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© 2003 American Society for Clinical Oncology Breast Cancer in Younger Women: Reproductive and Late Health Effects of Treatment
From the University of California Los Angeles (UCLA) Schools of Medicine and Public Health; Division of Cancer Prevention & Control Research, Jonsson Comprehensive Cancer Center at UCLA; Division of Geriatrics, Department of Medicine, and Department of Psychiatry and Biobehavioral Medicine, David Geffen School of Medicine at UCLA; Cousins Center for Psychoneurimmunology, UCLA Neuropsychiatric Institute, Los Angeles, CA. Address reprint requests to Patricia A. Ganz, MD, Division of Cancer Prevention and Control Research, UCLA Jonsson Comprehensive Cancer Center, A2-125 CHS, Box 956900, Los Angeles, CA 90095-6900; e-mail: pganz{at}ucla.edu.
Purpose: In 1997, we initiated a cohort study to evaluate quality of life (QOL) and reproductive health outcomes in younger female breast cancer survivors. Materials and Methods: Using listings from two tumor registries, we recruited women with stage 0, I, or II breast cancer who were 50 years or younger at diagnosis and were also disease-free survivors for 2 to 10 years. A mailed survey questionnaire assessed medical and demographic factors, health-related QOL, mood, outlook on life, and reproductive health outcomes.
Results: We recruited 577 women, who ranged in age from 30 to 61.6 years (mean, 49.5 years) and were surveyed approximately 6 years after diagnosis. Almost three fourths had received some form of adjuvant therapy. Amenorrhea occurred frequently as a result of treatment in women Conclusion: Overall QOL in younger women who survive breast cancer is good, but there is evidence of increased emotional disruption, especially among the youngest women. Factors that may contribute to poorer health perceptions and QOL include experiencing a menopausal transition as part of therapy, and feeling more vulnerable after cancer.
BREAST CANCER is primarily a disease of older women; only approximately 25% of incident cases occur in women younger than 50 years.1 However, the population bulge in this age group has increased the absolute number of younger women diagnosed with breast cancer in recent years. During the last decade the mortality rate from breast cancer has steadily declined, with the greatest gains among younger women, largely resulting from more widespread application of adjuvant therapy.2 Thus, this expanding population of breast cancer survivors deserves our attention. The literature suggests that adaptation and quality of life (QOL) after breast cancer diagnosis is more difficult for younger women.3–6 On standardized measures of depression and QOL, younger women often show greater changes in mood and poorer emotional functioning than older women,7–9 and they appear to experience more difficulties and disruptions from the disease and its treatments because of child-rearing activities and employment outside the home.10 There are also important reproductive health effects of adjuvant therapy that specifically affect younger women (eg, infertility and early menopause).11,12 In 1997, we initiated the Cancer and Menopause Study (CAMS) to evaluate the QOL and health outcomes of younger female survivors of breast cancer, with a specific focus on the reproductive and late health effects of treatment. The study was conducted in two phases: first, a survey focused on QOL and health outcomes; second, an in-person visit evaluated biomedical outcomes, including anthropometric measurements, blood pressure, cardiovascular lipids, reproductive hormones, and measurement of bone mineral density and body composition. Additional substudies focused on cognitive functioning and longitudinal assessment of bone density. This report introduces the CAMS study cohort and presents the main findings from the survey phase. Future reports will elaborate on other findings from the survey, such as the relationship between menopausal status and symptoms, as well as the prevalence and predictors of fatigue and physical activity in this cohort.
Study Design The National Cancer Institute Office of Cancer Survivorship provided initial funding for this study, and as a result, the initial goals of the study were to examine the feasibility of recruiting long-term cancer survivors (5 to 10 years after diagnosis) from the cancer center’s tumor registry, and to describe the effects of breast cancer treatments on gonadal function in younger women. Additional funding from the Department of Defense Breast Cancer Research Program allowed expansion of the study to breast cancer survivors 2 to 5 years after diagnosis and inclusion of survivors from a community hospital. The overall goal of the study was to have a sufficiently large sample of younger breast cancer survivors with stage 0, I, and II disease to examine the relationship between specific treatments and reproductive health outcomes.
