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Quality-of-Life Issues in Patients With Ductal Carcinoma In Situ

Quality-of-Life Issues in Patients With Ductal Carcinoma In Situ Abstract Ductal carcinoma in situ (DCIS) as we know it today is a clinical entity that is primarily discovered through the finding of microscopic calcifications on a screening mammogram. Asymptomatic women who are found to have DCIS receive treatments that are similar to women with invasive breast cancer and experience substantial psychological distress in spite of having an excellent prognosis and normal life expectancy. More research is needed to determine the best way to communicate with women about this condition and to match the extent of treatment with the risk of serious future disease. Clinical and research efforts should focus on reducing the anxiety and psychological distress associated with the diagnosis of DCIS. Thirty years ago, ductal carcinoma in situ (DCIS) was a rarely diagnosed entity, usually identified in a slowly growing palpable breast mass. The increasing use of mammography in the 1980s transformed this clinically diagnosed entity into one that is most frequently found as occult disease on a screening mammogram, often in an unsuspecting asymptomatic woman. Over the course of the past three decades, we have come to realize that DCIS lies along the spectrum of intraductal neoplasia of the breast, ranging from atypical ductal hyperplasia to invasive breast cancer (1). Moving back the age of mammographic screening to women in their 40s has played a large role in early detection of noninvasive disease and precipitating the rapid rise in the incidence of DCIS in this younger group of women (2). It is not unusual to see the entire spectrum of intraductal neoplasia identified in a single pathological specimen obtained from a woman who is found to have new microcalcifications on a screening mammogram. Indeed, some women who have their first screening mammogram in the fourth or fifth decade of life are confronted with a diagnosis of DCIS. What are the human costs of over diagnosis of a condition that is not malignant? What are the psychosocial and quality-of-life (QOL) implications for this common new disease entity, largely diagnosed at the time of mammographic screening? What do we know about the impact of a DCIS diagnosis on women’s lives and what type of research must we conduct in the future? What research questions about the outcomes of DCIS diagnosis and treatment need to be addressed? For women given a diagnosis of DCIS, there are many costs. They include time away from family, work, and social activities; the costs of treatment, both covered by insurance and out of pocket; the toxicity, which now includes rising rates of contralateral prophylactic mastectomy, intensive surveillance and biopsies, as well as changes in body image; and the interpersonal and existential challenges of living with the history of a condition that is close to a cancer diagnosis, but is not, and does not go away just because of local treatment. Not all DCIS in the breast will progress to invasive cancer, but it is hard to know how to successfully communicate this to women, and our treatment recommendations are not risk stratified. There is a labeling effect associated with the diagnosis of DCIS, similar to being labeled with the risk for cardiovascular disease as a result of hypertension or hypercholesterolemia. Fortunately, in the latter case, lifestyle strategies and medications will reduce the risk for mortality from a serious cardiovascular event. In contrast, being given a diagnosis of DCIS labels a woman as being at risk for invasive breast cancer. Although the mortality risk from DCIS is low, it is still treated just like breast cancer (surgery, radiation, endocrine therapy) and it is often confusing for patients to understand how it is different. Describing the continuum of cancer development is difficult for many physicians to explain (3), and women given this diagnosis are sometimes puzzled about why DCIS is treated just like invasive cancer if in fact it is not cancer (4). There is also a generalized fear of breast cancer in our society, and women who submit to mammographic screening are often stunned when an abnormality is detected. It is not surprising then, that a diagnosis of DCIS leads to increased anxiety and misperceptions about risk for cancer, and even death, among these women. Despite the large number of women diagnosed with DCIS each year, and the rapid increase in incidence in the past two decades, relatively little is known about the psychosocial impact of this diagnosis. Early reports in the late 1990s and early 21st century were often personal accounts or small qualitative studies that noted women's confusion and dissatisfaction with the treatment and prognostic information that they received (5,6). In addition, women were often confused about why, if DCIS is a noninvasive cancer, they needed mastectomy (standard of care for DCIS before trials of breast-conserving therapy was evaluated) when women with invasive cancer were receiving breast conservation therapy. Misinformation about risk of distant recurrence was common, although psychological distress with standard assessment measures was low (see Table 1). Table 1 Studies of psychosocial and quality-of-life outcomes in patients with ductal carcinoma in situ (DCIS)* First Author (year) (reference)  Patient characteristics  Measures  Outcomes  Comments  Amichetti (1999) (7)  DCIS (n = 83); 6 Italian institutions  Local questionnaire  “Good quality of life”; some anxiety and tension; good body image  All breast conservation; 54.5 mo since diagnosis  Bluman (2001) (6)  DCIS (n = 76); recruited from Duke tumor registry  Knowledge; satisfaction; perceived risk; CES-D; R-IES  Misperception of risk of recurrence; low depressive symptoms  1.9 y since diagnosis; 68% mastectomy  Rakovitch (2003) (8)  DCIS (n = 64); T1, T2, N0 (n = 164); tertiary Canadian center; consecutive patients; 1998–1999  Describe diagnosis; risk of recurrence; symptom assessment  DCIS more accurate at description; no significant difference in risk perception; similar rate of psychological distress  All treated with partial mastectomy; assessed within 4 mo of diagnosis  Casso (2004) (9)  Stage 0 (n = 28); stages I–IV (n = 188); Group Health Seattle, WA  SF-36; CARES-SF; CES-D  DCIS sample better on all measures  