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Prospective Changes in Quality of Life After Ductal Carcinoma-in-Situ: Results From the Nurses' Health Study

Larissa Nekhlyudov, Candyce H. Kroenke, Inkyung Jung, Michelle D. Holmes, Graham A. Colditz

From the Department of Ambulatory Care and Prevention, Harvard Medical School/Harvard Pilgrim Health Care; Department of Epidemiology, Harvard School of Public Health; and the Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA

Address reprint requests to Larissa Nekhlyudov, MD, MPH, Department of Ambulatory Care and Prevention, Harvard Medical School/Harvard Pilgrim Health Care, 133 Brookline Avenue, 6th Floor, Boston, MA 02215; e-mail: larissa_nekhlyudov{at}harvardpilgrim.org

	ABSTRACT

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

 
PURPOSE: The incidence of ductal carcinoma-in-situ (DCIS) of the breast has been increasing. However, uncertainties exist about its prognosis, optimal treatment, and effect on women's health-related quality-of-life (HRQoL). Our study assessed the prospective changes in HRQoL in women diagnosed with DCIS.

PATIENTS AND METHODS: Between 1992 and 2000, HRQoL was assessed at three 4-year intervals among women enrolled in two Nurses' Health Study cohorts using the Medical Outcomes Survey Short-Form 36 health survey. Using mixed effects and logistic regression modeling, we compared the prospective changes in HRQoL scores among women with and without DCIS.

RESULTS: The study included 114,728 women; 510 were diagnosed with DCIS during the study period. During 4 years, women with DCIS had small, but statistically significantly greater declines in the domains of role limitations due to physical problems (–6.74; SE, 1.69), vitality (–2.06; SE, 0.78), and social functioning (–2.40; SE, 0.93) than women without DCIS. Among those with DCIS, clinically significant declines were more often observed within 6 months of the diagnosis in the domains of social functioning (odds ratio, 1.78; 95% CI, 1.03 to 3.07) and mental health (odds ratio, 2.03; 95% CI, 1.09 to 3.79) than after 6 months after diagnosis.

CONCLUSION: Women with DCIS experienced small long-term declines in HRQoL, although these declines did not seem to be clinically important. Short-term clinically significant declines in the psychosocial domains were noted. In counseling women with DCIS, clinicians should provide reassurance but prepare them to deal with the short-term sequelae.

	INTRODUCTION

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More than 58,000 cases of ductal carcinoma-in-situ (DCIS), a localized precursor to invasive breast cancer, were diagnosed in the United States in 2005, accounting for more than 25% of all breast cancer diagnoses.¹ The recent increase in the incidence of DCIS has been significant and has mostly been attributed to the growing use of screening mammography.^2,3 Women diagnosed with DCIS face an uncertain prognosis, questions regarding appropriate treatment,⁴ possible physical and psychological consequences of surgery (often mastectomy),⁵ and an exaggerated fear of recurrence.^6-8 Consequently, DCIS may have untoward effects on women's health-related quality-of-life (HRQoL).

As noted in a recent Institute of Medicine report, the literature addressing HRQoL after DCIS is limited.⁹ Our review revealed two qualitative^7,10 and four quantitative studies^8,11-13 that suggested variable effects of DCIS on HRQoL. However, the studies were limited due to a lack of a comparison group,^8,11 a lack of an adjustment for preillness physical and psychological function,^8,11 use of nonstandardized measures of HRQoL,¹¹ and relatively small sample sizes.^12,13 To our knowledge, the only prospective study on HRQoL after DCIS was conducted within the original cohort of the Nurses' Health Study (NHS).¹³ This study focused on 599 women diagnosed with invasive breast cancer during 1992 to 1996 and included 160 women with in situ cancers. The small number of women with DCIS restricted the ability to draw conclusions from this study.

