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A Psychological Profile of Depressed and Nondepressed Women at High Risk for Breast Cancer
A Psychological Profile of Depressed and Nondepressed Women at High Risk for Breast Cancer DAVID K. WELLISCH, PH.D. NANGEL M. LINDBERG, PH.D.
This study examines the difference on several demographic and psychosocial variables between women at high risk for breast cancer above and below the cut-off point of a depression measure (Center for Epidemiological Study Depression Scale). Data are presented for 430 consecutive patients from the UCLA Revlon Breast Center High Risk Clinic. Women scoring above the depression cut-off point were younger, had more relatives with breast cancer, reported more symptoms of anxiety, and had more self-perceived vulnerability to breast cancer. In addition, women above the depression cut-off point were more likely to be single, childless, to have not viewed the results of the surgical treatment of their relative, and to feel more anxiety regarding screening practices (mammography, pap smears, and breast self-examinations). (Psychosomatics 2001; 42:330–336)
C
urrent estimates are that one out of nine women will develop breast cancer during her lifetime,1 with the risk being two to three times higher for women with a firstdegree relative with the disease.2 The literature has long shown depression to be a common and often debilitating reaction to the threat of long-term and potentially fatal diseases,3 to compromise quality of life, and to have deleterious effects on physical health outcomes, including possibly the progression of cancer.4 Depression is not only important for the distress it produces but also because it may have an impact on individuals’ physical well-being. Certainly in terms of suicidality, depression does claim lives, representing a considerable risk factor for suicide. In addition to suicide, depression is also associated with increased mortality and morbidity due to medical conditions and accidents, including longer hospitalizations, poorer prognoses for recovery, and reduced motivation for rehabilitation among chronically ill paReceived October 30, 2000; revised March 1, 2001; accepted March 15, 2001. From the Department of Psychiatry, UCLA School of Medicine, and the Revlon-UCLA Breast Center. Address reprint requests to Dr. Wellisch, Neuropsychiatric Institute and Hospital, Center for the Health Sciences, 760 Westwood Plaza, Los Angeles, CA 90024-1759. Copyright 䉷 2001 The Academy of Psychosomatic Medicine.
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tients.5–7 It has even been speculated that depression may interfere with the ability of medically ill or at-risk individuals to follow health regimes or to seek medical treatment.8 A possible link has also been suggested between depressed and altered immunological functioning, possibly affecting peoples’ resistance to certain illnesses.9,10 Recent studies have shown women at risk for breast cancer to experience high levels of distress, including depression, somatization, intrusive thoughts, and avoidance.11,12 Despite the distress it produces and the impact it may have on health outcomes, depression may often go unnoticed or untreated among women at familial risk for breast cancer, partly due to a lack of clear standards for diagnosing such at-risk populations and also because depression may be seen as an expected and understandable result of being at risk.13 If those caring for at-risk populations believe that depression is to be expected as an understandable result of the at-risk status, individuals may be denied useful psychological interventions. At the UCLA High Risk Clinic to date, we have conducted psychological assessments of 430 patients; as shown elsewhere, of that population, 24% were above the clinical cut-off point on a standardized depression measure, indicating they experience clinically significant symptoms Psychosomatics 42:4, July-August 2001
Wellisch and Lindberg of depression.14 Given that 76% of this sample does not report significant symptoms of depression, it becomes clinically relevant to profile the differences between patients reporting significant versus nonsignificant symptoms of depression. One way in which this is potentially important is that we have found the experience of depression and anxiety symptoms to affect health-related behaviors.14 This paper, therefore, is an attempt to begin to further profile a group of high-risk women who report clinically significant symptoms of depression on a standardized psychological test specifically measuring depression. METHOD
The average number of relatives afflicted with breast cancer was two, with a range of 0 to 26. Over 28% of participants reported having three or more relatives affected with breast cancer. For the present paper, data included in the analyses represent participants for whom complete responses were obtained for each instrument (N⳱301). Data were analyzed using depressive symptomatology as a grouping variable; participants were grouped according to their scores on the Center for Epidemiologic Studies Depression Scale (CES-D). Those scoring at or below 15 were considered to be nondepressed, whereas those scoring at or above 16 were considered to exhibit significant symptoms of depression.
Overview of Procedures Assessment Procedures These data are presented as part of a baseline stage of a larger research project conducted at the UCLA Revlon Breast Center High Risk Clinic. The High Risk Clinic is a multidisciplinary setting that serves patients considered to be at heightened risk for breast cancer either because of having one or more first-degree relatives with the illness or because of exhibiting precancerous breast changes. At the initial visit, patients are individually seen and counseled by an oncologist, a genetics counselor, a nurse practitioner, a nutritionist, and a psychologist; most patients also receive a mammogram. At each follow-up visit, patients are seen by specific members of the team according to the patient’s needs. Participants Data are presented for 430 consecutive patients from the High Risk Clinic who were approached and consented at the time of their initial visit to the clinic. Approximately 1% of the participants declined participation. Participants were between the ages of 15 and 78, with a mean age of 42.62. The majority were white (84.4%), married (60.6%), and had a college or advanced degree (72.6%). As shown in Table 1, most participants (n⳱362; 83.2%) had a family history of breast cancer but no precancerous breast changes; 21 participants (5.1%) had precancerous breast changes and no family history; and 25 participants (6.1%) reported both precancerous breast changes and a family history. Among patients with family history of breast cancer, most reported having a mother with the disease (n⳱271; 71.4%), while 62 (15.9%) had a sibling with breast cancer, and 50 (12.8%) had both a mother and one or more siblings with the illness. Psychosomatics 42:4, July-August 2001
The information presented here was obtained during the patients’ initial consultation with the team psychologist. After consenting, participants completed baseline questionnaires assessing depression and anxiety and a semistructured clinical interview, which provided psychosocial background information including their thoughts and feelings regarding health behaviors and their actual health practices. After the patient completed the questionnaires and the clinical interview, the psychologist remained available to answer questions regarding the study or to address specific issues brought up during the interview. Measures The data reported here are based on the following instruments. Center for Epidemiologic Studies Depression Scale (CES-D). The CES-D is a 20-question instrument that meaTABLE 1.
