Satisfaction with ovarian carcinoma risk-reduction strategies among women at high risk for breast and ovarian carcinoma†‡
Presented at the 44th Annual Meeting of the American Society for Clinical Oncology, Chicago, Illinois, June 1-5, 2007.
See editorial on pages 2588–9, this issue.
Women who are at high risk for breast and ovarian cancer have 2 major management options to reduce their risk of ovarian cancer: periodic screening (PS) or risk-reducing salpingo-oophorectomy (RRSO). Little is known regarding patient satisfaction levels with risk-reduction strategies. Thus, the authors sought to determine levels of patient satisfaction with PS versus RRSO and to identify factors that may influence satisfaction.
As part of a larger study, women who received testing for the breast cancer genes BRCA1 and BRCA2 were sent a follow-up questionnaire packet to explore issues related to cancer risk reduction. The authors report on the results from a variety of validated instruments, including the Satisfaction With Decision (SWD) scale, focused on the choice between PS and RRSO.
In total, 544 surveys were mailed, and 313 responses were received (58%). The overall satisfaction rate among respondents was high. The median SWD score was significantly higher in the RRSO group compared with the PS group (P < .001). BRCA mutation carriers had higher median SWD scores regardless of management type (P = .01). Low satisfaction scores were associated with high levels of uncertainty and the perception that the decision between PS and RRSO was difficult to make (P = .001). Satisfaction was unrelated to demographics, clinical factors, or concerns of cancer risk.
In the current study, the majority of women who were at high risk for breast and ovarian cancer were satisfied with their choice of risk-reduction strategy. Difficulty with decision making was associated with lower satisfaction levels. Improved education and support through the decision-making process may enhance overall levels of satisfaction. Cancer 2011. © 2010 American Cancer Society.
In 2009, ovarian cancer was the second most common gynecologic cancer in the United States, with an estimated incidence of 21,550 cases.1 Of these new diagnoses, up to 10% were attributable to hereditary causes, including patients with known mutations in the breast cancer genes BRCA1 and BRCA2.2-4 The lifetime risk of ovarian cancer for the general population is approximately 1.5%.5 In contrast, BRCA mutation carriers have a lifetime risk of ovarian cancer that ranges between 16% and 50%, depending on the specific mutation.4, 6 In addition, women who have a strong family history of breast and/or ovarian cancer and test negative for a known genetic mutation are at increased risk for this disease.7 Thus, the identification and treatment of women who are at high risk for ovarian cancer provides a significant opportunity for cancer-prevention strategies.
Women at high risk for ovarian cancer are offered 2 major options for risk reduction: periodic screening (PS) or risk-reducing salpingo-oophorectomy (RRSO). PS consists of biannual pelvic examination with transvaginal ultrasound and serum cancer antigen 125 (CA 125) determination. To date, the efficacy of this risk-reduction strategy has not been clearly demonstrated.8 RRSO is a surgical procedure that involves the removal of both ovaries and fallopian tubes, and it has demonstrated a definitive impact on cancer risk reduction. In general, RRSO provides an average ovarian cancer risk reduction between 80% and 96% and an additional breast cancer risk reduction between 50% and 60%.9-12 However, many women do not choose this option because of a desire for future fertility or concerns over the adverse effects of early oophorectomy, such as menopausal symptoms.
Thus, an exploration of the issues of quality of life and satisfaction among women who undergo RRSO is paramount. Current literature indicates that overall quality of life is quite similar among high-risk patients regardless of their choice of risk-reduction strategy (PS vs RRSO).13, 14 However, conflicting data have demonstrated that, despite reports of equivalent overall satisfaction, patients who received PS had higher levels of regret compared with patients who underwent RRSO.14 These data reveal a pressing need for the use of a validated instrument to assess patient satisfaction with risk-reduction strategy. Previously, our group published an article on the clinical factors associated with choosing a risk-reduction strategy among women with known positive BRCA mutation status and among all women who were tested for BRCA mutations at our institution.15, 16 The information from those studies was used to design the current study.