We therefore conducted this study to prospectively measure changes in HRQoL in a large sample of women enrolled in two NHS cohorts. We included 510 women who were diagnosed with DCIS from 1992 to 2000 and a comparison group of women who remained free of the disease. We explored short-term and long-term effects of DCIS on HRQoL for both groups.

	PATIENTS AND METHODS

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Study Design
The study was conducted within two NHS cohorts. The original NHS cohort was established in 1976 and enrolled 121,700 female registered nurses age 30 to 55. The NHS2 cohort was established in 1989 and included 116,671 female registered nurses age 25 to 42. Since enrollment, women in both cohorts have completed biannual surveys (with a follow-up rate of more than 90%), providing information on a variety of health risk factors, the occurrence of major illnesses, and social history.¹⁴ To assess HRQoL, the Medical Outcomes Study Short-Form 36 Health Survey (SF-36) has been administered to both cohorts every 4 years beginning in 1992 (1992, 1996, and 2000 for NHS) and in 1993 (1993, 1997, and 2001 for NHS2). Breast cancer–specific information was collected via a supplemental survey and medical record review. For the purposes of this analysis, we combined the results of the surveys obtained in the two NHS cohorts in 1992 and 1993 (referred to as 1992), 1996 and 1997 (referred to as 1996), and 2000 and 2001 (referred to as 2000).

Study Sample
In 1992, 162,691 women responded to the SF-36 survey (75,453 in NHS and 87,238 in NHS2); 165,784 responded to the survey in 1996 (83,569 in NHS and 82,215 in NHS2) and 168,230 responded to the survey in 2000 (82,468 in NHS and 85,762 in NHS2). Between 1992 and 2000, 1,023 women were diagnosed with DCIS (419 between 1992 and 1996; 604 between 1996 and 2000). For this analysis, we excluded 269 women with DCIS who did not complete the pre-DCIS surveys immediately before being diagnosed and therefore lacked a preillness assessment of HRQoL. We also excluded women with DCIS, invasive breast cancer, or other cancer except nonmelanoma skin cancer (n = 185) before the initial survey. We also excluded women whose DCIS diagnosis indicated the presence of lobular and/or invasive characteristics (n = 5). Two women diagnosed during 1996 to 2000 who did not respond to the main NHS survey and had missing information on key patient characteristics were excluded. To avoid bias due to misclassification, we excluded women who reported receiving chemotherapy, which is not a standard treatment option for women with DCIS (n = 17). Four women died before completing the follow-up (post-DCIS) functional assessment and were also excluded. Out of 541 eligible women who completed the pre-DCIS survey, 510 (94%) completed the post-DCIS surveys and are included in this analysis. A total of 114,218 women in the two cohorts who remained free of all cancers except nonmelanoma skin cancer and who completed all three HRQoL assessments in 1992, 1996, and 2000 were included as a comparison group.

HRQoL Assessment
We measured HRQoL using SF-36, a self-administered, 36-item questionnaire that measures HRQoL in eight domains including physical functioning, role limitations due to physical problems, role limitations due to emotional problems, vitality, bodily pain, social functioning, mental health, and general health perceptions.¹⁵ Each individual domain is scored from 0 (lowest level of functioning) to 100 (highest level). Declines of 5 to 26 points, depending on the domain, differentiate between patients with minor medical conditions such as controlled hypertension and those with serious conditions such as congestive heart failure.¹⁶ The instrument has been validated extensively.^15,17,18 In our study, we did not analyze the general health perceptions domain, which was incompletely assessed in the initial 1992 questionnaire.

Statistical Analyses
First, we used descriptive statistics to determine the pre-DCIS characteristics (as reported in the 1992 survey) of women who were later diagnosed with DCIS and those who remained free of DCIS. The characteristics included age, body mass index, activity level, smoking, alcohol use, family history of breast cancer, and comorbid conditions. These were categorized as listed in Table 1 and were adjusted for age (normalized to age 60). We chose this age to provide the reader with a clear reference point for interpreting the results: a 60-year-old postmenopausal woman. For women with DCIS, we assessed the types of treatment received, including lumpectomy, mastectomy, radiation, and hormone therapy (mostly tamoxifen).