Demographic information on participants n (%)
Risk Factors Family history of breast cancer only Precancerous breast changes only Family history and precancerous breast changes Relative with Breast Cancer Mother One or more sisters Mother and one or more sisters Number of Relatives with Breast Cancer One Two Three More than three
362 (83.2) 21 ( 5.1) 25 ( 6.1) 279 (71.4) 62 (15.9) 50 (12.8) 142 134 73 44
(39.2) (32.5) (17.6) (10.5)
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Depression and Breast Cancer sures depressive symptomatology. The test has excellent concurrent validity (levels up to r⳱0.72) and split-half and coefficient alpha reliability (r⳱0.85 for general population; r⳱0.90 for clinical population); the current study yielded an internal consistency score of 0.92. Although not constituting a clinical diagnosis of depression, scores at or above 16 on the CES-D are considered indicative of clinically significant symptoms of depression. State-Trait Anxiety Inventory (STAI-S and STAI-T). The STAI is a 40-question instrument that measures current level of anxiety (“state anxiety”) and a characterological or enduring level of anxiety (“trait anxiety”). Responses are on a 4-point Likert scale (“almost never”, “sometimes”, “often”, and “almost always”). This test has excellent concurrent validity (levels up to r⳱0.80) and reliability (r⳱0.77). The STAI manual reports high internal consistency for both the Trait scale and the State scale, which was replicated in this study with internal consistency scores of 0.89 (state anxiety) and 0.91 (trait anxiety). Perceived Risk of Breast Cancer. To assess personal risk for developing breast cancer, participants were asked to provide an estimate of their likelihood of developing breast cancer in their lifetime, on a scale of 0% to 100%, with higher scores indicating higher perceived risk of developing breast cancer. Computed Risk of Breast Cancer. The assessment of risk for developing breast cancer was conducted using the Gail model, which uses information including the subjects’ age of menarche, number of pregnancies, age at first live birth, number of previous breast biopsies, and number of first-degree relatives with breast cancer, to yield a risk score of the estimated true likelihood of developing breast cancer by age 80, on a scale of 0% to 100%, with higher scores indicating higher risk. Anxiety Regarding Screening Practices. Participants were asked to rate the level of anxiety they experienced about undergoing pap smear tests, obtaining regular mammography tests, and doing regular breast self-examinations (BSEs). Each screening practice was assessed by a separate item on a 4-point scale, ranging from 1 (“minimal”) to 4 (“maximum”). Compliance Regarding Screening Practices. Participants were asked to state their level of compliance with recommendations regarding performing BSEs and obtaining pap smears and mammograms. For each, compliance was assessed on a 3-point scale ranging from 1 (“generally compliant”) to 3 (“rarely compliant”). Similar self-reported measures for BSE frequency have been widely used in the field of breast cancer research.15,16 332
RESULTS Table 2 shows seven demographic and psychological variables for women scoring below and above the CES-D cutoff point (ⱖ16). As can be seen, five of the variables showed significant differences between the two groups. As shown, at their initial clinic visit, women scoring above the depression cut-off point are significantly younger (mean⳱40.58 years) than women scoring below the CES-D cut-off point (mean⳱43.98 years; t⳱2.29, P⳱0.02). Women scoring above the depression cut-off point have significantly more relatives with breast cancer (mean⳱2.33) than women below the depression cut-off point (mean⳱1.98; t⳱2.1, P⳱0.04). When estimating their own risk of developing breast cancer, women scoring above the CES-D cut-off point report higher personal risk estimates (mean⳱56.7%) than do women scoring below the cut-off point (mean⳱48.10%; t⳱2.28, P⳱0.02). In a comparison of the actual computed risk of the two groups, a nonsignificant trend emerged, with the actual risk of women above the CES-D cut-off being higher (mean⳱19.82%) than that of women below the cutoff point (mean⳱17.89; t⳱1.63, P⳱0.11). In terms of STAI State and Trait anxiety scores, women that scored above the CES-D cut-off point reported significantly higher levels of State anxiety (mean⳱50.36) than women that score below the cut-off point (mean⳱34.32; t⳱10.57, P⳱0.000). As shown, the same pattern emerged regarding Trait anxiety, with women scoring above the CES-D cut-off point reporting significantly higher levels of Trait anxiety (mean⳱50.03) than women scoring below the cut-off point (mean⳱33.69; t⳱13.66, P⳱0.000). As can be seen in Table 2, the patient’s age at the time of the afflicted relative’s diagnosis approached statistical significance (t⳱1.92, P⳱0.053), with women above the depression cut-off point reporting being younger (mean age⳱25.46) than those scoring below the cut-off point (mean⳱29.22) at the time of their relative’s diagnosis. Table 3 shows how women scoring below and above the clinical cut-off point of the depression measure are distributed along several psychosocial variables. As shown, women with no children are significantly overrepresented among those scoring as depressed on the CES-D (v2⳱5.3, df⳱1, P⳱0.03). Women that are single, divorced, or separated are also overrepresented in the group scoring above the CES-D cut-off point (v2⳱13.9, df⳱1, P⳱0.02). Finally, Table 3 also shows that women who did not see the results of their relative’s surgical treatment are also overrepresented in the group scoring above Psychosomatics 42:4, July-August 2001
Wellisch and Lindberg the clinical cut-off point of the CES-D (v2⳱5.25, df⳱1, P⳱0.03). Table 4 shows how women scoring below and above the clinical cut-off point of the CES-D differ on their selfreported compliance with and anxiety about screening procedures. As can be seen, no differences were found between the groups on their self-reported compliance with screening practices, including compliance with pap smear exams (F⳱0.06, P⳱0.80), mammograms (F⳱0.34, P⳱0.56), and BSEs (F⳱0.89, P⳱0.35). By contrast, however, significant differences emerged when assessing subjects’ anxiety regarding the screening practices. As shown, women scoring above the clinical cut-off point of the CES-D report significantly more anxiety regarding pap smears (mean⳱1.58 vs. mean⳱1.35, F⳱5.01, P⳱0.03), mammograms (mean⳱2.43 vs. mean⳱2.10, F⳱3.57, P⳱0.06), and BSEs (mean⳱2.52 vs. mean⳱1.93, F⳱ 15.47, P⳱0.00) than women scoring below the CES-D. DISCUSSION One of the most important findings of this study is that the presence of certain demographic characteristics in women attending high-risk programs should alert the clinician to
TABLE 2.
