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© 1999 American Society for Clinical Oncology Predictors of Sexual Health in Women After a Breast Cancer DiagnosisFrom the Schools of Medicine and Public Health and Division of Cancer Prevention and Control Research, Jonsson Comprehensive Cancer Center, University of California at Los Angeles, Los Angeles; Department of Psychology, University of Southern California, Los Angeles, CA; and Department of Psychiatry, Georgetown University Medical School, and Lombardi Cancer Center, Washington, DC. Address reprint requests to Patricia A. Ganz, MD, Division of Cancer Prevention and Control Research, Jonsson Comprehensive Cancer Center, A2-125 CHS Box 956900, 650 Circle Dr South, Los Angeles, CA 90095-6900; email pganz{at}ucla.edu
PURPOSE: To identify variables that might be predictive of sexual health (interest, dysfunction, and satisfaction) in a large sample of breast cancer survivors, with a validation conducted in a second, independent sample. PATIENTS AND METHODS: On the basis of a conceptual framework of sexual health in breast cancer survivors, we performed multivariable regression analyses to estimate sexual interest, dysfunction, and satisfaction in both samples. Additional analyses were performed using stepwise regression and recursive partitioning to explore in each sample the relative contributions of the independent variables toward predicting the outcome measures. RESULTS: The models for sexual interest accounted for at least 33% of the variance, and the significant predictors common to the two samples were having a new partner since the diagnosis of breast cancer, mental health score, and body image score. For sexual dysfunction, the models in the two samples explained at least 33% of the variance, and the common significant predictors were vaginal dryness, past chemotherapy use, and having a new partner since diagnosis. The sexual satisfaction models explained at least 27% of the variance, with the common significant predictors being the quality of the partnered relationship and sexual problems in the partner. CONCLUSION: Among the predictors of sexual health, several are mutable (vaginal dryness, emotional well-being, body image, the quality of the partnered relationship, and sexual problems in the partner), and these should be considered for future interventions to address the sexual health and well-being of breast cancer survivors.
SEXUAL PROBLEMS OCCUR with considerable frequency in breast cancer patients and extend beyond the acute phase of treatment.1-4 The more widespread adoption of breast-conserving surgical treatment (as compared with mastectomy) was expected to diminish the negative impact of treatment on quality of life and sexual functioning. Unfortunately, this goal has not been realized completely. Several prospective studies show no difference in quality-of-life outcomes or sexual functioning for breast cancer survivors on the basis of surgical treatment.1,2,5-7 However, few studies have examined quality of life or sexual functioning with standardized instruments and/or normative data from reference samples.3,8 In a recent study of a large cross-sectional sample of breast cancer survivors for whom on average 3 years had passed since diagnosis, we observed sexual functioning that was similar to that of age-matched healthy women. However, we did observe poorer sexual functioning in younger women who became prematurely menopausal because of chemotherapy and in women of all ages who received chemotherapy.9,10 The etiology of sexual dysfunction in breast cancer survivors has not been well studied. There are multiple predisposing factors, including pre-existing sexual problems, negative sexual self-schemas, and normal age-related changes in sexual functioning.11-14 Physiologic changes induced by chemotherapy are also important contributors. Induction of premature menopause can result in an estrogen deficiency state that increases the likelihood of hot flashes and poor vaginal lubrication that may contribute to sexual dysfunction.15-18 These symptoms are also a potential problem for older patients for whom hormone replacement therapy (HRT) is discontinued at the time of a breast cancer diagnosis. Furthermore, these symptoms may be exacerbated by tamoxifen adjuvant therapy.19 Beyond physical factors, Schultz et al20 suggest that psychologic reactions to cancer can also form the basis for sexual dysfunction in some women with cancer. Sexuality and intimacy are important survivorship concerns for breast cancer patients, yet health care providers and traditional psychosocial support programs often overlook these issues. As part of a research program studying the quality of life of breast cancer survivors, we have explored the relationship among a number of medical, demographic, treatment, and psychologic variables in relationship to sexual health. Using an a priori conceptual framework, we developed predictive models for sexual interest, sexual dysfunction and sexual satisfaction after breast cancer. The models were developed in one sample of breast cancer survivors and were validated in a second, independent sample. This article describes our findings and provides a background for clinical care and future research on sexual health in this patient population.