40–49 y at diagnosis; 5- to 10-y survivors, all stages  Janz (2005) (10)  Stage 0 (n = 555); stage I (n = 462); stage II (n = 239); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Physical and role function better in stage 0 (DCIS) (univariate); no difference in QOL by stage in multivariate model  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Nekhlyudov (2006) (11)  DCIS (n = 510); women without cancer (n = 114 728); Nurses’ Health Study, prospective cohort  SF-36  Small but statistically significantly greater declines in role—physical, vitality, and social functioning; social functioning and mental health most affected in first 6 mo after diagnosis  Clinical significance uncertain  van Gestel (2007) (12)  DCIS (n = 33); stage I (n = 91); recruited from tumor registry  SF-36; perceived disease impact; risk of recurrence  DCIS-slightly better scores on pain and mental health; similar perceived disease impact; no difference in risk perceptions  Mastectomy more common in DCIS; 2–3 y postdiagnosis  Janz (2007) (13)  Stage 0 (n = 598); stage I (n = 482); stage II (n = 253); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Fatigue, pain, treatment side effects, breast symptoms, arm symptoms did not differ; only sleep disturbance greater problem for invasive  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Partridge (2008) (14)  DCIS (n = 487); inception cohort followed for more than 18 mo  Risk perceptions; SF-36; HADS; R-IES  10% anxiety; 2% depression; SF-36 scores normal range; inaccurate perceptions of recurrence risk; anxiety predicts misperceptions  Enrolled within 3 mo of diagnosis; mastectomy in 34%  Lauzier (2010) (15)  DCIS (n = 107); invasive (n = 693); inception cohort in Quebec followed for more than 1 y  Psychiatric symptom index; SF-12 mental and physical scales  Similar psychiatric and mental distress for DCIS and invasive; better physical health for DCIS  Population-based cohort; recruited shortly after diagnosis  First Author (year) (reference)  Patient characteristics  Measures  Outcomes  Comments  Amichetti (1999) (7)  DCIS (n = 83); 6 Italian institutions  Local questionnaire  “Good quality of life”; some anxiety and tension; good body image  All breast conservation; 54.5 mo since diagnosis  Bluman (2001) (6)  DCIS (n = 76); recruited from Duke tumor registry  Knowledge; satisfaction; perceived risk; CES-D; R-IES  Misperception of risk of recurrence; low depressive symptoms  1.9 y since diagnosis; 68% mastectomy  Rakovitch (2003) (8)  DCIS (n = 64); T1, T2, N0 (n = 164); tertiary Canadian center; consecutive patients; 1998–1999  Describe diagnosis; risk of recurrence; symptom assessment  DCIS more accurate at description; no significant difference in risk perception; similar rate of psychological distress  All treated with partial mastectomy; assessed within 4 mo of diagnosis  Casso (2004) (9)  Stage 0 (n = 28); stages I–IV (n = 188); Group Health Seattle, WA  SF-36; CARES-SF; CES-D  DCIS sample better on all measures  40–49 y at diagnosis; 5- to 10-y survivors, all stages  Janz (2005) (10)  Stage 0 (n = 555); stage I (n = 462); stage II (n = 239); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Physical and role function better in stage 0 (DCIS) (univariate); no difference in QOL by stage in multivariate model  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Nekhlyudov (2006) (11)  DCIS (n = 510); women without cancer (n = 114 728); Nurses’ Health Study, prospective cohort  SF-36  Small but statistically significantly greater declines in role—physical, vitality, and social functioning; social functioning and mental health most affected in first 6 mo after diagnosis  Clinical significance uncertain  van Gestel (2007) (12)  DCIS (n = 33); stage I (n = 91); recruited from tumor registry  SF-36; perceived disease impact; risk of recurrence  DCIS-slightly better scores on pain and mental health; similar perceived disease impact; no difference in risk perceptions  Mastectomy more common in DCIS; 2–3 y postdiagnosis  Janz (2007) (13)  Stage 0 (n = 598); stage I (n = 482); stage II (n = 253); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Fatigue, pain, treatment side effects, breast symptoms, arm symptoms did not differ; only sleep disturbance greater problem for invasive  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Partridge (2008) (14)  DCIS (n = 487); inception cohort followed for more than 18 mo  Risk perceptions; SF-36; HADS; R-IES  10% anxiety; 2% depression; SF-36 scores normal range; inaccurate perceptions of recurrence risk; anxiety predicts misperceptions  Enrolled within 3 mo of diagnosis; mastectomy in 34%  Lauzier (2010) (15)  DCIS (n = 107); invasive (n = 693); inception cohort in Quebec followed for more than 1 y  Psychiatric symptom index; SF-12 mental and physical scales  Similar psychiatric and mental distress for DCIS and invasive; better physical health for DCIS  Population-based cohort; recruited shortly after diagnosis  * CARES-SF = Cancer Rehabilitation Evaluation System–Short Form; CES-D = Center for Epidemiologic Studies Depression (scale); EORTC QLQ = European Organization for Research and Treatment of Cancer Quality-of-Life Questionnaire; HADS = Hospital Anxiety and Depression Scale; R-IES = Revised Impact of Events Scale; SEER = Surveillance, Epidemiology, and End Results; SF-36 = Medical Outcomes Study 36-Item Short-Form Health Survey (Health Institute; New England Medical Center; Boston, MA). View Large In a recent study of an inception cohort of DCIS patients diagnosed between 2000 and 2004, Partridge et al. (14) found that about 10% of patients had substantial anxiety shortly after diagnosis, without significant depression, using the Hospital Anxiety and Depression Scale, which has clinical cut points for these symptoms. However, the women with DCIS had normal scores on a standardized measure of physical and emotional functioning measured with the Medical Outcomes Study 36-Item Short-Form Health Survey. However, these women demonstrated severe misperceptions about their risk of invasive disease and spread of the DCIS to other parts of their body. Over an 18-month follow-up period, there was little change in these inaccurate risk perceptions and there was a strong relationship between distress (anxiety and intrusive thoughts) and the misperceptions. These authors note that the heterogeneity of DCIS (ie, small/minimal low-risk lesions vs very large