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Psychosomatic Medicine 67:638-642 (2005)
© 2005 American Psychosomatic Society

ORIGINAL ARTICLES

Depressive Symptoms Predict Norepinephrine Response to a Psychological Stressor Task in Alzheimer’s Caregivers

Brent T. Mausbach, PhD, Joel E. Dimsdale, MD, Michael G. Ziegler, MD, Paul J. Mills, PhD, Sonia Ancoli-Israel, PhD, Thomas L. Patterson, PhD and Igor Grant, MD

From the Departments of Psychiatry (B.T.M., J.E.D., P.J.M.) and Medicine, University of California at San Diego (M.G.Z.); and Veterans Affairs San Diego Health Care System (S.A-I., T.L.P., I.G.), San Diego, CA.

Address correspondence and reprint requests to Brent Mausbach, PhD, Department of Psychiatry (0680), University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0680. E-mail: bmausbach{at}ucsd.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Objective: Increased depressive symptoms have been associated with increased basal plasma norepinephrine (NE), and may be associated with exaggerated NE response to stress. This exaggerated response may play a role in health consequences associated with caring for a loved-one with Alzheimer’s disease. The current study examined the relations between the level of depressive symptoms in spousal caregivers and the physiological response to a psychological stress task.

Methods: Fifty-five spousal caregivers (mean age 73 ± 8 years) completed the depression subscale of the Brief Symptom Inventory (BSI). Plasma NE levels were assessed before and immediately after a speech stressor conducted at the caregiver’s home. Hierarchical linear regression was used to determine whether caregiver depressive symptoms significantly improved prediction of change in NE levels beyond other factors theoretically and empirically related to NE.

Results: Level of depressive symptoms significantly predicted post-stressor change in NE levels (p < .01), even when controlling for age, caregiver distress, presence of caregiver hypertension, and care recipient level of cognitive function. Higher levels of depressive symptoms were associated with a greater plasma NE response to the psychological stress task.

Conclusions: Depressive symptoms may act to exaggerate NE response to the stress of caregiving, potentially leading to an allostatic load that might predispose caregivers to negative health consequences, including cardiovascular morbidity.

Key Words: depression • norepinephrine • psychological stress • caregivers • Alzheimer’s disease

Abbreviations: NE = norepinephrine; SAM = sympatho-adrenalmedullary; UCSD = University of California, San Diego; ADRC = Alzheimer’s Disease Research Center; AD = Alzheimer’s disease; BSI = Brief Symptom Inventory; CDR = Clinical Dementia Rating Scale.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Caring for a loved one with Alzheimer’s disease is a psychologically stressful experience that has been associated with increased risk for both physical and mental health consequences (1,2). Specifically, caregiving has been associated with poorer health (3), increased risk for mortality (4), and depression (5). More recently, caregiving was associated with increased risk of hypertension (6) and heart disease (7). The mechanisms of these cardiovascular risks are not understood, but dysregulation of sympatho-adrenalmedullary (SAM) responses to caregiving stress (8) may play a role. Caregivers, for example, have demonstrated elevated basal plasma catecholamine concentrations (9). In addition to having higher blood pressure (6), possibly reflecting increased vascular resistance secondary to a rise in circulating norepinephrine (NE) (10), caregivers also exhibit changes in the balance of molecules in blood relevant to coagulation. For example, higher concentrations of D-dimer, a procoagulant whose increase is predictive of myocardial infarction, have been noted in caregivers (11).

Caregivers who are depressed may be at increased risk for physical health consequences. Indeed, several reports have indicated that depressive symptoms constitute risk factors for cardiovascular disease and survival after myocardial infarctions (12–15). Interestingly, there appears to be a dysregulation of the noradrenergic system in depressed individuals (16), with several studies indicating that depressed individuals have elevated resting and standing NE levels (16–20).

