The Impact of Mastectomy Type on the Female Sexual Function Index (FSFI), Satisfaction with Appearance, and the Reconstructed Breast’S Role in Intimacy

Breast Cancer Res Treat DOI 10.1007/s10549-017-4174-z

CLINICAL TRIAL

The impact of mastectomy type on the Female Sexual Function Index (FSFI), satisfaction with appearance, and the reconstructed breast’s role in intimacy

1 2 3 4 1 1 K. Rojas • M. Onstad • C. Raker • MA Clark • A. Stuckey • J. Gass

Received: 20 February 2017 / Accepted: 22 February 2017 Ó Springer Science+Business Media New York 2017

Abstract group indicated sexual dysfunction. After adjusting for Background As mastectomy rates increase and overall receipt of chemotherapy and/or radiation, NSM had the survival for early breast cancer improves, a better under- lowest median desire score. There was a trend for the NSM standing of the long-term consequences of mastectomy is group to be the least satisfied with postoperative appear- needed. We sought to explore the correlation of specific ance, but also more likely to report that the chest was mastectomy type with the Female Sexual Function Index ‘‘often’’ caressed during intimacy. However, nearly 40% of (FSFI), body image satisfaction, and the reconstructed the NSM group reported that caress of the reconstructed breast’s role in intimacy. breast was unpleasant. Methods This study is a secondary analysis of a cross- Conclusion NSM offers patients the greatest opportunity sectional survey including a retrospective chart review. for preservation of their native skin envelope and poten- Patients at least one year from primary surgery were tially enhanced cosmetic outcome, but our results did not invited to complete the survey between 2012 and 2014. demonstrate superior sexual function or body image out- Baseline characteristics and survey responses were com- comes in this group. By highlighting surgical consequences pared between three mastectomy groups: total/modified of mastectomy preoperatively, surgeons may better set radical (TMRM), skin-sparing (SSM), and nipple-sparing realistic patient expectations regarding both aesthetic and (NSM). All patients underwent reconstruction. functional outcomes after breast cancer surgery. With Results Of 453 invited, 268 (59%) completed the survey. clearer expectations, patients will have a better opportunity Sixty underwent mastectomy with reconstruction: 16 for improved surgical decision-making. (27%) TMRM, 36 (60%) SSM, and 8 (13%) NSM. There were no significant differences in median total FSFI scores Keywords Breast cancer Á Mastectomy Á Sexuality Á between groups, yet median FSFI scores for the NSM Survivorship Á Intimacy Á Nipple sparing Á Mastectomy

& K. Rojas Background [email protected]