The assessment of patient satisfaction with PS versus RRSO is an area that may provide necessary information to appropriately guide and counsel women at high risk for breast and ovarian cancer regarding their risk-reduction options. To our knowledge, no study has directly measured satisfaction with ovarian cancer risk-reduction strategies using a validated instrument. The Satisfaction With Decision (SWD) scale addresses 6 key aspects of decision-making and has been validated to assess overall satisfaction with medical decisions.17 Therefore, we surveyed a cohort of women who were at high risk for breast and ovarian cancer to determine the level of satisfaction with risk-reduction management strategies and to identify the factors associated with level of satisfaction.
MATERIALS AND METHODS
Women who are at high risk for hereditary breast and ovarian cancer are referred to genetic counselors at The University of Texas M. D. Anderson Cancer Center (MDACC) who specialize in hereditary cancers unique to the female population. These women are identified based on established referral criteria from the Society of Gynecologic Oncologists (Table 1).18 If women choose to pursue genetic testing, then they receive extensive pretest and post-test counseling. Our group conducted a follow-up study to assess quality-of-life concerns and satisfaction with risk-reduction strategy in women who previously underwent genetic testing for high risk of developing breast and ovarian cancer as part of a multidepartmental effort among members of the Departments of Gynecologic Oncology, Breast Medical Oncology, and Behavioral Science at MDACC.
Table 1. Society of Gynecologic Oncologists Criteria for BRCA mutation testinga
|Personal history of both breast and ovarian/primary peritoneal/fallopian tube cancer|
|Women with ovarian cancer who have a close relative (first-degree, second-degree, or third-degree relative) with breast cancer at age ≤50 y or with ovarian cancer at any age|
|Women of Ashkenazi Jewish ancestry with ovarian cancer at any age|
|Women with breast or ovarian cancer at any age who have ≥2 close relatives with breast cancer at any age, particularly if at least 1 breast cancer at age ≤50 y|
Approval for this study was obtained through the institutional review board at our institution. Women who underwent testing for BRCA1 or BRCA2 mutations at our institution or who attended genetic counseling for a known mutation from January 1997 through July 2005 were identified through the MDACC Tumor Registry and Genetics Database. We created a questionnaire packet to ascertain demographic and clinical information as well as quality of life and beliefs regarding issues pertinent to women at high risk for developing breast and ovarian cancer. These questionnaires provided patients with a variety of statements to describe their perceptions about screening, chemoprevention strategies, and risk-reducing surgery using Likert-based scales. Several validated instruments to address health and well being, cancer-related anxiety, and satisfaction also were included. Additional demographic and clinical data were obtained from the electronic medical record and from genetic counseling charts.
The questionnaire packet was mailed to potential participants. Nonresponders received a follow-up telephone call 1 month after the initial mailing. A second mailing was performed at the 6-month time point and was followed by a final telephone call 1 month after the second mailing. After 1 year, participants who did not return the questionnaire were classified as nonresponders. Women who returned surveys received a $10 gift card to a book store for their participation. All participants provided implied written consent based on survey completion.
We report the data from women who chose between the risk-reduction strategies of PS and RRSO. Women who had a prior diagnosis of ovarian cancer or who underwent oophorectomy for benign indications were excluded. Women who did not complete the SWD were ineligible, because this was our primary outcome measure.
The Cancer Worry Scale (CWS) was used to determine the level of anxiety related to developing cancer.19 This instrument consists of 4 statements evaluated on a Likert-type scale addressing frequency of cancer-related worry, impact of worry on mood and functioning, and overall level of cancer-related worry. Scores range from 1 to 16, with higher scores indicating higher level of worry.19 The CWS was used to assess anxiety associated with development of both ovarian cancer and breast cancer, because it is known that RRSO has an impact on the risk of both cancer types.