In addition to elevated basal NE levels, depressed individuals appear to have an exaggerated NE response to physical stress. For example, studies show that depressed individuals have a greater percent increase in plasma NE levels in response to an orthostatic challenge (16,21). Caregivers with increased depressive symptoms may also be physiologically vulnerable to stressful psychological stimuli, such as changes in their loved ones’ cognitive, behavioral, and affective functioning as well as disruptive patient behaviors. This vulnerability seems particularly salient when considering the deficits in coping and problem-solving skills among depressed individuals (22,23). Therefore, we examined the NE response to an experimentally imposed psychological stressor in caregivers to spouses suffering from dementia. We hypothesized that increased levels of depressive symptoms would be associated with increased NE response to a psychologically stressful task.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Participants
All participants were spousal caregivers of Alzheimer’s disease (AD) patients recruited to participate in a study of elderly caregivers’ psychobiological responses to mental stress. The majority of participants were recruited from professional referrals (38%), the University of California San Diego (UCSD) Alzheimer’s Disease Research Center (ADRC; 31%), and media advertisements (13%). The remaining participants were recruited through a variety of other means, including community support groups, health fairs, and presentations at agencies providing services to AD caregivers. Participants were paid $50 for their enrollment in the study. The majority of caregivers (93%) identified themselves as Caucasian. The UCSD Institutional Review Board approved the protocol, and all subjects provided written informed consent.

To control for co-morbidities (e.g., physical illnesses, blood pressure, medications, etc.) and stress-related factors known to differ in spouse versus nonspouse caregivers, caregivers were required to meet a number of inclusion/exclusion criteria. Participants were required to be a spousal caregiver of someone with AD and living at home with their care recipient at the time of enrollment. Before enrollment, a documented diagnosis of AD must have been made by a physician. In addition, caregivers were required to be 55 years of age or older and free of serious medical conditions (e.g., cancer). Caregivers were excluded if they a) were taking ß-blocking medication, b) indicated daily use of nonsteroidal anti-inflammatory drugs or agents that alter NE responses to stressors, c) were taking steroids, d) had a blood pressure greater than 200/120 mm Hg, e) consumed aspirin daily, or f) were receiving treatment with anticoagulants. A total of 55 caregivers met these criteria and were enrolled in our study.

Procedures
A research nurse met with eligible caregivers in their homes, obtained informed consent, and administered a structured assessment of a) the caregiver’s general physical and psychological health, b) the severity of the AD patient’s dementia, c) the amount and type of assistance the caregiver provided, and d) stressors the caregivers’ experienced. At 8:00 AM the following morning, the research nurse arrived at the participant’s home to collect blood samples and administer the experimental stressor task. For this task, participants had an indwelling venous catheter placed for blood drawing and rested for 5 minutes, after which blood pressure and heart rate were assessed. Next, participants rested for 10 minutes, on which a second blood pressure reading was taken and an initial "resting" blood sample was collected. After a 5 minute recovery period, a third blood pressure reading was obtained and participants were instructed on the experimental stressor task. For this task, participants were given one of two stressor vignettes selected at random. In the first vignette, the participant was falsely accused of shoplifting (24). The second vignette involved an argument with an automobile repairman over costs. Previous studies have demonstrated that the two vignettes elicit comparable reactivity (25). Participants were given 3 minutes for mental preparation and then instructed to speak for 3 minutes in response to the vignette. Immediately after the 3-minute speech, a second blood sample was collected.

Measures

Norepinephrine Levels
We used a catechol-o-methyltransferase (COMT)-based radioenzymatic assay with a preconcentration step to extract norepinephrine from 1 ml plasma and concentrated it in 0.1 ml of dilute acid (26). This assay is 10 times as sensitive as standard assays for catecholamines. Blood samples were stored in ice and transferred to a –80°C freezer until assay.

Depressive Symptoms
The six-item depression subscale of the Brief Symptom Inventory (BSI) (27) was used to assess depressive symptoms. Participants were asked to rate each item on "how much it had caused distress during the past six months, including today." Each item was answered using a Likert scale with answers ranging from 0 (not at all) to 5 (extremely). The participant’s average response to the six items was used to calculate a depressive symptom score. Research indicates that the BSI depression scale is comparable with the Beck Depression Inventory and the Hamilton Rating Scale for Depression in accurately detecting cases of depression in the elderly (28). Further, the BSI depression scale is correlated with both the Beck Depression Inventory short form and the Hamilton Rating Scale for Depression (0.71 and 0.60, respectively) (28). Alpha reliability for the current participants was 0.80.