and/or high-grade tumors), along with the variability in treatment plans (ie, extent of surgery, use of radiation or endocrine therapy), exacerbates the confusion and misinformation that women experience. From this work and earlier publications, the literature supports the need for development of more effective communication tools for patients with DCIS, focusing on the nature of the disease and its risk for dissemination and for individualized treatment options and prognosis. There are several other studies that have used standardized measures of psychological distress and QOL to compare women with DCIS with women with invasive breast cancer. Most are cross-sectional, with assessments occurring several years after diagnosis, and usually compare women with DCIS to women with invasive breast cancer rather than healthy women (see Table 1). In a very recent publication, Lauzier et al. (15) examined psychological distress and physical health in the year after diagnosis of DCIS or invasive breast cancer as part of an inception cohort of patients treated in eight Quebec hospitals in 2003. Although physical functioning was better among the women with DCIS than those with invasive disease receiving chemotherapy, there was no significant difference in psychological distress between women with DCIS and invasive disease that had a worse prognosis (15). As noted earlier, DCIS development lies on the continuum from atypical ductal hyperplasia to invasive breast cancer, and as such, it may be more relevant to compare the psychosocial and QOL impact of a DCIS diagnosis with the health status of women who are either at high risk for breast cancer based on a preneoplastic biopsy or other risk factors using the Gail Risk Model or with healthy women at usual risk for breast cancer. To address this question, we have examined baseline pretreatment QOL data available from the National Surgical Adjuvant Breast and Bowel Project (NSABP) Study of Tamoxifen and Raloxifene (STAR) Trial and unpublished data from the NSABP B-35 trial (a comparison of adjuvant tamoxifen vs anastrozole in postmenopausal women with DCIS) to determine whether or not there are QOL differences between these two groups of women, who are both at high risk for invasive breast cancer. The women entered in these two trials were all postmenopausal and completed the same self-report QOL questionnaires before starting endocrine therapy. Women in the STAR trial had to have either lobular carcinoma in situ or a calculated 5-year Gail risk score of 1.67% or greater (16,17). Patients in the B-35 trial were required to have lumpectomy as treatment for their DCIS and were scheduled to have whole-breast irradiation (although it is possible, radiotherapy may have been initiated in some patients). They completed their QOL questionnaires at an average of 43 days after surgery at the time of randomization. Data are available from 1869 women who were in the STAR QOL study and 1275 who were enrolled in the B-35 QOL trial and are shown in Table 2. Table 2 Comparison of quality-of-life mean scores for Study of Tamoxifen and Raloxifene (STAR) and B-35 participants* Scale  STAR  B-35  P  SF-12 Physical†  49.3  47.1  <.0001  SF-12 Mental†  53.5  50.7  <.0001  MOS Vitality‡  65  58  <.0001  Symptom checklist summary score§  12.7  14.5  <.0001  Scale  STAR  B-35  P  SF-12 Physical†  49.3  47.1  <.0001  SF-12 Mental†  53.5  50.7  <.0001  MOS Vitality‡  65  58  <.0001  Symptom checklist summary score§  12.7  14.5  <.0001  * MOS = Medical Outcomes Study. † MOS SF-12 component summary scores; 50 represents the population mean and each 10 points represents a SD change in score. ‡ MOS Vitality scale measures energy and fatigue; a higher score represents greater energy. § A 20-item symptom checklist was used, and this represents a summary score for the total number of items and their severity; a higher score indicates more symptoms and/or greater severity. View Large The women in the STAR trial were slightly younger (mean age = 58 vs 61 years, P < .0001) with significantly fewer nonwhite participants (7% vs 12%, P < .0001). Women with DCIS who participated in B-35 reported worse physical and mental function, less energy, and more severe symptoms than healthy high-risk women who participated in STAR. The major difference in type of symptom reported was musculoskeletal aches and pains (data not shown), most likely reflecting the impact of recent breast cancer surgery for this group. Depressive symptoms were also more common among the B-35 participants, as well as significantly greater severity of problems with all aspects of sexual functioning on the MOS Sexual Functioning Scale (all Ps < .0001). As the prospective results of the B-35 trial become available, we will be able to track the longitudinal impact of adjuvant endocrine therapy in this DCIS patient population over time and compare them to the participants in the STAR trial. One of the greatest challenges facing clinicians and patients is the heterogeneity of DCIS histologically and prognostically. Is a one size fits all strategy still warranted today? Can we stratify risk and modify treatments? Can we find a better way to communicate risk to our patients with DCIS? DCIS as we know it today was created by the widespread introduction of screening mammography whose role was to detect invasive cancer rather than DCIS. For quite some time, there have been calls for more research on DCIS. In the 1998 report from the Breast Cancer Progress Review Group (18), it was noted, “These women will have near normal survival but may experience short- and long-term morbidity from treatment. DCIS is seriously understudied from a disease- and patient-focused outcomes perspective,” with a specific outcomes research recommendation to explore new mechanisms for studying patient outcomes in DCIS. Figure 1 identifies some of the most compelling QOL concerns related to DCIS. Figure 1 View largeDownload slide Ductal carcinoma in situ (DCIS) quality-of-life questions. Figure 1 View largeDownload slide Ductal carcinoma in situ (DCIS) quality-of-life questions. In the recent Institute of Medicine Report on Initial National Priorities for Comparative Effectiveness Research, DCIS ranked in the first quartile of research topics (19). Recent publications suggest that there is a risk for over diagnosis of breast cancer using screening mammography before the age of 50 years (20–22) and that there