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Psychosomatic Medicine 67:930-938 (2005)
© 2005 American Psychosomatic Society

ORIGINAL ARTICLES

Caregiving and Gingival Symptom Reports: Psychophysiologic Mediators

Peter P. Vitaliano, PhD, Rutger Persson, DDS, PhD, Asuman Kiyak, PhD, Hardeep Saini, BS and Diana Echeverria, PhD

From the Department of Psychiatry and Behavioral Sciences (P.P.V., H.S.), Department of Periodontics (R.P.), and Department of Oral and Maxillofacial Surgery (A.K.), University of Washington, Seattle, Washington; Battelle Centers for Public Health Research & Evaluation, Seattle, Washington (D.E.).

Address correspondence and reprint requests to Peter Vitaliano, PhD, Psychiatry & Behavioral Sciences, Box 356560, UW, Seattle WA 98195-6560. E-mail: pvital{at}u.washington.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Objective: We first assessed the association of caregiving with gingival symptom reports. We then assessed whether the observed relationship was mediated by psychophysiologic host factors.

Methods: Caregivers of spouses with Alzheimer’s disease (n = 123) were compared with demographically similar noncaregiver spouses (n = 117).

Results: The percentage of caregivers (17%) who reported gingival symptoms was twice that of noncaregivers (8.5%) (p < .05), despite the fact that caregivers and noncaregivers did not differ in oral health care. The relationship between caregiving and gingival symptom reports was mediated by psychophysiologic variables. Caregivers were higher on hassles (p < .05), depressed mood (p < .05), and metabolic risk (insulin, glucose, obesity; p < .05) than were noncaregivers. Greater gingival symptom reports were also associated with greater hassles (p < .01), depressed mood (p < .001), and metabolic risk (p < .001). Measures of subcutaneous fat, inflammation, and frank diabetes were related to gingival symptom reports but not to caregiver status.

Conclusions: A higher percentage of caregivers reported gingival symptoms than noncaregivers. These results have implications for research on aging, psychophysiology, and chronic stress.

Key Words: stress • caregiving • gingivitis • inflammation • diabetes • depression

Abbreviations: PD = periodontal disease; AD = Alzheimer’s disease; BDI = Beck Depression Inventory; NWLL = Northwest Lipids Laboratory; BMI = body mass index; ICD = International Classification of Diseases; NSAIDS = nonsteroidal anti-inflammatory drugs; LRS = likelihood ratio statistic; OR = odds ratio; CV = coefficient of variation; PCA = principal components analysis.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Gingivitis is a reversible inflammatory process of the gingival tissues that occurs in response to bacterial plaque. Symptoms include gums that bleed easily during brushing, flossing, or dental probing and/or gums that are swollen, sensitive to touch, or inflamed. Gingival inflammation varies along a continuum from early gingivitis (mild to moderate inflammation) to established gingivitis (extensive biofilm, redness, swelling, bleeding, and inflammatory infiltration) to periodontitis (periodontal attachment loss/alveolar bone loss and significant inflammation) (1).

Several studies have attempted to estimate the prevalences of gingivitis and periodontitis (periodontal disease, PD). One study found that over 50% of US adults had early to established gingivitis on an average of 3 to 4 teeth and 30% had PD as measured by 1 or more pockets of 4 mm or greater (2). A more recent US study of people 30 to 90 years of age found that 50% of Caucasians had gingival symptoms at 1 or more sites (3) and 35% had PD (4). According to the National Center for Health Statistics (5), almost 3 of every 10 adults over 65 years old have lost all of their teeth because of cavities and PD.

Progressive PD not only results in tooth loss but also is associated with elevated risks for systemic diseases (6,7). The US Department of Health and Human Services (8) noted that the mouth is a "mirror for general health well-being." Indeed, the epidemiology and natural history of gingivitis suggest that in many cases it progresses to irreversible PD (9,10). One study followed 565 men for 26 years. It found that men who approached 60 years of age and whose gingival sites bled on probing consistently over the course of the study had 70% greater attachment loss than did men who approached 60 years of age but whose gingival sites were not repeatedly inflamed. This occurred despite the fact that all men in the study practiced daily home care and received extensive dental care (11).