Care Receiver Cognitive Status
The Clinical Dementia Rating scale (CDR) (29) was administered by a research nurse to assess care receiver cognitive status. Care recipients received a score ranging from 0 (healthy) to 4 (severe dementia) on 6 domains, including memory, judgment/problem-solving, and orientation, with the average score on these domains indicating overall severity of dementia symptoms.

Caregiver Arterial Pressure
Both systolic and diastolic blood pressure were assessed using a Critikon Dinamap 8100 adult/pediatric noninvasive blood pressure monitor. As described above, the research nurse obtained three measurements before engaging in the psychological stressor task, and the average of the three systolic and diastolic blood pressure readings was used to calculate mean arterial pressure.

Caregiver Distress
Caregiver distress was assessed using the Neuropsychiatric Inventory-Caregiver Distress Scale (30). Each caregiver was asked to rate the emotional or psychological distress they experienced in relation to 12 dementia-related disturbances (e.g., dysphoria, agitation, irritability). Response options ranged from 0 (not at all) to 5 (very severely or extremely). A total distress score was calculated by summing responses to the 12 items. The Neuropsychiatric Inventory-Caregiver Distress Scale has demonstrated adequate reliability and validity, including high test-retest reliability (0.92), intra-class reliability (0.96), and significant correlation with other measures of caregiver stress (e.g., the Relatives’ Stress Scale) (31). For the current sample, Cronbach’s {alpha} was 0.82.

Statistical Analysis
For our primary analysis, we used hierarchical linear regression to determine whether depressive symptoms significantly improved prediction of change in NE levels beyond other factors theoretically and empirically related to NE. Before conducting the hierarchical regression, we regressed post-speech NE onto baseline (resting) NE, with unstandardized residuals from this analysis saved for use as the dependent variable (DV) in our primary regression analysis. For the hierarchical regression, independent variables were entered as blocks into the equation. During step 1, care receiver CDR score, caregiver age, caregiver mean arterial pressure, caregiver physical health, and caregiver distress were entered. BSI depression score was entered in step 2.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 NOTES
 REFERENCES
 
Demographic Characteristics of the Sample
Table 1 shows the subject characteristics. Caregivers averaged approximately 72 years of age and were predominately Caucasian. All participants had at least a high school education. The average impairment level of spouse care recipients, as measured by the Clinical Dementia Rating scale was between mild and moderate. Approximately 27% were taking antidepressant medication.


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  		TABLE 1. Demographic Characteristics of the Sample

 

Prediction of Change in Norepinephrine Levels
Correlations between variables used in this study are presented in Table 2.


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  		TABLE 2. Correlations Among Study Variables

 

Preliminary analyses indicated that the stress task produced a significant increase in NE levels from resting (M = 415 ± 167) to post-speech (M = 502 ± 183) (t(54) = –7.15, p < .001; see Figure 1). Results of the final regression model can be found in Table 3. As a set, CDR score, age, mean arterial pressure, and distress accounted for 13% of the total variance in pre- to post-speech NE (residual change score) (F(4,50) = 1.82; p = .139). In step 2, depressive symptoms significantly predicted NE response, accounting for an additional 9% of the variance explained (F(1,49) = 5.95; p = .027). Higher NE change was associated with higher depression scores, even after controlling for caregiver age, mean arterial pressure, care recipient cognitive decline, and caregiver distress.



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  		Figure 1. Pre- and post-speech NE levels for each participant.

 

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  		TABLE 3. Regression Model Predicting Residualized Change in Norepinephrine Levels

 

As seen in Table 3, the slope for depressive symptoms allows one to determine the increase in NE response at various levels of depression. For example, the difference in NE response for individuals scoring 0.20 (low/no depression) and 2.0 (significant depressive symptoms) on the BSI would be approximately 10 pg/ml and 99 pg/ml, respectively.

Given the high overlap between depression and anxiety and the influence of anxiety on NE, it is unclear if these results are specific to depressive symptoms or to negative affective states in general. Therefore, we conducted an additional regression analysis using BSI anxiety score in step 2 to determine if anxiety significantly predicted NE response. Results of this analysis indicated that anxiety was not a significant predictor of NE response (p = .78).