the likelihood of potentially severe depressive symptoms. In our study, women presenting with clinically significant symptoms of depression at their initial visit to our clinic tended to be younger than patients whose self-reported symptoms of depression did not place them at a clinically significant level. In addition, we found a very strong, although nonsignificant trend that may suggest that age at first exposure to cancer may constitute a risk factor for the later experience of depression; specifically, this nonsignificant trend (P⳱0.053) indicated that the younger women are at the time of their afflicted relative’s diagnosis, the more likely they may be to report symptoms of depression years later. It appears that the exposure to a relative’s breast cancer constitutes a traumatic stressor that leads to depressive symptomatology later in life. This finding is consistent with the cognitive model of depression20,21 that postulates that negative schemas develop from early negative experiences and lead to cognitive styles characterized by negative and pessimistic selection and interpretation of information. These cognitive styles in turn lead to depressive affect. This nonsignificant trend is also highly consistent with our clinical experience with hundreds of high-risk patients,
Demographic/psychosocial variables of high-risk women scoring below and above the CES-D clinical cut-off point
Variables Age at initial interview Below CES-D Above CES-D Total number of relatives with breast cancer Below CES-D Above CES-D Personal risk estimate Below CES-D Above CES-D Computed risk Below CES-D Above CES-D Age at relative’s diagnosis Below CES-D Above CES-D State Anxiety (STAI-S) Below CES-D Above CES-D Trait Anxiety (STAI-T) Below CES-D Above CES-D
N
MeanⴣSD Scores
t
Significance
230 71
43.98Ⳳ11.16 40.58Ⳳ10.25
2.29
0.02
231 70
1.98Ⳳ1.21 2.33Ⳳ1.27
2.1
0.04
173 55
48.10Ⳳ24.97 56.7Ⳳ22.77
2.28
0.02
223 70
17.89Ⳳ8.20 19.82Ⳳ8.83
1.63
0.11
223 72
29.22Ⳳ14.64 25.43Ⳳ14.22
1.95
0.053
236 74
34.32Ⳳ9.38 50.36Ⳳ11.96
10.57
0.000
237 73
33.69Ⳳ7.15 50.03Ⳳ9.42
13.66
0.000
Note: Significance results include trend ⬍0.15
Psychosomatics 42:4, July-August 2001
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Depression and Breast Cancer where we find that being younger at the time of first exposure to a close relative’s breast cancer introduces into life an unexpected level of vulnerability and unpredictability that later can become a “depressogenic theme” that effectively challenges the person’s sense of trust and safety and thereby alters many of her life expectations. It is clear that for a woman to have a mother diagnosed with breast cancer constitutes a traumatic event that elicits extreme fear, the perception of helplessness, and the potential for physical injury or death. For many individuals, depression appears to begin precisely with traumatic events such as parental loss or a threat to their attachment objects.8 Given the importance that actual or perceived risk to a parent has in the development of long-term depression,22 the fact that most women attending high-risk breast cancer clinics have a mother (82% in our sample) with the disease emphasizes the importance of closely attending to patients’ depressive symptomatology. Depressive affect and the depressive cognitive style with which these patients may present may affect their emotional well-being and health-related behaviors. In addition, having a mother with breast cancer places the daughter at risk for developing the disease herself and constitutes a separate stressor that elicits fear, a sense TABLE 3.
of helplessness, and the potential for physical injury or death. It seems then that having a mother with breast cancer constitutes a sort of double traumatic stressor, one involving a threat to an attachment object and one threatening the person herself. In this context, earlier exposure to maternal breast cancer is likely to be associated with depression, anxiety, and other forms of responses to traumatic stress. An additional finding in our study appears to be that “the more, the sadder.” That is, the sheer number of relatives affected with breast cancer makes a significant difference in the depressive symptomatology of at-risk women. The total number of relatives affected with breast cancer is often ignored or overlooked by researchers and practitioners alike. Frequently, the focus of attention is on one relative only. These data show the clinical importance of inquiring about all affected relatives. Therefore asking “how many?” as well as “who?” and “how close?” becomes a potentially critical question to identify individuals likely to have significant depressive symptoms. It is perhaps not surprising that patients scoring in the depressive range on the CES-D overestimate their personal risk compared to patients scoring in the nondepressed range. This is consistent with a “depressive triad” of a neg-
Number of women above and below the CES-D clinical cut-off point that have children, are married, and have seen the results of their relative’s surgery Below CES-D, N (%)
Variable Having children Having no children Single/Never Married Married Divorced/Separated Saw surgery results Did not see results
133 97 53 153 25 145 44
(82%) (70%) (68%) (81%) (66%) (80%) (66%)
Above CES-D, N (%) 30 41 25 35 12 37 23
(18%) (30%) (32%) (19%) (34%) (20%) (34%)
v2
Significance
5.3
0.03
13.9
0.02
5.25
0.03
Note: Percentage of participants scoring below and above the CES-D clinical cut-off point are shown for each row variable in parentheses.
TABLE 4.
Screening-related anxiety and compliance for women scoring below and above the CES-D clinical cut-off point CES-D Cut-Off Point
Variable Pap smear compliance Mammogram compliance Breast self-exam compliance Pap smear anxiety Mammogram anxiety Breast self-exam anxiety
Below
Above
F
Significance
1.2 1.52 1.9 1.35 2.10 1.93
1.18 1.6 2.0 1.58 2.43 2.52
0.06 0.34 0.89 5.01 3.57 15.47
0.80 0.56 0.35 0.03 0.06 0.000
Note: Compliance assessed on a 1-3 scale: 1⳱very compliant; 2⳱somewhat compliant; 3⳱noncompliant. Anxiety assessed on a 1-4 scale: 1⳱minimal; 4⳱maximum.
