Validation of an Enhanced Questionnaire Designed to Assess Stress and Social Support in Patients with Chronic

Periodontitis

By

Jill Levine

M.Sc Candidate

A thesis submitted in conformity with the requirements for the degree of Masters of Science

Graduate Department of Periodontology Faculty of Dentistry

University of Toronto

© Copyright by Jill Levine (2009)

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ABSTRACT Validation of an Enhanced Questionnaire Designed to Assess Stress and Social Support in Patients with Chronic Periodontitis Jill Levine Masters of Science, March 2009. Department of Periodontics, Faculty of Dentistry – University of Toronto Background: In this study, we enhanced a diagnostic questionnaire which had been previously developed to measure stress and social support. Methods: 101 patients with chronic periodontitis and 50 healthy control subjects completed our questionnaire package after which we analyzed the data for trends and associations. Results: Our enhanced questionnaire provided a valid and reliable measure of stress and social support in patients with chronic periodontitis. Conclusion: Our enhanced questionnaire provided both a valid and a reliable measure of stress and social support in patients with chronic periodontitis however requires further refinement to predict periodontal disease experience and severity.

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Acknowledgements This thesis would not have been possible without the support of and efforts of many

people. I first would like to thank my supervisor, Dr. Michael Glogauer, for his insight

and guidance. As well, I would like to thank my committee members Dr. Michael

Goldberg, Dr. David Locker, and Dr. Cameron Norman for all of their help and advice.

Thank you to Eshetu Atenafu and Dr. Herenia Lawrence for all of their help with the

statistics and to Dr. Howard Tenenbaum who went out of his way to help me with the

organization of the paper.

Thank you to my parents for their support and for all of their help with babysitting

Sephora so that I could work on my thesis.

Finally, thank you to my husband David Stastny for not only his help with the layout and

the figures for this paper, but also for all of his love, support, and encouragement. This

thesis is dedicated to him and to our daughter Sephora, who made this process a lot more

difficult, but at the same time, a lot more fun!

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TABLE OF CONTENTS Abstract …………………………………………………………………………….…..ii Acknowledgements ……………………………………………………………………iii List of Tables ……………………..………………………………………………....…vi List of Figures……………………………………………………………………….....vii Abbreviations ………………………………………………………………………….viii Introduction and Statement of the Problem …………………………………………..1 Review of the Literature ……………………………………………………………..…2

I) Etiology of Chronic Periodontitis…………..………………………………...2

II) Brief Description of Various Psychosocial Conditions of Interest…….….3 A) Stress ……………………………………………………………………….…3 B) Depression………………………………………………………………..……4 C) Social Support…………………………………………………………………4 D) Coping…………………………………………………………………………5

III) Questionnaires Used for Validation of Psychosocial Measures...………..5

IV) Impact of Psychosocial Health on Inflammatory Diseases…….………....6 A) Stress ……………………………………………………………………….…6 B) Depression………………………………………………………………..……7 C) Social Support…………………………………………………………………7

V) Impact of Psychosocial Health on Chronic Periodontitis………...………..9 A) Stress ………………………………………………………………………….9

i) Animal Studies …………………………..…….…………………..…..9 i) Human Studies ……….…………………..…………………..……….11

B) Depression………………………………………………………………....…13 C) Social Support………………………………………………………………..13 D) Coping………………………………………………………………………..14

VI) Putative Mechanisms Underlying the Impact of Psychosocial Factors on

Chronic Periodontitis…………………………………………………...………15

Objectives of the Study ………………………………………………………………...20 Hypotheses………………………………………………………………………………20

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Materials and Methods ………………………………………………………………...21 I) Study Population and Clinical Protocol………..…………………………...21

II) Overall Study …………………..…………………………………………...21 III) Statistical Analysis …………………..…..………………………………...22 Results …………………………………………………………………………………..24

I) Validation of the Enhanced Questionnaire…………………..…………...25 II) Test-Retest Reliability of the Enhanced Questionnaire...……………..…26 III) Preliminary Testing of the Relationship Between Stress, Social Support and Chronic Periodontitis……………………...………..31

(i) Bivariate Analysis ……………………………………………………32 (ii) Multivariate Analysis …………..…………………………………...41 Discussion ………………………………………………………………………………44 I) Questionnaire ……………………………………….……………………….44

II) Limitations of the Study …………….……………………………………..46 Summary and Future Direction ………………………………………………………48 Conclusions ……………………………………………………………………………..49 Appendix 1 – Questionnaire Package……………………………………...………….50 2 – Calibration……………………………………………………….……...58 3 – Percent of Total Responses for Enhanced Questionnaire……………64

4 – Interpretation of Intraclass Correlation Statistic…….……….……...68 5 – Test-Retest Reliability Tables……………….………………….……...69 References ………………………………………………………………………………71

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LIST OF TABLES Table 1: Demographics of Controls vs. Cases…………………………………………...24

Table 2: Demographics of Healthy Controls vs. Mild/Moderate vs. Severe Disease...….25

Table 3: Pearson’s Correlation …………………………..………………………………25

Table 4: Spearman’s Correlation …………………………..……………………………26

Table 5: Number of Participants for Test-retest Reliability Component of Study.……...26

Table 6: Intraclass Correlation Coefficient for Case and Control Groups……….……...27

Table 7: Mean Scores, Standard Deviations, and P-values for Case and Control

Groups……………………………………………………………………………………31

Table 8: Mean Scores, Standard Deviations, and P-values for Healthy Controls,

Mild/Moderate, and Severe Groups………………………………………………….….32

Table 9: Stress and Social Support for Cases vs. Controls

– based on data driven means ………………………………………………...…33

Table 10: Stress and Social Support for Healthy vs. Mild/Moderate vs. Severe

– based on data driven means ………………………………………………...…34

Table 11: Stress and Social Support for Cases and Controls

– based on Safa & Glogauer, 2007 driven means ……………………………….36

Table 12: Stress and Social Support for Healthy vs. Mild/Moderate vs. Severe

– based on Safa & Glogauer, 2007 driven means ……………………………….37

Table 13: Association Between Stress and Social Support……………………………...39

Table 14 – CES-D for Controls versus Cases…………………………………………...40

Table 15 - CES-D for Healthy vs. Mild/Moderate vs. Severe Disease……….…………40

Table 16: Logistic Regression Analysis – Cases vs. Controls…………………………..41

Table 17: Logistic Regression Analysis –Mild/Moderate Disease vs. Healthy…………42

Table 18: Logistic Regression Analysis –Severe Disease vs. Healthy.……………….…43

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LIST OF FIGURES

Figure 1a: Test-retest reliability – Acute stress ………...……..………………………...28

Figure 1b: Test-retest reliability – Chronic stress ………..……………………………...29

Figure 1c: Test-retest reliability – Social support…………………………………...…...29

Figure 1d: Test-retest reliability – Social involvement………….…..…………………...30

Figure 1e: Test-retest reliability – Social contact……………………...………………...30

Figure 2: Stress and Social Support for Cases and Controls

– based on data driven means…………………..………………………………….35

Figure 3: Stress and Social Support for Healthy vs. Mild/Moderate vs. Severe

– based on data driven means……………………………………………………...35

Figure 4: Stress and Social Support for Cases and Controls

– based on Safa & Glogauer, 2007 driven means………………………………….37

Figure 5: Stress and Social Support for Healthy vs. Mild/Moderate vs. Severe

– based on Safa & Glogauer, 2007 driven means………………………………….38

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ABBREVIATIONS ACTH: Adrenocorticotrophic hormone AG: Attached gingiva BI: Bleeding index CAL: Clinical attachment level CES-D: Center for Epidemiologic Studies Depression Scale CNS: Central nervous system CRH: Corticotrophic-releasing hormone E: Epinephrine Furc: Furcation GCF: Gingival crevicular fluid GI: Gingival index HPA axis: Hypothalamic-pituitary-adrenal axis IgA, IgG, IgM: Immunoglobulin A/G/M IL-1B: Interleukin 1-beta INF-gamma: Interferon-gamma LEQ: Life Events Questionnaire MMP: Matrix metalloproteinases Mob: Mobility MSPSS: Multidimensional Scale of Perceived Social Support NE: Norepinephrine NK cells: Natural killer cells NO: Nitric Oxide

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PD: Probing depth P. gingivalis: Porphyromonas gingivalis PI: Plaque index PMN: Neutrophils PNI: Psychoneuroimmunology PSS: Perceived Stress Scale Rec: Recession SAM axis: Sympathetic-adrenal medullary axis SP: Substance P T. forsythus: Tannerella forsythus TNF-a: Tumor Necrosis Factor – Alpha

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INTRODUCTION AND STATEMENT OF THE PROBLEM Periodontitis is inflammation and infection of the tissues that support the teeth. This

progressive disease, which is initiated and sustained by bacterial plaque, can lead to the

loss of the hard and soft connective tissues that retain the tooth within the jaw if left

untreated (Flemming, 1999). Studies point to several risk factors and risk indicators for

periodontitis including, amongst others: smoking, age, gender, poor oral hygiene and

systemic diseases such as diabetes mellitus (Albandar, 2002, Grossi et al., 1995, Grossi et

al., 1994). Growing evidence suggests that the psychosocial factors of stress, depression

and level of social support provoke changes in host defense mechanisms that modify

disease (Kloostra et al., 2006; Ng & Leung, 2006; Hugoson et al., 2002; Genco et al.,

1999; Breivik et al., 1996; Linden et al., 1996; Moss et al., 1996; Monterio da Silva et

al., 1995). The field of psychoneuroimmunology (PNI) focuses on how changes to the

relationships between the central nervous, the endocrine and the immune systems impact

health (Padgett & Glasser, 2003; Kiecolt-Glaser & McGuire, 2002; Rozlog et al., 1999).

Previous studies in our laboratory (Safa & Glogauer, 2007) have demonstrated that

patients with chronic periodontitis suffer from high levels of acute or chronic stress and

that patients suffering from acute stress are more likely to have severe disease. Observed

also was a trend for a higher proportion of the patients in the diseased category to have a

lower level of social support. Although these correlations are valid, the long and

unwieldy diagnostic questionnaire employed in these studies did not address all aspects

of the psychosocial background of the patient. Therefore, in order to enhance the use of a

questionnaire in a clinical setting, we identified and retained those questions which

yielded reliable information, deleted any questions that provide little or no information

and added a questionnaire designed to measure levels of depression. The result was a

concise, comprehensive version of our original questionnaire (Appendix 1). The

psychometric properties of this enhanced questionnaire were then tested to ensure

validity and reliability. Following this, the questionnaire was used to acquire data to

assess the relationships, if any, between stress, depression and level of social support in

patients with and without chronic periodontitis.

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REVIEW OF THE LITERATURE I) Etiology of Chronic Periodontitis Chronic periodontitis is an infectious inflammatory disease involving progressive

attachment and bone loss around the teeth. While it is initiated by bacterial plaque, the

pathogenesis of the disease is primarily affected by local and systemic factors that affect

the resistance of the host to infecting periodontal organisms (Page & Kornman, 1997;

Seymour, 1991), as well as by host defence mechanisms (Flemming, 1999). Examples of

local factors include pre-existing disease evidenced by deep probing depths, plaque

retentive areas and invasion of periodontal tissue by virulent organisms such as

Porphyromonas gingivalis (P.gingivalis), Tannerella forsythus (T. forsythus), formerly

known as Bacteriodes forsythus, and Treponema denticola. Recently identified examples

of systemic factors include diabetes mellitus, cigarette smoking, and neutrophil (PMN)

dysfunction (Genco, 1996; Johnson & Hill, 2004; Mealey & Oates, 2006). There is also a

growing body of evidence to suggest that stress, depression and level of social support

affects host defense mechanisms thereby influencing the progression of chronic

periodontitis (Genco et al., 1999).