Although such studies demonstrate that gingivitis is a significant etiological factor in subsequent PD, a susceptible host is also necessary for it to advance to PD (12). Physiologic, behavioral, psychological, and demographic host variables have been identified as risk factors that may promote the development/progression of gingivitis to PD (13). Associations between psychological host variables and acute necrotizing ulcerative gingivitis were first recorded in World War I when soldiers fighting in the trenches experienced infections so severe that they reported acute pain, often resulting in bone defects and tooth loss (14). Since then, relationships have been observed between PD and other chronic stressors such as financial problems (13) and the loss of a spouse (15). Reviews of this literature have shown, however, that researchers have failed to consider the simultaneous relationship of chronic stress, PD, and its mediators, despite the fact that the call was made for such studies more than 5 years ago (13).

In the current study, we examine relationships between chronic stress and gingival symptom reports, as well as their potential mediators. Although gingivitis predicts subsequent PD, gingival symptom reports may not be accurate estimates of gingivitis (16,17). Indeed, patients tend to underreport their gingival symptoms (18,19), possibly because they are unaware of them (17). To address this issue, we will assess whether gingival symptom reports are related to actual measures of inflammation (white blood cell count, C-reactive protein). If self-reports and inflammation measures are related in the expected direction, this should provide some support for the self-report measure.

Given the above literature, we first assessed whether chronic stress was associated with gingival symptom reports and, if so, whether host variables mediated these relationships. Depressed mood and perceived stress/hassles are potential psychological mediators of chronic stress and gingival symptom reports. Such factors are positively associated with chronic stress (20–23) and gingival symptoms/clinically diagnosed PD (24,25). Depression may influence poor oral health in several ways. It is related to elevations in IL-6, a proinflammatory cytokine (26) that inhibits production of IL-2 and a compound that protects tissues against infection (27). Depression is also associated with xerostomia either directly (28) or via the use of antidepressant medications (29,30). Reductions in salivary flow can limit the regulation of microbial populations and result in bacterial infections and greater risk for PD (31). Perceived stress may foster poor health via immune dysregulation. Such pathways are supported by relationships of chronic stress with increased risk of infection after injury (32) and delays in wound healing (33).

Potential physiologic mediators of the association between chronic stress and gingival symptoms include metabolic factors (insulin resistance (34); obesity/body fat (35)) and inflammation (e.g., C-reactive protein; white blood cell count, 36–39). Metabolic factors are associated with both chronic stress (40) and PD (38,39). Positive associations have been observed between glucose levels and PD in persons who were ostensibly free of diabetes, suggesting that PD may represent a prediabetic state (41). Additionally, persons with poorly controlled diabetes and who are 45 years or older are three times as likely to have PD as those free of diabetes. Such relationships are probably mediated by immune responses because the release of stress hormones modifies the effectiveness of the immune system to cause inflammation, which sets the stage for PD (42–44). Glucose elevations can also foster bacterial plaque and inflammation in periodontal pockets (45).

One chronic stressor that has received considerable attention is caring for a spouse with Alzheimer’s disease (AD) and other dementias. Spouse caregivers of persons with AD are exposed to unrelenting stressors. These include helping care recipients with maintenance and higher level activities of daily living and contending with a care recipient’s mood and behavioral problems (46). In meta-analyses, caregivers show higher risks for psychosocial (47) and systemic health (48) problems than do noncaregivers. Apart from the current study, however, no studies have compared the oral health of caregivers with noncaregivers. This is surprising because oral health problems are concomitants of systemic health, chronic stress, and aging.

Importantly, the same psychophysiologic factors that may mediate relationships of chronic stress and poor oral health in the general population may also be relevant to caregivers. Caregivers exhibit higher levels of depression than do noncaregivers (49–53). In addition, caregivers report more hassles than noncaregivers, and hassles are associated with greater insulin levels in caregivers than noncaregivers (54). Caregivers are also higher on measures of inflammation than are noncaregivers (55).