Third, to assess for short-term declines in HRQoL, we measured the 4-year difference in the scores among women diagnosed with DCIS. Based on earlier NHS study findings,¹³ we defined short term as 6 months from the time of DCIS diagnosis. In this analysis, we focused on clinically significant declines, defined as 10 points, based on the earlier NHS study and previously established norms.^13,16 We used logistic regression modeling to adjust for confounders, including women's characteristics, diagnosis period, surgery, tamoxifen, and radiation therapy. As a reference, we also calculated the age-adjusted (normalized to age 60) rates of clinically significant declines among women without DCIS.

	RESULTS

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Study Population
The analysis included 114,728 women who completed the HRQoL surveys between 1992 and 2000. Of those, 510 were diagnosed with DCIS between 1992 and 2000 (204 women between 1992 and 1996; 306 between 1996 and 2000). Women diagnosed in 1992 to 1996 were observed for a mean of 1.8 years (standard deviation [SD], 1.1 years; range, 0 to 4.3 years) from the time of their diagnosis until the QoL assessment in 1996, and 5.9 years (SD, 1.1 years; range, 3.9 to 8.7 years) until the QoL assessment in 2000. Those diagnosed in 1996 to 2000 were observed for a mean of 1.8 years (SD, 1.2 years; range, 0 to 4.3 years) until the QoL assessment in 2000.

As noted in Table 1, women with DCIS were older (mean, 52.4 years; SD, 10.5 years) compared with those who remained free of DCIS (mean, 47.8 years; SD, 11.5 years). After adjusting for age, women who developed DCIS had similar prediagnosis characteristics as those who remained free of DCIS, with the exception of family history of breast cancer (18.2% for those with DCIS and 11.3% for those without). Among those with DCIS, 278 (54%) had lumpectomy, 194 (38%) had mastectomy, and 38 (8%) had unknown surgical treatment; 210 (41%) had radiation and 172 (34%) had tamoxifen therapy. With the exception of being older at diagnosis (as expected in an aging cohort), the baseline characteristics of the women diagnosed during 1996 to 2000 were similar to those diagnosed during 1992 to 1996. The rates of mastectomy and radiation were similar, although tamoxifen use was lower among those diagnosed during 1992 to 1996 than 1996 to 2000 (15% v 46%).

Prospective Changes in HRQoL
Figure 1 represents the HRQoL scores obtained at three time points: 1992, 1996, and 2000. In most domains, the scores and the prospective changes were similar for women diagnosed with DCIS and those without DCIS. In the role limitations due to physical problems, there was a prospective decline of –4.08 points (SE, 2.67) among those diagnosed with DCIS during 1992 to 1996 and a decline of –1.38 points (SE, 0.11) for those without DCIS; a mean difference of –2.70 (SE, 2.67). Among those diagnosed with DCIS during 1996 to 2000, the prospective decline was greater (–10.49; SE, 2.17) than among those without DCIS (–1.05; SE, 0.11); the mean difference of –9.44 (SE, 2.17) was statistically significant (P < .0001). For bodily pain and vitality, the mean difference among those with and without DCIS was less pronounced in both time periods but was statistically significant for women diagnosed during 1996 to 2000 (–2.42; SE, 1.16 and –2.49; SE, 1.01, respectively). When we combined the prospective changes in the scores in the two periods (Table 2), we found that women with DCIS had statistically significantly greater declines in HRQoL than those experienced by women without DCIS in the domains of role limitations due to physical problems (mean difference, –6.32 points; SE, 1.71), vitality (mean difference, –1.93; SE, 0.79), and social function (mean difference, –2.46; SE 0.94). However, these differences did not seem to be clinically significant.