Recruitment Procedures Study invitation letters, written on the letterhead of a physician from the respective institutions, were mailed to all potentially eligible women along with a postage-paid response form to indicate interest in participating in the survey study. We excluded women who did not reside in the United States. For returned letters, attempts were made to update addresses through the hospital databases, and repeat mailings were performed. A second mailing was done at 2 weeks if there was no response; however, the research protocol was subsequently modified to allow a phone call to all nonrespondents. If the woman could not be reached after multiple attempts, she was classified as unreachable. Interested women were screened by telephone to confirm study eligibility (ability to read and understand English, being disease-free without a recurrence) and to describe the research in more detail. If eligible and interested in participation, the woman was mailed the study survey with a postage-paid return envelope, along with an informed consent form for signature. Systematic reminders (mail and phone) were used to ensure return of the surveys (details are provided in Pakilit et al13).
Instruments Demographic and breast cancer treatment information (type of surgery, chemotherapy, radiation therapy, and tamoxifen) were obtained using questions from a series of prior studies.7,9,10 Only surgical treatment information was reliably available from the tumor registry databases.14,15 Nineteen comorbid conditions were queried with the following response choices: "no, never," "yes, in past (> 1 year ago)," and "yes, now (during the past year)." If the response was "yes," respondents indicated whether medication was currently being taken for the condition. Conditions ranged from serious events such as stroke and heart attack, to thyroid conditions, diabetes, high blood pressure, depression, and osteoarthritis. The Breast Cancer Prevention Trial Symptom Checklist,16,17 a list of 42 everyday problems (such as hot flashes, headaches, vaginal dryness, breast tenderness) was used to describe current symptoms. Respondents rated how much they were bothered by each symptom during the last 4 weeks on a 5-point Likert-type severity scale from 0 (not at all) to 4 (extremely). This scale also has been used with breast cancer survivors to evaluate menopausal symptoms.9,18
Reproductive history and menopausal status were assessed through a series of questions adapted from the Study of Women Across the Nation.19 These questions ascertained current, precancer, and immediate postcancer menstrual histories, and whether menstrual periods stopped as a result of cancer treatments. Premenopausal was defined as regular menstrual periods, perimenopausal was defined as irregular periods or periods that stopped for 3 months or more and then resumed, and postmenopausal was defined as complete cessation of menstrual periods at least 6 months for current status and The RAND Short-form (SF)-36 (also known as the Medical Outcomes Study SF-36)20,21 and the Ladder of Life Scale22 were used to assess health-related QOL. The SF-36 contains eight individual scales: physical functioning; role function, physical; bodily pain; social functioning; emotional well-being; role function, emotional; vitality (energy and fatigue); and general health perceptions.20,21 Each scale is scored from 0 to 100, with 100 being the most favorable score. General population norms are available for the SF-36.23 The SF-36 can also be scored as two summary scales: a Physical Component Summary Scale (PCS) and a Mental Component Summary Scale (MCS).24 These scales are scored in reference to a normal population whose mean score is set at 50, with a score of 60 or 40 representing 1 standard deviation (SD) above or below the mean, respectively.24 The Ladder of Life scale22,25 has been widely used in epidemiologic and population studies and provides a global single-item QOL score. Ratings are made on a 10-point scale ranging from worst possible life to best possible life.
