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Journal of Clinical Oncology, Vol 24, No 1 (January 1), 2006: pp. 95-101
© 2006 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2006.10.064

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Psychological Distress in Men With Breast Cancer

Kate Brain, Buddug Williams, Rachel Iredale, Liz France, Jonathon Gray

From the Institute of Medical Genetics, School of Medicine, Cardiff University, University Hospital of Wales, Cardiff, United Kingdom

Address reprint requests to Kate Brain, PhD, Institute of Medical Genetics, School of Medicine, Cardiff University, Heath Park, Cardiff CF14 4XN, United Kingdom; e-mail: Kate.Brain{at}CardiffandVale.wales.nhs.uk


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
PURPOSE: This article reports the first United Kingdom study to examine the prevalence of psychological distress in men with breast cancer and the factors associated with increased distress.

PATIENTS AND METHODS: One hundred and sixty-one men with breast cancer completed a cross-sectional questionnaire that included measures of anxiety and depressive symptoms, cancer-specific distress, body image, coping, information and support needs, and clinical and demographic variables.

RESULTS: Clinical levels of anxiety and depressive symptoms were reported by 6% and 1% of men, respectively, while 23% reported high levels of cancer-specific distress. Anxiety was most strongly associated with avoidance coping and fear and uncertainty about the future (42% of the variance in anxiety scores, P < .001). Depressive symptoms were associated with altered body image (35% of the variance, P < .001). Body image, avoidance coping, referral to the study by a clinician, fear and uncertainty, and wanting to receive more gender-specific information together explained 51% of the variance in cancer-related distress (P < .001). Clinical and demographic factors did not account for a significant proportion of the variance in any of the distress measures.

CONCLUSION: Although the prevalence of clinical anxiety and depressive symptoms were low in this sample, almost a quarter of men experienced traumatic stress symptoms specific to breast cancer. Potential risk factors for distress include the use of avoidant coping strategies, negative body image, feelings of fear and uncertainty in relation to breast cancer, and unmet information needs. Suggestions are made for improving the information and support available to men with breast cancer.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
Breast cancer in men is rare. It is estimated that 1% of breast cancer cases diagnosed annually in the United Kingdom are men, with 240 men newly diagnosed in 2000,1 though a recent study suggests that the incidence may be increasing.2 The clinical features of this condition are similar to those seen in women, with hormonal, genetic, and environmental factors thought to play a role in its development.3,4

There is a lack of awareness among the public, as well as health professionals, that breast cancer can affect men, and treatment and management strategies are currently based on those used for women. Exploratory focus groups and interviews conducted with male and female breast cancer patients have highlighted a need for gender-specific information and support.5,6

Breast cancer in men is an under-researched area. In contrast, there has been a great deal of research regarding the psychological impact of other forms of cancer. Studies indicate that around a quarter of female breast cancer patients exhibit clinically significant distress in the first year after diagnosis,7-9 while studies of prevalence in men diagnosed with prostate cancer have yielded figures ranging from 0%10 to 38%11 reporting distress above Hospital and Anxiety Depression Scale threshold scores.12 Carrol et al13 and Ford et al14 identified clinically significant distress in approximately one quarter of patients who had been diagnosed with various forms of cancer. Other studies have measured specific cancer-related distress in patients with cancer, in particular intrusive thoughts and avoidance of such thoughts as measured by the Impact of Event Scale (IES).15 For example, Hampton and Frombach16 found high IES scores in 10% of male patients and 20% of female patients one year after diagnosis. Kaasa et al17 found high IES scores in 21% of a mixed sample of advanced-stage cancer patients, with significantly higher scores in women compared to men. It is unclear to what extent such findings can be extrapolated to men with breast cancer.

An understanding of the factors associated with distress in male breast cancer patients is important in identifying men who may benefit from increased emotional support. A range of studies has examined demographic and clinical factors risk factors for increased distress in patients with other forms of cancer. Younger age has consistently been associated with increased distress in cancer patients.10,18-20 In a sample of women recently diagnosed with primary breast cancer, factors including younger age and greater number of postsurgical treatments were associated with higher IES scores.21 Taniguchi et al22 found that unmarried men with cancer reported significantly higher distress compared to those who were married. Cancer stage is a key predictor of distress, with the potential for psychological distress occurring at various points including diagnosis, treatment, follow-up, and recurrence. Distress levels are typically elevated at the point of diagnosis,19 and may reappear on completing treatment due to the loss of regular contact with health care professionals.23 Treatment side effects of radiotherapy and hormone therapy, such as nausea, weight gain, pain and fatigue, may also cause distress,24 and breast surgery may generate concerns about body image.25,5 At present, the psychological effect of treatment factors on men with breast cancer is unknown.