is a possibility that many low-grade DCIS lesions might not progress after women become postmenopausal. The low event rate after a diagnosis of DCIS makes it unlikely that randomized clinical trials can be done to answer some of the important questions identified in Figure 2. Figure 2 View largeDownload slide Ductal carcinoma in situ (DCIS) outcomes questions. Figure 2 View largeDownload slide Ductal carcinoma in situ (DCIS) outcomes questions. In conclusion, DCIS is a very heterogeneous condition, and it is clear that there has been insufficient attention to the study of the impact of this diagnosis on women's lives and their perceptions of future cancer risk. The UK Breast Cancer Campaign performed a gap analysis that emphasized many of the deficiencies in our knowledge of the psychosocial aspects of breast cancer (23). DCIS is particularly challenging in this regard, as it lies on the continuum between precancerous changes in the breast and invasive cancer. Women who have a small focus of DCIS in a specimen that is largely made up of atypical ductal hyperplasia are entirely different from women whose entire breast is replaced by extensive high-grade DCIS. From the limited literature available, we know that women have serious misperceptions about what DCIS is and its risk for recurrence. There is an important need to provide accurate and useful information for women about the risks and benefits of various treatments for DCIS, as well the likely QOL and health outcomes associated with various treatments. From the scant literature available, women with a DCIS diagnosis appear more distressed than women who are at high risk for breast cancer and have psychological distress that may be similar to women with a diagnosis of invasive cancer. More research is necessary, specifically comparing women with DCIS with women without a cancer diagnosis to facilitate communication about the added burden of various treatments (eg, surgery, radiation, endocrine therapy)—especially their physical and psychosocial risks and benefits. Such information is needed to facilitate better-informed treatment decisions between health-care professionals and their patients. In addition, misperceptions about DCIS and risk of recurrence may influence adherence to preventive interventions and behaviors, as well as needed continued surveillance with screening mammography (24). Funding P.A.G. was supported in part by an American Cancer Society Clinical Research Professorship. References 1. Burstein HJ,  Polyak K,  Wong JS,  Lester SC,  Kaelin CM.  Ductal carcinoma in situ of the breast,  N Engl J Med ,  2004, vol.  350  14(pg.  1430- 1441) Google Scholar CrossRef Search ADS PubMed  2. Ernster VL,  Ballard-Barbash R,  Barlow WE, et al.  Detection of ductal carcinoma in situ in women undergoing screening mammography,  J Natl Cancer Inst ,  2002, vol.  94  20(pg.  1546- 1554) Google Scholar CrossRef Search ADS PubMed  3. Partridge A,  Winer JP,  Golshan M, et al.  Perceptions and management approaches of physicians who care for women with ductal carcinoma in situ,  Clin Breast Cancer ,  2008, vol.  8  3(pg.  275- 280) Google Scholar CrossRef Search ADS PubMed  4. Veronesi U,  Zurrida S,  Goldhirsch A,  Rotmensz N,  Viale G.  Breast cancer classification: time for a change,  J Clin Oncol ,  2009, vol.  27  15(pg.  2427- 2428) Google Scholar CrossRef Search ADS PubMed  5. De Morgan S,  Redman S,  White KJ,  Cakir B,  Boyages J.  ‘Well, have I got cancer or haven’t I?’ The psycho-social issues for women diagnosed with ductal carcinoma in situ,  Health Expect ,  2002, vol.  5  4(pg.  310- 318) Google Scholar CrossRef Search ADS PubMed  6. Bluman LG,  Borstelmann NA,  Rimer BK,  Iglehart JD,  Winer EP.  Knowledge, satisfaction, and perceived cancer risk among women diagnosed with ductal carcinoma in situ,  J Womens Health Gend Based Med ,  2001, vol.  10  6(pg.  589- 598) Google Scholar CrossRef Search ADS PubMed  7. Amichetti M,  Caffo O,  Arcicasa M, et al.  Quality of life in patients with ductal carcinoma in situ of the breast treated with conservative surgery and postoperative irradiation,  Breast Cancer Res Treat ,  1999, vol.  54  2(pg.  109- 115) Google Scholar CrossRef Search ADS PubMed  8. Rakovitch E,  Franssen E,  Kim J, et al.  A comparison of risk perception and psychological morbidity in women with ductal carcinoma in situ and early invasive breast cancer,  Breast Cancer Res Treat ,  2003, vol.  77  3(pg.  285- 293) Google Scholar CrossRef Search ADS PubMed  9. Casso D,  Buist D,  Taplin S.  Quality of life of 5-10 year breast cancer survivors diagnosed between age 40 and 49,  Health Qual Life Outcomes ,  2004, vol.  2  1pg.  25  Google Scholar CrossRef Search ADS PubMed  10. Janz NK,  Mujahid M,  Lantz PM, et al.  Population-based study of the relationship of treatment and sociodemographics on quality of life for early stage breast cancer,  Qual Life Res. ,  2005, vol.  14  6(pg.  1467- 1479) Google Scholar CrossRef Search ADS PubMed  11. Nekhlyudov L,  Kroenke CH,  Jung I,  Holmes MD,  Colditz GA.  Prospective changes in quality of life after ductal carcinoma-in-situ: results from the Nurses’ Health Study,  J Clin Oncol ,  2006, vol.  24  18(pg.  2822- 2827) Google Scholar CrossRef Search ADS PubMed  12. van Gestel YRBM,  Voogd AC,  Vingerhoets AJJM, et al.  A comparison of quality of life, disease impact and risk perception in women with invasive breast cancer and ductal carcinoma in situ,  Eur J Cancer ,  2007, vol.  43  3(pg.  549- 556) Google Scholar CrossRef Search ADS PubMed  13. Janz NK,  Mujahid M,  Chung LK, et al.  Symptom experience and quality of life of women following breast cancer treatment,  J Womens Health ,  2007, vol.  16  9(pg.  1348- 1361) Google Scholar CrossRef Search ADS   14. Partridge A,  Adloff K,  Blood E, et al.  Risk perceptions and psychosocial outcomes of women with ductal carcinoma in situ: longitudinal results from a cohort study,  J Natl Cancer Inst ,  2008, vol.  100  4(pg.  243- 251) Google Scholar CrossRef Search ADS PubMed  15. Lauzier S,  Maunsell E,  Levesque P, et al.  Psychological distress and physical health in the year after diagnosis of DCIS or invasive breast cancer,  Breast Cancer Res Treat ,  2010, vol.  120  3(pg.  685- 691) Google Scholar CrossRef Search ADS PubMed  16. Vogel VG,  Costantino JP,  Wickerham DL, et al.  Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: The NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 Trial,  JAMA ,  2006, vol.  295  23(pg.  2727- 2741) Google Scholar CrossRef Search ADS PubMed  17. Land SR,  Wickerham DL,  Costantino JP, et al.  Patient-reported symptoms and quality of life during treatment with tamoxifen or raloxifene for breast cancer prevention: The NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 Trial,  JAMA ,  2006, vol.  295  23(pg.  2742- 2751) Google Scholar CrossRef Search ADS PubMed  18. Report of the Breast Cancer Progress Review Group,  Charting the Course: Priorities for Breast Cancer Research ,  1998 National Cancer Institute  http://planning.cancer.gov/library/1998breastcancer.pdf. Accessed August 17, 2010 19. Board of Health Care Services, Institute of Medicine,  Initial National Priorities for Comparative Effectiveness Research ,  2009 National Academies Press  http://www.iom.edu/en/Reports/2009/ComparativeEffectivenessResearchPriorities.aspx. Accessed December 20, 2009 20. Zahl PH,  Maehlen J,  Welch HG.  The natural history of invasive breast cancers detected by screening mammography,  Arch Intern Med ,  2008, vol.  168  21(pg.  2311- 2316) Google Scholar CrossRef Search ADS PubMed  21. Nelson HD,  Tyne K,  Naik A,  Bougatsos C,  Chan BK,  Humphrey L.  Screening for Breast Cancer: An Update for the U.S. Preventive Services Task Force,  Ann Intern Med ,  2009, vol.  151  10(pg.  727- 737) Google Scholar CrossRef Search ADS PubMed  22. Thaler RH.  Gauging the odds (and the costs) in health screening,  New York Times   December 19, 2009. http://www.nytimes.com/2009/12/20/business/20view.html?_r=1&scp=7&sq=Thaler&st=nyt. Accessed December 20, 2009 23. Thompson A,  Brennan K,  Cox A, et al.  Evaluation of the current knowledge limitations in breast cancer research: a gap analysis,  Breast Cancer Res. ,  2008, vol.  10  2pg.  R26  Google Scholar CrossRef Search ADS PubMed  24. Nekhlyudov L,  Habel LA,  Achacoso NS, et al.  Adherence to long-term surveillance mammography among women with ductal carcinoma in situ treated with breast-conserving surgery,  J Clin Oncol ,  2009, vol.  27  19(pg.  3211- 3216) Google Scholar CrossRef Search ADS PubMed  Notes The author thanks Reena Cecchini, MS, from the NSABP Biostatistical Center for conducting the analyses related to the NSABP B-35 trial baseline quality-of-life data. © The Author 2010. Published by Oxford University Press. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png JNCI Monographs Oxford University Press

Quality-of-Life Issues in Patients With Ductal Carcinoma In Situ

JNCI Monographs , Volume 2010 (41) – Oct 1, 2010

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Publisher
Oxford University Press
Copyright
© The Author 2010. Published by Oxford University Press.
ISSN
1052-6773
eISSN
1745-6614
DOI
10.1093/jncimonographs/lgq029
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20956834
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Abstract

Abstract Ductal carcinoma in situ (DCIS) as we know it today is a clinical entity that is primarily discovered through the finding of microscopic calcifications on a screening mammogram. Asymptomatic women who are found to have DCIS receive treatments that are similar to women with invasive breast cancer and experience substantial psychological distress in spite of having an excellent prognosis and normal life expectancy. More research is needed to determine the best way to communicate with women about this condition and to match the extent of treatment with the risk of serious future disease. Clinical and research efforts should focus on reducing the anxiety and psychological distress associated with the diagnosis of DCIS. Thirty years ago, ductal carcinoma in situ (DCIS) was a rarely diagnosed entity, usually identified in a slowly growing palpable breast mass. The increasing use of mammography in the 1980s transformed this clinically diagnosed entity into one that is most frequently found as occult disease on a screening mammogram, often in an unsuspecting asymptomatic woman. Over the course of the past three decades, we have come to realize that DCIS lies along the spectrum of intraductal neoplasia of the breast, ranging from atypical ductal hyperplasia to invasive breast cancer (1). Moving back the age of mammographic screening to women in their 40s has played a large role in early detection of noninvasive disease and precipitating the rapid rise in the incidence of DCIS in this younger group of women (2). It is not unusual to see the entire spectrum of intraductal neoplasia identified in a single pathological specimen obtained from a woman who is found to have new microcalcifications on a screening mammogram. Indeed, some women who have their first screening mammogram in the fourth or fifth decade of life are confronted with a diagnosis of DCIS. What are the human costs of over diagnosis of a condition that is not malignant? What are the psychosocial and quality-of-life (QOL) implications for this common new disease entity, largely diagnosed at the time of mammographic screening? What do we know about the impact of a DCIS diagnosis on women’s lives and what type of research must we conduct in the future? What research questions about the outcomes of DCIS diagnosis and treatment need to be addressed? For women given a diagnosis of DCIS, there are many costs. They include time away from family, work, and social activities; the costs of treatment, both covered by insurance and out of pocket; the toxicity, which now includes rising rates of contralateral prophylactic mastectomy, intensive surveillance and biopsies, as well as changes in body image; and the interpersonal and existential challenges of living with the history of a condition that is close to a cancer diagnosis, but is not, and does not go away just because of local treatment. Not all DCIS in the breast will progress to invasive cancer, but it is hard to know how to successfully communicate this to women, and our treatment recommendations are not risk stratified. There is a labeling effect associated with the diagnosis of DCIS, similar to being labeled with the risk for cardiovascular disease as a result of hypertension or hypercholesterolemia. Fortunately, in the latter case, lifestyle strategies and medications will reduce the risk for mortality from a serious cardiovascular event. In contrast, being given a diagnosis of DCIS labels a woman as being at risk for invasive breast