As mentioned above, 27% of our sample reported taking anti-depressant medications. We conducted a subgroup analysis using only participants reporting no anti-depressant medication use. Results of this analysis yielded similar effects of depression on NE response.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
NOTES
 REFERENCES
 
The present study provides evidence that increased depressive symptoms predict the NE response to psychological stress in spousal caregivers of patients with Alzheimer’s disease. Our regression approach allows one to determine the average NE response at various levels of depression. These results expand on previous findings indicating that depression is associated with exaggerated NE response to physical stress (16,21) by demonstrating an increased NE response to psychological stress among those with elevated depressive symptoms. Alzheimer’s caregivers experience a great deal of psychological stress, often on a daily basis. This stress has been associated with increased risk of coronary artery disease (7). Depressive symptoms may act to exaggerate NE response to the stress of caregiving, potentially leading to an allostatic load that might predispose caregivers to negative health consequences, including cardiovascular morbidity (32,33).

Both deficits in coping and distorted cognitive appraisals may help explain the current findings. For example, avoidance coping has been associated with increased depression in patients with heart failure (23). Moreover, elevated depressive symptoms have been associated with reduced use of cognitive, behavioral, and interpersonal coping strategies and more distorted appraisals of stimuli (e.g., catastrophizing, personalization) (22). In the context of caregiving, increased depressive symptoms may be associated with catastrophic appraisals of negative caregiving situations such as disruptive care recipient behaviors. It is recommended that future studies examine this potential mediating effect of coping and cognitions on the relationship between depression and NE response to psychological stress.

In addition, we recommend that future research examine constructs that moderate the relationship between depressive symptoms and physiologic response to stress. Vitaliano et al. (34), for example, indicate that psychological factors (e.g., outlook in life and coping), along with social resources (e.g., social support), may moderate the relationship between exposure to stressors and caregiver distress. Perhaps these factors also moderate the relationship between depressive symptoms and NE response to stress.

Although caution should be exercised, one implication of this study is that decreasing depressive symptoms might normalize SAM tone and responsivity, perhaps reducing one’s risk for developing chronic physiological changes that could heighten risk of cardiovascular disease. Consistent with this notion, Grant et al. (35) noted that a simple intervention, providing short-term respite to caregivers, attenuated augmented catecholamine response to a mental stressor. Psychological interventions, which have been shown to decrease depressive symptoms in dementia family caregivers (36–39), may also be a means of reducing physiological arousal.

There are limits to the present study. For example, we did not examine the relationship between depression and NE response to a neutral (control) task. It may be that increased depressive symptoms produce greater NE response to a variety of "nonstressful" stimuli, such as repeating the alphabet to the interviewer. Future examinations including such a task would clarify the relationship between depressive symptoms and NE response.

Second, we examined the NE response to psychologically stressful stimuli at one point in time. It is not clear if the increased NE response, associated with depressive symptoms in our caregivers, is related to future health problems. Therefore, caution is urged in inferring long-term impact from these findings. However, since depression was associated with cardiovascular disease in other populations (13), the joint and separate effects of caregiver stress and depressive symptoms on SAM responsivity in caregivers are worthy of future study.

These results may not generalize to other populations. For example, it is unclear whether these results generalize to depressed noncaregiving samples. Future researchers should explore whether greater depressive symptoms are related to NE response in noncaregivers. Further, more research is needed with minority populations, younger populations, and nonspousal caregivers. Dementia caregivers, for example, report greater levels of depression than nondementia caregivers (3), and spouses of dementia patients report greater depressive symptoms than nonspouse caregivers (e.g., daughters) (40). There may also be differences in how these individuals appraise caregiving. For instance, research indicates that Hispanic caregivers may be at increased risk for depression than both Caucasian and African-American caregivers (41), but may be less burdened and may perceive caregiving more positively than other ethnic groups (42).

In conclusion, we find initial evidence that depressive symptoms may exacerbate the effects of psychological stress on catecholamine response in spousal Alzheimer’s caregivers. Chronic changes in basal NE and hyperarousability in the context of stress might lead to molecular (e.g., coagulation factors, adhesion molecules) and vascular (e.g., increased vascular resistance) changes that increase risk of cardiovascular disease in caregivers.


   NOTES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
REFERENCES
 

Received for publication January 4, 2005; revision received February 14, 2005.

DOI:10.1097/01.psy.0000173312.90148.97


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 

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