Coping strategies in response to cancer are likely to be important correlates of psychological distress in this group of men. Folkman and Lazarus’s26-28 theory of stress and coping suggests that the ways in which people cope with stressful events are critical in influencing the effects of these events on emotional responses. Although particular forms of coping are not inherently adaptive or maladaptive,29 studies of coping and distress in cancer patients suggest that avoidant coping strategies involving denial and behavioral disengagement tend to be associated with poor emotional outcomes, while engagement-oriented strategies (such as active coping and positive reframing) tend to facilitate emotional adjustment.30-33 Stanton and Snider19 found that avoidance was associated with high distress pre- and postsurgery in a sample of women with breast cancer. Conversely, engagement coping strategies involving active confrontation and acceptance have been associated with better psychological outcomes in women with early stage breast cancer34 and women undergoing biopsy for a suspicious breast lesion.35 To date, there have been no studies of coping in men with breast cancer.

This study reports findings from one phase of a multistage project, which was undertaken to explore the experiences of men diagnosed with breast cancer in the United Kingdom—the Men’s Attitudes Towards Cancer and Health (MATCH) project.36 A cross-sectional questionnaire employing standardized measures was conducted to examine the psychological impact of breast cancer in men. Other phases of the project involved qualitative interviews and focus groups to explore men’s experiences in greater depth.6 Specific aims of the survey were to examine (1) the prevalence of anxiety, depressive symptoms, and cancer-specific distress in men with breast cancer, and (2) concurrent associations between clinical, demographic, and psychosocial factors and distress in these men. It was hypothesized that higher distress would be associated with variables including younger age, more recent diagnosis, a greater number of cancer treatments, the use of avoidant coping strategies, altered body image, and unmet information and support needs. Understanding the psychological needs of men diagnosed with breast cancer would enable health care professionals to improve the quality of care, and to identify those men who may be at risk for significant psychological distress.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
Ethical approval for the MATCH project was obtained from a multicenter research ethics committee. During the period from October 2002 to December 2003, men with breast cancer were invited to take part in the study by cancer genetics clinicians located in regional genetics centers, or by breast care clinicians through the United Kingdom National Cancer Research Network. A total of 87 clinicians were issued patient information sheets and consent forms, and were encouraged to distribute them to all men with breast cancer in their care. Men were also recruited in response to media publicity about the study. Questionnaire packs were only sent to men once they had given written informed consent form to participate in the study. A total of 186 consent forms were returned: 138 via clinicians (74%) and 48 from media respondents (26%).

Due to the indirect nature of the recruitment process, it was not possible to estimate the total number of men who had been approached to participate in the study. From the 186 men who returned consent forms, 171 went on to complete questionnaires (92%). Data from 10 men were subsequently excluded due to the length of time since they had been diagnosed with breast cancer (> 10 years). Analyses were therefore based on 161 participants (82% from clinicians and 18% who self-referred).

Measures
General distress. The Hospital Anxiety and Depression Scale (HADS)12 is a 14-item assessment of psychiatric morbidity that provides two separate measures of anxiety (range, 0 to 21) and depression (range, 0 to 21). Higher scores indicate higher levels of anxiety and depression, respectively. Threshold scores of ≥ 11 on each scale are considered to indicate a probable diagnosis of clinical anxiety or depression.10 The HADS has been well validated.37 In the current study, Cronbach’s {alpha} scores for the internal consistency of subscales were satisfactory ({alpha} = .87 for anxiety, {alpha} = .76 for depression).

Cancer-specific distress. The IES15 is a 15-item measure of the frequency of intrusive thoughts and avoidance of traumatic thoughts related to a stressful event, in this case breast cancer. A total IES can be calculated, with cutoff points for low distress (below 8.5), moderate distress (8.5-18), and high distress (≥ 19; Horowitz, personal communication, August 1999). The IES has been used in a study of women recently diagnosed with primary breast cancer21 and men newly diagnosed with prostate cancer.10 Good internal reliability was found in this study (Cronbach’s {alpha} = .89).