View larger version (15K): [in this window] [in a new window]   Fig 1. Multivariable adjusted quality-of-life scores among women with and without ductal carcinoma-in-situ (DCIS). Scores adjusted for age, body mass index, activity, comorbidity, menopausal status, postmenopausal hormone use, smoking, alcohol, family history of breast cancer, and marital status. Bold lines indicate time periods during which DCIS was diagnosed. Statistically significant differences between the 1996 and 2000 scores among women with and without DCIS. P < .0001 and P < .05, respectively. SF-36, Medical Outcomes Study Short-Form 36 Health Survey.

Among women with DCIS, short-term clinically important declines (at least 10 points) were more common among women diagnosed within 6 months of the follow-up survey than among those diagnosed more than 6 months before the survey (Table 3), particularly in the domains of role limitations due to physical problems (42.7% v 30.0%), social function (30.5% v 21.1%), and mental health (21.1% v 10.5%). In multivariable analyses, we found that compared with women who were diagnosed more than 6 months before the survey, women more recently diagnosed were more likely have clinically significant short-term declines in the domains of social functioning (odds ratio, 1.78; 95% CI, 1.03 to 3.07) and mental health (odds ratio, 2.03; 95% CI, 1.09 to 3.79). We found no association with treatment in these domains. In comparison, among those who remained free of DCIS, the age-adjusted percentages of women who experienced at least a 10-point decline in these the two clinically significant domains during the 4-year period was 20% for social functioning and 12% for mental health.

	DISCUSSION

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Our findings add substantial new information regarding HRQoL among women with DCIS. In the prior NHS analysis, Michael et al¹³ measured HRQoL among 160 women with in situ cancers. Our study included substantially more women with DCIS, a wider age range, more recent functional assessment scores, and a longer follow-up period. Our findings that DCIS does not lead to untoward effects on HRQoL are consistent with the prior analysis, although we did not replicate the earlier finding that suggested a greater decline in vitality among women with DCIS. Our findings are also consistent with other studies of HRQoL among women with DCIS. Amichetti et al¹¹ found that women surveyed approximately 5 years after diagnosis had good overall HRQoL, although about half reported feeling tense, nervous, lonely, and anxious. Bluman et al⁸ reported that although women surveyed within 2 years of diagnosis were concerned about their risk of recurrences, few were depressed or psychologically distressed. In neither study was there a comparison group or an adjustment for preillness status.

Literature in the area of HRQoL among women with invasive breast cancer is more extensive and has shown that women experience psychosocial morbidity after diagnosis,^19-21 but regain their physical and psychological functioning by 1 year after surgery and remain highly functional thereafter.^22-24 However, among women with invasive breast cancer, prospective data from the NHS found declines in long-term function,¹³ particularly for women age 40 and younger.²⁵ Although this is in contrast to our results, it is possible that HRQoL outcomes among women with DCIS and invasive breast cancer may not be comparable, particularly at long-term follow-up. Whereas women with DCIS and invasive cancer face similar short-term treatment options, women with invasive breast cancer are more likely to experience the potentially lasting effects of chemotherapy²⁴ and axillary dissection,²⁶ as well as the greater chance of recurrence, metastases, and death as a result of breast cancer. Therefore, it is likely that the most important ramifications of short-term HRQoL would be related to mental rather than physical health. Interestingly, our short-term results suggested no association with treatment; however, our analysis was restricted by a relatively small number of women diagnosed within 6 months of the follow-up HRQoL assessment.

It is not clear why the women diagnosed more recently experienced a clinically and statistically greater significant decline in role limitations due to physical problems than those diagnosed during the earlier years. With the exception of being older at diagnosis (as expected in an aging cohort), women diagnosed in the later time period had similar baseline characteristics as those diagnosed during the earlier period. Although tamoxifen use was higher among women diagnosed in the later time period, we did not find an association between tamoxifen use and HRQoL scores. Whether other secular trends or women's changing expectations for physical functioning and/or a greater need to retain physical function after the diagnosis might explain these findings is unclear.