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Psychosomatics 42:4, July-August 2001
Wellisch and Lindberg ative view of self, the world, and the future.21 Even though both groups vastly overestimate their likelihood of getting breast cancer compared to their actual calculated risks, it is interesting that the computed risk for the depressive group is marginally (but not statistically significantly) higher than the nondepressed group. This suggests that depressive individuals’ self-assessment of their risk is not entirely distorted, at least in regard to real vulnerability of getting breast cancer. It is important to note that our finding of a heightened perception of personal vulnerability to breast cancer among at-risk women is in direct contrast to the fact that most women that develop breast cancer do not have a history of the disease and that only 5%–10% of breast cancers appear to be strongly hereditary.23 It was also not surprising to find that women with higher symptoms of depression also have higher symptoms of anxiety. This is consistent with observations of our clinic population that symptoms of depression and anxiety merge and present as an agitated ruminative depressive style. This is also consistent with the finding that depression and anxiety measures are often highly correlated.8 Regarding the finding of higher levels of depressive symptoms among unmarried and childless clinic patients, it is clear that this is not a picture unique to this at-risk population. The literature overwhelmingly indicates that women are more likely to be depressed than men8 and that the onset of their depressive symptoms tends to peak sharply in middle age.24 In addition, there is considerable evidence that being unmarried and having smaller social networks are factors associated with depressive symptomatology.25,26 We would therefore expect that, like women of normal risk, women at high risk for breast cancer would present more symptoms of depression if they are unmarried and childless. This finding underscores the importance of having strong and dependable sources of social support as a protective factor against depression and in coping with high-risk status. In this regard it is particularly important to note the evidence linking social support to individuals’ health habits and medical compliance.27,28
The finding that women who have avoided seeing the results of a relative’s breast cancer surgery present with higher levels of depression is important. This finding may be viewed as evidence that among women at familial risk for breast cancer, an avoidant coping style regarding a relative’s breast cancer surgery is not successful and may instead lead to the experience of considerable depressive symptoms. Our finding is consistent with previous studies showing that the use of avoidance coping strategies in emotional distress leads to higher levels of distress.29 In our clinic, we try to foster more vigilant coping styles, encourage feelings of mastery, and counter fearful withdrawal by supporting women’s attempts to view the results of a relative’s surgery. Finally, the data regarding anxiety, compliance with screening tests, and depression shows that at-risk women that present with high levels of depressive symptoms do have higher levels of anxiety regarding screening procedures. However, this does not translate into poorer patterns of compliance. Here again, feelings of depression and anxiety appear to coexist but not at a level intense enough to derail positive health behaviors regarding screening compliance. Some caution should be taken in interpreting the data regarding compliance given that the self-report of past behaviors may not be a fully reliable indicator of current or future behavior; however, because of the private nature of BSEs, such self-report measures remain the only vehicle on which this research field relies to assess the frequency of this screening procedure. Finally, it is important to note that given the high level of education and risk awareness of the participants in this study, the present findings may not generalize to other atrisk populations or to those that attend other breast cancer preventive programs. This research was supported by funds from the California Breast Cancer Research Program of the University of California, Grant 4BF-0002, to the second author, and in part by Ruth Weil Family, and Lawrence and Carol Mann Family.
References
1. American Cancer Society: Cancer Facts and Figures. New York, American Cancer Society, 1991 2. Anderson DE: Familial versus sporadic breast cancer. Cancer 1992; 70:1740–1746 3. Rodin G, Voshart K: Depression in the medically ill: an overview. Am J Psychiatry 1986; 143:696–705 4. Andersen BL, Kiecolt-Glaser J, Glaser R: A biobehavioral model of cancer stress and disease course. Am Psychol 1994; 49: 389–404
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5. Tsuang MT, Simpson JC: Mortality studies in psychiatry: should they stop or proceed? Arch Gen Psychiatry 1985; 42:69–78 6. Adams SG, Dammers PM, Saia TL, et al: Stress, depression, and anxiety predict average symptom severity and daily symptom fluctuation in systemic lupus erythematosus. J Behav Med 1994; 17:459–478 7. Thompson SC, Sobolew-Shubin A, Graham MA, et al: Psychological adjustment following a stroke. Soc Sci Med 1989; 28: 239–247
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Depression and Breast Cancer 8. Gotlib IH, Hammen CL: Psychological Aspects of Depression. New York, Wiley, 1992 9. Cohen S, Herbert TB: Health psychology: psychological factors and physical disease from the perspective of human psychoneuroimmunology. Annu Rev Psychol 1996; 47:113–142 10. Cohen SM, Tyrrell DA, Smith AP: Negative life events, perceived stress, negative affect, and susceptibility to the common cold. J Pers Soc Psychol 1993; 64:131–140 11. Gilbar O: Women with high risk for breast cancer: Psychological symptoms. Psychol Rep 1997; 80:800–802 12. Zakowski SG, Vladimarsdottir HB, Bovbjerg DH, et al: Prediction of intrusive thoughts and avoidance in women with family histories of breast cancer. Ann Behav Med 1997; 19:362–369 13. Massie MJ, Holland JC: Consultation and liaison issues in cancer care. Psychiatric Medicine 1987; 5:343–359 14. Lindberg N: Prediction of compliance and retention in high risk patients. Poster session presented at the California Breast Cancer Research Symposium. Los Angeles, CA, September, 1999 15. Kash KM, Holland JC, Halper MS, et al: Psychological distress and surveyance behaviors of women with a family history of breast cancer. J Natl Cancer Inst 1991; 84:24–30 16. Stefanek ME, Wilcox PJ: First-degree relatives of breast cancer patients: screening practices and provision of risk information. Cancer Detect Prev 1991; 15:379–384 17. Lerman C, Trock B, Rimer BK, et al: Psychological side effects of breast cancer screening. Health Psychol 1991; 10:259–267 18. Wellisch DK, Gritz ER, Schain W, et al: Psychological functioning of daughters of breast cancer patients. Psychosomatics 1991; 32:324–336
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19. Brain K, Norman P, Gray J, et al: Anxiety and adherence to breast self-examination in women with a family history of breast cancer. Psychosom Med 1999; 6:181–187 20. Beck AT: Depression: Clinical, Experimental, and Theoretical Aspects. New York, Harper & Row, 1967 21. Beck AT: Cognitive Therapy and the Emotional Disorders. New York, International Universities Press, 1976 22. Bowlby J: Attachment and Loss. Volume 1: Attachment. New York, Basic Books, 1969 23. Kelly P: Assessing Your Risk of Breast Cancer. New York, Holt, 2000 24. Lewinsohn PM, Duncan EM, Stanton AK, et al: Age at first onset for nonbipolar depression. J Abnorm Psychol 1986; 95:378–383 25. Brim JA, Witcoff C, Wetzel RD: Social network characteristics of hospitalized depressed patients. Psychol Rep 1982; 50:423–433 26. Golding JM: Role occupancy and role-specific stress and social support as predictors of depression. Basic and Applied Social Psychology 1989; 10:173–195 27. Umberson D: Family status and health behaviors: social control as a dimension of social integration. J Health Soc Behav 1987; 28:306–319 28. Christensen AJ, Smith TW, Turner CW, et al: Family support, physical impairment and adherence in hemodialysis: an investigation of main and buffering effects. J Behav Med 1992; 15: 313–326 29. Holahan CJ, Moos RH: Personality, coping, and family resources in stress resistance: a longitudinal analysis. J Pers Soc Psychol 1986; 51:389–395