Study Samples As part of a large program of research addressing quality of life, sexuality, and intimacy in breast cancer survivors, we recruited two independent samples of breast cancer survivors in two large metropolitan cities: Los Angeles, CA, and Washington, DC.9,21 Sample 1 included 863 breast cancer survivors who were recruited to complete a survey questionnaire between September 1994 and November 1995. Sample 2 included 1,094 breast cancer survivors who were recruited to complete a survey questionnaire between January 1996 and June 1997. For both studies, the eligibility criteria were identical and included: (1) having had a diagnosis of breast cancer (initial stage 0, I, or II); (2) between 1 and 5 years having passed since initial breast cancer diagnosis; (3) having completed local and/or systemic adjuvant cancer therapy; (4) currently being considered disease-free and not receiving cancer therapy other than tamoxifen; (5) having no prior history of treatment of other cancers, with the exception of noninvasive skin cancer and cervical cancer; (6) being able to read and write English; (7) providing informed consent; and (8) having no other major disabling medical or psychiatric conditions that would confound evaluation of health-related quality of life (subject recruitment discussed in detail in9,21). To be eligible for the current analyses, a woman had to be in a partnered relationship and sexually active within the past 6 months, as determined by self-report. Sexual activity with a partner did not require being married or in a heterosexual relationship. This left a total of 472 women from sample 1 and 662 from sample 2 who were studied for this report.
Conceptual Framework for Sexual Functioning and Satisfaction
Instruments and Procedures
Study Variables Measured in Relation to the Conceptual Framework Demographic and personal characteristics are individual attributes that preceded the cancer or were independent of the breast cancer diagnosis and treatment. These include age, ethnicity, patient comorbidity, and body mass index. Patient comorbidity was assessed through a checklist of medical and/or psychiatric problems. Breast cancer and related medical variables include time since diagnosis, type of surgery, chemotherapy treatment (yes or no), current tamoxifen use, hot flashes, vaginal dryness, and current menstrual status or change in hormone therapy. The items for hot flashes and vaginal dryness were taken from the Breast Cancer Prevention Trial Symptom Checklist.25 Body image after breast cancer was measured using the Cancer Rehabilitation Evaluation System (CARES) Body Image Subscale.26,27 CARES subscale scores range from 0 to 4 and measure the severity of problems, with higher scores indicating more difficulty. The three items in this subscale are "I am embarrassed to show my body to others because of my illness," "I am uncomfortable showing my scars to others," and "I am uncomfortable with the changes in my body." Partner relationship variables include partner sexual problems, whether the current partner was new since the breast cancer diagnosis, and the quality of the relationship as measured by the Revised Dyadic Adjustment Scale.28 This scale is a shortened version of the Dyadic Adjustment Scale,29 a self-report marital adjustment measure. The revised form has 14 items, and scores range from 0 to 69. The developers of the scale report mean values of 48.0 (SD, 9.0). Components of health-related quality of life were assessed using the 32-item Mental Health Index (MHI) and the General Health Perceptions Scale from the RAND 36-item Health Survey 1.0. The MHI is a 32-item scale developed for the Medical Outcomes Study (MOS).30 Scores range from 0 to 100, with higher scores indicating a more favorable mental health status. The mean score for the MHI in the MOS sample was 70.3 (SD, 16.2). The RAND 36-item Health Survey subscales31,32 are also scored from 0 to 100, with 100 being the most favorable score. Social support is measured by a short form of the MOS Social Support Measure.33 The full measure contains 19 items and is scored from 0 to 100, with higher scores indicating better social support. In consultation with the instrument's author (C.D. Sherbourne, personal communication, November 1995), we shortened the instrument to a 12-item scale, scored similarly to the longer version. Candidate variables for measurement of the various aspects of sexual health included the Watts Sexual Functioning Scale,34 the CARES Sexual Functioning Summary Scale, the CARES Sexual Interest and Sex Dysfunction subscales,26,27 and a single-item satisfaction measure. The sexual satisfaction item was taken from the Sexual History Form developed by Schover and Jensen.35 Our preliminary analyses showed a high correlation between the Watts scale and the CARES Sexual Functioning Summary Scale (r = -.68, P = .0001). The comparative brevity of the CARES Sexual Functioning Summary Scale (eight items v 17 items), as well as better compliance among subjects in completing scale items, led us to choose the CARES. Furthermore, the breakdown of the CARES Sexual Functioning Summary Scale into interest and dysfunction subscales, confirmed by our own factor analysis, which showed the same two distinct components of functioning, informed our decision to model sexual interest and dysfunction separately. Thus sexual interest was measured using the CARES Sexual Interest Subscale, and sexual dysfunction was measured using the CARES Sexual Dysfunction Subscale. Using an additional exploratory evaluation of the data with scatterplots (eg, CARES Sexual Functioning Summary Scale scores v sexual satisfaction scores), we determined that while sexual satisfaction and sexual functioning were strongly correlated, there were still many cases in which functioning and satisfaction were not congruent. Therefore, sexual satisfaction was modeled separately, using the single-item question from the Sexual History Form that asked about satisfaction with the current relationship. Table 1 shows the questionnaire items upon which our three outcome measures are based.