There are several strengths of our study. It is the largest study to date to assess the effect of DCIS diagnosis on women's HRQoL. Our data are prospective and took into account preillness function (previously noted to be an important predictor of postdiagnosis morbidity).²⁰ We included a comparison group with similar baseline characteristics and functional scores. We used a validated outcome measure that has been standardized in the general population and for which clinically significant effect sizes have been defined.¹⁶ We assessed short- and long-term HRQoL and explored for trends over time. Finally, the NHS cohort is stable, and has validated cancer diagnoses and extensive data on potential confounding factors.

Our study has some limitations. First, the SF-36 instrument was designed to measure HRQoL among patients with chronic diseases and may not be sensitive enough to capture subtle declines among women with DCIS. As a generic measure, it also does not capture the possible cancer-related sequelae such as sexual function and body image. Cancer- and/or breast cancer–specific measures, such as Cancer Rehabilitation Evaluation System, Functional Assessment of Cancer Therapy–Breast, European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire C30, and others,^21,27-31 may be more suitable. However, the use of these scales does not allow for a comparison of preillness to postillness changes in QoL and a comparison with healthy controls. Our results based on the SF-36 are supported by a previously reported good correlation between this measure and the pertinent subscales of the Cancer Rehabilitation Evaluation System instrument.³² Additional study of HRQoL after DICS using the breast cancer–specific instruments may be of value, although instruments specific to DCIS may need to be developed. Another possible limitation is that the findings from the NHS cohort may not be generalizable to other populations. Given that the participants are mostly white, educated, and due to their training, may be more proficient at navigating the health care system, they may be less likely to suffer from functional declines after DCIS diagnosis. Finally, the original NHS cohort did not collect information on cancer recurrences, thus including women with recurrences may have biased our results. However, given that the rate of DCIS recurrence is relatively low,⁴ it is likely that only a few women would have had a recurrence during this time period.

In conclusion, we found that although women with DCIS experienced short-term declines in the psychosocial domains of HRQoL, there seemed to be no clinically significant long-term functional status declines in the domains measured. In counseling women with DCIS, clinicians should provide reassurance but prepare women to deal with the short-term sequelae.

	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: Larissa Nekhlyudov, Candyce H. Kroenke, Inkyung Jung, Michelle D. Holmes, Graham A. Colditz Financial support: Graham A. Colditz Administrative support: Graham A. Colditz Provision of study materials or patients: Graham A. Colditz Collection and assembly of data: Michelle D. Holmes, Graham A. Colditz Data analysis and interpretation: Larissa Nekhlyudov, Candyce H. Kroenke, Inkyung Jung, Michelle D. Holmes, Graham A. Colditz Manuscript writing: Larissa Nekhlyudov, Candyce H. Kroenke, Graham A. Colditz Final approval of manuscript: Larissa Nekhlyudov, Candyce H. Kroenke, Inkyung Jung, Michelle D. Holmes, Graham A. Colditz

 

	ACKNOWLEDGMENTS

 
We thank Caroline Niu for completing the programming needs for this study and Suzanne Fletcher, MD, MSc, for providing input on earlier drafts of this manuscript.

	NOTES

 
Supported by the National Cancer Institute Grant No. RO1-CA87969 to the Nurses' Health Study; in part by an American Cancer Society Clinical Research Professorship (G.A.C.); and by the Institutional Training Grant in the Epidemiology and Prevention of Breast Cancer (Grant No. DAMD17-00-1-0165), Department of Defense, US Army Medical Research and Material Command (L.N.).

Presented in part at the national meeting of the Society of General Internal Medicine, Chicago, IL, May 13, 2004.

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

	REFERENCES

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Submitted October 19, 2005; accepted April 4, 2006.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Nekhlyudov, L. Articles by Colditz, G. A. Search for Related Content PubMed PubMed Citation Articles by Nekhlyudov, L. Articles by Colditz, G. A. Social Bookmarking                            What's this?