Journal of the National Cancer Institute Advance Access published online on February 12, 2008
JNCI Journal of the National Cancer Institute, doi:10.1093/jnci/djn010
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ARTICLES |
Risk Perceptions and Psychosocial Outcomes of Women With Ductal Carcinoma In Situ: Longitudinal Results From a Cohort Study
Affiliations of authors: Dana-Farber Cancer Institute, Brigham and Women's Hospital, Harvard Medical School, Boston, MA (AP, KA, EB, CK, MG, JL, JSdM, JW, KE, EW); Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, NC (ECD)
Correspondence to: Ann Partridge, MD, MPH, Dana-Farber Cancer Institute, Brigham and Women's Hospital, Harvard Medical School, 44 Binney St, Boston, MA 02115 (e-mail: ahpartridge{at}partners.org).
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ABSTRACT |
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Background: Ductal carcinoma in situ (DCIS) has a generally favorable overall prognosis, with a systemic recurrence rate of approximately 1%, a local recurrence rate after mastectomy of 1%, and a local recurrence rate after breast-conserving treatment of less than 10%. Preliminary studies have suggested that women with DCIS may overestimate their risk of disease recurrence. Few data exist regarding psychosocial outcomes for women with DCIS.
Methods: Women in Eastern Massachusetts with newly diagnosed DCIS were asked to participate in a longitudinal study of risk perceptions, psychosocial concerns, and health behaviors. Psychosocial outcomes after DCIS diagnosis and risk perceptions were evaluated at enrollment and at 9 and 18 months. All statistical tests were two-sided.
Results: Four hundred eighty-seven women with DCIS (64% of eligible participants) completed the enrollment survey. Overall quality of life was good among the women surveyed, and the substantial anxiety at enrollment decreased with time (P < .001). At enrollment, 54% perceived at least a moderate risk for DCIS recurrence in the next 5 years, 68% in their lifetime; 39% perceived at least a moderate risk for invasive cancer in the next 5 years, 53% in their lifetime; and 28% perceived at least a moderate likelihood of DCIS spreading to other places in their body. At 18 months after enrollment, perceived risks had not statistically significantly changed from those at enrollment (P = .38). Anxiety at enrollment was the factor that was most consistently and strongly associated with overestimation of future breast cancer–related risks (perceived moderate or greater risk vs less than moderate risk of DCIS recurring within 5 years: odds ratio [OR] = 4.0, 95% confidence interval [CI] = 1.6 to 9.9, P = .003; of invasive breast cancer within 5 years: OR = 4.3, 95% CI = 1.9 to 9.9, P < .001; and of invasive breast cancer during lifetime: OR = 5.3, 95% CI = 2.0 to 14.3, P < .001).
Conclusions: Many women with newly diagnosed DCIS have inaccurate perceptions of the breast cancer risks that they face, and anxiety is particularly associated with these inaccurate perceptions.
Prior knowledge Although women with ductal carcinoma in situ (DCIS) have good prognosis overall, studies have suggested that they overestimate their risks of DCIS recurrence and invasive breast cancer. Study design Quality of life, including risk perceptions and anxiety, of DCIS patients who underwent treatment was measured within 6 months of their diagnosis and again 9 months and 18 months later. Contribution Most women in the study overestimated their risks of DCIS recurrence and invasive breast cancer. Anxiety was consistently associated with these overestimated risk perceptions. Implication Future studies should investigate the impact of anxiety and overestimated perceptions of breast cancer risks on the treatment decisions of women with DCIS and test ways to reduce their anxiety and inaccurate risk perceptions. Limitations Nonresponder bias and the low proportion of older women in the study should be considered. Adjustment for multiple comparisons was not made, and because overestimation of risk was common in the study population the values of the odds ratios should not be taken as precise estimates of relative perceived risk.
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The incidence of ductal carcinoma in situ (DCIS) is increasing among American women. Until approximately 20 years ago, DCIS represented only a small percentage of all diagnosed breast cancers (1,2). The increasing use of screening mammography has had a substantial impact on the increasing frequency with which DCIS is diagnosed (3–5). According to data provided by the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute, the incidence of DCIS increased dramatically from 1983 to 1996 (6). Among women younger than 50 years, incidence increased 131% among white women and 190% among black women. Among white and black women aged 50 years and older, the increases observed were 275% and 313%, respectively (5). In 2006, nearly 62000 cases of DCIS were diagnosed in the United States, representing more than 20% of all breast cancer diagnoses (7).