We also included the Endocrine Subscale of the Functional Assessment of Cancer Therapy (FACT-ES), a validated tool that is used to assess symptoms commonly experienced by women after natural, surgical, or medically induced menopause.20 This scale consists of 18 items that address menopausal and sexual symptoms, including hot flashes. Low scores indicate higher levels of symptoms in a range from 0 to 72.20
Sexual function was measured using the Sexual Activity Questionnaire, a validated instrument that assesses relationship status, reasons for sexual inactivity (if applicable), and a 10-item scale that describes sexual functioning in terms of activity (habit), pleasure, and discomfort.21 High scores for pleasure reflect high satisfaction, and high scores for discomfort indicate higher levels of dryness and pain.21
The modified Body Image Scale is a 4-item scale that includes questions related to body appearance and scarring.22 It has been validated for use in patients with cancer who have undergone surgery that involves major alteration of body image. This includes loss of a body part or disfigurement that may occur with surgeries, such as mastectomy,22 colorectal surgery,23 and hysterectomy.24 Scores range from 0 to 16, with lower scores indicating lower levels of distress about body image.22
The Multidimensional Impact of Cancer Risk Assessment (MICRA) questionnaire was developed to address distress after the receipt of genetic testing results.25 This validated scale includes a variety of questions exploring the psychosocial issues that arise after genetic testing. For the purposes of the current study, we examined the 3 subscales within the general scale that cover specific issues regarding distress, uncertainty, and positive experiences after genetic testing. The distress, uncertainty, and positive experiences subscales are scored from 0 to 30, from 0 to 45, and from 0 to 20, respectively. It is noteworthy that, for the distress and uncertainty scales, higher scores represent a more negative impact of the genetic testing result. Conversely, in the positive experiences subscale, higher scores represent a positive experience after the disclosure of genetic testing results.25
Finally, patients without a diagnosis of ovarian cancer were asked to complete the SWD for their current ovarian cancer risk-reduction strategy: PS or RRSO. This validated scale consists of 6 questions that address the components of satisfaction and decision-making and has a score range from 6 to 30. Higher scores indicate higher levels of satisfaction with decision. The SWD underwent initial validation in a population of perimenopausal women who were facing the decision of whether or not to take hormone-replacement therapy.17 This scale has been used to measure satisfaction in patients who were receiving treatment for depression26 and prostate cancer.27 The SWD also has been used to predict compliance in patients who underwent head and neck surgery.28 In the current study, the SWD was used to determine overall patient satisfaction with risk-reduction strategy.
The SWD score was compared between the PS and RRSO cohorts. In addition, analyses of those patients who had low satisfaction scores were performed to determine the impact of demographics, clinical factors, or personal beliefs on satisfaction level. We also evaluated the association between satisfaction level and the quality-of-life measures described above.
A low satisfaction score was defined as a score in the lowest 10th percentile, and a high satisfaction score was defined as a score in the remaining 90th percentile. These levels were chosen based on the median value of the SWD scale within our population. To our knowledge, there is no known cutoff level for satisfaction based on existing literature that incorporates the SWD scale. Group comparisons of categorical variables were evaluated with chi-square tests and Fisher exact tests. Group comparisons of continuous variables were evaluated using t tests and Mann-Whitney tests. Linear regression analyses were performed to determine the impact of key variables on satisfaction score. All analyses were performed using SPSS software (version 17.0; SPSS, Inc., Chicago, Ill). A P value <.05 was considered statistically significant.
The questionnaire was mailed to 544 eligible women. Three hundred thirteen women (58%) responded within the study time frame of 12 months. Of those, 131 women (42%) were excluded from the current study because of a history of prior oophorectomy or an incomplete SWD score, leaving 182 (58%) valid questionnaires for the current analysis. The patients who were excluded from our analysis had an older median age and more commonly were parous and menopausal. Otherwise, there were no significant differences between the patients who were included in the analysis and those who were excluded in terms of race, education level, insurance status, or marital status.
A comparison of the key demographic and clinical features between the 2 risk-reducing cohorts is presented in Table 2. It is noteworthy that women in the PS group were significantly younger than women in the RRSO group (47.2 years vs 50.1 years; P = .02) and were less likely to be menopausal (48.3% vs 64.9%; P = .05). In addition, patients who underwent RRSO for ovarian cancer risk reduction were significantly more likely to have a BRCA mutation (53.2% vs 22.5%; P < .001) than patients who received PS. Women who underwent RRSO did so a median of 25.2 months before completing our questionnaire packet. Women in the study population received genetic testing results a median of 21.2 months before completing the study packets.