(i) The old theory of the pathogenesis of periodontitis focuses on bacterial etiology:

(Page & Kornman, 1997)

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(ii) New concepts in periodontitis, recognize the host response: (Page & Kornman, 1997)

II) Brief Description of Various Psychosocial Conditions of Interest

A) Stress

In the literature, there does not appear to be universal agreement for the definition of

stress. Stress can be defined as a state of imbalance within a person elicited by an actual

or a perceived discrepancy between environmental demands and the person's ability to

cope with these demands (Maes et al., 1987). Stress can also be defined as a state of

physiological or psychological strain caused by adverse physical or mental stimuli that

tends to disturb the functioning of an organism (Boyapati & Wang, 2007). The intensity

of, or the absence of, a stress response is determined by the perception of the situation

and one’s perceived ability to master it. Individual perceptions and the enacted coping

mechanisms are as important in determining health or disease as the stressors themselves

(Breivik et al., 1996; LeResche & Dworkin, 2002).

Definitions of acute and chronic stress are also inconsistent. Current stressor definitions

make the distinction between acute and chronic stressors with no established temporal

cut-off periods. Acute stressors refer to short-term and time-limited events while chronic

stressors denote conditions which are longer lasting and may not be attributed to a

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discrete event (Herbert & Cohen, 1993). Stress duration may be important because the

plausibility of stress-elicited hormones (ex. catecholamines, cortisol) affecting immune

outcomes depends on the duration of the stressor. Acute stress appears to have a boosting

effect on the immune system while chronic stress has a dampening effect (Olff, 1999).

B) Depression

Depressive disorder is a very common psychiatric illness that involves long-term

impairment of mood, thought and behavioral patterns. Depression presents with

dysphoria and sadness (a depressed mood), loss of interest or pleasure (anhedonia),

feelings of guilt or low self-worth, disturbed sleep or appetite, low energy and poor

concentration (Olff, 1999; Friedlander & Mahler, 2001).

C) Social Support

Social support is defined as the physical and emotional comfort given to an individual by

family, friends and significant others. When an individual knows that he or she is loved,

cared for, valued and generally thought well of, that person can be said to have a good

social support base (Maes et al., 1987). Social support can be measured structurally or

functionally; structurally via the presence or absence of interpersonal relationships or

functionally, via the functionality of that relationship. Structural measures of social

support include the number of contacts with family, friends, and community, as well as

the number of active memberships in formal and informal groups (Cohen & Syme, 1985).

Functional measures emphasize one’s perception of the relationship or of the perceived

resources available to themselves. Functional measures are good predictors of health

since the relationship between support and health is mediated by psychological

representations of available support as opposed to objective structural relations (Cohen &

Syme, 1985).

There are two models that demonstrate the positive effect of social support on health and

well being; the direct effect hypothesis and the buffering hypothesis. Direct effect argues

that social support enhances health due to the perception that others will provide aid in

the event of a stressful occurrence or that aid will be provided as a result of an integrated

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membership in a social network (Cohen & Syme, 1985). Buffering argues that social

support exerts its beneficial effects in the presence of stress, thereby reducing /

preventing a stress response and protecting people from the pathogenic effects of stress

(Cohen & Syme, 1985).

D) Coping

Coping is the ability to reduce, control or tolerate a state of stress. Coping efforts may be

directed at the demands themselves (problem-focused strategies) or at the emotional

reactions which often accompany those demands (emotion-focused strategies). Research

has shown that problem-focus coping is more beneficial than emotion-focused coping

(Newton, 2005; Reners & Brecx, 2007; Genco et al., 1999).

III) Questionnaires Used for Validation of Psychosocial Measures

The validity and reliability of our enhanced questionnaire was assessed.

The accuracy of our questionnaire was assessed by determining the degree of correlation

between itself and an already validated instrument or process that measures the same

parameter (WHO, 1997). For this study, our enhanced questionnaire was administered

alongside three validated standardized questionnaires: the Perceived Stress Scale (PSS),

the Life Events Questionnaire (LEQ) and the Multidimensional Scale of Perceived Social

Support (MSPSS). The PSS, a fourteen-item instrument used to measure the degree to

which a situation in one’s life is judged as stressful (Cohen et al., 1983), was used to

validate the acute stress section of our questionnaire. The LEQ, a twelve-item instrument

designed to measure common life events from the past six months that tend to be

threatening (Concoran & Fischer, 1998; Brugha & Cragg, 1990; Brugha et al., 1985;

Tennant & Andrews, 1976), was used to validate the chronic stress section. The MSPSS,

a twelve-item instrument designed to measure perceived social support from family,

friends and a significant other, was used to evaluate the social support section.

Respondents used a 7-point Likert-type scale (very strongly disagree to very strongly

agree) with each item (Concoran & Fischer, 1998; Zimet, 1988; Zimet et al., 1990;

Dahlem et al., 1991; Grassi et al., 2000).

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Test-retest reliability was assessed by re-administering the enhanced questionnaire to

patients one to two months after they had completed the original questionnaire. This time

period would be short enough to ensure predictive validity of the scale but long enough

that patients would not remember their previous answers (Cohen et al., 1983).

To augment our study, we added the Center for Epidemiologic Studies Depression Scale

(CES-D) to our questionnaire (Radloff, 1977). The CES-D consists of twenty items, each

representing a state characteristic of a depressed person (Radloff, 1986; Concoran &

Fischer, 1998) and measures the current level of depressive symptoms in the general

population. It has been validated against the clinical diagnosis of depression (Andresen et

al., 1994). Each item is rated on a four-point Likert-type scale to indicate the frequency

of their occurrence during the last week. Response options range from “rarely or none of

the time” to “most or all of the time” (Radloff, 1986; Concoran & Fischer, 1998). A

cutoff score of 16 or higher has been validated with DSM-III criteria as clinical

depression in a wide range of populations (Andresen et al., 1994).

IV) Impact of Psychosocial Health on Inflammatory Diseases

A) Stress

It has been proposed that stress is an important disruptive factor in the homeostatic

relationship between oral bacteria and the host’s immune system. A decreased immune

reaction to bacterial challenge enables bacteria to proliferate and invade the surrounding

tissues provoking an increased inflammatory response (Boyapati & Wang, 2007;

Albandar, 2002; Breivik et al., 1996; Linden et al., 1996; Grossi et al., 1995; Grossi et

al., 1994).

To investigate the effect that a psychosocial stressor (academic stress) might have on a

person’s ability to generate an immune response to a primary antigen, Glaser et al.

inoculated medical students with hepatitis B vaccines at the end of a series of

examinations. Of the students inoculated, one quarter seroconverted after the first

injection and were significantly less stressed and less anxious than those students who

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seroconverted after the second injection (Glaser et al., 1992; Kiecolt-Glaser & Glaser,

1995; Kiecolt-Glaser & McGuire, 2002; Kiecolt-Glaser et al., 2002). Evidence further

suggests that chronic stressors are associated with continued down-regulation of immune

function rather than adaptation. Changes in immunity and health were investigated in

both spousal dementia caregivers who had been providing care for an average of five

years and controls. Caregivers showed a down-regulation in cellular immunity relative to

controls and were sick more often (Kiecolt-Glaser et al., 1991; Kiecolt-Glaser & Glaser,

1992; Kiecolt-Glaser & McGuire, 2002; Kiecolt-Glaser et al., 2002).

Kiecolt-Glaser et al. studied the immunological response evoked by stress in first-year

medical students by measuring natural killer (NK) cell activity, total levels of plasma

immunoglobulin A, G, M, (IgA, IgG, and IgM) and salivary immunoglobulin-A. Blood

samples taken one month before a final examination were compared with samples taken

immediately prior to the exam. The results showed that NK cell activity declined

significantly from the first to the second blood sample. Also, both stressful life events and

loneliness had significant effects on NK activity with high scores on either measure

leading to lower levels of NK cells (Kiecolt-Glaser et al., 1984).

B) Depression

Apart from the obvious psychological effects, other functional aspects of depression have

been found to be associated with impairment of the immune system (Olff, 1999;

Friedlander & Mahler, 2001). For example, cortisol hypersecretion has been shown to be

a biological risk indicator for depression and may play a role in cognitive and emotional

processing and depression. Tse & Bond reported that cortisol secretion was significantly

associated with both depression and poor social functioning. These findings suggest that

poor social functioning is the mediator and elevated cortisol secretion is the predisposing

factor in depression (Tse & Bond, 2004).

C) Social Support

Social support, or the lack thereof, has been previously shown to have a direct impact on

an individual’s risk for infection. Overall, the quality of one's interpersonal relationships

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have health-related consequences. As an example, Cohen and Syme reported that

individuals with poor social support showed inhibitory effects in their immune system

(Cohen & Syme, 1985). Social marginality, a state often reflective of weak ties with

one's community, is a major factor and accounts for higher mortality rates from all

causes. One’s participation in a close-knit religious group has been associated with a

lower incidence of disease. Individuals who are married also have less illness and greater

longevity compared with those who are single (Pilisuk, 1982).

Studies have shown that social support is also related to increased psychological well-

being and lower incidence of physical illness. These studies used either questionnaire

data or were PNI studies. Questionnaire data collected from young military personnel

indicated that the group that had many negative life events and low satisfaction

concerning their social support showed higher rates of isolation, chronic illness and total

illnesses than did other groups (Sarason et al., 1985). Questionnaire data collected from

college students showed that individuals who had less social support were more likely to

be depressed (Pengilly & Dowd, 2000). Furthermore, social support was found to

moderate the relationship between stress and depression such that high stress / low

support individuals were more depressed. Individuals with high social support had similar

levels of depression regardless of their level of stress. Thus, it appeared that social

support can buffer the effect of stress on depression.

PNI studies have found a link between personal relationships and immune function.

Women whose husbands were being treated for urologic cancer, but had great social

support, had high NK cell activity and strong proliferative responses of peripheral blood

leukocytes to mitogen stimulation (Kiecolt-Glaser et al., 2002). Medical students who

reported better social support mounted a stronger immune response to a Hepatitis B

vaccine then did those with less support (Glaser et al., 1992). Poor marital quality was a

significant predictor of depression and generated a poor response on immunologic assays

(Kiecolt-Glaser et al., 1987). Women that had been recently separated from their

husbands had a significantly lower percentage of NK cells and helper cells than did

sociodemographically matched married women (Kiecolt-Glaser et al., 1987).

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V) Impact of Psychosocial Health on Chronic Periodontitis

A) Stress

The successful clinical management of a disease depends on whether or not the etiology

is clearly understood. With periodontal disease, it is essential to determine whether

psychosocial factors like stress give rise to, or exacerbate the pathologic process within

the periodontal structures. Several animal and human studies have explored the

hypothesis that stress is a causative factor of periodontal tissue destruction and chronic

periodontitis.

i) Animal studies:

As early as the 1950s, researchers used animal models to study the effects of stress on

periodontal tissues. In 1956, rats exposed to stress showed numerous signs of periodontal

destruction including the sloughing of the keratinized layers of epithelium in the gingival

tissue, splitting of the papilla at the junction of the oral and enamel epithelial cells,

degeneration of the connective tissue of the periodontal membrane and an overall

reduction in the number of osteoblasts and cementoblasts (Ratcliff, 1956). Others

showed similar results in a hamster. Histologic analysis of tissue specimens from stressed

animals revealed irregularities in both the arrangement of the fibres of the periodontal

membrane and the shape of the fibroblasts (Fedi, 1958).

The response of the periodontium to long-term stress caused by environmental stimuli

was also studied in the 1960’s by using both young adult male rats and hamsters. Stressed

rats showed marked and extensive endosteal osteoporosis in their interrradicular septi as

well as osteoclastic cell activity at the alveolar crest (Gupta and Blechman, 1960).

Gingival healing in hamsters was investigated and it was found that there was a delay in

the organization of the connective tissue in the wounded areas of stressed rats in

comparison to controls. Similarly, the regeneration of bone was reduced in the stressed

animals (Stahl, 1961).

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A more recent approach has been the study of stressors in combination with a P.

gingivalis challenge. Mice challenged with P. gingivalis and placed in isolation

(emotional stressor) under “cold” conditions (physical stressor) showed a suppression of

macrophages, increased secretion of nitric oxide (NO) and reduced secretion of cytokine

tumor necrosis factor – alpha (TNF-a). The authors speculated that the NO was

responsible for the accelerated periodontal destruction observed in stressed animals

(Shapira et al., 1999; Shapira et al., 2000). The impact of emotional stress on the humoral

response to P. gingivalis has also been studied in mice. Findings showed that chronic

psychological stress affected the localized response to P. gingivalis as evidenced by the

lower IgG ratio in stressed mice compared with controls (Houri-Haddad et al., 2003). The

effects of restraint stress on periodontal breakdown as a result of P. gingivalis-challenged

periodontitis, has also been investigated. Results showed that there was a physiologic

burden caused by restraint stress in rats, indicated by an elevation in the levels of the

hormone markers cortisol and corticosterone. Resistant stress alone did not induce

alveolar bone loss. The combination of restraint stress and P. gingivalis challenge

resulted in significantly higher attachment and alveolar bone loss and a decrease in

cytokine expression than did a P. gingivalis challenge alone (Nakajima et al., 2006).