DCIS is a complex clinical entity that is highly variable in its appearance, biology, and behavior (4,8). Age at diagnosis, extent of disease, pathologic subtype (comedo vs noncomedo, high grade vs low grade), and treatment all influence risk of recurrence (8). These factors, as well as patient preferences and physician recommendations, influence decisions about treatment options that include mastectomy, breast-conserving surgery with or without adjuvant radiation therapy, and adjuvant tamoxifen therapy. In the complex treatment decision-making process, it is often possible to lose sight of the fact that DCIS poses limited risks to a woman's overall mortality. Recent studies (9–11) have demonstrated the risk of systemic recurrence of breast cancer after a diagnosis of DCIS to be less than 1%, and associated breast cancer–specific mortality for women with DCIS is estimated to be 1% in long-term follow-up. Rates of local recurrence (either DCIS or invasive breast cancer) vary somewhat with treatment received and population studied. Rates of local recurrence after mastectomy are approximately 1% (11). Among women in a large placebo-controlled randomized trial of adjuvant tamoxifen therapy after breast-conserving surgery and radiation therapy for DCIS (10), 6% of women receiving placebo and 4% of women taking tamoxifen developed recurrent DCIS after 5 years. Rates of invasive breast cancer recurrence were 7% in the placebo group and 4% in the tamoxifen group. Thus, rates of breast cancer recurrence after conventional therapy for DCIS are generally low.
Small cross-sectional studies have suggested that women with DCIS may overestimate their risks of future breast cancer events (12–14). Inaccurate risk perceptions may have an effect on decision making, psychosocial outcomes, and subsequent health behaviors. The main objective of this study was to examine changes in risk perception and anxiety over time, our hypothesis being that DCIS-related depression and anxiety will decrease with time after diagnosis. Thus, we sought to identify a cohort of women newly diagnosed with DCIS and to evaluate risk perceptions and psychosocial outcomes at study enrollment and over the course of the ensuing 18 months.
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Subjects and Methods |
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Subjects
Consecutive women with newly diagnosed (
6 months) DCIS were identified from systematic review of pathology reports at participating regional hospitals in Eastern Massachusetts, including both academic centers and community-based hospitals, using the Rapid Case Registry of Dana-Farber/Harvard Cancer Center. After a woman with newly diagnosed DCIS was identified, her physician was contacted to obtain permission to invite her to participate in the study. Eligible women were then invited by mail to participate in this prospective cohort survey study. Patients who gave written informed consent were mailed surveys at enrollment, at 9 months, and at 18 months. Survey responses were collected by telephone interviews. The study received Institutional Review Board approval through each participating hospital.
Women were eligible for participation if they had a diagnosis of DCIS (without evidence of invasion, including microinvasion) and had either not yet completed surgical treatment or had undergone surgical treatment within 3 months before enrollment. Informed consent and an ability to understand written and spoken English or Spanish to the extent necessary to complete the questionnaires were required for participation. Women were excluded if they had a previous diagnosis of an invasive breast cancer.