Body image. The Body Image Scale (BIS)38 is a 10-item measure of body image changes in patients with cancer. A higher score indicates a negatively altered body image as a consequence of cancer. Body image has been identified as a key component of quality of life in cancer patients, particularly in relation to mastectomy versus breast conserving treatments.39-41 The BIS has been validated in patients with a range of cancer sites.38 In this study, internal consistency of the BIS was satisfactory ({alpha} = .89).

Coping. Coping was measured using a 28-item version of the COPE42 developed for use with breast cancer patients.33 It consists of 11 two-item scales and two three-item scales measuring a variety of ways of coping with breast cancer. Factor analysis was used to generate higher-order factors from the coping data in the present study. Two factors labeled engagement and avoidance were generated, consistent with previous studies.42,32 Higher scores indicate more frequent use of each form of coping. Engagement coping consisted of strategies including emotional support, positive reframing, and planning. Avoidance coping consisted of strategies including denial, behavioral disengagement, and substance use. The two scales demonstrated satisfactory internal consistency (engagement {alpha} = .89, avoidance {alpha} = .79).

Stress appraisal. Participants were asked to rate how stressful each of four specific cancer-related problems had been for them during the past month.30,43 Problems were related to physical ability, appearance or lifestyle; pain, symptoms or discomfort; fear and uncertainty about the future; and problems with family and friends due to breast cancer. Items were each rated on a five-point scale, where 1 was equal to "not at all stressful" and 5 was equal to "extremely stressful."

Information and support needs. Participants were asked whether they had wanted to receive further information specific to men with breast cancer, and whether they would like the opportunity to attend a support group of men with breast cancer. Items were included to gather demographic and clinical data from participants.

Statistical Analysis
Statistical analyses were computed using SPSS version 12.0 (SPSS Inc, Chicago, IL). The first stage involved description of the demographic and clinical characteristics of the study sample. Secondly, scores on standardized measures of psychological distress were examined using descriptive statistics. Thirdly, preliminary associations between distress indices and a range of demographic, clinical, and psychological variables were tested using independent t-tests for dichotomous variables and Pearson’s product moment correlations for continuous variables. (For independent t tests, Levene’s test for equality of variances was examined to account for the possibility of unequal variance of samples. In cases where F values were statistically significant at P < .01, separate variance estimates are reported.) Finally, variables that were significantly associated with distress at the 5% level were entered simultaneously into standard multiple regression equations to identify the salient factors associated with anxiety, depressive symptoms, and cancer-related distress. Multivariate outliers were sought and excluded following inspection of standardized residuals, together with the Mahalanobis distance statistic.44 There was no evidence of multicollinearity and all tolerance levels were acceptable.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
Sample Characteristics
Sample characteristics are displayed in Table 1. The average age of participants at the time of sample was 67 years. Most men were married or living with a partner, had been educated to at least secondary level, and were recruited to the study via clinicians. Thirty five percent of men reported having a family history of breast cancer. The mean time since diagnosis was 2.9 years. Most men reported having been treated with radical mastectomy (81%), hormone therapy (78%), and/or radiotherapy (54%), while a smaller proportion had undergone chemotherapy (27%) and/or lumpectomy (24%). Fifty three percent of men reported having more than one postsurgical treatment. Fifty five percent of men were currently undergoing breast cancer treatment including hormonal therapy, such as tamoxifen (n = 77), chemotherapy (n = 7) and radiotherapy (n = 3), and of these almost half reported that they were currently experiencing treatment side effects or symptoms. In men who had completed treatment, the mean time since completion was 2.09 years. More than half of the patients wanted to receive further information specific to breast cancer in men, and almost one third were interested in attending a patient support group.


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Table 1. Sample Characteristics (N = 161)

 
Prevalence of Psychological Distress
Table 2 indicates that the proportion of scores reaching the threshold for significant psychological distress varied from 1% on the HADS Depression scale, to 6% on the HADS Anxiety scale, and 23% on the global IES. Mean HADS scores were lower than those in a sample of men diagnosed with prostate cancer11(anxiety mean = 7.17, standard deviation [SD] = 4.36; depression mean = 5.09, SD = 3.80) and a sample of patients with various forms of cancer37(anxiety mean = 5.44, SD = 4.07; depression mean = 3.02, SD = 2.98).