In 2008, a randomized controlled study in rats investigated the effect of chronic stress on

bone loss and key inflammatory factors resulting from ligature-induced periodontitis. The

results demonstrated that plasma levels of corticosterone and catecholamines were

significantly increased in rats with restraint stress. Histometric analysis revealed that

ligature placement resulted in significant bone loss and that chronic stress significantly

increased the rate of periodontitis progression (i.e. bone loss) in ligated sites. Analysis

further demonstrated that chronic stress promoted a local imbalance in both the pro- and

anti-inflammatory cytokines in periodontal tissues. Interleukin 1-beta (IL-1B),

interleukin 10, interferon gamma (IFN-gamma) and RANKL (regulates osteoclast

differentiation and function) mRNA levels were increased significantly by inflammation

produced by ligature placement. It can be concluded that chronic stress significantly

increased bone loss resulting from ligature-induced periodontitis and was related to a

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local increase in pro-inflammatory and pro-resorptive factors and cytokines (Peruzzo et

al., 2008).

ii) Human Studies

Although clinical investigations aimed at studying the relationship between stress and

periodontal disease began in the 1950s, most were directed towards acute necrotizing

ulcerative periodontitis and not chronic periodontitis (Moulton et al., 1952).

Two of the earliest studies which investigated the association between stress and chronic

periodontitis were performed on psychiatric patients in the 1960s by both Belting &

Gupta and Davis & Jenkins. Belting & Gupta found that the severity of periodontal

disease was significantly greater among patients with psychiatric disorders than among

healthy controls. Moreover, the severity of periodontal disease increased as the degree of

anxiety intensified. Significant differences in severity persisted even when variables such

as the degree of calculus, brushing frequency and the habit of bruxism and clenching

were held constant in the two groups (Belting & Gupta, 1961). Davis & Jenkins found a

similar significant relationship between periodontal disease and mental stress (Davis &

Jenkins, 1962).

In the 1970s and 1980s, researchers continued their quest to find a link between stress

and chronic periodontitis. A series of case studies established that severe periodontal

bone loss in a group of young men was probably the result of severe emotional stress

associated with active duty in Vietnam (De Marco, 1976). However, it wasn’t until 1986

when a study by Green et al. reported a significant association between life events stress

and periodontal status in humans. In this study, gingival and periodontal pathology,

stressful life events and somatic symptoms were investigated (Green et al., 1986).

Since then, numerous studies have investigated the relationship between stress and

chronic periodontitis. Initial studies examined the relationship between occupational

stress and chronic periodontitis and showed that chronic stress associated with job and

financial strain could adversely affect the immune response thereby reducing resistance

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to infection (Ng & Leung, 2006). Marcenes & Sheiham found that lower work-related

mental demands, higher levels of marital quality and socio-economic status were

significantly associated with good periodontal health. Furthermore, work-related mental

demands were found to be associated with alterations in salivary flow and changes in the

immune system and not associated with risk-related behaviors such as dental attendance

and/or tooth-brushing frequency (Marcenes & Sheiham, 1992). A retrospective study by

Freeman and Gross found that occupational stress factors predicted pocket depth

(Freeman & Gross, 1993). Lastly, Linden et al. showed that increased age, lowered socio-

economic status, lowered job satisfaction and the presence of a type A personality

(characterized by competitiveness and excessive drive) could predict a loss in periodontal

attachment (Linden et al., 1996).

Later studies which were designed to better understand the general relationship between

stress and chronic periodontitis utilized case-control methodology and questionnaire data

to determine stress level and clinical data to determine periodontal status. Moss et al.

found an association between T. forsythus and case status. As well, measures of smoking

status and levels of antibodies for Actinobacillus actinomycetemcomitans & P. gingivalis

were higher in cases compared with controls (Moss et al., 1996). Croucher et al. showed

that both the number of negative life events and the number of negative life events

weighted by the impact of the event on the person were significantly associated with

periodontitis. Moreover, the observed association between negative life events and

periodontitis remained significant even after adjusting for smoking status (Croucher et

al., 1997). Teng et al. found a dose-response relationship between psychosocial stress and

chronic periodontitis (Teng et al., 2003).

Studies have also investigated the relationship between stress and healing after

periodontal therapy. Axtelius et al. investigated stress as it relates to the pathogenesis of

therapy-resistant periodontitis. Those patients who did not respond favorably to therapy

showed various indicators of stress and vulnerability both in the past and in the present.

Those patients also showed more passive dependence (submissively help seeking,

dependent on other people) in comparison to those who responded well and who had a

13

more rigid-compulsive stress coping behavior. The results emphasized the importance of

assessing the psychological profile of patients who do not respond to traditional

periodontal therapy (Axtelius et al., 1998). Vettore et al described a dose-response

relationship between an individual’s mean anxiety score and the severity of chronic

periodontitis observed. Furthermore, a relationship between anxiety and periodontal

healing was also reported given that non-stressed individuals showed a significant

improvement in periodontal parameters after treatment compared with individuals who

were stressed (Vettore et al., 2005). Kloostra et al., showed that patients with stress had

more pain and delays in wound healing after periodontal surgery than did those with less

stress (Kloostra et al., 2006).

B) Depression

Clinical depressive disorder is an affective disorder which has consistently demonstrated

immunologic challenges. Genco et al. in 1999 investigated the relationship of periodontal

disease in adults to stress, distress, and coping and found that depression was associated

with greater levels of clinical attachment loss (CAL) and alveolar bone loss (Genco et al.,

1999). Ng & Leung examined the relationship of periodontal disease to psychosocial

stress and found that depression was a significant risk indicator for CAL. Compared to

healthy subjects, there were trends of more severe psychological symptoms of depression

in those with more severe CAL (Ng & Leung, 2006). Moss et al. explored the role of

depression as a host factor which could influence the progression of chronic periodontitis

and found that an individual’s case status and presence of T. forsythus were associated

with higher levels of depression (Moss et al., 1996). More recently, Kloostra et al.

showed that the more depressed a patient was, the more pain they had post-periodontal

surgery, the stronger the pain medication they used, and the more delayed their wound

healing was after surgery (Kloostra et al., 2006).

C) Social Support

The relationship between marital status and periodontal disease has been investigated.

Marcenes & Sheiham in 1992 used questionnaire data to show that higher levels of

marital quality were significantly associated with better periodontal health status

14

(Marcenes & Sheiham, 1992). Croucher et al. assessed the role of life events in

periodontitis and found that marital status becomes statistically significant after adjusting

for all of the other variables (Croucher et al., 1997).

Merchant et al. utilized data from an ongoing Health Professionals questionnaire-based

prospective study in order to explore the association between anger expression, social

support and periodontitis in a cohort of middle-aged to older men. Men who had more

social support were less likely to develop periodontitis. Moreover, men who reported

having at least one close friend or who participated in religious services were at an even

greater reduced risk of developing periodontitis (Merchant et al., 2003).

D) Coping

An individual’s ability to cope with difficulties and problems as well as their past

experience with traumatic life events is important in determining an individual’s

susceptibility to periodontal infections (Hugoson et al., 2002). Numerous studies have

explored the relationship between coping with a stressor and chronic periodontitis.

Adequate coping behaviors, either low emotion-focused coping or high problem-focused

coping, combined with an internal locus of control, results in little or no effect on

periodontal status. By contrast, the inability to cope adequately with chronic stress leads

to more severe periodontal disease.

A large population-based, cross-sectional study by Genco et al. investigated whether

periodontal disease in adults was related to stress, distress, and / or coping strategies

(Genco et al., 1999). The results showed that stress (ie, financial strain) and depression

were associated with greater levels of CAL or alveolar bone loss. Furthermore,

individuals who possessed problem-based and not emotion–based coping strategies, even

when under financial strain, exhibited no more periodontal disease than those individuals

under no financial strain.

A retrospective case-control study conducted by Wimmer et al. evaluated the stress

coping patterns used by patients with periodontal disease and found that patients with

15

periodontitis used both distractive and defensive coping strategies more than active

coping strategies. In addition, a greater number of patients with severe disease had a

defensive coping style compared with patients with mild or moderate disease (Wimmer et

al., 2002). Hugoson et al. studied periodontal disease in relation to the prevalence of

negative life events and psychological factors, and showed that age, oral hygiene,

smoking, loss of a spouse and the personality trait of having an external locus of control

(characterized by poorly developed strategies to cope with stressful life events) was

significantly associated with an increased risk of severe periodontal disease (Hugoson et

al., 2002).

VI) Putative Mechanisms Underlying the Impact of Psychosocial Factors on

Chronic Periodontitis

Several mechanisms have been described that could explain why both stress and

depression are linked to chronic periodontitis. PNI studies have shown that physiological

responses to emotional stressors and depression can modulate the immune system

through the neural and endocrine systems. This might occur by 1) the release of

hypothalamic and pituitary hormones via the hypothalamic-pituitary-adrenal axis (HPA),

2) autonomic nervous system pathways, specifically the sympathetic-adrenal medullary

axis (SAM), and / or 3) the release of neuropeptides such as substance P (SP).

Alternatively, the stress response or depression could lead to behavioral changes which in

turn could have an impact on chronic periodontitis (Breivik et al., 1996; Genco et al.,

1998; Monterio da Silva et al., 1995).

There are two proposed models to evaluate the role of psychosocial stress and coping

behaviors in periodontal disease. The first model focuses on both the HPA and SAM axes

while the second model centers on the behavioral changes that might lead to

immunosupression (Genco et al., 1998; Monterio da Silva et al., 1995).

Model #1: Mental stress response which triggers either the HPA or SMA axis, resulting

in immunosuppressive effects.

16

In this model, activation of the central nervous system (CNS) by psychosocial stress

triggers the hypothalamus to release corticotrophic-releasing hormone (CRH) which in

turn stimulates the pituitary to release adrenocorticotrophic hormone (ACTH). It is this

latter step which causes the production of the cortisol by the adrenal cortex. Cortisol, a

glucocorticosteroid, depresses immunity by reducing the levels of secretory IgA, IgG,

and PMN function, all of which are important in protecting the host against periodontal

infection. Secretory IgA antibodies prevent and / or reduce the organism’s ability to

colonize the tooth surface whereas IgG antibodies are thought to exert protection by

modifying periodontal organisms for PMN killing. This cascade of decreased immune

surveillance activity can then give rise to increased susceptibility to disease thus leading

to periodontal infection and ultimately to the establishment of destructive periodontitis

(Genco et al., 1998; Monterio da Silva et al., 1995). Mental as well as physical stress can

also result in responses being transmitted to the autonomic nervous system and then to

the adrenal medulla, resulting in secretion of catecholamines such as epinephrine (E) and

norepinephrine (NE). Catecholamines upregulate prostaglandin and protease production

or activity which in turn could enhance periodontal destruction (Genco et al., 1998;

Monterio da Silva et al., 1995).

A feedback loop which regulates the inflammatory response is dependent upon effective

communication between the neuroendocrine and immune systems. That being said,

manifestations of systemic illness will be clinically evident if an inflammatory reaction

triggered by a psychological stressor is either profound or prolonged. There is no reason

to believe that chronic periodontitis would be any different in this regard (LeResche &

Dworkin, 2002).

17

Model #2: Mental stress response which leads to behavioral changes.

The second model states that the effects of stress are derived through stress-induced

alterations in the behavior of the host. These behaviors, which include smoking, poor oral

hygiene and poor compliance, likely play an important role in the initiation, progression

and response to the treatment of periodontitis. Furthermore, overeating (especially a high-

fat diet) also leads to the production of increased levels of cortisol which in turn could

lead to immunosupression and the development and progression of chronic periodontitis

(Genco et al., 1998; Monterio da Silva et al., 1995).