Measures
The enrollment and follow-up surveys included items on sociodemographic characteristics, treatment for DCIS, risk perceptions, and quality of life. Depression and anxiety were assessed with the 14-item Hospitalized Anxiety and Depression Scale (HADS), with scores of 11 or greater on the HADS anxiety and depression subscales considered indicative of substantial anxiety or depression, respectively, based on the validation of this measure (15). DCIS-related intrusive or avoidant thoughts were assessed with the 15-item Revised Impact of Event Scale (RIES), with women being asked to relate the answers to their diagnosis of DCIS; scores of 12 or greater on the RIES were considered to be indicative of substantial intrusive or avoidant thoughts based on validation studies of this measure (16–18). The 36-item short form of the Rand Medical Outcomes Study (MOS-SF36) was used to measure physical functioning, role limitations due to personal or emotional problems, bodily pain, general health perceptions, vitality, social functioning, emotional well-being, and perceived changes in health (19–21). Because one item regarding social functioning was omitted unintentionally from the 18-month MOS-SF36 survey, we were not able to calculate mental component subscale (MCS), physical component subscale (PCS), and social functioning subscale scores at this time point. A cut point of 50 was chosen for the MCS and PCS scores because this is the cutoff commonly used in the literature and was the mean score in a large population-based sample (22). Women were also asked during the enrollment interview to recall their physical and psychosocial health in the month before their diagnosis of DCIS using the MOS-SF36. The 20-item Medical Outcomes Study Social Support Survey (MOS-SS) was used to assess social support (22,23). Perceived risk of future breast cancer events (rated as 1 = very unlikely, 2 = unlikely, 3 = moderately likely, 4 = likely, and 5 = very likely) and perceived absolute risk (0%–100%) were assessed using items adapted from Lerman and Croyle (24) that had not been previously validated. These 20 items regarding perceived risk included 1) In your opinion, how likely is it that you will develop DCIS again within the next 5 years compared with other women your age? 2) In your opinion, how likely is it that you will develop DCIS again within your lifetime? 3) In your opinion, how likely is it that you will develop invasive breast cancer within the next 5 years compared with other women your age? 4) In your opinion, how likely is it that you will develop invasive breast cancer within your lifetime? 5) In your opinion, how likely is it that your DCIS will spread to other places in your body? Participants were also asked to estimate their perceived absolute risk of four of those five future breast cancer events (the perceived absolute risk of DCIS spreading item was unintentionally not included in the surveys). DCIS pathology was abstracted from medical records, and DCIS-directed therapy was obtained from the patient survey.
Statistical Analysis
Descriptive statistics were used to characterize the population. To assess the change in HADS depression, HADS anxiety, and RIES scores over time (enrollment, 9 months, and 18 months), we used a random effects model with a random intercept, which allowed the evaluation of scores over time while accounting for the correlation of scores within an individual. The analysis was done using PROC MIXED in SAS, and P values for change over time were based on F tests of the fixed effect of time. Mean differences and their 95% confidence intervals (CIs) between time points were estimated using contrasts within the random effects model in PROC MIXED. To compare outcomes measured at only two time points (ie, HADS at enrollment and at 18 months), we used two-sided paired t tests. McNemar's test was used to evaluate changes in levels of depression and anxiety and changes in risk perception. Pearson correlation coefficients (r) were calculated to assess the correlation between psychosocial variables. Logistic regression modeling using stepwise selection was used to evaluate factors associated with self-reported recurrence risk of "moderate" and greater. Candidate variables in the stepwise selection were as follows: age (65 vs >65), race (white vs other), education (less than college vs at least college), marital status (married or living as married vs other), employment status (employed full time vs other), financial status (money for special things vs other), comorbidity, HADS anxiety score at enrollment (<11 vs 
11), HADS depression score at enrollment (<11 vs 11), physician communication (good, very good, excellent vs poor, fair), RIES score at enrollment (<12 vs 12), satisfaction with treatment (satisfied vs other), physician primary in care (surgeon vs radiation oncologist or other vs medical oncologist), recalled MCS score at enrollment (<50 vs 50), recalled PCS score at enrollment (<50 vs 50), MCS score at enrollment (<50 vs 50), PCS score at enrollment (<50 vs 50), consultation with a medical oncologist (yes vs no), grade of DCIS (3,4,5 vs 1,2 vs unknown), presence of comedo necrosis (yes vs no), mastectomy performed (yes vs no), radiation received (yes vs no). Treatment variables included in candidate variables represented treatments received before enrollment. Analyses were done using SAS version 8.2 (SAS Institute Inc., Cary, NC). All statistical tests were two-sided, and P values less than .05 were considered statistically significant.
