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Journal of Clinical Oncology, Vol 24, No 18 (June 20), 2006: pp. 2815-2821 © 2006 American Society of Clinical Oncology. DOI: 10.1200/JCO.2005.04.2499 Sexual Problems in Younger Women After Breast Cancer Surgery
From the University of Georgia, Department of Child and Family Development, Athens, GA; Department of Public Health Sciences, Wake Forest University School of Medicine, Winston-Salem, NC; and the Comprehensive Breast Health Center, Brigham and Women's Hospital, Boston, MA Address reprint requests to Nancy E. Avis, PhD, Department of Public Health Sciences, Section on Social Sciences and Health Policy, Wake Forest University School of Medicine, Piedmont Plaza II, 2000 W First St, Winston-Salem, NC 27157-1063; e-mail: navis{at}wfubmc.edu
PURPOSE: To examine sexual problems in younger women diagnosed with breast cancer during the first year after surgery and to identify sociodemographic, medical, and psychosocial predictors of sexual problems.
PATIENTS AND METHODS: Women diagnosed with breast cancer age RESULTS: Analyses included 209 women sexually active at baseline (78.6% of total sample). Sexual problems were significantly greater immediately postsurgery compared with retrospective reports before diagnosis (P < .0001). Although problems gradually decreased over time, they were still greater at 1 year postsurgery than before diagnosis. In multivariate analyses controlling for sexual problems at prediagnosis, vaginal dryness, and lower perceived sexual attractiveness were consistently related to greater overall sexual problems. Chemotherapy was related to sexual problems only at baseline except for women who became menopausal as a result of chemotherapy, who continued to have problems. CONCLUSION: Findings substantiate the need to address potential sexual problems related to chemotherapy treatment and menopause among younger breast cancer survivors and to counsel women about possible remedies, particularly for vaginal dryness. Increasing feelings of sexual attractiveness may also help sexual problems, especially among women for whom these feelings were altered by surgery or treatment.
Breast cancer is the most common type of cancer among women in the United States and 211,240 cases of invasive breast cancer were expected in 2005.1 Approximately 26% of all newly diagnosed breast cancer cases occur among women younger than age 50.2 Studies have previously demonstrated that breast cancer and its treatment can negatively impact a woman's sexual functioning.3-12 Sexual problems may be especially prominent among younger women who are more vulnerable to changes in ovarian functioning resulting from chemotherapy and concerns about body image after surgery.7,9,13-15 Over 75% of women age 42 to 55 years in the general population report that sex is moderately to extremely important in their lives,16 and studies show that sexual problems are significantly related to reduced quality of life among younger breast cancer survivors.17,18 Given the increasing number of younger breast cancer survivors and the importance of sexual functioning, research is needed to better understand how breast cancer diagnosis and treatment impact the time course of sexual problems and factors contributing to these problems. This study focused on longitudinal changes in multiple domains of sexual functioning among younger women during the first year after surgery for breast cancer.
The majority of research in this area has been either cross-sectional and/or focused primarily on treatment-related predictors.3,19-29 The primary exception is the work of Ganz et al30 who conducted a large longitudinal study of sexual health of women after breast cancer diagnosis. Ganz et al30 present a conceptual model proposing factors that influence sexual health that includes demographic and personal characteristics, medical variables, body image, partner relationship, and health-related quality of life. This study uses this conceptual model to examine predictors of multiple domains of sexual problems at three time points after surgery among women diagnosed with breast cancer age The study objectives were to describe sexual problems following diagnosis and compare these to retrospective reports of sexual problems 6 months before diagnosis; to investigate postsurgery changes in specific domains of sexual problems, and; to determine how sociodemographic, medical, body image, partner relationship, and health-related quality of life are associated with sexual problems.
Sample Women newly diagnosed with breast cancer were referred by their surgeons from eight hospitals in the Greater Boston and New Hampshire areas to participate in a study evaluating two educational materials about breast cancer. Inclusion criteria were  50 years of age at diagnosis, first time diagnosis, and 4 weeks to 26 weeks postsurgery. The analytic sample for this article included women who reported being sexually active and responded to the sexual problem survey items.