Autonomic Nervous System

Activation of CNS Hypothalamus

(CRH)

Pituitary (ACTH)

Adrenal Cortex (Cortisol)

Adrenal Medulla (NE, E)

Prostaglandins and Proteases

Depressed Immunity

(sIgA, IgG, PMN)

Infection

Adequate Coping - + Inadequate Coping

Acute + + Chronic

- +

-

+

+ IL-1B, MMP +

+

+

Model 1: (Genco et al., 1998; Monterio da Silva et al., 1995)

Psychosocial Stress

Periodontal Disease

18

Neuropeptides - SP:

Emotional stressors can modulate the immune system and the release of pro- and anti-

inflammatory cytokines. Through the release of neuropeptides found within neural tissue,

SP, which is secreted from sensory C-type nerve fibres, may be of particular interest for

immune reactions in the gingiva and the periodontium when triggered by dental plaque

bacteria (Breivik et al., 1996). SP causes vasodilation, increased blood flow and can

enhance the microvascular permeability in the gingival connective tissues. The initial

action of SP is to promote and direct the inflammatory and immune response in infected

and/or damaged tissues. It has numerous effects such as the stimulation of neutrophil

chemotaxis, osteoclast stimulation, T-cell proliferation and antibody production, the

regulation of gingival fibroblast proliferation and the release and expression of IL-1B,

interleukin 6, and TNF-a. It is generally inhibitory at high concentrations and stimulatory

at low concentrations (Breivik et al., 1996; Azuma et al., 2004).

Psychosocial Stress

Periodontal Disease

Behavioral Change

Poor Oral Hygiene,Poor Compliance

Smoking Overeating (High-fat diet)

Cortisol

Bacterial Infection

+

+

+

+

+ +

+

+

Depressed Immunity

Model 2: (Genco et al., 1998; Monterio da Silva et al., 1995)

19

SP is detected in gingival tissues and gingival crevicular fluid (GCF) of both healthy

individuals and patients with periodontitis. However, the SP level of GCF is significantly

higher than that of healthy persons. The peripheral release of SP is regulated by stress

hormones such as NE and it has been shown that blocking SP-releasing nerves reduces

inflammation and immune cell mobilization in ligature-induced periodontitis in animals.

Thus, long-lasting emotional stress may increase SP release resulting in enhanced and/or

imbalanced inflammatory reactions. This may promote tissue damage and destruction of

alveolar bone, resulting in chronic periodontal disease (Azuma et al., 2004).

20

OBJECTIVES OF THE STUDY

(1) To validate an enhanced questionnaire designed to measure stress and social

support in patients with chronic periodontitis.

(2) To determine if patients with chronic periodontitis are under increased stress and

have more depressive symptoms compared to healthy controls.

(3) To determine if the social support level of patients with chronic periodontitis

differs from that of healthy controls

HYPOTHESES

(1) Our enhanced questionnaire is valid and reliable for measuring stress and social

support in patients with chronic periodontitis.

(2) Patients with chronic periodontitis suffer from greater perceived stress and

depression than those without periodontal disease.

(3) Patients with chronic periodontitis have less social support than those with no

periodontal disease.

21

MATERIALS AND METHODS

I) Study Population and Clinical Protocol

This study was approved by the Scientific and Ethics Review Board at the University of

Toronto prior to its commencement. The study protocol was explained to each potential

subject and written informed consent was obtained. Questionnaire packages (including

the enhanced questionnaire, the CES-D, the PSS, the LEQ, and the MSPSS) (Appendix

1) were given to patients who were diagnosed with chronic periodontitis at the Graduate

Periodontal Clinic at the Faculty of Dentistry, University of Toronto during the period of

September 2006 and May 2007. Identical packages were given to patients from the

Second Year Periodontal Recall Program at the Faculty of Dentistry, University of

Toronto during the period of January 2007 to March 2007. This formed the control group.

Re-test questionnaires were handed out to case patients and were mailed out to control

patients. All patients had until June 2007 to complete the follow-up questionnaire.

Sample size, as determined in the study by Safa & Glogauer, 2007, was found to be 30

per group to achieve adequate power.

Patients with chronic periodontitis were grouped into one of two groups based on severity

of disease; mild/moderate and severe. Severity was determined by probing depth (PD).

The mild/moderate group had fewer than 10 pockets that were greater than 5 mm and the

severe group had more than 10 pockets that were greater than 5 mm (Mancini et al.,

1999). Those in the control group had no clinical signs of periodontal disease (no PD >

5mm). In order to develop standardized measuring techniques which would enable a

consistent diagnosis, the first and second year Graduate Periodontal Residents were

calibrated to ensure inter-examiner reliability when assessing patients that were to be

included in this study. See Appendix 2 for details.

II) Overall Study

The primary objective of this investigation was to validate an enhanced questionnaire that

measured stress and social support in patients with chronic periodontitis. A secondary

22

objective was to compare the level of stress, depression, and social support in patients

with chronic periodontitis versus patients with no periodontal disease (a case control

study).

Electronic and manual searching of the literature was performed. Databases searched

included Medline (from 1950 to November Week 2 2008), Medline In-Process (up to

November 21 2008), PsychInfo (up to November 2008), and Health and Psychosocial

Instruments (from 1985 to April 2007). Manual searching was based on cited studies in

relevant papers. Two separate literature searches were conducted. The first searched for

validated questionnaires on depression, stress, and social support and the second searched

for general information on stress, depression, and social support.

The enhanced questionnaire used in this study was shortened to include only those

questions that were significantly associated with disease (Safa & Glogauer, 2007). The

questionnaire consisted of 21 questions in total; 4 on acute stress, 6 on chronic stress, and

11 on social support. The 11 questions on social support were subdivided into four social

support questions, two social involvement questions, and five social contact questions.

The CES-D was added to the package as a means to measure depression. The PSS, LEQ,

and MSPSS were included to validate the enhanced questionnaire (Appendix 1).

III) Statistical Analysis

Calibration: Statistical analysis consisted of calculations of percent agreement within a

pre-specified margin.

Questionnaire Data: Statistical analysis was performed to assess: concurrent validity, test-

retest reliability, and to examine the results of both of the enhanced questionnaire and the

CES-D. In order to assess the concurrent validity of the questionnaire, the analysis

consisted of: Pearson’s correlation coefficient and Spearman’s rank correlation

coefficient. In order to assess test-retest reliability of the questionnaire, the analysis

23

consisted of: Intraclass correlation coefficient and percent accuracy with its standard

error and 95% confidence interval.

To assess the relationship between stress, depression, social support and chronic

periodontitis, descriptive statistics (mean scores, standard deviations, and t-tests) were

used to describe the data. In addition, bivariate analysis was performed using Chi-squared

tests to analyze the results based on both data driven classification and on classification

based on a previous study by Safa & Glogauer, 2007. Multivariate analysis, to analyze

the association between stress and social support, used logistic regression to adjust for

other factors.

24

RESULTS

Of the 101 case patients with chronic periodontitis, 69 (68.32%) had mild/moderate

disease and 32 (31.68%) had severe disease. Fifty patients with no periodontal disease

were included as controls. The control group ranged in age from 43 to 76 years (59.94 +

16.22, mean + SD) and was significantly older than the case group which ranged in age

from 39 to 65 (52.76 + 12.81) (p = 0.008). The control group was also significantly older

than both the mild/moderate group (53.84 + 13.29) and the severe group (50.44 + 11.57)

(p=0.008) (Tables 1 and 2). Forty-three percent of the cases were male and 57% were

female (Tables 1 and 2). Of the 50 controls, 54% were female and 46% were male (Table

1). Approximately 26% of cases (21.74% had mild/moderate disease and 34.38% had

severe disease) were smokers compared with only 10% of controls (p = 0.03)) (Tables 1

and 2). Overall, both age and smoking status were confounding variables in this study.

See Appendix 3 for percent of total responses for each question of the enhanced

questionnaire.

Table 1: Demographics of Controls vs. Cases

Demographic

Characteristic of

Subjects

Controls

(N = 50)

Cases

(N = 101)

P-value

Age (Mean, SD) 59.94 + 16.22 52.76 + 12.81 0.008*

Sex (%)

M

F

46.00

54.00

43.00

57.00

0.73

Smokers (%)

Yes

No

10.00

90.00

25.74

74.26

0.02*

* statistically significant at 5% level

25

Table 2: Demographics of Healthy Controls vs. Mild/Moderate vs. Severe Disease

Demographic

Characteristic of

Subjects

Healthy

Controls

(N = 50)

Mild/Moderate

(N = 69)

Severe

(N = 32)

P-value

Age (Mean, SD) 59.94 + 16.22 53.84 + 13.29 50.44 + 11.57 0.008*

Sex (%)

M

F

46.00

54.00

42.65

57.35

43.75

56.25

0.94

Smokers (%)

Yes

No

10.00

90.00

21.74

78.26

34.38

65.63

0.03*

* statistically significant at 5% level

I) Validation of the Enhanced Questionnaire

We used a continuous scale to assess our data so as to not loose information by

categorization. We used Pearson’s correlation coefficient and found evidence of

moderate to low concurrent validity for the sections on chronic stress and social support.

This was demonstrated by a weak positive association between both chronic stress and

the LEQ (p = 0.03) and between social support and the MSPSS questionnaire (p = 0.001).

There was a non-significant trend towards validity for the acute stress section of the

questionnaire. See Table 3.

Table 3: Pearson’s Correlation

Pearson’s Correlation P-value

Acute Stress vs. PSS

(N = 149)

0.14 0.09

Chronic Stress vs. LEQ

(N = 150)

0.19 0.02 *

Social Support vs. MSPSS

(N = 150)

0.27 0.001 *

* statistically significant at 5% level

26

Similar results were found using Spearman’s rank correlation coefficient (Table 4).

Table 4: Spearman’s Correlation

Spearman’s Correlation P-value

Acute Stress vs. PSS

(N = 149)

0.13 0.12

Chronic Stress vs. LEQ

(N = 150)

0.21 0.01*

Social Support vs. MSPSS

(N = 150)

0.23 0.005 *

* statistically significant at 5% level

II) Test-Retest Reliability of the Enhanced Questionnaire

Thirty-two participants (31.68%) of the 101 cases and 17 participants (34%) of the 50

controls were used in the test-retest component of this study (Table 5).

Table 5: Number of Participants for Test-retest Reliability Component of Study

Group N Number of

Participants

Percentage of

Participants

Cases 101 32 31.68 %

Controls 50 17 34 %

In order to analyze the proportion of variance in scores which were related to the true

variance we assessed the test-retest reliability using the Intraclass correlation coefficient

(Table 6).

27

Table 6: Intraclass Correlation Coefficients for Case and Control Groups

Category on Enhanced

Questionnaire

Number of

Items

Cases Controls

Acute Stress 4 0.90 0.93

Chronic Stress 6 0.73 0.80

Total Stress 10 0.96 0.96

Social Support 4 0.60 0.46

Social Involvement 2 0.92 0.93

Social Contact 5 0.54 0.38

Total Social Support 11 0.92 0.87

Using the Landis and Koch criteria for interpretation of the Intraclass correlation

coefficient (see Appendix 4) the acute stress, total stress, social involvement, and total

social support had very good agreement for both cases and controls. The chronic stress

section had good agreement for both cases and controls. The social support questions for

cases and controls and the social contact questions for cases had moderate agreement,

while the social contact questions for controls had fair agreement.

Percent accuracy with its standard error and 95% confidence intervals were reported next.

(Figure 1a, b, c, d, e and Appendix 5). It was decided that a confidence interval that

included 50% was not reliable. For the case group, the two social involvement questions

had a low percent accuracy and a 95% confidence interval below 50%. Both

“Participation in activities” had a percent accuracy of: 56.25% and a 95% CI: 39.06 to

73.44 and “Attend religious services” had a percent accuracy of: 65.63% and a 95% CI:

49.17 to 82.08. The “Participation in activities” question also had a low percent accuracy

(47.06%) and a confidence interval below 50% for the control group (95% CI: 23.33 to

70.79).