Given previously observed relationships among chronic stress, psychophysiologic functioning, and poor oral health, we expected that spouse caregivers would report greater gingival symptoms than would noncaregiver spouses (Hypothesis 1). We also expected that this relationship would be mediated by psychological (depression, hassles) and physiologic (insulin, glucose, obesity, body fat, and inflammation) factors (Hypothesis 2). Because gingivitis and PD are associated with age (56,57), smoking (58), and chronic illnesses (7,59), we considered these as covariates (e.g., demographics, behaviors, medications, and illnesses) in testing our hypotheses. By comparing gingival symptom reports in older adult caregivers with older adult noncaregivers who are similar in demographic and illness profiles, we attempted to isolate reports of gingival symptoms associated with caregiving from those associated with age and illness.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Design and Participants
Because AD is a progressive degenerative disorder, we used it as a chronic stressor for spouse caregivers and compared them to noncaregivers. Caregiver couples were recruited from (1) mailings to physicians, (2) the University of Washington AD registry, (3) the AD Association, and (4) printed/electronic media. Criteria for care recipient inclusion were (1) living with one’s spouse, who is the primary caregiver, (2) age 55 or older, and (3) diagnosis of AD (DSM-IV criteria; 60) or possible/probable Primary Degenerative Dementia (NINCDS-ADRDA criteria; 61). Exclusion criteria are provided elsewhere (62). Caregivers had to function independently. Demographically similar noncaregivers were recruited from senior centers, retirement organizations, the UW Institute on Aging, and the media. Noncaregivers and their spouses had to be 55 years of age or older, functioning independently, and not providing care for another person. The UW institutional review board approved this study, and written informed consent was obtained from all participants. The sample consisted of 123 spouse caregivers and 117 noncaregiver spouses.

Measures
Systemic/oral health and medications were assessed using self-reports and medical records. Subjects were asked to report physical illnesses, symptoms, health care utilization, oral health, and oral health care in the last 3 months. Systemic illnesses were also coded from medical records. The coder (who was blind to the subject’s caregiver status) used Puckett’s (63) criteria to code diagnoses, treatment, prognosis, and medications. Quality controls (64) showed that in 90% of the records, treatment/International Classification of Diseases (ICD)-9 codes and/or diagnostic tests and dates were listed for systemic diseases (e.g., arteriosclerosis [ICD-9-CM code 414.0], angina [413.9], diabetes [250.0–250.5], etc.). Medications included antihypertensives, HRT, immunosuppressants, statins, nonsteroidal anti-inflammatory drugs (NSAIDs), antidepressants, etc. Some medications are not only relevant to inflammation (e.g., NSAIDs), but others (e.g., antidepressants and antihypertensives) may induce xerostomia.

Gingival symptoms were reported for the previous 3 months as part of the systemic/oral health survey described above. Two symptoms were assessed: "Please indicate (yes or no) whether you have: (1) gums that bleed easily and (2) red or swollen gums." Because each item was dichotomous (no = 0; yes = 1), the total score could vary from 0 to 2.

Physiological measures included C-reactive protein, white blood cell count, plasma glucose, insulin, obesity, and intra-abdominal fat. Subjects fasted for 12 hours and abstained from smoking and consuming alcohol/caffeine before arriving at the UW Medical Center at 9 AM. A nurse used heparinized syringes to collect blood from the hand/forearm of each seated subject. After plasma was separated by centrifugation, it was frozen at –70°C, transported in dry ice, and later analyzed at the Northwest Lipids Laboratory (NWLL).

Measures of Inflammation
C-reactive protein was assayed using a high-sensitivity particle-enhanced immunonephelometry method (65). Polystyrene particles coated with monoclonal antibodies to CRP were agglutinated when mixed with samples containing CRP. The between-assay coefficient of variation (CV) was <3%. White blood cell differential was collected in an EDTA whole-blood tube, inverted immediately, mixed with anticoagulant, and assessed using an automated cell counter. The CV was <2%. C-reactive protein and WBC count were subjected to a principal components analysis (PCA) that produced a composite that explained 54% of their variance. This composite of inflammation measures was expected to be positively related to gingival symptom reports.