cancer. Although the mortality risk from DCIS is low, it is still treated just like breast cancer (surgery, radiation, endocrine therapy) and it is often confusing for patients to understand how it is different. Describing the continuum of cancer development is difficult for many physicians to explain (3), and women given this diagnosis are sometimes puzzled about why DCIS is treated just like invasive cancer if in fact it is not cancer (4). There is also a generalized fear of breast cancer in our society, and women who submit to mammographic screening are often stunned when an abnormality is detected. It is not surprising then, that a diagnosis of DCIS leads to increased anxiety and misperceptions about risk for cancer, and even death, among these women. Despite the large number of women diagnosed with DCIS each year, and the rapid increase in incidence in the past two decades, relatively little is known about the psychosocial impact of this diagnosis. Early reports in the late 1990s and early 21st century were often personal accounts or small qualitative studies that noted women's confusion and dissatisfaction with the treatment and prognostic information that they received (5,6). In addition, women were often confused about why, if DCIS is a noninvasive cancer, they needed mastectomy (standard of care for DCIS before trials of breast-conserving therapy was evaluated) when women with invasive cancer were receiving breast conservation therapy. Misinformation about risk of distant recurrence was common, although psychological distress with standard assessment measures was low (see Table 1). Table 1 Studies of psychosocial and quality-of-life outcomes in patients with ductal carcinoma in situ (DCIS)* First Author (year) (reference)  Patient characteristics  Measures  Outcomes  Comments  Amichetti (1999) (7)  DCIS (n = 83); 6 Italian institutions  Local questionnaire  “Good quality of life”; some anxiety and tension; good body image  All breast conservation; 54.5 mo since diagnosis  Bluman (2001) (6)  DCIS (n = 76); recruited from Duke tumor registry  Knowledge; satisfaction; perceived risk; CES-D; R-IES  Misperception of risk of recurrence; low depressive symptoms  1.9 y since diagnosis; 68% mastectomy  Rakovitch (2003) (8)  DCIS (n = 64); T1, T2, N0 (n = 164); tertiary Canadian center; consecutive patients; 1998–1999  Describe diagnosis; risk of recurrence; symptom assessment  DCIS more accurate at description; no significant difference in risk perception; similar rate of psychological distress  All treated with partial mastectomy; assessed within 4 mo of diagnosis  Casso (2004) (9)  Stage 0 (n = 28); stages I–IV (n = 188); Group Health Seattle, WA  SF-36; CARES-SF; CES-D  DCIS sample better on all measures  40–49 y at diagnosis; 5- to 10-y survivors, all stages  Janz (2005) (10)  Stage 0 (n = 555); stage I (n = 462); stage II (n = 239); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Physical and role function better in stage 0 (DCIS) (univariate); no difference in QOL by stage in multivariate model  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Nekhlyudov (2006) (11)  DCIS (n = 510); women without cancer (n = 114 728); Nurses’ Health Study, prospective cohort  SF-36  Small but statistically significantly greater declines in role—physical, vitality, and social functioning; social functioning and mental health most affected in first 6 mo after diagnosis  Clinical significance uncertain  van Gestel (2007) (12)  DCIS (n = 33); stage I (n = 91); recruited from tumor registry  SF-36; perceived disease impact; risk of recurrence  DCIS-slightly better scores on pain and mental health; similar perceived disease impact; no difference in risk perceptions  Mastectomy more common in DCIS; 2–3 y postdiagnosis  Janz (2007) (13)  Stage 0 (n = 598); stage I (n = 482); stage II (n = 253); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Fatigue, pain, treatment side effects, breast symptoms, arm symptoms did not differ; only sleep disturbance greater problem for invasive  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Partridge (2008) (14)  DCIS (n = 487); inception cohort followed for more than 18 mo  Risk perceptions; SF-36; HADS; R-IES  10% anxiety; 2% depression; SF-36 scores normal range; inaccurate perceptions of recurrence risk; anxiety predicts misperceptions  Enrolled within 3 mo of diagnosis; mastectomy in 34%  Lauzier (2010) (15)  DCIS (n = 107); invasive (n = 693); inception cohort in Quebec followed for more than 1 y  Psychiatric symptom index; SF-12 mental and physical scales  Similar psychiatric and mental distress for DCIS and invasive; better physical health for DCIS  Population-based cohort; recruited shortly after diagnosis  First Author (year) (reference)  Patient characteristics  Measures  Outcomes  Comments  Amichetti (1999) (7)  DCIS (n = 83); 6 Italian institutions  Local questionnaire  “Good quality of life”; some anxiety and tension; good body image  All breast conservation; 54.5 mo since diagnosis  Bluman (2001) (6)  DCIS (n = 76); recruited from Duke tumor registry  Knowledge; satisfaction; perceived risk; CES-D; R-IES  Misperception of risk of recurrence; low depressive symptoms  1.9 y since diagnosis; 68% mastectomy  Rakovitch (2003) (8)  DCIS (n = 64); T1, T2, N0 (n = 164); tertiary Canadian center; consecutive patients; 1998–1999  Describe diagnosis; risk of recurrence; symptom assessment  DCIS more accurate at description; no significant difference in risk perception; similar rate of psychological distress  All treated with partial mastectomy; assessed within 4 mo of diagnosis  Casso (2004) (9)  Stage 0 (n = 28); stages I–IV (n = 188); Group Health Seattle, WA  SF-36; CARES-SF; CES-D  DCIS sample better on all measures  40–49 y at diagnosis; 5- to 10-y survivors, all stages  Janz (2005) (10)  Stage 0 (n = 555); stage I (n = 462); stage II (n = 239); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Physical and role function better in stage 0 (DCIS) (univariate); no difference in QOL by stage in multivariate model  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Nekhlyudov (2006) (11)  DCIS (n = 510); women without cancer (n = 114 728); Nurses’ Health Study, prospective cohort  SF-36  Small but statistically significantly greater declines in role—physical, vitality, and social functioning; social functioning and mental health most affected in first 6 mo after diagnosis  Clinical significance