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Originally published as JCO Early Release 10.1200/JCO.2005.02.0081 on May 1 2006 © 2006 American Society of Clinical Oncology. Objective Cancer-Related Variables Are Not Associated With Depressive Symptoms in Women Treated for Early-Stage Breast Cancer
From the Department of Psychiatry, the Rebecca and John Moores University of California San Diego Cancer Center, and Department of Family and Preventive Medicine, University of California, San Diego, CA; for the Women's Healthy Eating and Living (WHEL) Study Group Address reprint requests to Wayne A. Bardwell, PhD, Department of Psychiatry, 9500 Gilman Dr, Mail Code 0804, University of California San Diego, La Jolla, CA 92093-0804; e-mail: wabardwell{at}ucsd.edu
PURPOSE: Women with breast cancer are thought to be vulnerable to depression for reasons associated with impact of diagnosis, treatment, and metabolic/endocrine changes. While the literature shows that most of these women do not become clinically depressed, 15% to 30% report elevated depressive symptoms that may be clinically important. The purpose was to identify and determine the relative importance of predictors of depressive symptoms in women treated for early-stage breast cancer.
PATIENTS AND METHODS: A total of 2,595 women (
RESULTS: Results of the binary logistic regression analysis were significant (overall R2 = 32.4%). Before entry of psychosocial variables, younger age, being unmarried, poorer physical functioning, and more vasomotor and gastrointestinal symptoms were significant risk factors for elevated depressive symptoms (R2 = 16.1%), but objective cancer-related variables were not. After inclusion of psychosocial variables in the model ( CONCLUSION: Depressive symptoms in women treated for early-stage breast cancer are not associated with objective cancer-related factors. Rather, they are most strongly linked with many subjective psychosocial variables.
Depression, the most common affective disorder in cancer, has a major impact on quality of life.1-5 Depressive disorders occur in 3% to 55% of women with breast cancer, usually within 6 months of diagnosis.3,10,11 Other studies suggest that 20% to 30% experience ongoing distress, even years after initial treatment.12,13 Estimates vary due to differences in timing, depression definitions/scales, and populations studied.4,14 Untreated depression is associated with poorer medical adherence,6,7 longer hospital stays, and increased morbidity and possibly mortality in breast cancer.8,9 Thus, identification of patients likely to experience depression is critical to ongoing care. While studies of mood in medical patients typically focus on major depressive disorder, interest is growing regarding the importance of subsyndromal levels of depressive symptoms.15 Depression can be viewed as a spectrum disorder in which increasing symptoms have an increasing impact on function. We use this spectrum approach here. In the literature on depression in breast cancer, various risk factors have been identified. Previous studies varied in sample size, constructs assessed, and populations examined. It is challenging to identify a set of factors that are consistently linked with depression in this population. Risk may be associated with cancer or treatment (cancer severity,16 treatment type,14,17-19 pain as treatment adverse effect,20 less time since diagnosis5), personal characteristics (younger age,5,17,20-22 minority status11), and health behaviors (less physical activity,22 diet23). In addition, physical functioning/symptoms (pain,5,16,17 vasomotor symptoms/menopause,5,14 impaired functioning5,16,17,21,24) have been linked with depression in this group. Kendler et al25 reported that various aspects of psychosocial functioning are related to depressive symptoms in women in the general population. Such factors have also been linked with depression in breast cancer, and include social deficits,5,16,20,26 pessimism,5,13,27 lower self-esteem,20 ambivalence over negative emotional expression,5 psychiatric history,16,28 and sleep disturbance.5 Thus, psychosocial factors, particularly social and personality variables, are most frequently linked with depression in breast cancer. Regarding cancer-related variables, treatment, specifically systemic treatments, is often,17-19,24 but not always,11,20,29-33 identified as a risk factor. Of personal characteristics, younger age5,17,20-22 is consistently cited. In addition, impaired physical functioning5,16,17,21,24 and physical symptoms5,14,16,17 are often linked with worse depression in this group. Poor health behaviors are less-frequently reported.22,23 Kendler et al25 concluded that a full understanding of depression requires consideration of a wide range of risk factors. Thus, predictors of depressive symptoms are varied, requiring an approach broad enough to encompass disparate domains. The biopsychosocial approach outlines one framework for understanding how illness, treatment, and other factors act in concert to influence a patient's experience of life in general and illness in particular.34 This systems