Measures of Metabolic Regulation
Glucose was measured by the combined Abbott Analyzer’s catalytic activities of hexokinase and glucose-6-phosphate dehydrogenase. The CV was <3%. Insulin was assessed using a radioimmunoassay PEG-accelerated method with 48-hour incubation. The primary antibody is a guinea pig antibody, the precipitating antibody is a goat anti-guinea pig antibody and the tracer is mono-iodo-tyr-A14-insulin. The CV was <3%. Body mass index (BMI) was assessed by weighing individuals in street clothes and measuring their height without shoes. Obesity was defined as ≥90th percentile of BMI (weight in kilograms/height in meters2) on the age and gender norms of the NWLL. A PCA of glucose, insulin, and obesity resulted in a metabolic risk composite that explained 64% of the variance in these measures and provided an estimate of insulin resistance (40). We expected it to be positively related to gingival symptom reports (38,39).

Subcutaneous fat was assessed via CT scans using a GE 8800 Scanner with 120 KVP, variable MA 9.8 second scan time, 10-mm slice thickness, and large-body calibration settings. Fat density was defined as –50 to –250 HU. Circumferences were obtained of the abdomen at umbilicus (lumbar vertebrae 4–5) and the right leg, midthigh, halfway between greater trochanter and superior aspect of the patella. A density contour program determined the cross-sectional area of fat in each depot (66). Computerized area measurements were made from each scan (total tissue, total fat, and IAF). The CVs are <1% (66). A PCA explained 67% of the variance in these measures. This subcutaneous body fat composite was expected to be positively related to gingival symptom reports.

Behavioral factors were assessed using self-reports. Smoking was assessed by 3 items: "Do you currently smoke cigarettes?" "Do you currently smoke cigars?" and "Do you currently smoke a pipe?" Oral health care was assessed using 3 items: "Please indicate (yes, no) if you (1) brush your teeth twice daily, (2) floss daily, (3) schedule regular dental check-ups."

Psychological factors were assessed using self-report and interviewer measures we employed previously (67,68). The Hassles Scale (69) examines the frequency/severity of hassles in work, family, social environment, and finances in the past month. The internal consistency reliability coefficient was 0.81, a value comparable to that in the literature (69). The Beck Depression Inventory (BDI, short form; 70) is a 13-item self-report measure with a 4-point Likert response scale used to assess the severity of affective/cognitive depressive symptoms. The internal consistency reliability coefficient was 0.76. Scores of 0 to 4 suggest no/minimal depression, 5 to 7 suggest mild depression, 8 to 15 suggest moderate depression, and scores greater than 15 suggest severe depression (70). The Hamilton Depression Rating Scale (71; 24-item version) interview was used to assess symptoms of depression present for at least 2 days, from 0 (absent) to 4 (severe). The internal consistency reliability was 0.82. Scores of 20 or greater suggest a depressive state in older adults (72). We expected these factors to be positively related to gingival symptom reports.

Statistical Analyses
Marginal distributions were examined and transformations were obtained in cases of skew. Relationships were examined for caregiver status with gingival symptom reports and for these two variables with other variables of interest. Because the outcome was dichotomous ("no reported gingival symptoms" versus "at least 1 reported gingival symptom"), we used logistic regression to test hypotheses. Logistic regression uses maximum likelihood to estimate standard errors. At least 50 cases are required per predictor (73). Here, the minimum case-to-variable ratio was 240/4 = 60. Analyses were conducted as follows: At step 1, caregiver status (coded 1 = caregiver, 2 = noncaregiver) was entered. The significance of its ß weight was examined as a test of the first research hypothesis. If it was significant, we then tested the second hypothesis at step 2. We also examined the two parts of mediation and confounding, the correlation of caregiver status with a putative mediator or confounder and the partial correlation of gingival symptom reports with a putative mediator or confounder, while controlling for caregiver status. Potential mediators included psychophysiologic variables. Potential confounders included demographic variables, medications/illnesses, and behaviors. Candidates for mediation and confounding were independently examined at step 2 in the regressions. Those that were significant were included in 1 equation to evaluate their unique contributions. At each step, outliers were examined to guard against spurious results.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 NOTES
 REFERENCES
 
Univariate Comparisons
Caregivers and noncaregivers did not differ in sex, race, age, education, income, diagnoses (e.g., diabetes, etc.), and most medications (e.g., NSAIDs, antihypertensives) as coded from medical records and self-reports (Table 1). Across both samples, the percentage of women was 63%, the mean age was 71.0 years (SD = 8.4), and the range was 55 to 89 years. The mean education was 15.2 years (SD = 2.6 years) and the range was 11 to 24 years. Finally, the mean income was $49,092 (SD = $27,784), range was $12,000–$200,000, and median was $44,030.