uncertain  van Gestel (2007) (12)  DCIS (n = 33); stage I (n = 91); recruited from tumor registry  SF-36; perceived disease impact; risk of recurrence  DCIS-slightly better scores on pain and mental health; similar perceived disease impact; no difference in risk perceptions  Mastectomy more common in DCIS; 2–3 y postdiagnosis  Janz (2007) (13)  Stage 0 (n = 598); stage I (n = 482); stage II (n = 253); Detroit and Los Angeles SEER Registry  EORTC QLQ-30; EORTC QLQ-BR23  Fatigue, pain, treatment side effects, breast symptoms, arm symptoms did not differ; only sleep disturbance greater problem for invasive  DCIS as the reference; interview completed mean 7.2 mo after diagnosis  Partridge (2008) (14)  DCIS (n = 487); inception cohort followed for more than 18 mo  Risk perceptions; SF-36; HADS; R-IES  10% anxiety; 2% depression; SF-36 scores normal range; inaccurate perceptions of recurrence risk; anxiety predicts misperceptions  Enrolled within 3 mo of diagnosis; mastectomy in 34%  Lauzier (2010) (15)  DCIS (n = 107); invasive (n = 693); inception cohort in Quebec followed for more than 1 y  Psychiatric symptom index; SF-12 mental and physical scales  Similar psychiatric and mental distress for DCIS and invasive; better physical health for DCIS  Population-based cohort; recruited shortly after diagnosis  * CARES-SF = Cancer Rehabilitation Evaluation System–Short Form; CES-D = Center for Epidemiologic Studies Depression (scale); EORTC QLQ = European Organization for Research and Treatment of Cancer Quality-of-Life Questionnaire; HADS = Hospital Anxiety and Depression Scale; R-IES = Revised Impact of Events Scale; SEER = Surveillance, Epidemiology, and End Results; SF-36 = Medical Outcomes Study 36-Item Short-Form Health Survey (Health Institute; New England Medical Center; Boston, MA). View Large In a recent study of an inception cohort of DCIS patients diagnosed between 2000 and 2004, Partridge et al. (14) found that about 10% of patients had substantial anxiety shortly after diagnosis, without significant depression, using the Hospital Anxiety and Depression Scale, which has clinical cut points for these symptoms. However, the women with DCIS had normal scores on a standardized measure of physical and emotional functioning measured with the Medical Outcomes Study 36-Item Short-Form Health Survey. However, these women demonstrated severe misperceptions about their risk of invasive disease and spread of the DCIS to other parts of their body. Over an 18-month follow-up period, there was little change in these inaccurate risk perceptions and there was a strong relationship between distress (anxiety and intrusive thoughts) and the misperceptions. These authors note that the heterogeneity of DCIS (ie, small/minimal low-risk lesions vs very large and/or high-grade tumors), along with the variability in treatment plans (ie, extent of surgery, use of radiation or endocrine therapy), exacerbates the confusion and misinformation that women experience. From this work and earlier publications, the literature supports the need for development of more effective communication tools for patients with DCIS, focusing on the nature of the disease and its risk for dissemination and for individualized treatment options and prognosis. There are several other studies that have used standardized measures of psychological distress and QOL to compare women with DCIS with women with invasive breast cancer. Most are cross-sectional, with assessments occurring several years after diagnosis, and usually compare women with DCIS to women with invasive breast cancer rather than healthy women (see Table 1). In a very recent publication, Lauzier et al. (15) examined psychological distress and physical health in the year after diagnosis of DCIS or invasive breast cancer as part of an inception cohort of patients treated in eight Quebec hospitals in 2003. Although physical functioning was better among the women with DCIS than those with invasive disease receiving chemotherapy, there was no significant difference in psychological distress between women with DCIS and invasive disease that had a worse prognosis (15). As noted earlier, DCIS development lies on the continuum from atypical ductal hyperplasia to invasive breast cancer, and as such, it may be more relevant to compare the psychosocial and QOL impact of a DCIS diagnosis with the health status of women who are either at high risk for breast cancer based on a preneoplastic biopsy or other risk factors using the Gail Risk Model or with healthy women at usual risk for breast cancer. To address this question, we have examined baseline pretreatment QOL data available from the National Surgical Adjuvant Breast and Bowel Project (NSABP) Study of Tamoxifen and Raloxifene (STAR) Trial and unpublished data from the NSABP B-35 trial (a comparison of adjuvant tamoxifen vs anastrozole in postmenopausal women with DCIS) to determine whether or not there are QOL differences between these two groups of women, who are both at high risk for invasive breast cancer. The women entered in these two trials were all postmenopausal and completed the same self-report QOL questionnaires before starting endocrine therapy. Women in the STAR trial had to have either lobular carcinoma in situ or a calculated 5-year Gail risk score of 1.67% or greater (16,17). Patients in the B-35 trial were required to have lumpectomy as treatment for their DCIS and were scheduled to have whole-breast irradiation (although it is possible, radiotherapy may have been initiated in some patients). They completed their QOL questionnaires at an average of 43 days after surgery at the time of randomization. Data are available from 1869 women who were in the STAR QOL study and 1275 who were enrolled in the B-35 QOL trial and are shown in Table 2. Table 2 Comparison of quality-of-life mean scores for Study of Tamoxifen and Raloxifene (STAR) and B-35 participants* Scale  STAR  B-35  P  SF-12 Physical†  49.3  47.1  <.0001  SF-12 Mental†  53.5  50.7  <.0001  MOS Vitality‡  65  58  <.0001  Symptom checklist summary score§  12.7  14.5  <.0001  Scale  STAR  B-35  P  SF-12 Physical†  49.3  47.1  <.0001  SF-12 Mental†  53.5  50.7  <.0001  MOS Vitality‡  65  58  <.0001  Symptom checklist summary score§  12.7  14.5  <.0001  * MOS = Medical Outcomes Study. † MOS SF-12 component summary scores; 50 represents the population mean and each 10 points represents a SD change in score. ‡ MOS