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Table 2. Descriptive Statistics for HADS and IES Scores

 
Preliminary Associations Between Psychological Distress and Demographic, Clinical, and Psychological Variables
Table 3 illustrates the pattern of concurrent associations between the distress measures and dichotomous demographic, clinical, and psychological variables. Significantly higher depressive symptoms and IES scores were reported by men who had a mastectomy and who were experiencing comorbid symptoms. Men who were unmarried or noncohabiting and who had been referred to the study by a clinician also reported significantly higher IES scores. The latter finding may indicate selection bias of referring clinicians, although it is possible that men who entered the study through media announcements were less representative than clinician-referred men, since distress scores for the former were lower than reference norms for other cancer patients.10,37 There was a significant effect of having gender-specific information needs on anxiety, depressive symptoms, and IES scores. Men who expressed interest in attending a support group had significantly higher IES scores than those who did not. These variables were included in subsequent regression analyses.


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Table 3. Preliminary Relationships Between Psychological Distress and Dichotomous Variables (N= 161)

 
As indicated in Table 4, higher levels of anxiety, depressive symptoms, and cancer-related distress were significantly correlated with continuous variables including younger age, altered body image, more frequent use of engagement and avoidance coping, and greater perceived stressfulness of cancer-related problems relating to physical ability, pain or symptoms, and fear and uncertainty about the future. None of the raw correlations suggested multicollinearity (ie, none exceeded 0.80.)


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Table 4. Preliminary Relationships Between Psychological Distress and Continuous Variables

 
Multiple Regression Analyses
Table 5 summarizes the results of standard multiple regression. HADS anxiety was independently associated with more frequent use of avoidance coping (P ≤ .01) and a high level of fear and uncertainty about the future (P ≤ .05). Together, these variables accounted for 42% of the variance in anxiety scores (F = 10.58; P < .001). Avoidance coping made the largest unique contribution to the variance in anxiety scores. Altered body image (P ≤ .001) was the most salient factor associated with depression, accounting for 35% of the variance in HADS depression scores (F = 6.19, P < .001). Cancer-related IES score was independently related to referral source (P ≤ .01), fear and uncertainty (P ≤ .01), avoidance coping (P ≤ .01), poor body image (P ≤ .01), and the presence of gender-specific information needs (P ≤ .05). These variables together explained 51% of the variance in IES scores (F = 8.58, P < .001).


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Table 5. Summary of Standard Regression Analyses Including Standardized Regression Coefficients (ß), t Values, and Significance Levels

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
To our knowledge, this is the first study to examine the prevalence of psychological distress and factors associated with increased distress in a sample of men with breast cancer. Scores for anxiety and depression were lower than those found in other studies of patients with various forms of cancer, as well as men diagnosed with prostate cancer, suggesting that a breast cancer diagnosis in men does not catalyze global maladjustment. A further possibility is that cancer-specific measures such as the IES are more sensitive than global measures of anxiety and depression, hence the level of distress detected depends on the measures that are used.10 Cancer-specific anxiety was more frequently reported than general anxiety and depressive symptoms, with almost one quarter of men experiencing high levels of intrusive thoughts about breast cancer and avoidance of such thoughts. Previous research indicates lower levels of IES-measured distress in men with other forms of cancer,16,17 suggesting that cancer-specific distress may indeed be more prominent than general distress in men diagnosed with breast cancer. Breast cancer encompasses a range of specific stressors that may threaten men’s emotional well being, for example concerns about masculinity, fear of stigma, and a sense of isolation associated with the general lack of awareness and information about the condition.

The salient factors associated with psychological distress in this study included the use of avoidance coping strategies, fear and uncertainty about the future, altered body image, and unmet information needs in relation to breast cancer. These variables accounted for a moderate to strong proportion of the variance in distress scores. However, demographic and clinical variables were not significantly related to distress. Similarly, Cordova et al20 did not find significant associations between distress in female breast cancer patients and clinical factors including recency of diagnosis and treatment, type of surgery, or number of treatments. A larger study is needed to identify the impact of these variables on psychological well being in men at various stages of breast cancer.