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This study examines the difference on several demographic and psychosocial variables between women at high risk for breast cancer above and below the cut-off point of a depression measure (Center for Epidemiological Study Depression Scale). Data are presented for 430 consecutive patients from the UCLA Revlon Breast Center High Risk Clinic. Women scoring above the depression cut-off point were younger, had more relatives with breast cancer, reported more symptoms of anxiety, and had more self-perceived vulnerability to breast cancer. In addition, women above the depression cut-off point were more likely to be single, childless, to have not viewed the results of the surgical treatment of their relative, and to feel more anxiety regarding screening practices (mammography, pap smears, and breast self-examinations). (Psychosomatics 2001; 42:330–336)
C
urrent estimates are that one out of nine women will develop breast cancer during her lifetime,1 with the risk being two to three times higher for women with a firstdegree relative with the disease.2 The literature has long shown depression to be a common and often debilitating reaction to the threat of long-term and potentially fatal diseases,3 to compromise quality of life, and to have deleterious effects on physical health outcomes, including possibly the progression of cancer.4 Depression is not only important for the distress it produces but also because it may have an impact on individuals’ physical well-being. Certainly in terms of suicidality, depression does claim lives, representing a considerable risk factor for suicide. In addition to suicide, depression is also associated with increased mortality and morbidity due to medical conditions and accidents, including longer hospitalizations, poorer prognoses for recovery, and reduced motivation for rehabilitation among chronically ill paReceived October 30, 2000; revised March 1, 2001; accepted March 15, 2001. From the Department of Psychiatry, UCLA School of Medicine, and the Revlon-UCLA Breast Center. Address reprint requests to Dr. Wellisch, Neuropsychiatric Institute and Hospital, Center for the Health Sciences, 760 Westwood Plaza, Los Angeles, CA 90024-1759. Copyright 䉷 2001 The Academy of Psychosomatic Medicine.
330
tients.5–7 It has even been speculated that depression may interfere with the ability of medically ill or at-risk individuals to follow health regimes or to seek medical treatment.8 A possible link has also been suggested between depressed and altered immunological functioning, possibly affecting peoples’ resistance to certain illnesses.9,10 Recent studies have shown women at risk for breast cancer to experience high levels of distress, including depression, somatization, intrusive thoughts, and avoidance.11,12 Despite the distress it produces and the impact it may have on health outcomes, depression may often go unnoticed or untreated among women at familial risk for breast cancer, partly due to a lack of clear standards for diagnosing such at-risk populations and also because depression may be seen as an expected and understandable result of being at risk.13 If those caring for at-risk populations believe that depression is to be expected as an understandable result of the at-risk status, individuals may be denied useful psychological interventions. At the UCLA High Risk Clinic to date, we have conducted psychological assessments of 430 patients; as shown elsewhere, of that population, 24% were above the clinical cut-off point on a standardized depression measure, indicating they experience clinically significant symptoms Psychosomatics 42:4, July-August 2001
Wellisch and Lindberg of depression.14 Given that 76% of this sample does not report significant symptoms of depression, it becomes clinically relevant to profile the differences between patients reporting significant versus nonsignificant symptoms of depression. One way in which this is potentially important is that we have found the experience of depression and anxiety symptoms to affect health-related behaviors.14 This paper, therefore, is an attempt to begin to further profile a group of high-risk women who report clinically significant symptoms of depression on a standardized psychological test specifically measuring depression. METHOD
The average number of relatives afflicted with breast cancer was two, with a range of 0 to 26. Over 28% of participants reported having three or more relatives affected with breast cancer. For the present paper, data included in the analyses represent participants for whom complete responses were obtained for each instrument (N⳱301). Data were analyzed using depressive symptomatology as a grouping variable; participants were grouped according to their scores on the Center for Epidemiologic Studies Depression Scale (CES-D). Those scoring at or below 15 were considered to be nondepressed, whereas those scoring at or above 16 were considered to exhibit significant symptoms of depression.
Overview of Procedures Assessment Procedures These data are presented as part of a baseline stage of a larger research project conducted at the UCLA Revlon Breast Center High Risk Clinic. The High Risk Clinic is a multidisciplinary setting that serves patients considered to be at heightened risk for breast cancer either because of having one or more first-degree relatives with the illness or because of exhibiting precancerous breast changes. At the initial visit, patients are individually seen and counseled by an oncologist, a genetics counselor, a nurse practitioner, a nutritionist, and a psychologist; most patients also receive a mammogram. At each follow-up visit, patients are seen by specific members of the team according to the patient’s needs. Participants Data are presented for 430 consecutive patients from the High Risk Clinic who were approached and consented at the time of their initial visit to the clinic. Approximately 1% of the participants declined participation. Participants were between the ages of 15 and 78, with a mean age of 42.62. The majority were white (84.4%), married (60.6%), and had a college or advanced degree (72.6%). As shown in Table 1, most participants (n⳱362; 83.2%) had a family history of breast cancer but no precancerous breast changes; 21 participants (5.1%) had precancerous breast changes and no family history; and 25 participants (6.1%) reported both precancerous breast changes and a family history. Among patients with family history of breast cancer, most reported having a mother with the disease (n⳱271; 71.4%), while 62 (15.9%) had a sibling with breast cancer, and 50 (12.8%) had both a mother and one or more siblings with the illness. Psychosomatics 42:4, July-August 2001
The information presented here was obtained during the patients’ initial consultation with the team psychologist. After consenting, participants completed baseline questionnaires assessing depression and anxiety and a semistructured clinical interview, which provided psychosocial background information including their thoughts and feelings regarding health behaviors and their actual health practices. After the patient completed the questionnaires and the clinical interview, the psychologist remained available to answer questions regarding the study or to address specific issues brought up during the interview. Measures The data reported here are based on the following instruments. Center for Epidemiologic Studies Depression Scale (CES-D). The CES-D is a 20-question instrument that meaTABLE 1.