Analysis Strategy and Statistical Methods Standard statistical methods were used in all analyses. Chi-square or t test methods were used in comparing categorical and continuous measures, respectively, between samples 1 and 2. Pearson product-moment correlations were used to investigate relationships among pairs of continuous predictor variables and among predictor-outcome pairs in sample 1. Analysis of variance or t test methods were used in comparing mean values of the three continuous outcome measures among predictor categories in both samples. Ordinary least squares regression was used to estimate the sexual interest, dysfunction, and satisfaction models in samples 1 and 2. The sexual interest and sexual dysfunction subscales were log-transformed to conform to ordinary least squares regression assumptions. Finally, we used stepwise regression and binary recursive partitioning (using the CART software36,37 [Salford Systems, San Diego, CA]) to explore in each sample the relative contributions of independent variables toward predicting the outcome measures.
Characteristics of the Patient Samples The demographic and medical characteristics of the two patient samples are shown in Table 2. On average, sample 1 was 52 years of age (range, 31 to 87 years). The women in sample 2 had a similar average age (mean age, 53 years; range, 29 to 83 years), but the age distribution was significantly different (P = .007), with fewer women younger than 50 years old in sample 2. The ethnic distribution of the samples is representative of the patient populations with early-stage breast cancer in the two metropolitan cities from which they were recruited; however, sample 2 had slightly more white respondents (P = .045). On average, approximately 3 years had passed since their breast cancer diagnosis when the women completed the survey questionnaire. More than half of the women had received breast-conserving surgery and almost half of those with mastectomy had received reconstruction. Surgical patterns differed slightly between the two samples (P = .036), with breast-conserving surgery more frequent in sample 2. Adjuvant chemotherapy was frequently used in both study samples, and more than 40% of women in both samples were taking tamoxifen adjuvant therapy at the time of participation in the study. Menstrual and menopausal hormone history was described for these women with the following categories: menstruating now, stopped menstruating after breast cancer treatment, was postmenopausal at diagnosis and on HRT, and was postmenopausal at diagnosis and not on HRT. As can be seen in Table 2, there were some differences between the two samples (P = .001), with the more recent sample having more women who had stopped menstruating after diagnosis or discontinued HRT at the time of diagnosis.
Although these patient samples overlapped in treatment years, the more recently treated sample (sample 2) had somewhat higher rates of breast-conserving surgery and more frequent changes in menstrual or hormonal status (Table 2). Despite this, there were no significant differences in rates of symptoms (hot flashes, vaginal dryness), other health conditions, or body mass index (Table 3). However, with regard to the partnered relationship, the patients in sample 2 reported more often that their partner had sexual functioning problems (P = .038), and their scores on the Revised Dyadic Adjustment Scale were somewhat poorer (P < .001). There were no significant differences between the two samples in body image scores, general health perceptions, mental health, social support, or sexual satisfaction (Table 3). However, sample 2 reported greater problems with sexual interest (P = .008) and sexual dysfunction (P = .010).
Relationships Among the Dependent and Independent Variables
Correlations of our continuous predictor variables with the three outcome measures (not shown) revealed significant associations between all three dependent variables and social support, dyadic adjustment, and the MHI. General health was correlated with the two CARES measures (interest and dysfunction), and body image was correlated with the CARES Sexual Interest Subscale. Age and time since diagnosis were not significantly correlated with any of the outcome measures.