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  		TABLE 1. Demographic, Health, Psychosocial, Physiologic, Behavioral, and PD Risk of Caregivers and Noncaregivers

 

Caregivers were higher on Hamilton (t [238] = 4.6, p < .001), Beck (t [238] = 5.4, p = .001), and Hassles (t [238] = 4.6, p = .05) Scales and use of antidepressants (p = .01). No caregivers/noncaregivers met Hamilton criteria for depression. On the BDI, 71% of caregivers and 85% of noncaregivers exhibited no/minimal depression; 16% of caregivers and 13% of noncaregivers exhibited mild depression; and 13% of caregivers and 2% of the noncaregivers exhibited moderate depression.

When the two gingival symptoms were examined separately, the percentage of persons who reported "gums that bleed easily (in the last 3 months)" was 12% for caregivers and 4.5% for noncaregivers, {chi}2 = 6.2 (1) = 0.01. The percentage of persons who reported "red, swollen, or tender gums (in the last 3 months)" was 11% for caregivers and 6% for noncaregivers, {chi}2 = 2.4 (1) = 0.11. When these two symptoms were summed for a total symptom score, it varied from 0 to 2. The percentage of persons with no reported symptoms was 83% for caregivers and 91.5% for noncaregivers; the percentage of persons with one symptom was 11% for caregivers and 6.5% for noncaregivers. Finally, the percentage of persons with two symptoms was 6% for caregivers and 2% for noncaregivers, {chi}2 = 4.3 (2) = 0.12. To increase the power of the test, we combined persons with 1 and 2 symptoms. This resulted in 17.1% (21/123) of caregivers who reported at least 1 symptom and 8.5% of noncaregivers (10/117) ({chi}2 = 3.9, p = .05). Hence, the percent of caregivers with one or more reported gingival symptoms was twice that of noncaregivers.

Caregivers and noncaregivers did not differ in C-reactive protein, white blood cell count, and the composite of inflammation measures. Caregivers were higher on insulin (t [238] = –3.3, p < .01), glucose (t [238] = –3.6, p < .01), obesity (t [238] = –3.9, p < .01), metabolic risk (t [238] = –4.1, p < .01) and the body fat composite (t [238] = –4.1, p < .01). No differences occurred in smoking. Persons were considered smokers if they currently smoked cigarettes, cigars, or pipes. Of those who smoked, the majority smoked cigarettes. Only two persons smoked a pipe (1 male caregiver and 1 male noncaregiver), and 1 male noncaregiver smoked a cigar daily. Oral health care was not related to caregiver status. On the item "Do you brush your teeth twice daily," 76.1% of caregivers and 72.9% of noncaregivers reported yes, {chi}2 (1) = 0.61. On the item "Do you schedule regular dental check-ups," 84.3% of the caregivers and 79.1% of the noncaregivers reported yes, {chi}2 (1) = 0.87. On the item "Do you floss daily," 42.6% of the caregivers and 55.8% of the noncaregivers reported yes, {chi}2 (1) = 3.4, p < .07.

Logistic regression models are presented in Table 2. For each model, column 1 contains predictors included at each step. Columns 2 to 5 contain the coefficient for each predictor (B), its standard error (SE), the Wald Statistic, significance, and Exp (B) or log of the coefficient (the odds of gingival symptom reports for a one-unit increase in the predictor).