approach can be used to understand depressive symptoms in medical patients, involving objective (observable) and subjective (self-report) variables as risk factors.34,35 These prior studies have contributed significantly to the literature in this area. Of the studies cited above, those specifically focusing on breast cancer and depressive symptoms had sample sizes ranging from 21 to 331 patients (averaging 145 patients), plus a well-powered study (n = 1,866) which was narrowly focused on the impact of caregiving.36 Other studies were restricted in terms of characteristics of populations studied (low income,33 overweight,22 estrogen-deficient,18 young20 women). The Ganz et al21 and Schag et al24 studies were quite encompassing in terms of domains assessed, but used a general outcome variable: psychosocial risk/distress. Thus, the relative importance of each reported risk factor vis-à-vis depressive symptoms in breast cancer remains uncertain. Our purpose was to determine which previously-identified risk factors would remain significant in analyses having sufficient power to examine a large number of variables with depressive symptoms as the outcome. Here we compare the relative importance of a range of risk factors versus depressive symptoms in 2,595 women treated for early-stage breast cancer. This study is powered to simultaneously evaluate these predictors in a single model, shedding light on the relative importance of each predictor while controlling for the others. In a prior study,37 we observed that cancer-related variables were not meaningfully related to general mental health in these women. Coupled with the fact that this study is limited to women with early-stage breast cancer, we hypothesize that objective breast cancer-related variables will be less significant predictors of depressive symptoms than other variables not directly related to the disease.
Participants Participants were from the Women's Healthy Eating and Living (WHEL) Study—a randomized trial of a dietary intervention on breast cancer recurrence/survival38: 3,088 women (  4 years postcompletion of initial treatment for stage I ( 1 cm) -IIIA disease). Recruitment occurred at seven clinical sites in California, Oregon, Arizona, Texas; strategies included letters to women on tumor registries, referrals from oncologists and community outreach programs, and local media advertisements. Internal review boards at each site approved the study; participants consented before enrolling. The current analyses use data before randomization for 2,595 women having complete data (women who responded to all variables described below).
Measurement
Depressive symptoms.
The 8-item Center for Epidemiologic Studies-Depression Scale screening form (CES-Dsf) was developed to identify people likely to have a mood disorder. It was recently used to assess depression in studies of hormone-replacement therapy and QOL40 and depression and postmenopausal cardiovascular sequelae.41 Scores The RAND-36 Item Health Survey (RAND-36) emotional well-being subscale measures general psychological distress. It was used as a continuous outcome variable to replicate findings when using the CES-Dsf. The CES-Dsf was strongly inversely correlated with this subscale (r = –0.71), suggesting construct/convergent validity. Cancer-related variables. Objective cancer-related variables (verified via records review by WHEL site staff) include diagnosis date/stage, treatment, tamoxifen use. Personal characteristics. Demographics were obtained by interview. Body mass index (BMI) was calculated using weight/height measurements (kg/m2) from clinic visits.
Health behaviors.
Current smoking was self-reported. Physical activity was assessed by questionnaire and converted into metabolic equivalents (METs).45 Total energy expenditure was obtained by weighting time/week by METs: mild activity/walking
Physical functioning/symptoms.
The RAND-36 physical health factor was included as a measure of physical functioning. A 34-item self-report inventory assessed symptom occurrence/severity: 0 (none) to 3 (severe).48 Factor analysis37 yielded a 5-factor solution (overall
Psychosocial functioning.
The RAND-36 measures aspects of health relevant to functional status and well-being49 and is valid/reliable (
Statistical Analysis
Statistical techniques.
The high/low CES-Dsf groups were compared on predictors using Analytic approach. The purpose of the analyses was to determine the relative importance of risk factors in multivariate models. Because of the breadth of constructs included and because their relative importance has not been fully established, mediating/moderating effects were not tested. A hierarchical design (forced entry) was chosen for the binary logistic and linear regression models. Cancer-related variables entered first to determine if they explained significant variance in depressive symptoms by themselves. Personal characteristics (block 2), health behaviors (block 3), and physical functioning/symptoms (block 4) followed. Finally, because they were expected to explain the most variance, psychosocial variables entered last (block 5).