Predictors of Sexual Interest in Sample 1
Predictors of Sexual Dysfunction in Sample 1
Predictors of Sexual Satisfaction in Sample 1
Validation of the Models in Sample 2 The sexual dysfunction model in sample 2 (column 4 of Table 5) also showed a slight decline in explanatory power, accounting for 33% of variance, as compared with 38% in sample 1. Predictors that remained significant in the second sample were vaginal dryness, history of chemotherapy, and having a new partner. No longer significant in this sample were having stopped menstruating and having had to stop taking HRT. Additional predictors that became significant in the second sample were being African-American (reporting less dysfunction than white women), time since diagnosis (a greater time interval was associated with more dysfunction), dyadic adjustment (a better relationship associated with less dysfunction), mental health (more favorable mental health associated with less dysfunction), and remaining premenopausal (less dysfunction in comparison to being postmenopausal and not taking HRT at diagnosis). The results of the sexual satisfaction model in sample 2 are shown in the last column of Table 5. This model accounted for slightly more (29% v 27%) of the variance in the sexual satisfaction score and had two predictors in common with the model developed in sample 1. These were having a partner with sexual problems (less satisfaction) and having better dyadic adjustment (greater satisfaction). Several additional predictors were identified in this second sample and included ethnicity (women in the "other" category—who were neither African-American nor white—reporting greater satisfaction than white women), currently taking tamoxifen (less sexual satisfaction), having a new partner (greater satisfaction), and having a higher mental health score (greater sexual satisfaction). It is interesting that in this sample the following variables were not significant predictors: age-partner problem interaction, having had a mastectomy without reconstruction, body image, and having stopped menstruating or having HRT discontinued at the time of diagnosis.
Evaluation of the Multivariable Regression Models Using Alternative Methods The shaded boxes in Table 5 indicate variables that were selected for inclusion in the respective models by both data-driven techniques. For all three dependent measures, the strong relationships we found persisted from one sample to the next and were detected by two different model selection methodologies. In the case of sexual interest, the roles of mental health and body image were clearly established. Vaginal dryness was by far the strongest predictor of sexual dysfunction. In the case of sexual satisfaction, the importance of the partner relationship and the partner's sexual health was also strong and clear.
Sexual health in chronic disease is a relatively understudied area.35,38 We believe that this is one of the first studies to develop and evaluate a comprehensive framework for understanding sexual health in women after a breast cancer diagnosis. The major strengths of the study are the large number of subjects from two metropolitan areas, the development of multivariable models in one sample with validation in a second, independent sample, and the relatively large amount of variance in sexual interest, dysfunction, and satisfaction explained by the predictive models. Below we discuss the following implications of this research: What are the most important predictors of sexual health in breast cancer survivors and are any of them modifiable? How do these findings compare to results from relevant samples of healthy women? How should clinicians and researchers use this information? In this study, we have demonstrated that for sexually active breast cancer survivors in a partnered relationship, among the most important and consistent predictors of sexual health are the presence or absence of vaginal dryness, emotional well-being, body image, the quality of the partnered relationship, and whether or not the woman's partner has sexual problems. These variables were consistent across two independent samples and contribute to models that explain about one third of the variance in sexual interest, dysfunction, and satisfaction. Importantly, and consistent with our prior work in a different sample of breast cancer patients,2 the type of breast cancer surgery (eg, use of breast-conserving treatment) was not predictive of sexual health after breast cancer when mediating variables were controlled in the analysis. In examining the variables that were predictors of sexual health, we must ask ourselves whether any are potentially mutable and what interventions might be entertained to improve sexual health in these breast cancer survivors. Highest on the list is vaginal dryness, for which better medical remedies are needed for use in this population. Vaginal moisturizers and lubricants39 may be useful and were used by many women in the study; however, for many women they do not provide the relief that estrogen can provide for this critical symptom. Although the use of systemic estrogen is usually proscribed in this patient population,17 many survivors may wish to consider topical estrogen therapy as an alternative. Newer delivery devices, such as the estradiol-releasing silicone vaginal ring Estring (Pharmacia & Upjohn, Inc, Uppsala, Sweden) are thought to have a lower risk of systemic hormone absorption40 and may be acceptable for this patient population. Physicians and their patients may wish to choose this approach to treatment of sexual dysfunction, and this may be sufficient for many breast cancer survivors. Other mutable factors identified in the models are emotional well-being and the quality of the partnered relationship. Both of these may be addressed successfully as part of individual or couples therapy. Identification and treatment of individuals who are distressed may be a key to helping improve sexual health. Finally, with the advent of therapies now available to assist with male sexual dysfunction,41 it may be possible to address the sexual problems of the