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  		TABLE 2. Models From Logistic Regressions of Variables Predicting and Mediating Relationship of Caregiver Status With Gingival Symptom Reports

 

Hypothesis 1: Caregivers Will Report Greater Gingival Symptoms Than Noncaregivers
Model 1 shows that caregiver status predicts gingival symptom reports, B = –0.79, standard error of B = 0.41, Wald’s t = 3.74, p < .05. The likelihood ratio statistic (LRS) = {chi}2 (1) = 3.96, p < .05. The Cox-Snell statistic shows that caregiver status explained 2% of the variance in reported gingival symptoms. Consistent with the logistic model the odds ratio (OR) was computed by using the B for caregiver status as the exponent of e. The last column (Exp (B)) suggests that gingival symptom reports in noncaregivers are only 0.45 those of caregivers or gingival symptom reports for caregivers is 2.1 times those of noncaregivers (i.e., 1/ 0.45).

Potential Mediators/Confounders
No demographic, medication, or illness variables were related to both caregiver status and gingival symptom reports (Table 3). In contrast, hassles, BDI, insulin, and the metabolic and body fat composites were related to both caregiver status and gingival symptom reports. The composite of inflammation measures was not associated with caregiver status, but it was associated with gingival symptom reports (r = 0.13, p < .05). The latter relationship, although small, provided some support for the validity of the gingival symptom reports.


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  		TABLE 3. Correlations of Potential Mediators and Confounders of the Relationship of Caregiver Status With Gingival Symptom Reports

 

Hypothesis 2: Psychophysiological Mediators of the Relationship of Caregiver Status and Gingival Symptom Reports
Potential mediators in Table 3 were used in the regressions (models 2–7, Table 2). Column 2 (Table 2) includes the betas for model 2 when metabolic risk entered the equation. The B for metabolic risk is significant, B = 0.46, Wald statistic = 7.1, p < .01. Hence persons with higher metabolic risk reported more gingival symptoms. Also the B for caregiver status is now –0.67 and is no longer significant (p < .11). These results help to explain the greater gingival symptom reports for caregivers.

Model 3 shows that BDI also mediates the greater gingival symptom reports for caregivers versus noncaregivers. When BDI enters the equation, the B for caregiver status (–.52) is no longer significant (p < .22). Importantly, BDI is related to both gingival symptom reports, Wald Statistic = 5.1, p = .02 and to caregiver status (see Table 3). Model 4 shows that the hassles measure also mediates the greater gingival symptom reports for caregivers versus noncaregivers. When the hassles measure enters the equation, the B for caregiver status (–.58) is no longer significant (p < .17). Importantly, hassles is related to both gingival symptom reports, Wald statistic = 10.1, p = .002, and to caregiver status (Table 3). Models 5 and 6 show that body fat and inflammation are not mediators, because they are not related to gingival symptom reports in the presence of caregiving.

Because metabolic risk, BDI, and hassles were mediators in separate models, we examined them together in model 7 to see if they were independent. When these were in the model together, caregiver status was nonsignificant, but metabolic risk (p = .04) and hassles (p = .04) were significant. In the presence of hassles, BDI dropped out of the model, suggesting that hassles was a stronger correlate of gingival symptom reports. The LRS = {chi}2 (3) = 18.8 was significant, p = .001, and the Cox-Snell statistic suggested that model 7 explained 8% of the variance (i.e., metabolic risk and hassles explained 6% more variance in gingival symptom reports beyond caregiver status). Finally, metabolic risk and hassles have ORs of about 1.4 and 1.1, suggesting that the odds of gingival symptom reports increase by a factor of 1.4 and 1.1 for each one-unit increase in these factor scores. Clearly, the practical importance of metabolic risk is greater than that of hassles as measured by their ORs. Note also that when examined without the metabolic composite, BDI has a greater ß than hassles (model 3 versus model 4). This occurs because after controlling for caregiver status, BDI is more related to gingival symptom reports than are hassles; however, because metabolic risk and depression are more related in magnitude (r = 0.28, p < .001) than are metabolic risk and hassles (r = 0.18, p < .01), metabolic risk dampens the influence of depression more than it does the influence of hassles when they are in the equation together.

