocrine mechanisms, as well as on the way of life. Similarly, periodontitis is a complex disease with multiple contributing factors, from genetic variability to immunity, bacteria variation and local factors. Finally, behavioural changes under the influence of stress, such as smoking, diet, oral hygiene habits and dental visits are not sufficiently taken into account.

In future studies, collaboration of different disciplines is needed to understand at a preclinical level the basic mechanisms of the effects of stress on periodontal disease. Before arriving at clinical evaluation, the markers or state that better reflect the effect of stress should be identified, as well as how these can be correlated with periodontal disease. Prospective studies should be elaborated with a larger number of people who develop periodontitis. Evaluation of co-factors and comorbidities should be taken under consideration, and standardised thresholds of the disease should be used to ensure comparable results. Finally, an interesting issue that has not yet been evaluated is whether a bidirectional relationship exists between stress and periodontitis: not only whether stress is associated with periodontitis, but whether periodontitis acts as a stressor for the individual. Future investigation could also include the effect of those two conditions in both directions.

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