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Results |
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Study Population
Eight hundred sixteen women with newly diagnosed DCIS were identified in Eastern Massachusetts between October 15, 2000, and May 3, 2004 (Fig. 1). Forty-six women identified were ineligible because they did not read or speak English or Spanish or were found to have microinvasive or invasive breast cancer; six patients could not be contacted. Of the remaining 764 eligible patients, 487 (64%) enrolled and responded to the enrollment questionnaire. The mean [SD] time from diagnosis until study registration was 5.5 [2.0] months. Two hundred five women declined to participate when contacted ("active declines"), and 72 women did not respond in spite of repeated attempts to contact them. Four hundred twenty-six women (87% of those enrolled) completed the 9-month questionnaire, and 392 women (80% of those enrolled) completed the 18-month questionnaire. Participants were enrolled through eight participating institutions, with each institution contributing a range of 4–204 participants. No statistical difference in enrollment by site was observed, but women who enrolled in the study were younger on average at diagnosis than women who did not (mean [SD] age of enrolled women vs that of women who were identified but did not enroll, 53.9 [10.9] years vs 57.4 [12.5] years; P < .001). Examining the participant characteristics and psychosocial measures collected at baseline between the 374 patients who completed all follow-up questionnaires and the 113 who did not complete at least one follow-up questionnaire, the only statistically significant difference was in the patient's financial status (73% vs 61%, respectively, said they "had money for special things"; P = .01).
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Participant Characteristics
Participant and disease characteristics were collected at enrollment (Table 1). Thirty-four percent of study subjects reported that they underwent mastectomy, and 50% of respondents received radiation therapy. Forty-three percent reported that they took tamoxifen. When women were asked to select the type of physician who was most influential in their care, 83% selected a surgeon, 10% a medical oncologist, 5% a radiation oncologist, and 2% another subspecialist. Ninety-seven percent of respondents indicated that their perception of communication with their most influential physician was good, very good, or excellent. Eighty-eight percent of patients indicated that they were satisfied with the care they received for their DCIS. Seventy-seven percent of participants reported having seen a medical oncologist during their care. Women reported a high degree of social support at enrollment, with a median MOS Social Support Scale Score of 92.1 (range = 13.2–100.0).
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Psychosocial Outcomes
At enrollment, 10% of women reported substantial anxiety and 2% reported depression by the HADS (Table 2). Anxiety decreased over time, and levels of depression remained low throughout the study period (Table 2). McNemar's test comparing the proportion of patients with anxiety at enrollment with those at 18 months suggested that fewer women were anxious over time (P = .06). The difference in mean HADS anxiety scores between baseline and 18 months using mixed modeling was highly statistically significant (estimated mean difference between baseline and 18 months = –0.46, 95% CI = –0.79 to –0.14; P = .006). McNemar's test comparing the proportion of patients with depression scores at enrollment and 18 months did not reveal any statistically significant changes in the proportion of women reporting substantial depressive symptoms over time. The mean HADS depression scores, however, did change statistically significantly over time between enrollment and 18 months, with an estimated mean decrease of –0.29 (95% CI = –0.54 to –0.03). When women were asked to consider their DCIS when answering RIES questions, the mean overall RIES score was 15.9 at enrollment, indicative of a substantial degree of DCIS-related intrusive or avoidant thoughts (Table 2). Individual RIES scores at enrollment ranged from 0 to 58. RIES scores decreased over time: the estimated mean decrease in RIES between enrollment and 18 months using a mixed model revealed a statistically significant improvement (mean = –5.9, 95% CI = –7.1 to –4.7; P < .001). The avoidance and intrusion subscales also revealed statistically significant improvements over time using the mixed model.
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When participants were queried at enrollment, they recalled generally favorable physical and mental functioning in the month before diagnosis, with a mean score of 54.6 on the MOS-SF36 PCS and 52.6 on the MCS (Table 3). PCS and MCS scores at enrollment were only slightly lower than those before diagnosis, and women continued to report relatively favorable quality of life overall at 18 months when compared with normal population scores (25). However, notable declines were seen in the general health, vitality, and mental health subscales, which dipped below normal population scores for similarly average-aged women at 18 months for the vitality and mental health subscales (comparative population normal scores by age not shown).
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Risk Perceptions
Women were queried about their perceived future breast cancer risks both at enrollment and at follow-up (Tables 4 and 5). At enrollment, 54% of women believed that they had at least a moderate likelihood of developing DCIS again in the next 5 years, and 68% believed that they had at least a moderate likelihood of developing DCIS again in their lifetime. Thirty-nine percent of women believed that there was at least a moderate likelihood of developing invasive breast cancer in the next 5 years, and 53% believed that there was at least a moderate likelihood of developing it in their lifetime. Finally, 28% of respondents believed there was at least a moderate likelihood of DCIS spreading to other places in their body. At 18 months, mean perceived risk had not changed substantially (P = .38). Women were also asked to provide a numeric estimate of their absolute risk ("perceived absolute risk") of four specific future breast cancer events. Although the ranges of perceived absolute risks were wide, a choice of "very unlikely" or "unlikely" was associated with a median perceived absolute risk of 3%–5%; a choice of "moderate" was associated with a median absolute risk of 25%–30%, and a choice of "likely" or "very likely" was associated with a median absolute risk of 60%–70%.