Participant Characteristics Participants averaged 53 years of age (range = 28 to 74) and were highly educated; 71% were married. Mean BMI was 27.4 kg/m2 (overweight).62 Eighty-five percent were white non-Hispanic, 5% were Hispanic, 4% were African American, and 4% were Asian/Pacific Islander—representative of the general breast cancer population. More than 1/3 were diagnosed with stage I, 56% had stage II, and 5% had stage IIIA disease. The sample was uniformly distributed regarding time since diagnosis (23% 1 year; 33% 1 to 2 years; 24% 2 to 3 years; 20% 3 to 4 years); 60% were being treated with tamoxifen. Only 5% were current smokers. Participants averaged 841 METs of physical activity/wk. Regarding alcohol intake, 16% reported none, 71% averaged one or fewer drinks per day, 9% averaged 1 to 2 drinks per day, and 4% averaged more than two drinks per day. Nearly one-third (32%) met all three National Cancer Institute dietary recommendations, 30% met two, 24% met one, and 14% met none. We compared women with and without complete data (t test). None of the differences for variables in Table 1 were statistically significant; thus, we have no evidence of nonrandomness. Social desirability was not meaningfully associated with any variable; therefore, response bias was not controlled.
t and  2 TestsThe groups did not differ on cancer-related variables (Table 1). High CES-Dsf women were younger, more likely to be unmarried and obese, more sedentary and included more smokers. The high CES-Dsf group had worse physical functioning and more pain, vasomotor, genitourinary, and GI symptoms; worse social functioning, less optimism, and more ambivalence over negative emotional expression, hostility, life events, and sleep disturbance.
Binary Logistic Regression
Before including psychosocial variables, the following explained a significant portion of variance in CES-Dsf group (in order of strength of association): RAND-36 physical health (t = 37.329, P .001), age ( 60 v < 50 years: t = 26.101, P .001), gastrointestinal symptoms (t = 11.662, P .001), being married (t = 10.606, P .001), vasomotor symptoms (t = 10.410, P .001). After including psychosocial variables, none of the cancer-related, personal characteristic, health behavior or physical functioning/symptoms variables remained significant. Life events (t = 50.746, P .001), optimism (t = 47.250, P .001), ambivalence over negative emotional expressiveness (t = 14.592, P .001), sleep disturbance (t = 13.316, P .001), social strain (t = 11.335, P .001), and social support (t = 11.197, P .001) were significant. In exploratory analyses, the women were grouped based on years since diagnosis. Separate binary logistic regressions were conducted per group to determine if relationships of cancer-related variables versus CES-Dsf group varied by time since diagnosis. None of the cancer-related variables were statistically significant predictors of depression in any of the time groups.
Linear Regression
After the psychosocial variables entered, RAND-36 physical health (ß = 0.142, t = 7.219) and age (ß = 0.102, t = 5.867) remained significant. In addition, optimism (ß = 0.300, t = 17.605), social support (ß = 0.161, t = 9.364), sleep disturbance (ß = –0.119, t = –7.219), social strain (ß = –0.124, t = –7.142), ambivalence over negative emotional expressiveness (ß = –0.114, t = –7.061), life events (ß = –0.075, t = –4.631), negative emotional expressiveness (ß = –0.070, t = –4.615), and education (ß = –0.050, t = –3.231) were significant (all P
Breast cancer occurs in a psychosocial context, various aspects of which can influence a woman's reaction to diagnosis, treatment, and survivorship. Impaired functioning, life stressors, and other perturbations independent of cancer can dramatically influence psychological functioning, perhaps because the patient was rendered more vulnerable by the cancer or because of premorbid personality factors. It appears that these contextual variables, more than objective cancer-specific variables, better predict risk for elevated depressive symptoms in women treated for early-stage breast cancer. Variable selection was guided by a biopsychosocial approach, and the breast cancer and general depression literature. In univariate analyses, women reporting more depressive symptoms were more obese and reported worse physical functioning and more physical symptoms. They were younger and less likely to be married, more sedentary, and more likely to smoke. They reported poorer social functioning, were less optimistic, more conflicted over expressing negative emotions, more hostile, had more major life stressors, and had disturbed sleep. They did not differ on cancer-related variables, though a trend was observed for fewer tamoxifen users to be depressed. The nonsignificance of cancer-related variables was confirmed in hierarchical binary logistic regression. Before entering psychosocial variables, women who were younger and unmarried, with poorer overall physical health and more vasomotor and gastrointestinal symptoms were at greater risk. At this point, predictors