There have been many studies of coping in women with a breast cancer diagnosis, but few studies of coping in male cancer patients. In this study, coping efforts directed at avoidance —for example through denial, behavioral disengagement, and substance use—emerged as significant correlates of higher distress in men with breast cancer. This is consistent with previous studies of coping in female breast cancer patients.19,33,34 Paradoxically, attempts to cope with long-term distress by avoiding or suppressing unwanted intrusive thoughts may exacerbate such thoughts, creating a vicious circle of intrusion and avoidance.45,46 Although particular coping strategies are not inherently adaptive or maladaptive, studies have consistently shown associations between the use of avoidance coping and negative affect, and between engagement coping and positive affect.30,32 Coping efforts directed at engagement did not emerge as significant correlates of distress in the current sample. However, preliminary associations between distress and coping indicated that greater use of all forms of coping correlated with higher levels of distress, suggesting that coping may be ineffective in this group. An alternative interpretation is that heightened distress was driving higher use of all coping strategies. However, it is recognized that the cross-sectional nature of the study precludes any causal inference, therefore conclusions cannot be drawn regarding the extent to which alternative coping strategies were helpful in ameliorating distress. Although prospective studies support the idea that avoidance coping predicts poor adjustment to breast cancer,19,34 further research is needed to explore relationships between coping and emotions experienced over the course of breast cancer. Nevertheless, this study provides preliminary evidence that counseling and support aimed at reducing avoidance may have beneficial effects in men with breast cancer.

This study emphasizes the need for increased awareness and information about breast cancer in men. Gender-specific information needs, and fear and uncertainty about the future, contributed significantly to the experience of distress in this sample, as did negative perceptions of personal appearance after breast cancer. Having a disease which affects predominantly women may threaten a man’s sense of masculinity and engender feelings of isolation.47 Men would benefit from receiving information early in the referral process about treatment options, side effects, symptoms, survival rates, cancer recurrence, and the potential impact on quality of life and body image. Health care professionals have an important role to play in providing information and support to men with breast cancer, as well as informing them about the availability of formal support networks.48 Almost one third of men in our sample were interested in attending a patient support group. Practical suggestions for improving information and awareness include the use of leaflets with information on male breast cancer and a photograph of a male mastectomy, local matching schemes and telephone help-lines, as well as raising public awareness through the media.47 Studies suggest that men may be less likely than women to disclose distress and seek help,49,50 and it is possible that health care providers may underestimate the psychosocial impact of breast cancer on men. Screening for psychological distress is therefore essential, so that men who may benefit from additional emotional support can be identified early on in the referral process.6 General screening tools such as the HADS may underestimate the prevalence of distress in men with breast cancer, and disease-specific measures such as the IES should be used in combination with generic measures.

We acknowledge the methodological limitations of this study. Due to the indirect nature of the recruitment process, it was not possible to estimate the overall number of men who had been approached to participate in the study. The extent to which the current findings can be generalized is therefore unclear. Potential sources of bias are acknowledged, including possible selection bias of clinicians who identified and referred patients to the study. In addition, the cross-sectional design of the study limits conclusions that can be drawn regarding the direction of associations between distress and coping. Prospective studies are needed to capture the pattern of distress as men progress from diagnosis to treatment and beyond, and to explore which coping strategies are most adaptive at different stages of the breast cancer experience.


    Authors’ Disclosures of Potential Conflicts of Interest
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
The authors indicated no potential conflicts of interest.


    Author Contributions
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 

Conception and design: Kate Brain, Jonathon Gray, Rachel Iredale, Liz France

Provision of study materials or patients: Jonathon Gray

Collection and assembly of data: Kate Brain, Buddug Williams, Rachel Iredale, Liz France

Data analysis and interpretation: Kate Brain, Jonathon Gray, Buddug Williams, Rachel Iredale, Liz France

Manuscript writing: Kate Brain, Jonathon Gray, Buddug Williams, Rachel Iredale, Liz France

Final approval of manuscript: Kate Brain, Jonathon Gray, Buddug Williams, Rachel Iredale, Liz France

 


    Acknowledgment
 
The Acknowledgement is included in the full-text version of this article, available online at www.JCO.org. It is not included in the PDF (via Adobe® Acrobat Reader®) version.

We thank all of the men who took part in the Men’s Attitudes Towards Cancer and Health project. Clinical expertise was provided by Peter Barrett-Lee consultant oncologist at Velindre Hospital in Cardiff, UK. The National Cancer Research Network was extremely helpful in aiding study recruitment, and Stephen Wilshere provided invaluable lay representation. Thanks also to Christine Atwell, Julia Hafner, and June Williams for their administrative support, and to Bethan Henderson and Daphne Russell for reading earlier drafts of this article.


    NOTES
 
Supported by Grant No. J1196B40A from the Breast Cancer Campaign (B.W.) and Grants No. J1196W24L from Wellcome Trust and RCUF014 Cancer Research UK (K.B.). R.I., E.F., and J.G. are funded by Tenovus, the cancer charity.

Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Authors’ Disclosures of...
 Author Contributions
 REFERENCES
 
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Submitted October 20, 2004; accepted October 17, 2005.


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