Demographic information on participants n (%)
Risk Factors Family history of breast cancer only Precancerous breast changes only Family history and precancerous breast changes Relative with Breast Cancer Mother One or more sisters Mother and one or more sisters Number of Relatives with Breast Cancer One Two Three More than three
362 (83.2) 21 ( 5.1) 25 ( 6.1) 279 (71.4) 62 (15.9) 50 (12.8) 142 134 73 44
(39.2) (32.5) (17.6) (10.5)
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Depression and Breast Cancer sures depressive symptomatology. The test has excellent concurrent validity (levels up to r⳱0.72) and split-half and coefficient alpha reliability (r⳱0.85 for general population; r⳱0.90 for clinical population); the current study yielded an internal consistency score of 0.92. Although not constituting a clinical diagnosis of depression, scores at or above 16 on the CES-D are considered indicative of clinically significant symptoms of depression. State-Trait Anxiety Inventory (STAI-S and STAI-T). The STAI is a 40-question instrument that measures current level of anxiety (“state anxiety”) and a characterological or enduring level of anxiety (“trait anxiety”). Responses are on a 4-point Likert scale (“almost never”, “sometimes”, “often”, and “almost always”). This test has excellent concurrent validity (levels up to r⳱0.80) and reliability (r⳱0.77). The STAI manual reports high internal consistency for both the Trait scale and the State scale, which was replicated in this study with internal consistency scores of 0.89 (state anxiety) and 0.91 (trait anxiety). Perceived Risk of Breast Cancer. To assess personal risk for developing breast cancer, participants were asked to provide an estimate of their likelihood of developing breast cancer in their lifetime, on a scale of 0% to 100%, with higher scores indicating higher perceived risk of developing breast cancer. Computed Risk of Breast Cancer. The assessment of risk for developing breast cancer was conducted using the Gail model, which uses information including the subjects’ age of menarche, number of pregnancies, age at first live birth, number of previous breast biopsies, and number of first-degree relatives with breast cancer, to yield a risk score of the estimated true likelihood of developing breast cancer by age 80, on a scale of 0% to 100%, with higher scores indicating higher risk. Anxiety Regarding Screening Practices. Participants were asked to rate the level of anxiety they experienced about undergoing pap smear tests, obtaining regular mammography tests, and doing regular breast self-examinations (BSEs). Each screening practice was assessed by a separate item on a 4-point scale, ranging from 1 (“minimal”) to 4 (“maximum”). Compliance Regarding Screening Practices. Participants were asked to state their level of compliance with recommendations regarding performing BSEs and obtaining pap smears and mammograms. For each, compliance was assessed on a 3-point scale ranging from 1 (“generally compliant”) to 3 (“rarely compliant”). Similar self-reported measures for BSE frequency have been widely used in the field of breast cancer research.15,16 332
RESULTS Table 2 shows seven demographic and psychological variables for women scoring below and above the CES-D cutoff point (ⱖ16). As can be seen, five of the variables showed significant differences between the two groups. As shown, at their initial clinic visit, women scoring above the depression cut-off point are significantly younger (mean⳱40.58 years) than women scoring below the CES-D cut-off point (mean⳱43.98 years; t⳱2.29, P⳱0.02). Women scoring above the depression cut-off point have significantly more relatives with breast cancer (mean⳱2.33) than women below the depression cut-off point (mean⳱1.98; t⳱2.1, P⳱0.04). When estimating their own risk of developing breast cancer, women scoring above the CES-D cut-off point report higher personal risk estimates (mean⳱56.7%) than do women scoring below the cut-off point (mean⳱48.10%; t⳱2.28, P⳱0.02). In a comparison of the actual computed risk of the two groups, a nonsignificant trend emerged, with the actual risk of women above the CES-D cut-off being higher (mean⳱19.82%) than that of women below the cutoff point (mean⳱17.89; t⳱1.63, P⳱0.11). In terms of STAI State and Trait anxiety scores, women that scored above the CES-D cut-off point reported significantly higher levels of State anxiety (mean⳱50.36) than women that score below the cut-off point (mean⳱34.32; t⳱10.57, P⳱0.000). As shown, the same pattern emerged regarding Trait anxiety, with women scoring above the CES-D cut-off point reporting significantly higher levels of Trait anxiety (mean⳱50.03) than women scoring below the cut-off point (mean⳱33.69; t⳱13.66, P⳱0.000). As can be seen in Table 2, the patient’s age at the time of the afflicted relative’s diagnosis approached statistical significance (t⳱1.92, P⳱0.053), with women above the depression cut-off point reporting being younger (mean age⳱25.46) than those scoring below the cut-off point (mean⳱29.22) at the time of their relative’s diagnosis. Table 3 shows how women scoring below and above the clinical cut-off point of the depression measure are distributed along several psychosocial variables. As shown, women with no children are significantly overrepresented among those scoring as depressed on the CES-D (v2⳱5.3, df⳱1, P⳱0.03). Women that are single, divorced, or separated are also overrepresented in the group scoring above the CES-D cut-off point (v2⳱13.9, df⳱1, P⳱0.02). Finally, Table 3 also shows that women who did not see the results of their relative’s surgical treatment are also overrepresented in the group scoring above Psychosomatics 42:4, July-August 2001
Wellisch and Lindberg the clinical cut-off point of the CES-D (v2⳱5.25, df⳱1, P⳱0.03). Table 4 shows how women scoring below and above the clinical cut-off point of the CES-D differ on their selfreported compliance with and anxiety about screening procedures. As can be seen, no differences were found between the groups on their self-reported compliance with screening practices, including compliance with pap smear exams (F⳱0.06, P⳱0.80), mammograms (F⳱0.34, P⳱0.56), and BSEs (F⳱0.89, P⳱0.35). By contrast, however, significant differences emerged when assessing subjects’ anxiety regarding the screening practices. As shown, women scoring above the clinical cut-off point of the CES-D report significantly more anxiety regarding pap smears (mean⳱1.58 vs. mean⳱1.35, F⳱5.01, P⳱0.03), mammograms (mean⳱2.43 vs. mean⳱2.10, F⳱3.57, P⳱0.06), and BSEs (mean⳱2.52 vs. mean⳱1.93, F⳱ 15.47, P⳱0.00) than women scoring below the CES-D. DISCUSSION One of the most important findings of this study is that the presence of certain demographic characteristics in women attending high-risk programs should alert the clinician to
TABLE 2.