1 Despite long-term results from randomized clinical trials The Program in Women’s Oncology, Women & Infants demonstrating no overall survival advantage of mastec- Hospital Breast Health Center, Warren Alpert School of Medicine/Brown University, Providence, RI, USA tomy over breast conservation therapy, an increasing proportion of patients with early-staged breast cancer opt for 2 Department of Gynecologic Oncology, MD Anderson Cancer Center, Houston, TX, USA mastectomy [1–3]. A recent population-based California Cancer Registry study showed that the rate of bilateral 3 Division of Research, Women and Infants’ Hospital of Rhode Island, Providence, RI, USA mastectomy increased from 2 to 11% between 1998 and 2011. The increase was greater among women less than 4 Center for Health Policy and Research, Department of Quantitative Health Sciences, University of Massachusetts 40 years, with the bilateral mastectomy rate rising from 4 Medical School, Worcester, MA, USA to 33% during that time period [4]. Disturbingly, when 123 Breast Cancer Res Treat patients opting for mastectomy were queried later regard- carcinoma in situ between 2000 and 2013; and all women ing motivators to contralateral prophylactic mastectomy were one year or more from primary surgery. Patients less (CPM), overall survival was listed as a contributing factor than 21 years of age and those not fluent in the English [5]. Nonetheless, data from the prophylactic surgical set- language were excluded. ting indicate that while most women are content with their This Institutional Review Board-approved cross-sec- choice, 27–30% voice feeling of loss of femininity and tional survey included a retrospective chart review of body image dissatisfaction [6]. participants. Surveys were collected at the time of office Women facing breast cancer diagnoses are confronted with visits as a part of cancer surveillance at a breast health unique psychosocial challenges. Contemporary data have center. For those who desired to complete the survey at demonstrated that breast cancer patients experience depression home, a stamped, self-addressed envelope was provided. and anxiety, alteration of femininity, and changes in self-per- All surveys were de-identified and linked to a password- ception of attractiveness [7–11]. Similarly, a significant pro- protected key to protect patient privacy. portion of patients experience a decline in parameters of sexual The questionnaire included the Female Sexual Function function after breast cancer including sexual interest, desire, Index (FSFI). The FSFI is a 19-item instrument that has and arousal, as well as breast sensitivity and pleasure [12]. been validated as a tool to measure sexual function among Studies have found that 33–78% of women report a negative women with cancer, and it has been recognized as the most impact on their sex life after a breast cancer diagnosis [8, 13]. frequently used tool to measure sexual function in this Sexual dysfunction in breast cancer survivorship has been population [24]. It assesses six domains of sexuality most strongly associated with the receipt of chemotherapy, including desire, arousal, lubrication, orgasm, satisfaction, which could be secondary to the chemotherapy’s known and pain. Sexual dysfunction has been identified as an FSFI hormonal disruptions or the connotation associated with the score\26.55, with higher scores indicating higher levels of receipt of chemotherapy itself [8, 14–16]. Studies have been sexual function. less clear about the impact of surgical modality on sexuality The FSFI portion of the analysis was limited to 43 in survivorship, although more recent studies suggest that patients who did not have 8 or more 0 or missing responses, breast conservation therapy may be less disruptive than thereby excluding those who were not likely to be suffi- mastectomy with or without reconstruction [17–21]. ciently sexually active for the FSFI to be a valid assessment Sexual intimacy has been found to help relieve the of sexual functioning, a method similar to those described burden of cancer diagnosis and treatment, and assist in the in a validation study by Baser [24]. recovery process [22]. However, little is known about the The questionnaire also contained seven investigator- effect of different surgical treatment strategies on a generated questions (see Fig. 1) similar to some used pre- patient’s perception of self, level of comfort in intimacy, viously by Rowland et al. which focused on themes such as and role of the treated and reconstructed breast in intimacy. satisfaction with chest appearance, comfort with their Didier et al. compared 310 women with nipple-areolar partner seeing the chest, and the role of the patient’s breast complex (NAC) preservation and 143 without successive in intimacy before and after surgery [25]. The importance NAC reconstruction and found that sparing of the NAC led of the treated breast in intimacy, as well as the patient’s to improved patient satisfaction, body image, and psy- perception of pleasure with stimulation or caress of the chosocial adjustment but a validated assessment tool of reconstructed breast was also assessed. All question sexual function was not employed [23]. Therefore, sexual responses used a Likert scale. function outcomes between three reconstructed mastec- Demographic information, medical history, tumor data, tomy groups: total/modified radical mastectomy (TMRM), and treatment course were collected by retrospective skin-sparing mastectomy (SSM), and nipple-sparing mas- chart review (see Table 1). Demographic information tectomy (NSM) need to be more clearly described. In this included age and BMI. Past medical history included the study, we sought to explore the impact of mastectomy type presence of cardiovascular disease, psychiatric diagnoses, on sexual function as measured by the Female Sexual and use of psychiatric medications at the time of survey Function Index (FSFI), satisfaction with appearance, and completion. Tumor data included tumor pathology, stage, the reconstructed breast’s role in intimacy. laterality, and receptor status. Treatment course included surgery type, timing of surgery, whether a prophylactic or therapeutic contralateral surgery was performed, Methods chemotherapy and endocrine therapy type, and reconstruction data. Patients were recruited for study participation from a single All statistical analyses were performed using Statistical institution between 2012 and 2014. Eligible patients Analysis System (SAS) version 9.3 (SAS institute, Cary underwent surgery for invasive breast cancer or ductal NC). Demographic information, tumor type, treatment 123 Breast Cancer Res Treat