As well, three of the social contact questions had a low percent accuracy and a 95%

confidence interval below 50% for both cases and controls. These three social contact

28

questions were: “Parents/parents in-law” (65.63%; 95% CI: 49.17 to 82.08 and 64.71;

95% CI: 41.99 to 87.42, for cases and controls respectively), “Brothers/sisters” (65.63%;

95% CI: 49.17 to 82.08 and 70.59%; 48.93 to 92.25, for cases and controls respectively),

and “Close friends/relatives” (65.63%; 95% CI: 49.17 to 82.08 and 64.17%; 95% CI:

41.99 to 87.42, for cases and controls respectively).

Prop

ortio

n of

sam

e re

spon

ses

Acute stress questions

29

Chronic stress questions

Prop

ortio

n of

sam

e re

spon

ses

Prop

ortio

n of

sam

e re

spon

ses

Social support questions

30

Overall, there was evidence to conclude that test-retest reliability was present for the

enhanced questionnaire for both cases and controls. Weaker question categories were

Social contact questions

Social involvement questions

Prop

ortio

n of

sam

e re

spon

ses

Prop

ortio

n of

sam

e re

spon

ses

31

social contact questions for the control group, which only had fair agreement. When

examining specific questions, weaker questions included the social involvement

questions: “Participation in activities” for the control group, “Attend religious services”

and “Participation in activities” for the case group, and the social contact questions

“Parents/parents in-law,” “Brothers/sisters,” and “Close friends/relatives” for both the

cases and control groups.

III) Preliminary Testing of the Relationship Between Stress, Social Support and

Chronic Periodontitis

Mean scores, standard deviations, and results of t-tests were reported in Tables 7 and 8

for stress and social support measures from the enhanced questionnaire. Data were

reported for cases, healthy controls, patients with mild/moderate, and patients with severe

chronic periodontitis.

Table 7: Mean Scores, Standard Deviations, and P-values for Case and Control

Groups

Category on

Enhanced

Questionnaire

Number

of Items

Possible Range

of Scores

Cases (N=101)

(mean score + SD)

Controls (N = 50)

(mean score + SD)

P-value

Acute Stress 4 0 - 4 0.46 + 0.73 0.40 + 0.61 0.64

Chronic Stress 6 0 - 6 2.31 + 1.73 2.14 + 1.65 0.57

Total Stress 10 0 - 10 2.76 + 1.94 2.54 + 1.81 0.50

Social Support 4 0 - 4 3.61 + 0.91 3.58 + 0.81 0.82

Social Involvement 2 0 - 8 2.68 + 2.51 2.68 + 2.53 0.99

Social Contact 5 0 - 20 10.96 + 4.28 9.00 + 2.51 0.001*

Total Social

Support

11 0 - 32 17.26 + 5.54 15.26 + 3.76 0.01*

* statistically significant at 5% level

32

Table 8: Mean Scores, Standard Deviations, and P-values for Healthy Controls,

Mild/Moderate, and Severe Groups

Category on

Enhanced

Questionnaire

Healthy Controls

(N = 50)

(mean score + SD)

Mild/Moderate

(N = 69)

(mean score + SD)

Severe

(N = 32)

(mean score + SD)

P-value

Acute Stress 0.40 + 0.61 0.49 + 0.78 0.38 + 0.61 0.66

Chronic Stress 2.14 + 1.65 2.28 + 1.76 2.38 + 1.68 0.82

Total Stress 2.54 + 1.81 2.77 + 1.96 2.75 + 1.92 0.80

Social Support 3.58 + 0.81 3.55 + 0.99 3.75 + 0.67 0.55

Social

Involvement

2.68 + 2.53 2.59 + 2.48 2.88 + 2.59 0.87

Social Contact 9.00 + 2.51a 10.59 + 4.06a,b 11.75 + 4.68b 0.005*

Total Social

Support

15.26 + 3.76a 16.74 + 5.40a.b 18.38 + 5.76b 0.02*

* statistically significant at 5% level

Means with the same superscript letter are not significantly different using the Tukey

HSD Test.

(i) Bivariate Analysis:

Acute stress, chronic stress, total stress, social support, social involvement, social contact,

and total social support were analyzed in relation to healthy versus mild/moderate versus

severe disease, without adjusting for other factors. The data were analyzed based on both

data driven classification and on classification based on a previous study by Safa &

Glogauer, 2007, using Chi-squared analysis. Mean scores were the total mean score for

all subjects. Percentages above the mean for measures of stress, indicated that stress was

present. Percentages above the mean for social support, indicated that social support was

present.

a) First, data were analyzed based on data driven classification. See Tables 9 and 10 and

Figures 2 and 3.

33

Table 9: Stress and Social Support for Cases vs. Controls

– based on data driven means

Category on Enhanced

Questionnaire (mean score)

Cases (N=101)

(% above mean)

Controls (N=50)

(% above mean)

P-value

Acute Stress

(0.13)

34.69 34.69 NS

Chronic Stress

(0.43)

52.53 50 0.77

Total Stress

(0.31)

46.53 44 0.77

Social Support

(0.88)

80.20 76 0.55

Social Involvement

(1.37)

48.51 50 0.86

Social Contact

(2.09)

56.44 34 0.009*

Total Social Support

(1.52)

54.46 36 0.03*

* statistically significant at 5% level

34

Table 10: Stress and Social Support for Healthy vs. Mild/Moderate vs. Severe

– based on data driven means

Category on Enhanced

Questionnaire

(mean score)

Healthy

(N=50)

(% above mean)

Mild/Moderate

(N=69)

(% above mean)

Severe

(N=32)

(% above mean)

P-value

Acute Stress

(0.13)

34.69 35.29 33.33 0.99

Chronic Stress

(0.43)

50 51.47 54.84 0.91

Total Stress

(0.31)

44 44.93 50 0.86

Social Support

(0.88)

76 78.26 84.38 0.66

Social Involvement

(1.37)

50 44.93 56.25 0.56

Social Contact

(2.09)

34 50.72 68.25 0.008*

Total Social Support

(1.52)

36 50.72 62.50 0.06

* statistically significant at 5% level

35

Perc

ent o

f sub

ject

s ab

ove

mea

n sc

ore

Sections of questionnaire

Perc

ent o

f sub

ject

s ab

ove

mea

n sc

ore

Sections of questionnaire

36

Chi-squared analysis of disease status using classified/dichotomized data derived from

means as above or below the mean on the enhanced questionnaire, showed no significant

association between acute stress, chronic stress, or total stress and disease status (p>0.05).

There was a trend, however, for cases and patients with more severe disease to have more

total stress than controls.

Chi-squared analysis demonstrated that social contact and total social support were

correlated significantly and positively with disease status. Patients in the ‘case’ group had

significantly more social contact (p = 0.009) and total social support (p = 0.03) than

patients in the control group. As well, patients with severe disease had more social

contact than those with mild/moderate disease, who had more social contact than those

who were healthy (p = 0.008).

b) Next, data was analyzed using the classification based on a previous study by Safa &

Glogauer 2007. See Tables 11 and 12 and Figures 4 and 5.

Table 11: Stress and Social Support for Cases and Controls

– based on Safa & Glogauer, 2007 driven means

Category on Questionnaire

(mean score)

Cases (N=101)

(% above mean)

Controls (N=50)

(% above mean)

P-value

Acute Stress

(0.12)

33.66 34 0.97

Chronic Stress

(0.61)

29.70 22 0.32

Social Support

(0.87)

80.20 76 0.55

37

Table 12: Stress and Social Support for Healthy vs. Mild/Moderate vs. Severe

– based on Safa & Glogauer, 2007 driven means

Category on

Questionnaire

(mean score)

Healthy

(N=50)

(% above mean)

Mild/Moderate

(N=69)

(% above mean)

Severe

(N=32)

(% above mean)

P-value

Acute Stress

(0.12)

34 34.78 31.25 0.94

Chronic Stress

(0.61)

22 28.99 31.25 0.59

Social Support

(0.87)

76 78.26 84.38 0.66

Perc

ent o

f sub

ject

s ab

ove

mea

n sc

ore

Sections of questionnaire

38

Chi-squared analysis of disease status using the classification based on a previous study

by Safa & Glogauer 2007, showed no significant association between stress or social

support and disease status (p>0.05).

Perc

ent o

f sub

ject

s ab

ove

mea

n sc

ore

Sections of questionnaire

39

c) Data were then analyzed to investigate the association between stress and social

support, using Chi-squared analysis. See Table 13.

Table 13: Association Between Stress and Social Support

Social Support (%) No Social Support (%) P-value

Acute Stress

(N=51)

49.02 50.98

No Acute Stress

(N=96)

48.96 51.04 0.99

Chronic Stress

(N=77)

37.66 62.34

No Chronic Stress

(N=72)

59.72 40.28 0.007*

Total Stress

(N=69)

36.23 63.77

No Total Stress

(N=82)

58.54 41.46 0.006*

* statistically significant at 5% level

When analyzing the combined data for all cases and controls, no significant association

between acute stress and social support (p = 0.99) was found. Both chronic stress and

total stress showed a significant association with social support (p = 0.007 and p = 0.006,

respectively). The above findings showed that 59.72% of subjects who had social support

scores above the mean (high social support) had chronic stress scores below the mean

(low stress), while 62.34% of subjects who had social support scores below the mean

(low social support) had chronic stress scores above the mean (high stress). Accordingly,

58.54% of subjects who had social support scores above the mean (high social support)

had total stress scores below the mean (low stress), while 63.77% of subjects who had

40

social support scores below the mean (low social support) had total stress scores above

the mean (high stress).

Overall, there was a significant, inverse, association between social support and chronic

and total stress. Subjects who had increased social support had decreased chronic and

total stress, while subjects who had decreased social support had increased chronic and

total stress. There was no significant association between social support and acute stress.

d) Chi-squared analysis was then completed to investigate the results of the depression

scale used in this study, the CES-D. A score of 16 or greater on the questionnaire

indicated depression (Andresen et al.,1994). See Table 14 and 15.

Table 14 - CES-D for Controls versus Cases

Controls (%) Cases (%) P-value

CES-D score <16 80 74.26

CES-D score >16

(depression)

20 25.74

0.44

Table 15 - CES-D for Healthy vs. Mild/Moderate vs. Severe Disease

Healthy

Controls (%)

Mild / Moderate (%) Severe (%) P-value

CES-D score

<16

80 75.36 71.88

CES-D score

>16 (depression)

20 24.64 28.13

0.69

The results showed that there was insufficient evidence of a significant association in

CES-D scores between the controls and cases (p = 0.44) or between the healthy vs.

mild/moderate vs. severe groups (p = 0.69). There was a trend towards cases having more

depression than controls and a trend for patients with severe disease having more

depression than patients with mild/moderate disease and healthy controls.

41

(ii) Multivariate Analysis:

Acute stress, chronic stress, total stress, social support, social involvement, social contact,

and total social support were entered into logistic regression equations which provided

odds ratios (controlling for other variables) and were evaluated in relation to cases versus

controls, mild/moderate disease versus healthy patients, and severe disease versus healthy

patients. All variables were dichotomized at their mean scores. The goodness of fit of the

models was checked and it was found that the fit was good for the models.

Multivariate Analysis for Cases versus Controls

The odds ratios comparing cases to controls are presented in Table 16 for stress and

social support variables. Those with social contact were 2.31 times more likely to be

cases as compared to controls (p = 0.04). Also those with total social support were 2.35

times more likely to be cases as compared to controls (p = 0.03). These differences were

statistically significant.

Table 16: Logistic Regression Analysis – Cases vs. Controls

Parameter Adjusted OR* P-value

Acute Stress 1.67 0.24

Chronic Stress 1.15 0.74

Total Stress 1.14 0.76

Social Support 1.21 0.69

Social

Involvement

0.95 0.89

Social Contact 2.31 0.04**

Total Social

Support

2.35 0.03**

*from separate models controlling for: age, gender, smoking status and

either stress or social support.

** statistically significant at 5% level

42

Multivariate Analysis for Mild/Moderate Disease versus Healthy

The odds ratios comparing mild/moderate disease versus healthy are presented in Table

17 for stress and social support variables. There were no significant associations in this

analysis.