the likelihood of potentially severe depressive symptoms. In our study, women presenting with clinically significant symptoms of depression at their initial visit to our clinic tended to be younger than patients whose self-reported symptoms of depression did not place them at a clinically significant level. In addition, we found a very strong, although nonsignificant trend that may suggest that age at first exposure to cancer may constitute a risk factor for the later experience of depression; specifically, this nonsignificant trend (P⳱0.053) indicated that the younger women are at the time of their afflicted relative’s diagnosis, the more likely they may be to report symptoms of depression years later. It appears that the exposure to a relative’s breast cancer constitutes a traumatic stressor that leads to depressive symptomatology later in life. This finding is consistent with the cognitive model of depression20,21 that postulates that negative schemas develop from early negative experiences and lead to cognitive styles characterized by negative and pessimistic selection and interpretation of information. These cognitive styles in turn lead to depressive affect. This nonsignificant trend is also highly consistent with our clinical experience with hundreds of high-risk patients,
Demographic/psychosocial variables of high-risk women scoring below and above the CES-D clinical cut-off point
Variables Age at initial interview Below CES-D Above CES-D Total number of relatives with breast cancer Below CES-D Above CES-D Personal risk estimate Below CES-D Above CES-D Computed risk Below CES-D Above CES-D Age at relative’s diagnosis Below CES-D Above CES-D State Anxiety (STAI-S) Below CES-D Above CES-D Trait Anxiety (STAI-T) Below CES-D Above CES-D
N
MeanⴣSD Scores
t
Significance
230 71
43.98Ⳳ11.16 40.58Ⳳ10.25
2.29
0.02
231 70
1.98Ⳳ1.21 2.33Ⳳ1.27
2.1
0.04
173 55
48.10Ⳳ24.97 56.7Ⳳ22.77
2.28
0.02
223 70
17.89Ⳳ8.20 19.82Ⳳ8.83
1.63
0.11
223 72
29.22Ⳳ14.64 25.43Ⳳ14.22
1.95
0.053
236 74
34.32Ⳳ9.38 50.36Ⳳ11.96
10.57
0.000
237 73
33.69Ⳳ7.15 50.03Ⳳ9.42
13.66
0.000
Note: Significance results include trend ⬍0.15
Psychosomatics 42:4, July-August 2001
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Depression and Breast Cancer where we find that being younger at the time of first exposure to a close relative’s breast cancer introduces into life an unexpected level of vulnerability and unpredictability that later can become a “depressogenic theme” that effectively challenges the person’s sense of trust and safety and thereby alters many of her life expectations. It is clear that for a woman to have a mother diagnosed with breast cancer constitutes a traumatic event that elicits extreme fear, the perception of helplessness, and the potential for physical injury or death. For many individuals, depression appears to begin precisely with traumatic events such as parental loss or a threat to their attachment objects.8 Given the importance that actual or perceived risk to a parent has in the development of long-term depression,22 the fact that most women attending high-risk breast cancer clinics have a mother (82% in our sample) with the disease emphasizes the importance of closely attending to patients’ depressive symptomatology. Depressive affect and the depressive cognitive style with which these patients may present may affect their emotional well-being and health-related behaviors. In addition, having a mother with breast cancer places the daughter at risk for developing the disease herself and constitutes a separate stressor that elicits fear, a sense TABLE 3.
of helplessness, and the potential for physical injury or death. It seems then that having a mother with breast cancer constitutes a sort of double traumatic stressor, one involving a threat to an attachment object and one threatening the person herself. In this context, earlier exposure to maternal breast cancer is likely to be associated with depression, anxiety, and other forms of responses to traumatic stress. An additional finding in our study appears to be that “the more, the sadder.” That is, the sheer number of relatives affected with breast cancer makes a significant difference in the depressive symptomatology of at-risk women. The total number of relatives affected with breast cancer is often ignored or overlooked by researchers and practitioners alike. Frequently, the focus of attention is on one relative only. These data show the clinical importance of inquiring about all affected relatives. Therefore asking “how many?” as well as “who?” and “how close?” becomes a potentially critical question to identify individuals likely to have significant depressive symptoms. It is perhaps not surprising that patients scoring in the depressive range on the CES-D overestimate their personal risk compared to patients scoring in the nondepressed range. This is consistent with a “depressive triad” of a neg-
Number of women above and below the CES-D clinical cut-off point that have children, are married, and have seen the results of their relative’s surgery Below CES-D, N (%)
Variable Having children Having no children Single/Never Married Married Divorced/Separated Saw surgery results Did not see results
133 97 53 153 25 145 44
(82%) (70%) (68%) (81%) (66%) (80%) (66%)
Above CES-D, N (%) 30 41 25 35 12 37 23
(18%) (30%) (32%) (19%) (34%) (20%) (34%)
v2
Significance
5.3
0.03
13.9
0.02
5.25
0.03
Note: Percentage of participants scoring below and above the CES-D clinical cut-off point are shown for each row variable in parentheses.
TABLE 4.
Screening-related anxiety and compliance for women scoring below and above the CES-D clinical cut-off point CES-D Cut-Off Point
Variable Pap smear compliance Mammogram compliance Breast self-exam compliance Pap smear anxiety Mammogram anxiety Breast self-exam anxiety
Below
Above
F
Significance
1.2 1.52 1.9 1.35 2.10 1.93
1.18 1.6 2.0 1.58 2.43 2.52
0.06 0.34 0.89 5.01 3.57 15.47
0.80 0.56 0.35 0.03 0.06 0.000
Note: Compliance assessed on a 1-3 scale: 1⳱very compliant; 2⳱somewhat compliant; 3⳱noncompliant. Anxiety assessed on a 1-4 scale: 1⳱minimal; 4⳱maximum.