1. How satisfied are you with the appearance of 5. During the past 4 weeks, how often was your your chest? chest caressed or otherwise sexually stimulated [] Very satisfied during sexual activity? [] Moderately satisfied [] Almost always or always [] About equally satisfied and dissatisfied [] Most times (more than half the time) [] Moderately dissatisfied [] Sometimes (about half the time) [] Very dissatisfied [] A few times (less than half the time) 2. How comfortable are you with your partner [] Almost never or never seeing your chest without clothing? [] Was not sexually active during the last 4 weeks [] Very comfortable [] Moderately comfortable Questions 6 and 7 are only for patients who have undergone [] About equally comfortable and uncomfortable lumpectomy or mastectomy with reconstruction. If you have [] Moderately uncomfortable undergone mastectomy alone without reconstruction, skip question 6 [] Very uncomfortable and 7. 3. How important of a role does your chest play in intimacy and sex for you? 6. How much is your treated breast a part of [] Very important intimacy for you? [] Somewhat important [] Very much a part [] Not very important [] Somewhat a part [] No role at all [] Not much of a part 4. How important of a role did your chest play in [] Not at all intimacy and sex for you before your surgery 7. How pleasurable is it to have your treated and treatment for breast cancer? breast caressed or stimulated? [] Very important [] Very pleasurable [] Somewhat important [] Moderately pleasurable [] Not very important [] Not pleasurable but not unpleasant [] No role at all [] Moderately unpleasant [] Very unpleasant

Fig. 1 Seven investigator-generated questions course, and survey responses between three mastectomy (TMRM), 36 (60%) skin-sparing (SSM), and 8 (13%) groups: TMRM, SSM, and NSM were compared. Survey nipple-sparing (NSM). responses were adjusted for the receipt of chemotherapy As shown in Table 1, the NSM group trended towards and/or radiation (with p value reported as pcr). Categorical being younger median age (46.5) versus TMRM (52.5) and variables were compared using Chi square or Fisher’s exact SSM (50.5) (p = 0.1). Related to this, the NSM group was test, and continuous variables were compared by Wilcoxon also more likely to be premenopausal (75%), versus rank-sum test or Kruskal–Wallis test. Comparisons were TMRM (25%) and SSM (50%) (p = 0.06). TMRM was adjusted for age group, menopausal status, or chemother- significantly more likely to have received chemotherapy apy using the Van Elteren test for continuous variables, and (81.3%) followed by SSM (47.2%) and NSM (25%) the Cochran–Mantel–Haenszel test for categorical vari- (p = 0.02). TMRM was also significantly more likely to ables. Two-tailed p-values less than 0.05 were considered have undergone radiation (62.5%), whereas 19.4% of SSM statistically significant. and no NSM patients underwent radiation (p = 0.001). There were no significant differences in BMI, history of cardiovascular disease, history of psychiatric diagnosis or Results use of psychiatric medication, tumor stage, receipt of bilateral surgery, or history of current or past endocrine Of 453 invited participants, 268 (59%) completed the therapy between groups. survey. Sixty patients underwent mastectomy with recon- There were no significant differences in postoperative struction: 16 (27%) total/modified radical mastectomy total median FSFI scores between groups (Table 2).

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Table 1 Mastectomy type Mastectomy type TMRM SSM NSM p-value group demographics Total 16 (26.7) 36 (60.0) 8 (13.3)

Age Median (range) 52.5 (40–71) 50.5 (30–74) 46.5 (36–56) 0.1 BMI \25 4 (26.7) 15 (41.7) 5 (62.5) 0.6 25–29 6 (40.0) 14 (38.9) 2 (25.0) 30? 5 (33.3) 7 (19.4) 1 (12.5) Menopausal status Premenopausal 4 (25.0) 18 (50.0) 6 (75.0) 0.06 Postmenopausal 12 (75.0) 18 (50.0) 2 (25.0) Cardiovascular disease Yes 4 (26.7) 10 (29.4) 0 (0) 0.3 History of psychiatric diagnosis No 14 (87.5) 27 (75.0) 8 (100) 0.6 Depression 1 (6.3) 7 (19.4) 0 (0) Unknown 1 (6.3) 2 (5.6) 0 (0) Current psychiatric medication use (n = 15) (n = 34) Yes 5 (33.3) 10 (29.4) 1 (12.5) 0.7 Bilateral cancer Yes 2 (12.5) 1 (2.8) 0 0.2 Tumor Stage Stage 0 (DCIS only) 2 (13.3) 8 (22.2) 1 (12.5) 0.8 Stage 1 7 (46.7) 17 (47.2) 4 (50.0) Stage 2 3 (20.0) 9 (25.0) 2 (25.0) Stage 3 2 (13.3) 1 (2.8) 1 (12.5) Stage 4 1 (6.7) 1 (2.8) 0 Bilateral surgery Yes 10 (62.5) 17 (47.2) 5 (62.5) 0.5 Contralateral prophylactic mastectomy Yes 9 (56.3) 16 (44.4) 4 (50.0) 0.8 History of chemotherapy Yes 13 (81.3) 17 (47.2) 2 (25.0) 0.02 History of radiation therapy Yes 10 (62.5) 7 (19.4) 0 0.001 Endocrine therapy Any current 6 (37.5) 20 (55.6) 6 (75.0) 0.2 Any current or prior 10 (62.5) 22 (61.1) 6 (75.0) 0.8 TMRM total/modiﬁed radical mastectomy, SSM skin-sparing mastectomy, NSM nipple-sparing mastectomy