Procedure
Measures Sexual problems. Sexual Problems were measured by the Medical Outcomes Study (MOS) Sexual Functioning Scale,31 which contains four questions assessing different problem areas: lack of interest in sexual activity, difficulty becoming aroused, difficulty relaxing and enjoying sex, and difficulty achieving orgasm. Each item has a 4-point Likert response scale ranging from: (1) not a problem; (2) little problem; (3) somewhat of a problem, and; (4) very much of a problem. An overall sexual problem score was calculated as the sum of these four domain scores and rescaled from 0 to 100, with lower scores indicating fewer sexual problems. The MOS has good psychometric properties, has been used with breast cancer patients,4,31,32 and as a generic measure of sexual functioning, allows for comparisons with other populations.31,33,34 At baseline, women reported on sexual problems since diagnosis and retrospectively on sexual problems for the 6 months before their diagnosis. At FU1 and FU2 they reported on their sexual problems for the previous 4 weeks. Sociodemographic variables. Sociodemographic variables included age at diagnosis, present partner status (partnered/nonpartnered), level of education, employment status, and ethnicity. Medical variables included cancer stage, surgery type (including reconstruction), type of adjuvant treatment, time since surgery, menopausal status (pre, peri, naturally post, and surgical), and vaginal dryness. Vaginal dryness was included only at FU1 and FU2 as we inadvertently did not ask about symptoms at baseline. Partner relationship. Relationship satisfaction was measured by the Index of Marital Satisfaction, which consists of 25 items regarding degree of satisfaction with one's partner.35 Each item is ranked on a 7-point Likert scale (1 = none of the time, 7 = all of the time) measuring the degree of satisfaction. The Index of Marital Satisfaction has documented validity and reliability in the general population.36 Quality of life. Global quality of life was measured by the single item Visual Analog Scale where respondents rate their overall quality of life over the past 2 weeks on a scale from 1 to 100. The Functional Assessment of Cancer Therapy-Breast scale (FACT-B)37 measured cancer-specific quality of life in five areas of well being: social/family, physical, functional, emotional, and breast cancer specific concerns. Women rated how problematic each item had been during the past 7 days (1 = not at all problematic, 5 = very much a problem). Higher scores indicated better quality of life. Body image, sexual attractiveness, and satisfaction with sex life. Satisfaction with body and breast appearance was adapted from the 7-item Body Image Index.38 A question from the FACT-B additional concerns subscale "I feel sexually attractive" was included in analyses to assess feelings of sexual attractiveness. The FACT-B item "I am satisfied with my sex life" assessed satisfaction. Intervention. Type of educational material (videotape or pamphlet). Statistical Methods. Means and standard deviations summarized MOS sexual problems during each survey and at 6 months before diagnosis. Paired t-tests compared changes in sexual function relative with prediagnosis and across the various surveys. Each sexual problem domain was dichotomized as few or no problems versus moderate to severe problems. McNemar's tests assessed changes relative to prediagnosis and across the various surveys. Linear regression models examined characteristics associated with sexual problems at each survey. Time from surgery was used as a continuous variable as were variables other than sociodemographic and medical factors. All sociodemographics were determined at the initial survey. Sexual problems and other variables were determined at each survey time. A backward stepping algorithm was used to remove nonsignificant effects from the models at the .05 level of significance. Data from all three surveys were combined to assess changes over time in overall sexual function and to determine if the effects of the covariates were consistent over time. Because women completed their initial survey at various time points (4 weeks to 24 weeks from initial cancer surgery) and then at 6 weeks and 6 months after the initial survey, the time since surgery (the date of survey completion minus the date of surgery) was used in the analyses. A mixed model analysis of variance assessed changes in sexual problems during the first year postsurgery. Time was used as a continuous variable (truncated to the week past surgery) as were variables other than sociodemographic and medical factors. An autoregressive covariance structure was used to model the correlation within subjects over time since measures closer in time should be more highly correlated. Interactions between covariates and time were initially considered to see if the effects of the covariates changed over time. A backward stepping algorithm removed nonsignificant interactions and main effects from the model at the .05 level of significance.
Sample Characteristics A total of 323 women were referred by their surgeons and 301 met the eligibility criteria. A total of 268 women completed the baseline interview for a response rate of 89%. Two women were subsequently excluded because they were older than age 50 at diagnosis, leaving a sample of 266 women. Study retention was excellent with 245 women (92%) completing FU2. Women were excluded from the present analyses if at baseline they responded "no" to the question: "Have you been sexually active within the past year?" (n = 55) or did not respond to any of the sexual problem survey items (n = 2). The characteristics of the remaining sample of 209 are summarized in Table 1. Age at diagnosis ranged from 29 years to 50 years with a median of 43 years. Most women were married or in a partnered relationship (88%), 92% were white, 76% had at least some college education, and 69% worked full- or part-time.