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To determine which factors were associated with the overestimated perceived risk of DCIS spreading to other parts of the body, we compared the 28% of participants who perceived at least a moderate likelihood of DCIS spreading to other parts of the body with the remaining 72% of participants (this analysis was restricted to the 345 women with complete data). A logistic regression model revealed that substantial DCIS-related intrusive or avoidant thoughts at enrollment (ie, RIES scores
12) were associated with the belief that DCIS would spread to other body parts (odds ratio [OR] = 3.1, 95% CI = 1.9 to 5.1, P < .001) (Table 6). Non–statistically significant covariates included age, race, education, marital status, employment, financial status, comorbidity, anxiety by HADS, depression, medical oncology care/consultation, and satisfaction with treatment, treatment received including mastectomy or not, grade of DCIS, and presence of comedo necrosis. We also conducted logistic regression models using the same variables to evaluate factors associated with higher risk perceptions at enrollment of other potential future breast cancer events (Table 6). Anxiety as measured by the HADS (ie, score 11) was the variable that was most consistently and strongly associated with heightened risk perceptions (perceived DCIS recurring within 5 years: OR = 4.0, 95% CI = 1.6 to 9.9, P = .003; invasive breast cancer within 5 years: OR = 4.3, 95% CI = 1.9 to 9.9, P < .001; and invasive breast cancer during lifetime: OR = 5.3, 95% CI = 2.0 to 14.3, P < .001; Table 6). HADS, RIES, and MCS scores were highly correlated with one another (anxiety with depression, r = 0.64; anxiety with RIES, r = 0.54; anxiety with MCS, r = –0.53; depression with RIES, r = 0.42; depression with MCS, r = –0.52; RIES with MCS, r = –0.36; all P < .001), and different psychosocial outcomes were statistically significant in the different models.
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Discussion |
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TopAbstractContext and CaveatsSubjects and MethodsResultsDiscussionFundingReferencesNotes |
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In this study, we found that a substantial proportion of patients diagnosed with DCIS harbor grossly inaccurate perceptions of their risks of recurrent DCIS or invasive breast cancer, including the development of metastatic disease. Perceptions of increased risk of recurrence, including ipsilateral recurrence, did not seem to be diminished in women who underwent a mastectomy, despite the fact that mastectomy substantially decreases the risk of local recurrence after DCIS. Strikingly, more than 25% of the women in our study believed that they had a moderate or greater chance of DCIS spreading to other places in their bodies despite the fact that metastatic breast cancer actually occurs following a diagnosis of DCIS less than 1% of the time (9–11). Previous research has revealed that women in general vastly overestimate their risk of developing breast cancer (26–28). Moreover, once diagnosed with breast cancer, they tend to overestimate their risk of recurrence (12,29). Although decision making about treatment is complex, there is little doubt that women will be limited in their ability to participate in informed decision making if they harbor gross misperceptions about the health risks they face.
Our study expands on previous studies of risk perceptions in women with DCIS. The large size of this study and longitudinal nature of the cohort allowed us to evaluate several outcomes over time among many women. In previous smaller cross-sectional studies (12–14), women with DCIS have been found to have knowledge deficits about DCIS and to have similar risk perceptions and levels of distress as women with early invasive breast cancer. Our study reveals that these inaccurate risk perceptions do not appear to change over time and demonstrates the strong relationship between distress and inaccurate risk perceptions.
Prior qualitative studies provide insight into the heightened risk perceptions among women with DCIS. In a study of 26 women with a history of DCIS, De Morgan et al. (30) found that some women were confused about the diagnosis, that is, whether DCIS truly was cancer, and about whether or not they were at risk of death from DCIS. In another qualitative study, Webb and Koch (31) revealed that women with DCIS had limited knowledge about their disease and treatment options and were confused about their prognosis. This lack of knowledge, confusion, and potential ambiguity regarding the disease may contribute to inaccurate risk perceptions.