Table 2. Demographic and Clinical Characteristics of the Study Population (N = 182)
|Age: Median [range], y||47.2 [22-85]||50.1 [40-76]||.02|
| White||97 (80.8)||55 (88.7)||.40|
| Hispanic||13 (10.8)||4 (6.5)|| |
| Asian||7 (5.8)||2 (3.2)|| |
| Black||3 (2.5)||0 (0)|| |
| Other||0 (0)||1 (1.6)|| |
|Married/living with partner||96 (80)||46 (74.2)||.37|
| Some high school||3 (1.7)||0 (0)||.56|
| High school graduate/GED||13 (7.6)||5 (7.4)|| |
| Some college/technical school||44 (25.6)||14 (20.6)|| |
| College graduate/higher degree||112 (65.1)||49 (72.1)|| |
|Ashkenazi Jewishc||17 (14.5)||11 (18.6)||.48|
|BRCA1/2 mutation||27 (22.5)||33 (53.2)||<.001|
|Any family history|
| Breast cancer||99 (82.5)||55 (88.7)||.27|
| Ovarian cancer||39 (32.5)||24 (38.7)||.40|
|Personal history of breast cancer||89 (74.2)||48 (77.4)||.64|
Overall satisfaction levels among all women at who were high risk for breast and ovarian cancer were high in this study, and the median SWD score was 29 (range, 14-30). Women who chose RRSO as their risk-reduction strategy were more satisfied compared with women who chose PS (median SWD, 30.0 vs 26.5; P < .001). BRCA-positive women also demonstrated higher satisfaction levels regarding their decision compared with their BRCA-negative counterparts regardless of risk-reduction strategy (median SWD, 30 vs 28; P = .01). Further comparison of the SWD scale between the PS and RRSO groups revealed that more women in the PS group were ambivalent in terms of each component of satisfaction with risk-reduction strategy (Table 3).
Table 3. Ambivalence on the Satisfaction With Decision Scale Based on Risk-Reduction Strategy
|I am satisfied that I was adequately informed about the issues important to my decision||6 (5)||4 (6.5)||.74|
|The decision I made was the best decision possible for me personally||19 (15.8)||1 (1.6)||.002|
|I am satisfied that my decision was consistent with my personal values||17 (14.2)||0 (0)||.001|
|I expect to successfully carry out (or continue to carry out) the decision I made||19 (15.8)||0 (0)||<.001|
|I am satisfied that this was my decision to make||11 (9.2)||0 (0)||.02|
|I am satisfied with my decision||14 (11.7)||1 (1.6)||.02|
An analysis was performed to determine whether any demographic, clinical, or personal factors were associated with lower satisfaction levels (ie, SWD scores less than the 10th percentile). There were no demographic or clinical features associated significantly with satisfaction in this study, including race, parity, menopausal status, or marital status at the time of questionnaire completion (data not shown). After adjusting for age, parity, and risk-reduction strategy, the only significant predictor of a high level of satisfaction with decision was RRSO as the risk-reduction strategy (β = 3.1; 95% confidence interval, 1.86-4.33; P < .001).
In the questionnaire, patients were given an opportunity to express feelings and perceptions regarding their BRCA diagnoses and their options for risk-reduction strategies. The complete list of statements provided is available in Table 4. It is noteworthy that low satisfaction scores were associated with the patient's perception that the decision between RRSO and PS was difficult to make (Table 4).
Table 4. Association of Personal Perceptions Regarding Risk-Reduction With Level of Satisfaction With Risk-Reduction Strategy
|“It is hard for me to decide whether I should do ovarian cancer screening or have prophylactic (preventive) surgery to remove my ovaries”||n = 157||8 (61.5)||25 (17.4)||.001|
|“Having my ovaries removed is the only way to reduce my worry of developing breast cancer”||n = 137||2 (20)||12 (9.4)||.27|
|“The best way for me to lower my risk of getting breast cancer is to have prophylactic surgery to remove my ovaries”||n = 139||3 (30)||51 (39.5)||.74|
|“Prophylactic surgery to remove the ovaries is too drastic a measure to prevent cancer”||n = 153||0 (0)||20 (14.4)||.22|
|“I avoid having ovarian cancer screening because the procedures are painful”||n = 162||0 (0)||2 (1.4)||1.0|
|“I am reluctant to undergo ovarian cancer screening because the procedures are embarrassing”||n = 169||0 (0)||4 (2.7)||1.0|
|“It is difficult to get ovarian cancer screening because my insurance may not pay for the tests.” (n = 146)||n = 146||0 (0)||19 (14.8)||.13|
|“Having ovarian cancer screening is hard for me because I worry about getting abnormal results”||n = 164||2 (11.1)||24 (16.4)||.74|
We also assessed the impact of anxiety about future risk of cancer on patient satisfaction with risk-reduction strategy. There was no association between the level of satisfaction and the degree of breast or ovarian cancer-related worry (Table 5). On the basis of our analysis of the MICRA instrument, stress level after genetic test disclosure was not associated with low satisfaction. However, higher levels of uncertainty after genetic test result disclosure were associated with lower levels of satisfaction (P = .02) (Table 5).