To illustrate the relationships of hassles and metabolic risk with both caregiving and gingival symptoms, we created tertiles for these mediators and crossed them to form a 3 x 3 table of 9 cells. Table 4 shows differences between the cells formed by the lowest tertiles and the highest tertiles of hassles and metabolic risk. In the cell defined by the lowest tertiles, 30% of the subjects were caregivers, 7% reported gingival symptoms, none were hyperinsulinemic (had insulin values ≥13), hyperglycemic, or obese. However, in the cell defined by the highest tertiles, 71% were caregivers, 26% reported gingival symptoms, 87% were hyperinsulinemic, 39% were hyperglycemic, and 84% were obese.


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  		TABLE 4. Percentages of Caregivers and Gingival Symptoms, Hyperinsulinemia, Hyperglycemia, and Obesity: Stratified by Lowest/Highest Tertiles of Metabolic Risk and Hassles

 


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
NOTES
 REFERENCES
 
In this study, twice as many spouse caregivers reported gingival symptoms as spouse noncaregivers. A relationship between chronic stress and gingivitis was first recorded in World War I when the gums of soldiers fighting in the trenches were infected to such an extent that their teeth became loose and the tips between their teeth eroded away, leaving disfiguring craters and bone loss (14,74). Since this observation, studies have shown relationships between various forms of stress and oral disease. Persons with high levels of financial stressors have a two-fold greater likelihood of developing PD (7), an OR similar to the one observed here for caregiver status with gingival symptom reports. Another study found that military deployment (24) is also a risk factor for PD, with deployed Gulf War veterans being more likely to report heart disease (OR = 2.5), posttraumatic stress (OR = 14.9), depression (OR = 5.1), and PD (OR = 1.8) than those not deployed (24).

Of great relevance here is a recent study that examined a community sample of 298 dentate individuals 50 to 80 years of age (15). It found that the OR of severe PD with bereavement was 2.69 (p < .01). This study is important to the current study for several reasons. First, PD was assessed using clinical and radiographic examinations and not self-reports. Second, the sample used was very similar in age to the current study’s samples. Third, the type of chronic stress examined in each study was similar. Indeed, caregiving for a person with AD is a dress rehearsal for bereavement (48). Finally, the OR of bereavement with severe PD was greater than those of other well-known risk factors with severe PD (e.g., age and plaque index). This study greatly expanded knowledge about chronic stressors as risk factors for poor oral health.

In the current study, we tried to advance research in this area by examining potential mechanisms of the relationship of chronic stress with oral health. We found that the association of caregiver status with gingival symptom reports was not confounded by demographic, medical illnesses, and medications (e.g., NSAIDs, antidepressants, antihypertensives), but it was mediated by hassles and depressed mood, factors related to both chronic stress (20–23) and gingival symptom reports (75). Consistent with previous work (76), we observed a positive relationship between BDI scores and gingival symptom reports (r = 0.19, p < .001). BDI was also associated with less brushing twice a day (r = –0.16, p = .01), and a trend existed for BDI to be associated with less daily flossing (r = –0.13, p = .055). However, oral health care was not related to gingival symptom reports (see Table 3). In fact, when daily brushing and flossing were entered in model 3 (Table 2) to predict gingival symptom reports, they failed to influence BDI’s mediation of the relationship of caregiver status with gingival symptom reports.

Ancillary analyses also revealed that BDI scores were positively associated with the composite of inflammation measures (white blood cell count and C-reactive protein) (r = 0.19, p = .001). Both depression and chronic inflammation are related to elevations in IL-6, a component of C-reactive protein and a pro-inflammatory cytokine (26) that inhibits production of IL-2. IL-2 is important because it protects tissues against infection (27). Here we did not assess IL-6 and IL-2. We did show, however, that the inflammation composite was positively associated with gingival symptom reports (Table 3). These results are consistent with research that has observed relationships of PD with elevated white blood cell count (36–38,77), C-reactive protein (38,78), and depression (75).

Gingival symptom reports were also related to frank diabetes. This result is consistent with current knowledge about periodontitis and IDDM (79,80). Indeed, plaque, calculus, gingival index, and attachment loss are all greater in diabetics than nondiabetics, but these groups have similar oral health care (34). However, because diabetes was unrelated to caregiver status, it did not mediate the relationship of caregiver status with gingival symptom reports. Rather, an indicator of prediabetes, the metabolic risk composite, was related to both caregiver status and gingival symptom reports. One might ask how this could have occurred.