At the initial survey, the majority of women (64%) were premenopausal. Forty-five percent had a mastectomy as their definitive surgery (women who had both a lumpectomy and mastectomy were classified in the mastectomy category); two thirds of those who had a mastectomy had reconstructive surgery. Over half of the women received chemotherapy (56%), 47% had radiation therapy, and 28% had hormone therapy. Women ranged from 4 weeks to 23 weeks postsurgery at baseline (median = 11.3 weeks), 11 weeks to 34 weeks postsurgery at FU1 (median, 20.9 weeks.), and 28 weeks to 58 weeks postsurgery at FU2 (median, 38.7 weeks.). Four women had surgeries after baseline that affected their surgery classification category (three subsequently had mastectomies without reconstruction and one had a mastectomy with reconstruction).
Trends Over Time
Women experienced problems in all MOS sexual functioning domains compared with retrospective reports of prediagnosis problems (Table 3). Compared with prediagnosis levels, considerably more women reported problems with interest (42% v 19%; P < .0001), sexual arousal (33% v 17%; P < .0001), difficulty relaxing and enjoying sex (33% v 12%; P < .0001), and reaching orgasm (23% v 8%; P < .0001) in the early months after surgery. Problems were still significantly greater than prediagnosis levels at FU2 in all domains except arousal. There was no significant change over time in reports of partner lacking interest in sex or in satisfaction with sex life.
Predictors of Sexual Problems Bivariate analyses assessed the unadjusted associations between predictors and MOS sexual problems at each survey. Vaginal dryness, chemotherapy, body image, feeling sexually attractive, relationship satisfaction, global quality of life, and the FACT-B subscales were all significantly related to sexual function at some time point (data not shown). None of the following variables was significantly related to overall sexual problems: age, partner status, education, employment status, ethnicity, baseline menopause status, change in menopause status, cancer stage, surgery type, hormone therapy, or intervention group. Women who had breast reconstruction surgery did not show a different pattern. Multivariate results controlling for prediagnosis sexual problems showed that lower perceived sexual attractiveness was associated with greater sexual problems at all time points (Table 4). Chemotherapy was significantly related to sexual problems at baseline, but not at FU1 or FU2. Vaginal dryness, which was not obtained at baseline, was highly significant at FU1 and FU2. At baseline, lower functional well being was also related to sexual problems. By FU2, cancer stage and emotional well being were significant.
The longitudinal mixed model analysis assessing changes over time and controlling for prediagnosis sexual problems showed women with better physical and social well being, greater perceived sexual attractiveness, and those who received radiation reported fewer sexual problems (Table 5). There was a significant interaction between time and chemotherapy (P = .02). For those receiving chemotherapy, sexual problems decreased over time (P = .0049), while scores remained relatively unchanged for women who did not receive chemotherapy (P = .6998). The interaction shows that the effect of chemotherapy became weaker over time (Table 5).
We further examined the relationship between chemotherapy and change in menopause status (from baseline to FU2) on sexual problems (Table 6) and found a significant interaction (P = .008). Of the women receiving chemotherapy, those who experienced a menopausal transition reported more sexual problems than those without a transition (P = .015). However, when vaginal dryness was included in the model, the effect of menopausal transition was no longer significant (P = .069). For women who did not receive chemotherapy, too few women transitioned for analyses.
This research is one of the few studies addressing sexual problems specifically among younger women after breast cancer surgery that also looks at multiple domains, multiple predictors, and the interaction between menopause and chemotherapy. Although sexual problems decreased over time, women reported more problems at each time point following surgery compared with their retrospective prediagnosis reports. Other studies observing women over time post-diagnosis have found similar results.27,28,39 Studies comparing breast cancer survivors with healthy women have found that breast cancer survivors report more sexual problems than healthy controls.4,5 Women in the present study reported more problems on the MOS than healthy women in the Breast Cancer Prevention Trial33 and healthy men in the Prostate Cancer Prevention Trial.34 At trial baseline, less than 10% of Breast Cancer Prevention Trial participants age 35 years to 49 years reported problems in each of the MOS sexual problem areas, with lack of interest being most problematic. However, retrospective reports of sexual problems prediagnosis also were higher in our sample, which could be due to recall bias. Our mean sexual problems score at follow-up is quite similar to that found for women with other chronic conditions in the Medical Outcomes Study.31 We found that in general, chemotherapy was related to greater sexual problems early after surgery, but not further from surgery. Other studies have shown that the impact of chemotherapy on sexual problems extends beyond the first year after treatment 3,4,7,8,19-21,32 However, the impact of chemotherapy on menopausal status appears to be an important factor. Ganz et al7 found that sexual functioning was