334
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Wellisch and Lindberg ative view of self, the world, and the future.21 Even though both groups vastly overestimate their likelihood of getting breast cancer compared to their actual calculated risks, it is interesting that the computed risk for the depressive group is marginally (but not statistically significantly) higher than the nondepressed group. This suggests that depressive individuals’ self-assessment of their risk is not entirely distorted, at least in regard to real vulnerability of getting breast cancer. It is important to note that our finding of a heightened perception of personal vulnerability to breast cancer among at-risk women is in direct contrast to the fact that most women that develop breast cancer do not have a history of the disease and that only 5%–10% of breast cancers appear to be strongly hereditary.23 It was also not surprising to find that women with higher symptoms of depression also have higher symptoms of anxiety. This is consistent with observations of our clinic population that symptoms of depression and anxiety merge and present as an agitated ruminative depressive style. This is also consistent with the finding that depression and anxiety measures are often highly correlated.8 Regarding the finding of higher levels of depressive symptoms among unmarried and childless clinic patients, it is clear that this is not a picture unique to this at-risk population. The literature overwhelmingly indicates that women are more likely to be depressed than men8 and that the onset of their depressive symptoms tends to peak sharply in middle age.24 In addition, there is considerable evidence that being unmarried and having smaller social networks are factors associated with depressive symptomatology.25,26 We would therefore expect that, like women of normal risk, women at high risk for breast cancer would present more symptoms of depression if they are unmarried and childless. This finding underscores the importance of having strong and dependable sources of social support as a protective factor against depression and in coping with high-risk status. In this regard it is particularly important to note the evidence linking social support to individuals’ health habits and medical compliance.27,28
The finding that women who have avoided seeing the results of a relative’s breast cancer surgery present with higher levels of depression is important. This finding may be viewed as evidence that among women at familial risk for breast cancer, an avoidant coping style regarding a relative’s breast cancer surgery is not successful and may instead lead to the experience of considerable depressive symptoms. Our finding is consistent with previous studies showing that the use of avoidance coping strategies in emotional distress leads to higher levels of distress.29 In our clinic, we try to foster more vigilant coping styles, encourage feelings of mastery, and counter fearful withdrawal by supporting women’s attempts to view the results of a relative’s surgery. Finally, the data regarding anxiety, compliance with screening tests, and depression shows that at-risk women that present with high levels of depressive symptoms do have higher levels of anxiety regarding screening procedures. However, this does not translate into poorer patterns of compliance. Here again, feelings of depression and anxiety appear to coexist but not at a level intense enough to derail positive health behaviors regarding screening compliance. Some caution should be taken in interpreting the data regarding compliance given that the self-report of past behaviors may not be a fully reliable indicator of current or future behavior; however, because of the private nature of BSEs, such self-report measures remain the only vehicle on which this research field relies to assess the frequency of this screening procedure. Finally, it is important to note that given the high level of education and risk awareness of the participants in this study, the present findings may not generalize to other atrisk populations or to those that attend other breast cancer preventive programs. This research was supported by funds from the California Breast Cancer Research Program of the University of California, Grant 4BF-0002, to the second author, and in part by Ruth Weil Family, and Lawrence and Carol Mann Family.
References
1. American Cancer Society: Cancer Facts and Figures. New York, American Cancer Society, 1991 2. Anderson DE: Familial versus sporadic breast cancer. Cancer 1992; 70:1740–1746 3. Rodin G, Voshart K: Depression in the medically ill: an overview. Am J Psychiatry 1986; 143:696–705 4. Andersen BL, Kiecolt-Glaser J, Glaser R: A biobehavioral model of cancer stress and disease course. Am Psychol 1994; 49: 389–404
Psychosomatics 42:4, July-August 2001
5. Tsuang MT, Simpson JC: Mortality studies in psychiatry: should they stop or proceed? Arch Gen Psychiatry 1985; 42:69–78 6. Adams SG, Dammers PM, Saia TL, et al: Stress, depression, and anxiety predict average symptom severity and daily symptom fluctuation in systemic lupus erythematosus. J Behav Med 1994; 17:459–478 7. Thompson SC, Sobolew-Shubin A, Graham MA, et al: Psychological adjustment following a stroke. Soc Sci Med 1989; 28: 239–247
335
Depression and Breast Cancer 8. Gotlib IH, Hammen CL: Psychological Aspects of Depression. New York, Wiley, 1992 9. Cohen S, Herbert TB: Health psychology: psychological factors and physical disease from the perspective of human psychoneuroimmunology. Annu Rev Psychol 1996; 47:113–142 10. Cohen SM, Tyrrell DA, Smith AP: Negative life events, perceived stress, negative affect, and susceptibility to the common cold. J Pers Soc Psychol 1993; 64:131–140 11. Gilbar O: Women with high risk for breast cancer: Psychological symptoms. Psychol Rep 1997; 80:800–802 12. Zakowski SG, Vladimarsdottir HB, Bovbjerg DH, et al: Prediction of intrusive thoughts and avoidance in women with family histories of breast cancer. Ann Behav Med 1997; 19:362–369 13. Massie MJ, Holland JC: Consultation and liaison issues in cancer care. Psychiatric Medicine 1987; 5:343–359 14. Lindberg N: Prediction of compliance and retention in high risk patients. Poster session presented at the California Breast Cancer Research Symposium. Los Angeles, CA, September, 1999 15. Kash KM, Holland JC, Halper MS, et al: Psychological distress and surveyance behaviors of women with a family history of breast cancer. J Natl Cancer Inst 1991; 84:24–30 16. Stefanek ME, Wilcox PJ: First-degree relatives of breast cancer patients: screening practices and provision of risk information. Cancer Detect Prev 1991; 15:379–384 17. Lerman C, Trock B, Rimer BK, et al: Psychological side effects of breast cancer screening. Health Psychol 1991; 10:259–267 18. Wellisch DK, Gritz ER, Schain W, et al: Psychological functioning of daughters of breast cancer patients. Psychosomatics 1991; 32:324–336
336
19. Brain K, Norman P, Gray J, et al: Anxiety and adherence to breast self-examination in women with a family history of breast cancer. Psychosom Med 1999; 6:181–187 20. Beck AT: Depression: Clinical, Experimental, and Theoretical Aspects. New York, Harper & Row, 1967 21. Beck AT: Cognitive Therapy and the Emotional Disorders. New York, International Universities Press, 1976 22. Bowlby J: Attachment and Loss. Volume 1: Attachment. New York, Basic Books, 1969 23. Kelly P: Assessing Your Risk of Breast Cancer. New York, Holt, 2000 24. Lewinsohn PM, Duncan EM, Stanton AK, et al: Age at first onset for nonbipolar depression. J Abnorm Psychol 1986; 95:378–383 25. Brim JA, Witcoff C, Wetzel RD: Social network characteristics of hospitalized depressed patients. Psychol Rep 1982; 50:423–433 26. Golding JM: Role occupancy and role-specific stress and social support as predictors of depression. Basic and Applied Social Psychology 1989; 10:173–195 27. Umberson D: Family status and health behaviors: social control as a dimension of social integration. J Health Soc Behav 1987; 28:306–319 28. Christensen AJ, Smith TW, Turner CW, et al: Family support, physical impairment and adherence in hemodialysis: an investigation of main and buffering effects. J Behav Med 1992; 15: 313–326 29. Holahan CJ, Moos RH: Personality, coping, and family resources in stress resistance: a longitudinal analysis. J Pers Soc Psychol 1986; 51:389–395
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