Table 5. Association of Quality-of-Life Instrument Scores With the Level of Satisfaction With Risk-Reduction Strategy
|Ovarian Cancer Worry score (n = 175)||6.0||6.0||.10|
|Breast Cancer Worry score (n = 175)||8.0||7.5||.93|
|Functional Assessment of Cancer Therapy-Endocrine (n = 181)||60.0||59.0||.71|
|Sexual Activity Questionnaire|
| Pleasure (n = 130)||8.0||10.0||.25|
| Discomfort (n = 127)||3.5||3.0||.44|
| Habit (n = 119)||1.0||1.0||.37|
|Body Image Scale (n = 144)||8.0||4.0||.05|
| Distress (n = 176)||1.0||2.0||.91|
| Positive experiences (n = 175)||7.0||6.0||.68|
| Uncertainty (n = 173)||16.5||12.0||.02|
Given the impact of sexual functioning and endocrine-related symptoms on quality of life reported in previous studies of women at high risk for breast and ovarian cancer,13, 29-31 we assessed the association between satisfaction level and median scores from the Sexual Activity Questionnaire (SAQ) subscales, the FACT-ES, and the Body Image Scale (BIS) (Table 5). None of the SAQ subscale scores were associated significantly with satisfaction level. In addition, patients who had low SWD scores had FACT-ES scores similar to the those of patients who had high SWD scores. Patients who had lower satisfaction levels did have a higher median score on the BIS, indicating higher levels of distress with respect to body image (8 vs 4; P = .05).
The main finding from our study was that women who were at high risk for breast and ovarian cancer were very satisfied with their choice of risk-reduction strategy. To date, a review of the literature reveals that our study is the first to demonstrate this with a validated instrument that measures satisfaction. It is noteworthy that the patients who chose RRSO demonstrated higher levels of satisfaction compared with the patients who chose PS. High satisfaction also has been demonstrated in several studies of women who underwent mastectomy for breast cancer risk reduction.32
Lower satisfaction levels among women who choose PS compared with women who choose RRSO may be caused in part by the difficulty of decision-making with regard to a high-risk management strategy. Certainly, RRSO is the more definitive option and allows no further room for ambivalence or conflict. RRSO, as a surgical procedure, offers a permanent outcome that cannot be reversed. In contrast, women who receive PS theoretically still can opt for RRSO at some point in the future. The possibility of being able to switch from PS to RRSO may introduce some level of uncertainty in women who choose PS, possibly contributing to less overall satisfaction in knowing that a woman has made the “correct choice.” Response shift, or the change in one's internal evaluation of well being, may be another reason for high satisfaction levels in women who chose RRSO. It makes sense intuitively that, once a woman has undergone RRSO, her thinking would “recalibrate” to accept and validate her choice of risk-reducing strategy.33
Women in the low-satisfaction group also reported higher levels of uncertainty after the disclosure of genetic test results on the MICRA. The uncertainty subscale of the MICRA covers a broad range of topics, including uncertainty about the risk of cancer, the impact of genetic test results on family, and frustration regarding uncertain guidelines for cancer risk reduction.25 Patients in the PS group demonstrated conflicted feelings about their choice of risk-reduction strategy and lack of a definitive plan of action. The finding of higher levels of ambivalence on each component of the SWD scale among women who chose PS suggests that these women still may be considering their risk-reduction options.
Furthermore, BRCA-positive respondents had higher levels of satisfaction than respondents who were BRCA negative. If uncertainty is a cause for low satisfaction levels, then the higher satisfaction observed among BRCA mutation carriers may be attributed to the clear set of guidelines for risk reduction provided to this population. Conversely, women with uninformative negative BRCA results are left without a concrete explanation for their high-risk status. This result is by no means a definitive negative, and women with this result often are left with no clear idea whether they are free of risk or are high-risk carriers of a mutation not yet discovered. Thus, they may choose PS as a risk-reduction strategy but experience uncertainty regarding their decision.