Depressive symptoms and affect were measured with two instruments. The Center for Epidemiologic Studies–Depression Scale (CES-D) is a reliable and valid 20-item self-report scale developed for the general population to measure depressive symptoms over the last week.26 Normative data are available for healthy women.16,27–29 Higher scores indicate greater risk of depression, with scores The Sexual Activity Questionnaire31 is a reliable and valid scale that was developed for the British tamoxifen prevention trial for use with healthy women at risk for breast cancer32 and also has been used with breast cancer survivors.10 The Sexual Activity Questionnaire has three scales: pleasure, discomfort, and habit (frequency of activities). Higher scores on each scale indicate greater pleasure, more discomfort, and greater frequency of activities. In an earlier study of breast cancer survivors, we developed a 12-item scale to measure perceptions of life after cancer, on the basis of a review of the literature, focus groups with cancer survivors, and clinical experience.9 Example items include "Surviving breast cancer has changed my outlook on life," "I get less worried about trivial things," and "I feel more vulnerable now, as if the world is a more dangerous place." Respondents indicate the extent to which they believe their outlook has changed on a 5-point scale, ranging from 0 (not at all) to 4 (very much). Factor analysis in the original sample9 yielded two factors. The first factor includes six items assessing changes in perspectives and priorities and was used as a measure of positive meaning. The second factor includes five items assessing fears about recurrence and about one’s body, and was used as a measure of vulnerability.
Statistical Considerations
Recruitment Results Recruitment results are shown in Figure 1  . Briefly, we received data for 1,454 potentially eligible women from the two tumor registries. Fourteen were excluded (incorrect histology or duplicate listings), for an initial mailing to 1,440 women. Mailed responses from 72.5% (n = 1,029) were received; 77% of these women expressed interest in participating in the study. Of these, 8% were ineligible, leading to a survey mailing to 736 women. From this sample, 577 women returned usable questionnaires and they comprise the study cohort for this report (final response, 56%; 577 of 1,029 potentially eligible respondents).
We made multiple attempts to contact the nonrespondents (Pakilit et al13). Of the 411 nonrespondents, 84% could not be contacted by either telephone or mail, 7% were found to be deceased, and 9% were ineligible because they could not read or understand English. We observed a significantly higher response rate to our invitation letter for women recruited from the cancer center registry (75.4% v 65.4%; P < .0001), as well as a higher response rate from white (P = .003) and more recently diagnosed women (P = .01). These same demographic characteristics were significantly related to agreement to be mailed the study survey. The final sample of 577 included 415 women recruited from the cancer center from 873 invitations mailed, and 162 from the community hospital from 567 invitations mailed.
Description of the Study Cohort
There were low rates of current or past comorbid conditions. Few women had a history of cardiovascular disease (stroke, < 1%; myocardial infarction, < 1%); however, 15% had a history of current or past hypertension, and 3.5% reported a history of current or past diabetes. More commonly reported conditions were migraine headaches (31%), anemia (31%), depression (34%), uterine fibroids (27%), hypothyroidism (16%), hyperthyroidism (5%), and asthma (10%). A small number of women reported a past or present diagnosis of arthritis (osteoarthritis, 7%; rheumatoid arthritis, 3%).
Menopause, Reproductive, and Fertility Findings
Pregnancy with at least one live birth was reported in 373 (65%) of the survey respondents (Table 3  ). Only 5% of women reported a pregnancy and live birth after the breast cancer diagnosis. Twenty percent reported that before breast cancer they were planning or hoping to have children, and 11% (n = 61) reported that they had considered getting pregnant since the breast cancer diagnosis. For these 61 survivors, 19% reported that they were not planning a pregnancy as a result of physician recommendation, 17% said they were not planning a pregnancy because they were worried about the risks, and 29% said they were not planning a pregnancy for other reasons that were primarily related to age or their personal relationship situation (categories were not mutually exclusive). However, 7% reported that they had been trying to become pregnant, 17% reported that they did become pregnant, and 12% indicated that they had specific plans or fertility treatments underway (categories were not mutually exclusive). Fifteen percent indicated that they were still considering a pregnancy and that they were undecided.
Current Symptoms
QOL Outcomes Table 4 presents QOL outcomes by age at diagnosis. Overall, these women reported high levels of physical functioning on the individual subscales of the SF-36 and the PCS. However, there were substantial decrements in the vitality (energy) scale score, with the lowest scores in the youngest age group (P = .03). For these women, the vitality scale score is approximately 0.5 SD below normal for that age group.20 Social and emotional functioning scores were lowest in the youngest women (P = .007 for social; P = .009 for emotional), with an age-related gradient in these scales. Similarly, on the MCS, the youngest women were more than 0.5 SD below the population norm for that measure (P = .0002). Scores on the CES-D and the PANAS are consistent with the SF-36 emotional functioning scale, with more depressive symptomatology, lower positive affect, and more negative affect in the youngest women. Ladder of Life scores did not differ by age, nor were there age-related differences in sexual functioning or outlook on life.