woman's partner, thus improving couples' sexual relationships. Not surprisingly, the quality of the partnered relationship (dyadic adjustment) was one of the most important predictors of sexual satisfaction in the two samples of breast cancer survivors. In addition, the presence of sexual problems in the partner contributed further explanatory power to the prediction of patient satisfaction. Addressing these intimacy and relationship issues would likely contribute to improvements in sexual satisfaction, even in those individuals whose sexual interest and dysfunction scores are only modestly diminished. Conversely, women with good quality partnered relationships may fare better than women with poor relationships when the level of sexual dysfunction is high due to treatment toxicity or a premature menopause syndrome. In our previous evaluation of the entirety of sample 1, including sexually active and inactive women,10 we observed relative stability in sexual activity in the post–breast cancer diagnosis period. That is, only 8.9% of women who were sexually active at breast cancer diagnosis were no longer active at the time of the survey; conversely, 3.8% of women who were sexually inactive at breast cancer diagnosis were active at the time of the survey. This suggests that pre-existing patterns of sexual behavior are likely to influence postdiagnosis activities and that for individuals for whom an active sex life is important, it will be maintained. How do these results compare to other samples of healthy women? First, about 58% of the breast cancer survivors who we studied were sexually active and in a partnered relationship. These results are quite similar to other studies of healthy women, with current sexual activity reported in 64% of postmenopausal women in one study22 and in 65% of healthy high-risk women participating in the Breast Cancer Prevention Trial.25 These latter rates did not control for partnership status, as in this study. Therefore, the rates of sexual activity (generally thought of as intercourse) among breast cancer survivors are similar to those in healthy women. Beyond simple rates of various sexual activities and behaviors,42 there are few studies that have measured sexual functioning and satisfaction in healthy women. The Massachusetts Women's Health Study is a population-based, prospective, longitudinal study of healthy women aged 45 to 55 years who were recruited in 1992 and were followed over a period of time.43 Some sexual functioning data from this study are available for a small sample of 353 white women, and the results in these women have been described in comparison to a similar cohort of men. The results reported to date are primarily descriptive and are thus not comparable to the data available in our breast cancer survivor sample. A more relevant sample of healthy women are those who were recruited to participate in the Postmenopausal Estrogen Progesterone Intervention (PEPI) trial,22 a randomized, double-masked trial investigating the physiologic benefits and risks of HRT in postmenopausal women aged 45 to 64 years. The PEPI trial used an extensive battery of measures that were similar to those used in our study to evaluate quality of life, sexual functioning, and symptoms, including a common measure of sexual functioning.34 The results from the Watts scale in our breast cancer survivors are similar to those reported in the baseline data from the healthy women participating in the PEPI trial.9,10 In the PEPI trial sample, Greendale et al developed a model of sexual health using a range of predictor variables, some of which overlap with those used in our study. Although vaginal dryness was less frequently reported in the PEPI trial sample (36% of those who were sexually active, compared with about 55% in our samples of breast cancer survivors), vaginal dryness was still a significant predictor of overall sexual functioning, as well as of desire, arousal, and satisfaction. The measures of emotional well-being used in the PEPI study were somewhat different, yet they were also important predictors of overall sexual functioning and satisfaction, as measured with different dependent variables. Thus, it seems that many of the significant predictors found in our model are common to healthy women whose sexual health has been assessed in a similar way. As with many studies, this research has raised as many questions as it has potentially answered. We are encouraged by the consistency with which our conceptual framework and statistical models have measured important variables that are significantly associated with sexual health in breast cancer survivors. The validation in a second large sample with multiple statistical approaches is reassuring. Nevertheless, it will be important to conduct prospective, longitudinal studies to increase our understanding about the relationships among the predictor variables. For example, what aspects of breast cancer treatment lead to vaginal dryness? Is it the absence of HRT, the induction of premature menopause, the direct effects of chemotherapy on the vaginal epithelium, or an interaction of all of these factors? Furthermore, are there interventions for vaginal dryness, emotional well-being, and partner relationships that can significantly improve sexual health in breast cancer survivors? Do prediagnostic, generalized attitudes about one's sexuality, such as sexual self-schema, predict which survivors will be most likely to be troubled by sexual difficulties following breast cancer, as Andersen et al44 have found for gynecologic cancer patients? Finally, who is really troubled by these changes in sexual health? Is it only a few among the survivor population or is it all? We hope that these and other questions will be answered by the research stimulated by this report.
We are grateful to the many physicians and patients who have supported our research in Los Angeles and Washington, DC. Supported by grant no. R01 CA63028 from the National Cancer Institute
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Copyright © 1999 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