Table 17: Logistic Regression Analysis –Mild/Moderate Disease vs. Healthy

Parameter Adjusted

OR*

P-value

Acute Stress 1.84 0.19

Chronic Stress 1.09 0.84

Total Stress 1.11 0.87

Social Support 1.04 0.95

Social

Involvement

0.85 0.69

Social Contact 1.84 0.15

Total Social

Support

1.90 0.13

* from separate models controlling for: age, gender, smoking status and

either stress or social support.

43

Multivariate Analysis for Severe Disease versus Healthy

The odds ratios comparing severe disease versus healthy are presented in Table 18 for

stress and social support variables. Patients with social contact were 5.26 times more

likely to have severe disease as opposed to being healthy (p = 0.007). Also patients with

total social support were 5.75 times more likely to have severe disease as opposed to

being healthy (p = 0.008). These differences were statistically significant.

Table 18: Logistic Regression Analysis –Severe Disease vs. Healthy

Parameter Adjusted

OR*

P-value

Acute Stress 1.12 0.86

Chronic Stress 1.31 0.67

Total Stress 1.11 0.87

Social Support 1.85 0.38

Social

Involvement

1.48 0.47

Social Contact 5.26 0.007**

Total Social

Support

5.75 0.008**

* from separate models controlling for: age, gender, smoking status and

either stress or social support.

** statistically significant at 5% level

Overall, when the data were analyzed using multivariate analyses, it showed that there

was insufficient evidence to confirm a meaningful association between stress and

periodontal disease status. There was evidence of an association between social contact

and total social support with disease status when controls and cases were compared as

well as when healthy controls and patients with severe disease were compared. Patients in

both the case and severe disease categories had significantly more social contact and total

social support than healthy controls.

44

DISCUSSION

Questionnaires designed to investigate acute and chronic stressors, depression and social

support among patients with periodontal disease were utilized in this study. Statistical

analysis of the data collected from individuals with and without disease was performed to

validate our enhanced questionnaire and to establish a relationship between periodontal

disease status and levels of stress, depression and social support. The results and

limitations of this study are discussed below.

I) Questionnaire

Our primary objective was to determine both the validity and the test-retest reliability of

our enhanced questionnaire designed to specifically measure levels of stress and social

support in patients with chronic periodontitis. Overall, our data showed that the sections

on chronic stress and social support were valid and that the section on acute stress

revealed a trend towards being validated. Furthermore, the questionnaire’s test-retest

reliability for both the case group and the control group was conclusive.

Our secondary objective was to test our enhanced questionnaire in combination with the

CES-D in order that we may establish a relationship between stress, depression and social

support in patients with chronic periodontitis.

Initially, we sought to determine if patients with chronic periodontitis were under

increased stress and showed more depressive symptoms compared to healthy controls.

Previous work has suggested that stress, when in combination with bacteria and dental

plaque-induced inflammation, triggers a sustained and inappropriate HPA axis response,

a SAM axis response, a release of neuropeptides, and / or behavioral changes. It has been

hypothesized that these changes when taken together may increase the susceptibility of an

individual to periodontal disease. (Page, 1991; Genco et al., 1998; Monterio da Silva et

al., 1995, Hugoson et al., 2002). Similarly, depression has also been shown to be related

to chronic periodontal disease (Olff, 1999; Ng & Leung, 2006). However, in our study,

both bivariate and multivariate analyses showed that there was no significant association

between stress or depression and chronic periodontitis. That being said, there was a trend

45

for patients with periodontal disease to have more total stress and more depression than

those without disease. Incidentally, patients with severe disease tended to have greater

levels of total stress and more depression than patients with mild/moderate disease.

Bivariate analysis did however show a significant inverse association between social

support and both chronic stress and total stress. Patients who had increased social support

had decreased chronic and total stress whereas patients who had decreased social support

had increased chronic and total stress.

Next we wanted to establish whether differences in the level of social support existed

between these patients. Cohen and Syme in 1985 indicated that the social support of an

individual, regardless of that person’s level of stress, may directly enhance their health

and well-being. Alternatively, social support may act as a buffer thereby reducing or

eliminating the effects of the stressful experience (Cohen & Syme, 1985). In this study,

bivariate and multivariate analyses showed that both cases and patients with severe

disease had significantly more social contact and total social support than patients

without periodontal disease. Surprisingly, this finding refutes our third hypothesis.

The reasons for our inability to show a statistically significant difference in stress and

depression between patients with and without disease and that patients with disease had

significantly more social support than those without, could be explained by our patient

demographics. Our bivariate analyses did not control for the fact that patients without

disease were both older and smoked more than those with disease. By comparison,

smoking and age were controlled for in our multivariate analysis which showed acute

stress to have a trend toward significance (increased acute stress in diseased patients) in

both the case versus control analysis (p = 0.24) and the healthy versus mild/moderate

disease analysis (p = 0.19).

An accurate understanding of the risks and modifying factors of chronic periodontitis are

key to it’s successful clinical management. Unfortunately, dentists and specialists alike

have not been properly trained to effectively assess the psyche of a patient. Kloostra et

al. reported that periodontists are neither knowledgeable nor confident in their abilities to

46

treat patients with stress and in particular those patients who are clinically depressed

(Kloostra et al., 2007). Thus, validated questionnaires designed to assist a dental care

professional in the determination of a patient’s psychosocial condition would be useful

for the management of chronic periodontitis in routine dental or periodontal practice.

II) Limitations of the Study

It could be argued that PNI markers of stress should replace the use of questionnaires

when measuring a person’s mental health. However, such tests are not practical in a

clinical setting and would likely increase the cost of care substantially. By contrast,

questionnaires could be routinely used by dentists as a means of collecting pertinent

information about a patient’s stress level in nonintrusive way. Moreover, the collection of

such information would enable the dentist to take into account a patient’s stress during

the course of periodontal treatment. It is equally important to take into account people’s

perceptions of each event as the total number of life events may not be related to any

health outcome variable. This should be attainable by way of the questionnaire.

Interestingly, this may explain why some studies fail to demonstrate an association

between life-events and health (Croucher et al., 1997).

A true limitation of our study was our working definition of disease. Regrettably, studies

that examine the relationship between chronic periodontitis and stress and/or social

support utilize different criteria when defining the disease state. For example, some use

the criteria proposed by Machtei et al., 1992, which defines established periodontitis as

two or more individual teeth with CAL of >6mm and who also have one or more sites

with PD >5mm (Linden et al., 1996; Moss et al., 1996). In our study, a patient was

classed as having mild/moderate disease if they had fewer than 10 pockets with a PD

greater than 5 mm. Those classed as severe had more than 10 pockets with a PD greater

than 5 mm (Mancini et al., 1999). Patients with no clinical signs of periodontal disease

(no PD > 5mm) were classed as having no disease and treated as controls. It is this

inconsistency in defining disease status may have limited our ability to generalize our

findings.

47

Self-reported personal information which can be perceived as sensitive and thus, makes it

difficult to collect, was also considered a limitation of our study for several reasons. First,

our study was voluntary. Second, it is likely that some of the respondents choose to either

under-report or over-report. Third, a social desirability bias may have also been

introduced as there is a tendency of respondents to reply in a manner that will be viewed

favorably by others.

Individual perceptions of social strain and measures of physiologic distress may not

always equate with one another. An individual may readily report high levels of strain but

will be functioning at a very healthy level whereas an individual who reports low levels

of strain may be physiologically distressed. Thus, despite the complexity of an

individual’s social environment, every effort should be made to uncover common

patterns of social characteristics and circumstances (Moss et al., 1996). Perhaps the

questionnaire used in our study failed to adequately determine how respondents function

with their level of stress.

A final limitation may have been the fact that the patient’s stress response reported

reflected only recent symptoms and therefore was not related to the observed periodontal

disease which is a chronic event (Peruzzo et al., 2007). It is possible that the respondents

in this study consisted of patients at various stages of the periodontal disease process and

that symptoms of stress reported may not have correlated with disease status.

48

SUMMARY AND FUTURE DIRECTION

In summary, we demonstrated both the validity and the reliability of our enhanced

questionnaire designed to measure the level of stress and social support in patients with

chronic periodontitis. Furthermore, this questionnaire when administered in combination

with the CES-D, revealed a trend for cases and patients with more severe disease to have

increased total stress and depression compared with those without disease. There was

also a significant inverse association between social support and both chronic and total

stress which proves that stress-reduction protocols have some value in the management of

periodontal disease.

This questionnaire, if administered with the CES-D, could be used to by dental care

professionals to assess the levels of stress, depression and social support seen in patients

with periodontal disease. We hypothesize that this would help to establish both the

etiology and the prognosis of the disease.

Future research should further validate the acute stress section of our questionnaire and

be tested alongside the CES-D with a larger sample size and more consistent

demographics. In doing so, we speculate that an association between stress, depression,

social support and chronic periodontal disease would be revealed. Following

confirmation of these associations by longitudinal studies, it would be advised that such a

questionnaire be incorporated into patient charts so as to permit a more holistic approach

to the management of chronic periodontitis.

49

CONCLUSIONS

- Our enhanced questionnaire provides a valid and a reliable measure of stress and

social support in patients with chronic periodontitis.

- There was a trend for cases and patients with more severe disease to have

increased total stress and increased depression compared to healthy controls.

- There was a significant inverse association between social support and both

chronic and total stress.

50

APPENDIX 1 – QUESTIONNAIRE PACKAGE

INFORMATION AND CONSENT FORM

STRESS AND SOCIAL SUPPORT STUDY INVESTIGATORS: DRS. JILL LEVINE AND MICHAEL GLOGAUER

DEPARTMENT OF PERIODONTOLOGY, FACULTY OF DENTISTRY, UNIVERSITY OF TORONTO

INTRODUCTION: This research project is being carried out in the Department of Periodontology at the Faculty of Dentistry, University of Toronto. Dr. Glogauer is the supervising faculty member for this project. Dr. Levine is a dentist as well as graduate student in the Department of Periodontology. You have been asked to participate in this study because you are currently a patient in one of the clinics of the Faculty of Dentistry. PURPOSE: The purpose of this study is to assess the relationship of stress and social support to periodontal disease. The information obtained from patients taking part in this study may be valuable to future diagnosis, treatment and management of this disease. PROCEDURES: The project asks that you complete questionnaires on social support, stress, and depression. Information about your medical and dental history will also be obtained from your chart. You will be given a questionnaire to fill out in the future for comparison. RISKS OF PARTICIPATION: Since these are questionnaires on stress, social support, and depression, there exists the risk of upset of the participant. Please refer to the List of Resources on page three. There is no direct benefit to the participant, as the information gathered from this study may be valuable for future research. BENEFITS OF PARTICIPATION: It is expected that the information obtained from patients taking part in this study may be valuable for a better understanding of periodontal disease. By participating in this study you will be contributing to the production of new and potentially illuminating knowledge about periodontal disease. CONFIDENTIALITY: You will not be identified in any way. The questionnaire is coded and will not contain your name or any identifying feature, except a number code. The information that you provide will be coded and summarized with the information from all other patients taking part in this study. PARTICIPATION: Your participation in this study is strictly voluntary. Not participating will have no bearing on the treatment you receive or access to future treatment. You may leave the study at any time without consequence. If you wish to participate, please sign the consent form that follows.

51

QUESTIONS: If you have questions about your rights as a research subject, you may contact Dr. Rachel Zand, Manager, Research Ethics Office, telephone 416-946-3389. CONSENT: I acknowledge that the research procedures described on the attached form, and of which I have a copy, have been explained to me and that any questions that I have asked have been answered to my satisfaction. I have been informed of the alternatives to participation in this study. I know that I may ask now, or in the future, any questions I have about the study or the research procedure. I understand that while I will not benefit directly from the study, the information gained may assist both researchers and education professionals to better understand periodontal disease. I have been assured that records relating to my care will be kept confidential and that no information will be released or printed that would disclose my personal identity without my permission. I understand that I am free to withdraw from the study at any time. I further understand that if the study is not completed, or there is withdrawal from it at any time, the quality of dental care for me will not be affected. I hereby consent to participate. _______________________ ____________________ ____________ Patient’s name (Please Print) Patient’s Signature Date

52

Enhanced Questionnaire: A) PLEASE CIRCLE THE RESPONSE THAT FOR YOU BEST ANSWERS THE QUESTION. Have any of the following things happened to you or

anyone close to you (that is your spouse/partner,

children, relatives or close friends), in the past 12

months.