Recent evidence (32–34) also shows that there are disparate patterns of care for women with DCIS, with rates of mastectomy, radiation therapy, and axillary lymph node sampling varying substantially by factors that include surgeon practice pattern, hospital volume, and geographic region. Inaccurate risk perceptions among women with DCIS may result from physician discomfort about the diagnosis, poor or inadequate communication of risks to patients, or an inability of patients to understand the risks (30,35).
The finding that psychosocial distress was the factor most strongly and consistently associated with inaccurate risk perceptions in the present study is not surprising. What is uncertain, however, is whether inaccurate risk perceptions lead to increased distress or if higher levels of distress lead to inaccurate risk perceptions. In a randomized study of the effect of individualized risk counseling vs general health counseling in women at risk for breast cancer, Lerman et al. (36) found that in both groups, two-thirds of women continued to substantially overestimate their lifetime breast cancer risks following counseling. Importantly, risk counseling did not improve comprehension in the large proportion of women who had high levels of anxiety at baseline.
The complexity of breast cancer treatment decisions is likely compounded by the anxiety that a woman may experience following a diagnosis of breast cancer. Several previous studies (37–52) have found that anxiety and fear of cancer recurrence are major issues for many breast cancer survivors. Therefore, efforts to provide more accurate risk information are not likely to be effective unless these patients’ breast cancer anxieties are also addressed. Because women with DCIS may be labeled as having precancer, they may receive less psychosocial support from individual health-care providers and the health-care system as a whole than women who are diagnosed with invasive breast cancer (30).
This longitudinal evaluation of women with DCIS provides insight into the risk perceptions and psychosocial outcomes of women with DCIS. The use of pathology review at multiple centers to identify women with newly diagnosed DCIS minimized selection bias and enhances the generalizability of our findings. However, nonresponder bias should be considered in interpreting the results. In particular, older women may not be well represented in this study as evidenced by our analysis of enrollment by age. It is also possible that some women did not understand the questions that we were asking regarding risk perception. The finding that perceived absolute risks among patients tracked in a predictable manner with qualitative assessments adds validity to our findings. Because the measures of psychologic distress were correlated in our population, we cannot identify one scale over another to preferentially measure distress that predicts inaccurate risk perception. However, our models consistently indicate that psychologic distress (measured in different ways) is associated with inaccurate risk perception. In addition, the finding that psychosocial distress was so consistently associated with inaccurate perceptions of each risk evaluated implies that the results from our models are not spurious, although such a possibility is a concern when using stepwise regression methods, and suggests that women did understand the questions and consistently overestimate the risks they face. However, it must be noted that adjustments for multiple comparisons were not made in this study and the odds ratios presented should not be used to make numeric relative comparisons between groups, considering that the referent group was less than 50% of the study population and thus odds ratios are likely to be much larger than relative risks in this case (53).
In conclusion, a substantial proportion of women with DCIS overestimate the future breast cancer risks they face. Although women with DCIS appear to experience a reasonably favorable overall quality of life, some DCIS survivors may suffer from increased distress and poor mental health that may be related to inaccurate, increased perceptions of breast cancer risks. Clinicians who are caring for the increasing number of women who are diagnosed with DCIS should be aware of these inaccurate perceptions and attempt to minimize them. Interventions to improve risk perceptions and the associated anxiety surrounding a diagnosis of DCIS will likely require a multifaceted approach, including improving clinician knowledge and understanding of DCIS, improving communication of risks to patients, and intervening to treat baseline anxiety and anxiety associated with a diagnosis of DCIS. Future research should assess the impact of altered risk perceptions on treatment decision making among women with DCIS and test interventions to ameliorate anxiety and inaccurate risk perceptions in this growing population of cancer survivors.
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Funding |
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Dana-Farber/Harvard Cancer Center Specialized Program of Research Excellence in Breast Cancer (5 P50 CA89393-03).
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NOTES |
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A. Partridge, K. Adloff, E. Blood, and E. Winer had full access to all of the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis.
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Manuscript received July 6, 2007; revised November 30, 2007; accepted January 9, 2008.
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J Natl Cancer Inst 2008 100: 228-229.
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