Quality-of-life assessment after the choice of a risk-reduction strategy has focused mainly on the sequelae of RRSO. In general, RRSO appears to have a positive impact on cancer-related anxiety and the overall perception of risk and a negative impact on sexual functioning and endocrine-related symptoms.13, 29-31 Therefore, we theorized that the higher satisfaction levels observed in patients who chose RRSO may be related to decreased levels of cancer-related anxiety. It is noteworthy that this was not the case in our patient population. Furthermore, the adverse effects associated with RRSO, including endocrine-related symptoms and sexual dysfunction, were not associated significantly with level of satisfaction. Our data suggest that women who chose RRSO were willing to accept the trade-offs of the increased likelihood of experiencing endocrine-related symptoms and sexual dysfunction with a decreased risk of developing ovarian cancer.
We also hypothesized that the factors associated with regret after tubal sterilization would be associated with regret after surgical risk reduction. On the basis of literature from the United States, young age is a key factor implicated in regret after sterilization.34-36 Therefore, we believed that younger women who had not yet completed childbearing would have lower satisfaction levels with RRSO. However, this theory was not supported by our data, because the median age of women who underwent RRSO was older, indicating that patients had completed childbearing before their surgery. In addition, after adjusting for age, parity, and type of risk-reduction strategy, only RRSO was associated with higher satisfaction levels.
Overall, there is a paucity of data addressing quality of life and satisfaction in this group of patients. A prospective study comparing the quality of life of 38 patients who underwent RRSO with that of 37 patients who received PS revealed decreased physical and sexual functioning at the 1-month time point. This difference was negligible at the 6-month time point.37 The largest study comparing quality of life between these 2 risk reduction strategies revealed no difference in overall quality of life between RRSO and PS respondents at a nonspecified time point. Despite reporting decreased sexual functioning and increased vasomotor symptoms, 86% of women in that study stated that they would choose RRSO for risk reduction if given the choice again.13 This led us to hypothesize that there were factors other than sexual functioning and vasomotor symptoms that had an impact on satisfaction with the choice of a risk-reduction strategy.
In 2001, Swisher and colleagues reported on patient satisfaction and regret associated with the choice of management strategy among 60 women who were at high risk for ovarian cancer.14 To our knowledge, the Swisher et al interview study and our study are the only 2 published studies that have compared satisfaction between the 2 risk-reduction strategies. In their study, Swisher et al observed that 28 of 30 women (93%) who chose RRSO were satisfied compared with 27 of 30 women (90%) who chose PS as their risk-reduction strategy. However, that study also demonstrated that only 2 women (7%) in the RRSO group expressed regret about their decision, whereas 15 women (50%) expressed regret regarding the decision to pursue PS.14 It is interesting to note that no validated instrument was used for the measurement of satisfaction. In the study by Swisher et al, regret appeared to be related to inconsistent recommendations for screening. This correlates well with our finding that uncertainty after the disclosure of genetic test results was associated with low levels of satisfaction with risk-reduction strategy.
The strengths of our study include the use of a validated instrument to measure satisfaction, a large sample size, and an excellent response rate. In addition, we are fortunate to have an excellent genetic counseling department, which provided consistent information to all patients regarding their risk-reduction options. However, our study is limited because of a lack of baseline data regarding anxiety and baseline functioning. In addition, data collection was not conducted prospectively, and our data represent the symptoms and feelings of patients at a single point in time. Despite these issues, our findings reveal a potential opportunity to intervene at the time a woman makes her decision between risk-reduction strategies by providing the information and support necessary to ensure patient satisfaction with the choice of risk-reduction strategy.
In conclusion, the current study demonstrates that there is a subset of women who are unsatisfied with their decision to pursue PS for risk reduction. Prospective studies and focus groups will be essential to determine the optimal method for improving patient satisfaction levels after risk-reduction management decision.
CONFLICT OF INTEREST DISCLOSURES
This work was funded by National Institutes of Health Training Grant 5T32CA10164202 (to S.N.W. and R.A.L.).