most impaired for women no longer menstruating after chemotherapy, a finding also supported by Lindley et al.8 Two other studies that found a long-term effect of chemotherapy20,21 only studied premenopausal women. Other studies did not examine the interaction between chemotherapy and change in menopause status,4,19 or compare women who had chemotherapy with those who did not.4 Our data and other studies suggest that the onset of vaginal dryness from abrupt menopause is the important factor affecting sexual functioning.4,7,40 The long-term impact of chemotherapy on sexual functioning is thus related to its impact on ovarian functioning. Younger women whose ovarian function returns after chemotherapy and women already postmenopausal may show only short-term effects of chemotherapy, while women whose ovarian function is severely affected by chemotherapy may show longer-term effects. Research that includes pre- and/or perimenopausal women receiving chemotherapy needs to take menopausal status change into consideration. As found in other studies, sexual problems in younger women were not related to sociodemographic factors or type of breast cancer surgery.3,19,21,23,24,41 In addition to vaginal dryness and prediagnosis sexual function, the strongest consistent predictor of overall sexual problems in multivariate analyses was lower perceived sexual attractiveness, which could be a result of chemotherapy/surgery or reflective of a generally negative self view. Body image (which is more general than sexual attractiveness), partner relationship, or global quality of life were not related to overall sexual problems in multivariate analyses. Similar to other studies30,40 we found some differences by sexual domain. Although all domains were problematic compared with retrospective reports at each time point, interest in sexual activity was the most problematic domain postsurgery and remained the most problematic over time. This suggests that problems with sexual interest may last longer than other domains and that research should make distinctions among various aspects of sexual functioning. Understanding specific aspects of sexual problems that affect younger women and extend over time is relevant for oncologists. Younger women experiencing menopause after chemotherapy may benefit from treatment for vaginal dryness. Vaginal rings, a form of estrogen that dispenses low doses of estrogen with little systemic absorption, and lubricants may prove beneficial. Although sexual functioning is an important quality of life issue for women, it may be difficult for patients to initiate discussion and clinicians should routinely raise the topic. Interventions to help women feel more sexually attractive may be beneficial, especially among women for whom these feelings were altered as a result of treatment or surgery. There are several limitations of this study. Although characteristic of many samples of breast cancer patients, this sample is relatively homogeneous (mostly white, educated, and partnered women), which limits its generalizability. Retrospective recollections of prediagnosis sexual functioning could be biased positively or negatively, based on each woman's cancer experience. The time frames for recalling sexual problems differed for prediagnosis (6 months before diagnosis), baseline (since diagnosis), and the last two surveys (4 weeks), and could account for some of the differences in sexual functioning scores. However, we suspect that in general most women responded to these items based on recent experiences. Because women not currently sexually active, and perhaps experiencing more problems, did not complete the MOS questions, our data may underestimate sexual problems. Overall, our results suggest that younger women experience the most sexual problems in the months immediately after surgery and treatment. Although problems diminish over time, some women still report problems 1 year after surgery. Results support the need for more research on how chemotherapy impacts sexual functioning among those patients who experience a premature chemical menopause and for interventions to assess, treat, and monitor sexual problems after initial surgery for younger women with breast cancer.
We gratefully acknowledge the following institutions for their assistance in patient recruitment: New Hampshire Oncology-Hematology (Robert Friedlander, MD), Boston Medical Center (Marianne Prout, MD), Mt Auburn Hospital (Clair Beard, MD), Massachusetts General Hospital (Michele Gadd, MD), Brigham and Women's Hospital (Carolyn Kaelin, MD), Roswell Park Cancer Institute (Noma Roberson, RN, PhD), Sylvester Comprehensive Cancer Center (Sharlene Weiss, RN, PhD), and Dana-Farber Cancer Institute (Eric Winer, MD).
The authors indicated no potential conflicts of interest.
Conception and design: Stephanie R. Burwell, Nancy E. Avis Financial support: Nancy E. Avis Administrative support: Nancy E. Avis Provision of study materials or patients: Carolyn Kaelin, Nancy E. Avis Collection and assembly of data: Nancy E. Avis Data analysis and interpretation: Stephanie R. Burwell, L. Douglas Case, Carolyn Kaelin, Nancy E. Avis Manuscript writing: Stephanie R. Burwell, L. Douglas Case, Carolyn Kaelin, Nancy E. Avis Final approval of manuscript: Stephanie R. Burwell, L. Douglas Case, Carolyn Kaelin, Nancy E. Avis
Supported by Grant No. R01CA64716 from the National Cancer Institute. Presented in poster format at the American Psychosocial Oncology Society meeting in Orlando, FL, January 29-February 1, 2004. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2006 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