Yes No Not

Applicable

1. Was there a serious illness? Y N NA

2. Did a close friend die? Y N NA

3. Was there a marital separation or divorce? Y N NA

Did any of the following experiences happen to you in

the past two months? Yes No

Not

Applicable

4. Had a child move back into the house? Y N NA

B) PLEASE CIRCLE THE RESPONSE THAT FOR YOU BEST ANSWERS THE QUESTION The following describes some situations

that sometimes come up in people’s lives.

Please indicate whether these things are

not true, somewhat true, very true or not

applicable for you at this time.

Not

True

(NT)

Somewhat

True

(ST)

Very

True

(VT)

Not

applicable

(NA)

1. There is too much pressure on you to be like other people.

NT ST VT NA

2. You don’t have enough money to take vacations.

NT ST VT NA

3. You find it is too difficult to find someone compatible with you.

NT ST VT NA

4. You have to go to social events alone and you don’t want to.

NT ST VT NA

5. You don’t have time for your favorite leisure time activities.

NT ST VT NA

6. You would like to move but you cannot. NT ST VT NA

53

C) PLEASE CIRCLE THE ANSWER THAT FOR YOU BEST DESCRIBES THE QUESTION. YES NO

Do you have someone you can confide in or talk to about your private feelings or concerns?

Y N

Do you have someone you can really count on to help you out in a crisis situation? Y N

Do you have someone you can really count on to give you advice when you are making important personal decisions?

Y N

Do you have someone who makes you feel loved and cared for? Y N

PLEASE PUT A CHECK MARK IN THE COLUMN THAT BEST DESCRBIES YOUR RESPONSE.

Not at all

At least once a year

At least 3 or 4

times a year

At least once a month

At least once a week

How often did you participate in meetings or activities sponsored by voluntary organizations or associations (such as school groups, church social groups, civic, or fraternal clubs) in the past 12 months? If you belong to many, just think of the ones in which you are most active.

Other than on special occasions (such as weddings, funerals or baptisms), how often did you attend religious services or religious meetings in the past 12 months?

The next few questions are about contact in the past 12 months with persons who do not live with you. Contact could either be in person, by phone, by mail or e-mail. If you have more than one person in a category – for example, several sisters- think of the one with whom you have the most contact. How often did you have contact with (fill each line with the categories below)?

_____Your parents or parents-in-law _____Your grandparents _____Your children and/or their spouses _____Your brothers or sisters _____Your close friends and/or other relatives

0= don’t have any 1= never 2= less than once a month 3= once a month 4= more than once a month

54

Center for Epidemiologic Studies Depression Scale Below is a list of the ways you might have felt or behaved. Please tell me how often you have felt this way during the past week. 1 = Rarely or none of the time (less than 1 day). 2 = Some or a little of the time (1-2 days). 3 = Occasionally or a moderate amount of time (3-4 days). 4 = Most or all of the time (5-7 days).

DURING THE PAST WEEK: _____ 1. I was bothered by things that usually don’t bother me.

_____ 2. I did not feel like eating; my appetite was poor.

_____ 3. I felt that I could not shake off the blues even with help from my

family or friends.

_____ 4. I felt that I was just as good as other people.

_____ 5. I had trouble keeping my mind on what I was doing.

_____ 6. I felt depressed.

_____ 7. I felt that everything I did was an effort.

_____ 8. I felt hopeful about the future.

_____ 9. I thought my life had been a failure.

_____ 10. I felt fearful.

_____ 11. My sleep was restless.

_____ 12. I was happy.

_____ 13. I talked less than usual.

_____ 14. I felt lonely.

_____ 15. People were unfriendly.

_____ 16. I enjoyed life.

_____ 17. I had crying spells.

_____ 18. I felt sad.

_____ 19. I felt that people disliked me.

_____ 20. I could not get “going.”

55

Perceived Stress Scale

The questions in this scale ask you about your feelings and thoughts during the last month. In each case, you will be asked to indicate how often you felt or thought a certain way. Although some of the questions are similar, there are differences between them and you should treat each one as a separate question. The best approach is to answer each question fairly quickly. That is, don’t try to count up the number of times you felt a particular way, but rather indicate the alternative that seems like a reasonable estimate.

For each question choose from the following alternatives: 0. Never 1. Almost never 2. Sometimes 3. Fairly often 4. Very often

_____ 1. In the last month, how often have you been upset because of something that

happened unexpectedly? _____ 2. In the last month, how often have you felt that you were unable to control the

important things in your life? _____ 3. In the last month, how often have you felt nervous and stressed? _____ 4. In the last month, how often have you dealt successfully with irritating life

hassles? _____ 5. In the last month, how often have you felt that you were effectively coping

with important changes that were occurring in your life? _____ 6. In the last month, how often have you felt confident about your ability to

handle your personal problems? _____ 7. In the last month, how often have you felt that things were going your way? _____ 8. In the last month, how often have you found that you could not cope with all

the things that you had to do? _____ 9. In the last month, how often have you been able to control irritations in your

life? _____ 10. In the last month, how often have you felt that you were on top of things? _____ 11. In the last month, how often have you been angered because of things that

happened that were outside of your control? _____ 12. In the last month, how often have you found yourself thinking about things

that you have to accomplish? _____ 13. In the last month, how often have you been able to control the way you spend

your time? _____ 14. In the last month, how often have you felt difficulties were piling up so high

that you could not overcome them?

56

Life Events Questionnaire Have any of the following life events or problems happened to you during the last 6 months? Please check the box or boxes corresponding to the month or months in which any event happened or began. 1

month ago

2 months ago

3 months ago

4 months ago

5 months ago

6 months ago

N/A

1. You yourself suffered a serious illness, injury, or an assault.

2. A serious illness, injury, or assault happened to a close relative.

3. Your parent, child, or spouse died.

4. A close family friend or another relative (aunt, cousin, grandparent) died.

5. You had a separation due to marital difficulties.

6. You broke off a steady relationship.

7. You had a serious problem with a close friend, neighbor, or relative.

8. You became unemployed or you were seeking work unsuccessfully for more than one month.

9. You were fired from your job.

10. You had a major financial crisis.

11. You had problems with the police and a court appearance.

12. Something you valued was lost or stolen.

57

Multidimensional Scale of Perceived Social Support Read each statement carefully. Indicate how you feel about each statement by circling the appropriate number using the following scale: 1 = Very strongly disagree 2 = Strongly disagree. 3 = Mildly disagree. 4 = Neutral. 5 = Mildly agree. 6 = Strongly agree. 7 = Very strongly agree.

1. There is a special person who 1 2 3 4 5 6 7 is around when I am in need. 2. There is a special person with 1 2 3 4 5 6 7 whom I can share joys and sorrows. 3. My family really tries to help me. 1 2 3 4 5 6 7 4. I get the emotional help and 1 2 3 4 5 6 7 support I need from my family. 5. I have a special person who is a 1 2 3 4 5 6 7 real source of comfort to me. 6. My friends really try to help me. 1 2 3 4 5 6 7 7. I can count on my friends when 1 2 3 4 5 6 7 things go wrong. 8. I can talk about my problems 1 2 3 4 5 6 7 with my family. 9. I have friends with whom I can 1 2 3 4 5 6 7 share my joys and sorrows. 10. There is a special person in my 1 2 3 4 5 6 7 life who cares about my feelings. 11. My family is willing to help 1 2 3 4 5 6 7 me make decisions. 12. I can talk about my problems 1 2 3 4 5 6 7 with my friends.

58

APPENDIX 2 – Calibration

Calibration Methods:

The purpose of calibration was to develop standardized measuring techniques to ensure

that one is scoring the same condition the same way every time it is observed. The first

and second year Graduate Periodontal Residents at the Faculty of Dentistry, University of

Toronto were calibrated in order to help ensure inter-examiner reliability when assessing

patients that were to be included in this study.

The calibration training schedule consisted of an introduction to calibration by means of a

presentation and a calibration manual. Next, there was a session in which there was a

question and answer period about the calibration measures and practice with a scale in

order to calibrate the amount of probing force used during assessments. The amount of

force that everyone was calibrated to was 0.25 N (Armitage, 2004). Calibration was

performed on patients on two separate occasions. Three residents were calibrated on the

first day and three other residents were calibrated on the second day. All residents were

calibrated to the same gold standard, an assistant professor and head of Periodontology at

the Faculty of Dentistry.

The inclusion criteria for admission of patients into the calibration exercise were: 1) good

health, 2) minimum of 5 teeth/quadrant, 3) mild/moderate or severe chronic periodontitis,

and 4) two or more non-adjacent sites in a posterior sextant with greater or equal to 2mm

CAL and greater or equal to 5mm PD.

The exclusion criteria for patients in the calibration exercise were: 1) antibiotic

prophylaxis, 2) poor cooperation, 3) clinically significant chronic or acute illness (AIDS,

herpes, cardiovascular diseases, uncontrolled diabetes, etc), and 4) PD greater or equal to

10mm, grade 3 furcation and/or grade 3 mobility.

59

The nine clinical measurements that were performed for calibration were: Gingival index

(GI), Plaque index (PI), PD, Recession (Rec), CAL, Bleeding index (BI), Furcation

(Furc), Mobility (Mob), and Amount of attached gingiva (AG) (Lenton, 1997).

Examiners conducted patient examinations such that the gold standard performed an

examination on three quadrants in each patient, and each resident examined one random

quadrant per patient. Care was taken to ensure that each resident had an opportunity to

examine all quadrants and that the number of examinations for a given quadrant was

balanced across examiners, so that each quadrant was measured no more than twice.

After all calibration sessions, the data was compiled and statistical analysis carried out to

compare inter-examiner reliability between each resident and the gold standard. The

results were analyzed to see if each resident was calibrated or if there was need for any

further training.

Clinical Measurements for Calibration: (1) GI 0 Absence of inflammation.

1 Mild inflammation – slight change in colour and little change in texture.

2 Moderate inflammation – moderate glazing, redness, edema, and hypertrophy.

Bleeding on pressure.

3 Severe inflammation – marked redness and hypertrophy. Tendency to spontaneous bleeding. Ulceration.

60

(2) PI **Plaque index is determined by thickness of plaque in a buccal/lingual orientation. 0 No plaque in gingival area.

1 A film of plaque adhering to the free gingival margin and adjacent area of the

tooth. The plaque may be seen in situ by using the probe on the tooth surface.

2 Moderate accumulation of soft deposits within the gingival pocket or on the adjacent tooth surface and gingival margin which can be seen with the naked eye.

3 Abundance of soft matter within the gingival pocket and/or on the adjacent tooth surface and gingival margin (1-2mm thick).

(3) PD

Record probing depth at the deepest site at each of: distobuccal, mid-buccal, mesiobuccal, distolingual, mid-lingual, and mesiolingual areas.

(4) Rec

Each measure of recession (FGM to CEJ measurement) will be recorded immediately following the probing depth measurement at the same location.

Positive Number When the FGM is located apical to the CEJ.

Negative Number When the FGM is located coronal to the CEJ.

Zero When the FGM is located at the CEJ.

(5) CAL CAL = probing depth plus distance from free gingival margin to cemento-enamel junction. (6) BI 0 No evidence of bleeding following probing.

1 Evidence of bleeding within 15 seconds of probing.

61

(7) Furc – Hamp Classification (use Nabers probe) Grade 1 Horizontal penetration < 3mm.

Grade 2 Horizontal penetration > 3mm.

Grade 3 Through and through lesion.

(8) Mob 0 Physiologic mobility only.

1 The tooth can be moved less than 1 mm in a buccolingual or mesiodistal direction.

2 The tooth can be moved 1 mm or more in a buccolingual or mesiodistal direction

but does not exhibit abnormal mobility in an occlusoapical direction.