explained approximately 16% of variance in depression status. Including subjective psychosocial variables doubled the explained variance; however, none of the other identified risk factors remained significant in their presence. Subjective report of social functioning, personality, life stressors, and sleep disturbance were the only significant predictors in the final model. We attempted to replicate these findings using RAND-36 emotional well-being as a continuous outcome measure. The amount of variance explained by each block of variables was similar to the logistic regression results. Specific risk factors included poorer physical health and younger age, in addition to psychosocial variables. Differences from the binary logistic regression model may be because RAND-36 emotional well-being is a continuous, general measure of psychological symptoms. However, cancer-related variables remained nonsignificant. Findings suggest that objective aspects of cancer are not determinants of depressive symptoms in women who had completed treatment for early-stage breast cancer. Rather, subjective psychosocial factors carry the most weight, as has been previously observed.11,63 This conclusion is bolstered by our observation that rates of elevated depressive symptoms for women in the current study were remarkably similar to rates reported in at least two other studies of women in the general population.41,44 The literature is mixed in terms of the importance of cancer-related variables as correlates of mood in breast cancer. Some suggest that depression varies by stage16 or treatment17-19,24; others found no effects for cancer-specific factors.11,20,29-33 One might expect that as more time elapses since diagnosis/treatment, mood effects would decrease. However, the likelihood of reporting elevated depressive symptoms was evenly distributed by time since diagnosis. In exploratory analyses, we examined if women who experienced treatment-induced menopause might report more depressive symptoms than premenopausal women or those with natural menopause. We found no such differences. Most women treated for breast cancer do not become depressed; however, a significant number do. Our observations that cancer-related variables were not meaningful predictors of depression, and that the prevalence of depression in our sample is comparable to the general population, suggest that depression has little to do with the cancer itself. While it is critical that clinicians be alert to risk factors, they cannot rely on cancer-related variables for this purpose. Rather, the subjective experiences of these women (eg, life stress, low social support, sleep disturbance) are more salient risk factors for elevated depressive symptoms. Participants were well-educated, mostly white non-Hispanic women treated for early-stage breast cancer and motivated to take part in a dietary study. While demographically representative of women with breast cancer overall, this could limit generalizability of findings in women with different demographics or later-stage disease. Because these are cross-sectional data, causality cannot be determined. Much of the data were self-reported and subject to response bias. However, responses were not influenced by socially desirable responding.37 There is always a trade-off between using more detailed scales and respondent burden. We relied on the CES-Dsf to measure mood, which primarily taps cognitive/affective aspects of distress and is less likely to be complicated by neurovegetative symptoms of cancer or treatment. While the CES-Dsf has been used to measure depression in other studies,40,41 some authors suggest that it does not accurately discriminate individuals who meet mood disorder criteria. Therefore, we refer to women with elevated CES-Dsf scores as having clinically significant depressive symptoms. Our outcome measures are not cancer-specific. Cancer-related predictors might be more strongly linked with cancer-specific outcomes. Future studies might include a structured interview for depression or self-report instruments designed for diagnosis, and examine mediating/moderating effects of the identified risk factors.
The authors indicated no potential conflicts of interest.
Supported by Grants No. NCI CA69375; NIH M01-RR00070, M01-RR00079, M01-RR00827; the Walton Family Foundation; UCOP BCRP 7KB-0097; the Lance Armstrong Foundation; the Susan G. Komen Foundation POP0504026. Presented in part at the 2003 California Breast Cancer Research Program Conference, San Diego, CA, September 12-14, 2003, and the Academy of Psycho-Somatic Medicine Conference, Coronado, CA, November 19-23, 2003. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2006 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
R2 = 16.3%), none of the preceding variables remained significant. Greater risk for depressive symptoms was associated with stressful life events, less optimism, ambivalence over expressing negative emotions, sleep disturbance, and poorer social functioning. 
= .73, providing evidence of adequate internal consistency of scale items). 