Additional analyses were conducted to explore the age differences in mental health. We hypothesized that younger women would be more adversely affected by cancer-related changes that were age-inappropriate, specifically going through menopause. We evaluated the association between the menopausal transition and the MCS scores in each age group. Results showed that among women aged 24 to 34 years at diagnosis, those who went through menopause after cancer treatment reported significantly lower MCS scores (mean, 41.9; SD, 14.5) than those who did not go through menopause (mean, 48.1; SD, 9.1), although this difference did not reach statistical significance (P = .10). In contrast, MCS scores in the older age categories of this cohort were not related to the development of menopause.
We next examined the QOL outcomes according to the type of adjuvant therapy that had been received. Because treatments were significantly different across the age groups (Table 2
Predictors of QOL
Table 5
In a series of research studies with breast cancer patients and survivors during the last 15 years, we have consistently observed that younger women with breast cancer were at greater risk for psychologic distress than older women,7–9,33 and were at an increased risk for fatigue.34 They also seem to be at greater risk for sexual dysfunction, especially in association with treatment-related changes in menstrual status.9,35 These earlier studies included women whose average age at diagnosis was about 55 years. Our findings related to psychologic distress and younger age have been replicated by others.3,36,37 Some of these issues were recognized, and a decade ago the National Institutes of Health sponsored a special conference on Breast Cancer in Younger Women, the proceedings of which were published in 1994.38 In addition to reviewing the epidemiology, risk factors, and predictors of outcome in younger women with breast cancer, the conference reviewed the late effects of adjuvant therapy in younger women,39 a range of reproductive health issues,40–42 and psychosocial issues and survival.4,43–45 As a result of that conference, considerable interest and funding opportunities were generated related to examination of the special concerns of younger women with breast cancer. The CAMS research program introduced in this article is a direct result of those efforts. To date, there are few published studies focusing specifically on younger women with breast cancer.5,46,47 Both Bloom et al5 and Allen et al47 recruited cohorts of newly diagnosed younger women with breast cancer as part of intervention studies designed to address specific psychosocial needs and concerns of younger women. An additional study describes an inception cohort of 183 premenopausal breast cancer patients who were observed prospectively for 1 year to determine the rate of amenorrhea in relationship to primary treatment.12 We believe that the CAMS study sample described here is the first examination of a cohort of younger, long-term breast cancer survivors (mean of 6 years after diagnosis). In addition, the focus on the interface of reproductive health outcomes and QOL in the CAMS sample responds to a unique set of issues in this survivor population.