3 The tooth can be moved 1 mm or more in both buccolingual or mesiodistal and occlusoapical directions.

(9) AG – only record if it is minimal (< 2mm) Measure the amount of attached gingiva (distance between the crest of the ginigival margin to the MGJ minus depth of the sulcus/pocket) at mid-buccal and mid-lingual areas of each tooth. Calibration Results: All calibration subjects were adults recruited from the Graduate Periodontal Program at

the University of Toronto. Six female patients and two male patients who were an

average age of 53 years old (range of 41 to 70 years) participated in the calibration

training. All patients had generalized chronic periodontitis, with three having severe

disease, three having moderate disease, and two having mild disease.

The summary of the calibration results can be seen in the table below. This table shows

the percentage of exact agreement and agreement +/- 1mm for the calibrated measures.

All of the measures are important for establishing a diagnosis of chronic periodontitis;

however, severity of disease was determined by PD +/- 1mm and this was the measure

that we were most concerned with. From the literature, it was found that in order to

62

establish inter-examiner reliability, PD should be +/- 1mm 90% or more of the time. This

percentage would be lower for Rec and again lower for CAL due to the accumulation of

error with these measures (Polson, 1997). We modified this and wanted PD to be +/-

1mm 80% or more of the time.

Calibration Summary of Results: Clinical Measurement: Range of Percentage of

Agreement: Probing depth + 1mm

83.85% - 96.88%

Recession + 1mm

86.98% - 95.83%

CAL + 1mm

78.13% - 100%

GI exact

57.14% - 74.29%

GI +1

57.14% - 74.29%

PI exact

60% - 85.71%

PI +1

97.14% - 100%

Mobility exact

57.14% - 88.57%

Mobility +1

91.43% - 100%

BOP exact

54.17% - 78.13%

Furcations exact

45.83% - 96.43%

Min. attached gingiva exact

22.5% - 100%

The figure below displays a graph of PD within +/- 1mm, showing the percentage

agreement and 95% confidence intervals for each resident. It can be seen that 3/6

residents were above the 90% cut- off and all of the 6 residents were above the 80% cut-

off.

63

Figure: Comparing Inter-examiner Reliability for PD +/- 1mm

Probing Depth +/- 1mm

0.8698

0.9688

0.93230.9375

0.8646

0.8385

0.75

0.8

0.85

0.9

0.95

1

1 2 3 4 5 6

Examiners

Prop

ortio

n

In general, there was a trend for PD, Rec, and CAL to be associated with the gold

standard. This means that one can say that the examiners were calibrated with respect to

PD, Rec, and CAL. In general BOP, GI, PI, Furc, Mob, and AG were not as clearly

associated with gold standard. This means that examiners were generally not calibrated to

the gold standard with respect to BOP, GI, PI, Furc, Mob, and AG.

64

APPENDIX 3 – Percent of Total Responses for Enhanced Questionnaire Table 1: Percent of Total Responses for Cases for Enhanced Questionnaire - Stress Acute Stress Questions: No

(score = 0) Yes (score = 1)

N/A

1. Was there a serious illness? 76 (75.25%)

21 (20.79%)

4 (3.96%)

2. Did a close friend die? 80 (79.21%)

18 (17.82%)

3 (2.97%)

3. Was there a marital separation or divorce? 88 (87.13%)

5 (4.95%)

8 (7.92%)

4. Had a child move back into the house? 82 (81.19%)

2 (1.98%)

17 (16.83%)

Chronic Stress Questions: NT

(score = 0) ST/VT (score = 1)

N/A

1. There is too much pressure on you to be like other people.

56 (55.45%)

35 (34.65%)

10 (9.90%)

2. You don’t have enough money to take vacations.

33 (32.67%)

64 (63.37%)

4 (3.96%)

3. You find it is too difficult to find someone compatible with you.

50 (49.50%)

38 (37.62%)

13 (11.88%)

4. You have to go to social events alone and you don’t want to.

65 (64.36%)

22 (21.78%)

14 (13.86%)

5. You don’t have time for your favorite leisure time activities.

55 (54.46%)

42 (41.58%)

4 (3.96%)

6. You would like to move but you cannot. 62 (61.39%)

32 (31.68%)

7 (6.93%)

Table 2: Percent of Total Responses for Cases for Enhanced Questionnaire – Social Support Social Support Questions:

No (score = 0)

Yes (score = 1)

1. Do you have someone you can confide in or talk to about your private feelings or concerns?

11 (10.89%) 90 (89.11%)

2. Do you have someone you can really count on to help you out in a crisis situation?

7 (6.93%) 94 (93.06%)

3. Do you have someone you can really count on to give you advice when you are

14 (13.86%) 87 (86.14%)

65

making important personal decisions? 4. Do you have someone who makes you feel loved and cared for?

7 (6.93%) 94 (93.06%)

Social Involvement Questions:

“Not at all”(score = 0)

“At least once a year” (score = 1)

“At least 3 or 4 times a year” (score = 2)

“At least once a month” (score = 3)

“At least once a week” (score = 4)

1. How often did you participate in meetings or activities sponsored by voluntary organizations or associations in the past 12 months?

43 (42.57%) 16 (15.84%) 19 (18.81%) 9 (8.91%) 14 (13.86%)

2. Other than on special occasions, how often did you attend religious services or religious meetings in the past 12 months?

45 (44.55%) 20 (19.80%) 14 (13.86%) 6 (5.94%) 16 (15.84%)

Social Contact Questions:

“Don’t have any” (score = 0)

“Never” (score = 1)

“Less than once a month” (score = 2)

“Once a month” (score = 3)

“More than once a month” (score = 4)

1. Parents or parents-in-law

37 (36.63%) 2 (1.98%) 6 (5.94%) 9 (8.91%) 47 (46.53%)

2.Grandparents 92 (91.09%) 1 (1.00%) 3 (2.97%) 1 (1.00%) 4 (3.96%) 3. Children and/or their spouses

40 (39.60%) 0 (0%) 1 (0.10%) 0 (0%) 60 (59.41%)

4. Brothers or sisters 18 (17.82%) 7 (6.93%) 19 (18.81%) 10 (9.90%) 47 (46.53%) 5. Close friends and/or relatives

3 (2.97%) 1 (1.00%) 12 (11.88%) 12 (11.88%) 73 (72.28%)

66

Table 3: Percent of Total Responses for Controls for Enhanced Questionnaire - Stress Acute Stress Questions: No

(score = 0) Yes (score = 1)

N/A

1. Was there a serious illness? 37 (74%)

11 (22%)

2 (4%)

2. Did a close friend die? 42 (84%)

6 (12%)

2 (4%)

3. Was there a marital separation or divorce? 41 (82%)

3 (6%)

6 (12%)

4. Had a child move back into the house? 38 (76%)

0 (0%)

12 (24%)

Chronic Stress Questions: NT

(score = 0) ST/VT (score = 1)

N/A

1. There is too much pressure on you to be like other people.

34 (68%)

14 (28%)

2 (4%)

2. You don’t have enough money to take vacations. 21 (42%)

29 (58%)

0 (0%)

3. You find it is too difficult to find someone compatible with you.

24 (48%)

21 (42%)

5 (10%)

4. You have to go to social events alone and you don’t want to.

34 (68%)

12 (24%)

4 (8%)

5. You don’t have time for your favorite leisure time activities.

31 (62%)

18 (36%)

1 (2%)

6. You would like to move but you cannot. 33 (66%)

13 (26%)

4 (8%)

Table 4: Percent of Total Responses for Controls for Enhanced Questionnaire – Social Support Social Support Questions:

No (score = 0)

Yes (score = 1)

1. Do you have someone you can confide in or talk to about your private feelings or concerns?

6 (12%) 44 (88%)

2. Do you have someone you can really count on to help you out in a crisis situation?

1 (2%) 49 (98%)

3. Do you have someone you can really count on to give you advice

8 (16%) 42 (84%)

67

when you are making important personal decisions? 4. Do you have someone who makes you feel loved and cared for?

6 (12%) 44 (88%)

Social Involvement Questions:

“Not at all” (score = 0)

“At least once a year” (score = 1)

“At least 3 or 4 times a year” (score = 2)

“At least once a month” (score = 3)

“At least once a week” (score = 4)

1. How often did you participate in meetings or activities sponsored by voluntary organizations or associations in the past 12 months?

22 (44%) 6 (12%) 7 (14%) 6 (12%) 9 (18%)

2. Other than on special occasions, how often did you attend religious services or religious meetings in the past 12 months?

25 (50%) 10 (20%) 3 (6%) 4 (8%) 8 (16%)

Social Contact Questions:

“Don’t have any” (score = 0)

“Never” (score = 1)

“Less than once a month” (score = 2)

“Once a month” (score = 3)

“More than once a month” (score = 4)

1. Parents or parents-in-law

35 (70%) 2 (4%) 0 (0%) 1 (2%) 12 (24%)

2.Grandparents 46 (92%) 1 (2%) 1 (2%) 2 (4%) 0 (0%) 3. Children and/or their spouses

28 (56%) 0 (0%) 2 (4%) 2 (4%) 18 (36%)

4. Brothers or sisters 9 (18%) 0 (0%) 8 (16%) 14 (28%) 19 (38%) 5. Close friends and/or relatives

2 (4%) 2 (4%) 5 (10%) 4 (8%) 37 (74%)

68

APPENDIX 4 – Interpretation of Intraclass Correlation Coefficient Statistic Landis and Koch’s Criteria: > 0.8 = Very good agreement > 0.6 - 0.8 = Good agreement > 0.4 - 0.6 = Moderate agreement > 0.2 - 0.4 = Fair agreement < 0.2 = Poor agreement

69

APPENDIX 5 – Test-Retest Reliability Tables

Test-Retest Reliability for Cases

Question Number Number &

Proportion of

Same Response

95% Confidence Interval

n(%) Lower Upper

A1 – acute stress 28 (90.32 %) 0.7992 1.0000

A2 28 (90.32 %) 0.7992 1.0000

A3 27 (90.00 %) 0.7926 1.0000

A4 24 (92.31 %) 0.8207 1.0000

B1 – chronic stress 21 (72.41 %) 0.5615 0.8868

B2 26 (92.86 %) 0.8332 1.0000

B3 21 (84.00 %) 0.6963 0.9837

B4 20 (76.92 %) 0.6073 0.9312

B5 21 (70.00 %) 0.5360 0.8640

B6 22 (78.57 %) 0.6337 0.9377

C1 – social support 29 (90.63 %) 0.8053 1.0000

C2 28 (87.50 %) 0.7604 0.9896

C3 29 (90.63 %) 0.8053 1.0000

C4 30 (93.75 %) 0.8536 1.0000

D1 – social involve 18 (56.25 %) 0.3906 0.7344

D2 21 (65.63 %) 0.4917 0.8208

E1 – social contact 21 (65.63 %) 0.4917 0.8208

E2 28 (87.50 %) 0.7604 0.9896

E3 29 (90.63 %) 0.8053 1.0000

E4 21 (65.63 %) 0.4917 0.8208

E5 21 (65.63 %) 0.4917 0.8208

70

Test-Retest Reliability for Controls

Question Number Number &

Proportion of

Same Response

95% Confidence Interval

n(%) Lower Upper

A1 – acute stress 13 (76.47 %) 0.5631 0.9663

A2 16 (94.12 %) 0.8293 1.0000

A3 12 (100%) 1.0000 1.0000

A4 10 (90.91 %) 0.7392 1.0000

B1 – chronic stress 13 (76.47 %) 0.5631 0.9663

B2 15 (88.24 %) 0.7292 1.0000

B3 12 (75.00%) 0.5378 0.9622

B4 12 (80.00%) 0.5976 1.0000

B5 12 (70.59 %) 0.4893 0.9225

B6 13 (92.86 %) 0.7937 1.0000

C1 – social support 14 (82.35 %) 0.6423 1.0000

C2 15 (88.24 %) 0.7292 1.0000

C3 15 (88.24 %) 0.7292 1.0000

C4 16 (94.12 %) 0.8293 1.0000

D1 – social involve 8 (47.06 %) * 0.2333 0.7079

D2 15 (88.24%) 0.7292 1.0000

E1 – social contact 11 (64.71 %) 0.4199 0.8742

E2 17 (100%) 1.0000 1.0000

E3 13 (76.47 %) 0.5631 0.9663

E4 12 (70.59 %) 0.4893 0.9225

E5 11 (64.71 %) 0.4199 0.8742

* insufficient evidence of being a reliable response

71

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