Fasting glucose (>110), which is used to diagnose diabetes, did not contribute to the metabolic composite’s mediation of chronic stress and gingival symptom reports. As with diabetes, glucose was only related to gingival symptom reports (Table 3). In contrast, insulin was the primary driver of the metabolic composite’s status as a mediator. It was associated with both caregiver status and gingival symptom reports (Table 3). In fact, 71% of the persons in the highest tertile of metabolic risk and hassles were caregivers, 26% reported gingival symptoms, 87% were hyperinsulinemic, and only 39% were hyperglycemic (Table 4). In contrast, only 30% of the participants in the lowest tertile were caregivers, 7% reported gingival symptoms, and none were hyperinsulinemic or hyperglycemic. Interestingly, we previously observed this identical pattern of elevated insulin in independent samples of caregivers and noncaregivers (n = 152) (68).

The current results are subject to limitations. First, we relied on self-reports of gingival symptoms. Such reports may underestimate the true prevalence of gingivitis (18,81). In fact, Pitiphat et al. (17) noted that this underestimate "suggested that many patients with PD appear to be unaware of their conditions [p. 122]." Despite these problems, the current study found that gingival symptom reports were associated with signs of infections as indicated by higher white blood cell counts and C-reactive protein levels. To our knowledge no previous study has examined relationships between gingival symptom reports and actual measures of inflammation. A second disadvantage to this study is that we did not assess saliva flow. Reductions in salivary flow can limit the regulation of microbial populations and result in bacterial infections and increased risk for PD (31). We did, however, examine relationships of gingival symptom reports with medications that are known to be related to xerostomia (e.g., antidepressants, antihypertensives). Such medications were unrelated to gingival symptom reports. Another disadvantage to this study is that, as with all caregiver research, it is observational (48). Because spouse caregivers have shared the same risk factors (stress, diet, etc.) as their AD care recipients, they may be at higher risk for developing systemic problems independent of caregiving. One cannot create caregiving in a laboratory to assess whether it causes illness. However, researchers could still design doubly prospective studies and examine persons before they are caregivers and before they have health problems (48). A third limitation is our inability to explain the diverse relationships that occurred between gingival symptoms with the BDI versus the Hamilton Depression Scale. One potential explanation is that the BDI was developed to assess a broad spectrum of depression and it has therefore been widely used in community samples such as those in the current study. In contrast, the Hamilton was developed for more clinical groups and has been widely used in psychopharmacolog studies. Indeed, in the current study, the BDI showed some levels of mild and moderate depression in caregivers but minimal severe depression, and this was consistent with the lack of measurable depression using the Hamilton. A final disadvantage of this study is that it is cross-sectional. Such a design limits one’s ability to specify the directionality of relationships. Although we do not believe gingival symptoms could influence caregiver status, they may influence depression. Such directional relationships can only be tested using a longitudinal design.

Despite these limitations, this investigation has some advantages. This is the first study to examine and demonstrate greater gingival symptom reports in caregivers than noncaregivers and to examine mediators relevant to the health of caregivers, care recipients, and older adults (48,82). Many caregivers are over 65 (83) and experience age-related declines in oral health and age-associated comorbidities. Family caregivers provide 80% of long-term care and make humanitarian and economic contributions to society (84,85). Factors that negatively affect such support may have deleterious effects on the formal system at a time when demand is increasing. Interventions that reduce distress and insulin resistance should also benefit caregiver oral health.

We thank the NIMH, RO1 MH43267, RO1 MH57663, and NIDCR RO1 DE12215; Mark Wener, MD, for the C-reactive protein/WBC analyses; and the UW Clinical Research Center, Nutrition Center, Alzheimer’s Center, and the Northwest Lipid Laboratory.


   NOTES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
REFERENCES
 

Received for publication November 29, 2004; revision received July, 7, 2005.

DOI:10.1097/01.psy.0000188485.65153.7b


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 

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