In this report, we have confirmed a substantial degree of psychologic distress in younger women after breast cancer that persists many years after the diagnosis. This is especially evident in the youngest women who were between 25 and 34 years of age at diagnosis, who reported significantly poorer emotional and social function and lower levels of energy than population norms from women without a breast cancer history. Although there is a gradient of emotional dysfunction from the youngest to the oldest women in this cohort (Table 4 The findings from these models are also consistent with our prior research in a broader age range of breast cancer survivors,10 in which the number of comorbid conditions and emotional and physical functioning predicted health perceptions, and being African-American and having better emotional functioning predicted better QOL. On the basis of other research, it is not surprising that the predictors in these two models are somewhat different, given that other studies have shown that the general health perceptions scale more often is predicted by physical factors (eg, comorbid conditions or decreased physical abilities),49 and that single-item QOL scales draw on both physical and emotional predictors (eg, emotional functioning and social support).50 For this sample of younger women with breast cancer, it appears that specific treatments for breast cancer have had little direct influence on subsequent QOL, with the exception of the menopause transition, which is a result of adjuvant treatment. The confirmation of these predictive models in this second independent sample of breast cancer survivors provides additional support for these observations. Emerging from this report, as well as in other research from our group,51 is some evidence that African-American women may fare better after breast cancer than other ethnic groups. In our other research, we have found that African-American women report finding more meaning in life after breast cancer,51 and this provides support for a possible mechanism by which these ethnic differences occur. How do we reconcile the differences and similarities in QOL outcomes across diverse studies and age groups of breast cancer survivors? Consistent with the broader literature on QOL outcomes in younger women with breast cancer, the emotional impact of the disease is substantial, and most evident in the youngest women. Younger women are at a time in life when a serious disease like cancer is not anticipated and is disruptive. In addition, the impact of treatment on reproductive health may contribute to changes in emotional well-being. Indeed, our results suggest that treatment-related menopause was particularly problematic for the youngest women and was associated with poorer emotional functioning. Women who are older at diagnosis (eg, the oldest women in this cohort) may have greater emotional resiliency from prior life experiences that are brought to bear when facing a cancer diagnosis. However, older women may have less physical resiliency in the face of breast cancer treatments because of underlying comorbid conditions or increasing physical limitations associated with age.9,10 The divergence between physical and emotional functioning in relationship to age is generally observed in healthy populations (SF-36 norms20), and the age-related differences in the impact of breast cancer diagnosis and treatment on emotional and physical functioning may represent an exaggeration of these normative findings. There are several important limitations of this study. First, although we attempted to recruit as representative a sample as possible of younger breast cancer survivors, many women were not accessible or declined to participate in the study. This was especially true among some ethnic minority women and women from the community hospital.13 It is challenging to identify cancer survivors who might participate in research studies, yet cancer registries provide us with one of the best sources.13 It is possible that the women who responded to the study invitation were more resilient and higher functioning, and therefore, we may be underestimating the impact of breast cancer in younger women. In addition, as with any survey study, there may be inaccuracies in self-report of information on health history, reproductive health, emotional concerns, or other topics that we queried. Finally, these younger breast cancer survivors were recruited from one large urban area, and their experiences may not represent those of all younger women with breast cancer. Despite these limitations, we believe that this report describes one of the largest and most diverse cohorts of younger breast cancer survivors in the literature to date. Our findings provide important insights into the late effects of this disease in younger women. Despite its known effect on reproductive health, systemic adjuvant therapy did not appear to have negatively influenced either physical or emotional functioning in these younger women, and instead, women who either did not choose or were not advised to have adjuvant therapy fared somewhat worse emotionally. However, it is clear that loss of reproductive function (early menopause), the loss of the ability to have children, and many specific symptoms are associated with breast cancer treatments. The descriptive findings in this report may be useful to clinicians and patients, and it is important for us to acknowledge that many symptoms and problems persist long beyond the acute phase of breast cancer treatment.
The authors indicated no potential conflicts of interest.
We are grateful for the excellent support provided by Amber Pakilit and Laura Abraham, who were the research assistants for this study. In addition, we express our great appreciation to the women who participated in this study.
Supported by funding from the National Cancer Institute (P30 CA16042), the Susan G. Komen Foundation, and the US Department of Defense (DAMD 17-98-1-1810). P.A.G. was also supported through an American Cancer Society Clinical Research Professorship.
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Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
40 years at diagnosis, and treatment-associated menopause was associated with poorer health perceptions. Across the cohort, physical functioning was quite good, but the youngest women experienced poorer mental health (P = .0002) and less vitality (energy; P = .03). Multiple regression analyses predicting QOL demonstrated better outcomes in African-American women, married or partnered women, and women with better emotional and physical functioning, whereas women who reported greater vulnerability had poorer QOL. 
2 tests were used to compare the distribution of medical and demographic categoric variables across age groups. One-way analysis of variance was used to compare medical and QOL continuous variables across age groups. Analysis of covariance was used to create and compare least-squares means of QOL variables by adjuvant therapy group, adjusting for age, time since diagnosis, race, current tamoxifen use, and current menopausal status. Linear regression was used to model general health perceptions and the Ladder of Life score. 