Vitality scale measures energy and fatigue; a higher score represents greater energy. § A 20-item symptom checklist was used, and this represents a summary score for the total number of items and their severity; a higher score indicates more symptoms and/or greater severity. View Large The women in the STAR trial were slightly younger (mean age = 58 vs 61 years, P < .0001) with significantly fewer nonwhite participants (7% vs 12%, P < .0001). Women with DCIS who participated in B-35 reported worse physical and mental function, less energy, and more severe symptoms than healthy high-risk women who participated in STAR. The major difference in type of symptom reported was musculoskeletal aches and pains (data not shown), most likely reflecting the impact of recent breast cancer surgery for this group. Depressive symptoms were also more common among the B-35 participants, as well as significantly greater severity of problems with all aspects of sexual functioning on the MOS Sexual Functioning Scale (all Ps < .0001). As the prospective results of the B-35 trial become available, we will be able to track the longitudinal impact of adjuvant endocrine therapy in this DCIS patient population over time and compare them to the participants in the STAR trial. One of the greatest challenges facing clinicians and patients is the heterogeneity of DCIS histologically and prognostically. Is a one size fits all strategy still warranted today? Can we stratify risk and modify treatments? Can we find a better way to communicate risk to our patients with DCIS? DCIS as we know it today was created by the widespread introduction of screening mammography whose role was to detect invasive cancer rather than DCIS. For quite some time, there have been calls for more research on DCIS. In the 1998 report from the Breast Cancer Progress Review Group (18), it was noted, “These women will have near normal survival but may experience short- and long-term morbidity from treatment. DCIS is seriously understudied from a disease- and patient-focused outcomes perspective,” with a specific outcomes research recommendation to explore new mechanisms for studying patient outcomes in DCIS. Figure 1 identifies some of the most compelling QOL concerns related to DCIS. Figure 1 View largeDownload slide Ductal carcinoma in situ (DCIS) quality-of-life questions. Figure 1 View largeDownload slide Ductal carcinoma in situ (DCIS) quality-of-life questions. In the recent Institute of Medicine Report on Initial National Priorities for Comparative Effectiveness Research, DCIS ranked in the first quartile of research topics (19). Recent publications suggest that there is a risk for over diagnosis of breast cancer using screening mammography before the age of 50 years (20–22) and that there is a possibility that many low-grade DCIS lesions might not progress after women become postmenopausal. The low event rate after a diagnosis of DCIS makes it unlikely that randomized clinical trials can be done to answer some of the important questions identified in Figure 2. Figure 2 View largeDownload slide Ductal carcinoma in situ (DCIS) outcomes questions. Figure 2 View largeDownload slide Ductal carcinoma in situ (DCIS) outcomes questions. In conclusion, DCIS is a very heterogeneous condition, and it is clear that there has been insufficient attention to the study of the impact of this diagnosis on women's lives and their perceptions of future cancer risk. The UK Breast Cancer Campaign performed a gap analysis that emphasized many of the deficiencies in our knowledge of the psychosocial aspects of breast cancer (23). DCIS is particularly challenging in this regard, as it lies on the continuum between precancerous changes in the breast and invasive cancer. Women who have a small focus of DCIS in a specimen that is largely made up of atypical ductal hyperplasia are entirely different from women whose entire breast is replaced by extensive high-grade DCIS. From the limited literature available, we know that women have serious misperceptions about what DCIS is and its risk for recurrence. There is an important need to provide accurate and useful information for women about the risks and benefits of various treatments for DCIS, as well the likely QOL and health outcomes associated with various treatments. From the scant literature available, women with a DCIS diagnosis appear more distressed than women who are at high risk for breast cancer and have psychological distress that may be similar to women with a diagnosis of invasive cancer. More research is necessary, specifically comparing women with DCIS with women without a cancer diagnosis to facilitate communication about the added burden of various treatments (eg, surgery, radiation, endocrine therapy)—especially their physical and psychosocial risks and benefits. Such information is needed to facilitate better-informed treatment decisions between health-care professionals and their patients. In addition, misperceptions about DCIS and risk of recurrence may influence adherence to preventive interventions and behaviors, as well as needed continued surveillance with screening mammography (24). Funding P.A.G. was supported in part by an American Cancer Society Clinical Research Professorship. References 1. Burstein HJ,  Polyak K,  Wong JS,  Lester SC,  Kaelin CM.  Ductal carcinoma in situ of the breast,  N Engl J Med ,  2004, vol.  350  14(pg.  1430- 1441) Google Scholar CrossRef Search ADS PubMed  2. Ernster VL,  Ballard-Barbash R,  Barlow WE, et al.  Detection of ductal carcinoma in situ in women undergoing screening mammography,  J Natl Cancer Inst ,  2002, vol.  94  20(pg.  1546- 1554) Google Scholar CrossRef Search ADS PubMed  3. 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Nekhlyudov L,  Habel LA,  Achacoso NS, et al.  Adherence to long-term surveillance mammography among women with ductal carcinoma in situ treated with breast-conserving surgery,  J Clin Oncol ,  2009, vol.  27  19(pg.  3211- 3216) Google Scholar CrossRef Search ADS PubMed  Notes The author thanks Reena Cecchini, MS, from the NSABP Biostatistical Center for conducting the analyses related to the NSABP B-35 trial baseline quality-of-life data. © The Author 2010. Published by Oxford University Press.

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JNCI MonographsOxford University Press

Published: Oct 1, 2010

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