However, NSM had a total median FSFI score meeting Turning to the investigator-generated questions, there criteria for sexual dysfunction (24.00). In regards to the was a trend for the NSM group to be the least likely to FSFI domains, NSM also had the lowest median desire report appearance satisfaction (50%) compared to TMRM score (2.40) (p = 0.03). This difference persisted when (68.8%) and SSM (66.7%) when controlling for receipt of controlling for receipt of chemotherapy and/or radiation chemotherapy and/or radiation (pcr = 0.1) (Table 3). A (pcr = 0.04). Additionally, women who underwent SSM greater proportion of NSM (25%) reported discomfort had a signiﬁcantly greater median sexual satisfaction score being seen by their partner compared to TMRM (12.5%) (5.20) than women who underwent TMRM (4.40) or NSM and SSM (22.2%), though non-signiﬁcant. The role of the

(4.80) (p = 0.005, pcr = 0.002). chest in sex and intimacy non-signiﬁcantly declined for all

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Table 2 FSFI results among Variable TMRM SSM NSM p-value mastectomy types Total, n (row %) 10 26 7 FSFI total score (n = 9) (n = 21) (n = 6) Median (range) 27.10 (16.10–30.60) 30.20 (9.20–36.00) 24.00 (17.40–31.90) 0.2 FSFI-desire (n = 10) (n = 25) (n = 7) Median (range) 3.60 (1.20–4.80) 3.60 (1.20–6.00) 2.40 (1.20–4.20) 0.03 FSFI-satisfaction (n = 9) (n = 26) (n = 7) Median (range) 4.40 (2.80–5.60) 5.20 (2.40–6.00) 4.80 (1.20–5.20) 0.005 TMRM total/modified radical mastectomy, SSM skin-sparing mastectomy, NSM nipple-sparing mastectomy mastectomy groups pre- to postoperatively. There was a femininity in 310 nipple-sparing mastectomy patients and trend for NSM to more frequently report that, postopera- 143 patients who did not retain their native nipple-areolar tively, their chest was ‘‘often’’ caressed or stimulated complex. Although the patients in both Didier’s and the during sexual activity (66.7%) when compared to SSM present study were similar in age, menopausal status was (48.2%) and TMRM (15.4%) (p = 0.06), which was sig- not reported by Didier and colleagues. The surgical groups nificant when controlling for receipt of chemotherapy and/ in Didier’s study were not stratified by stage but rather or radiation (pcr = 0.04). However, 37.5% of NSM candidacy for NSM based on tumor location, also limiting described stimulation or caress of their reconstructed breast appropriate comparison. In the Didier study, patients as unpleasant compared to no TMRM and 24.2% SSM. without a NAC reported a greater decrease in femininity, (p = 0.1). appearance dissatisfaction postoperatively, and discomfort being seen by their partner when compared to the NSM group, distinct from our results. Furthermore, the Didier Discussion results suggested that NAC preservation yielded a higher level of satisfaction with both appearance of the nipple, Women who undergo NSM with reconstruction have the which we did not specifically measure, and in the sensi- greatest opportunity for preservation of their native skin tivity of the nipple, which seems to contradict our results. envelope, and theoretically, a natural cosmetic outcome. However, in concert with our results, Didier et al. did not Given body image dissatisfaction and sexual function have find a significant difference in the impact of nipple- been linked, we sought to explore these outcomes for preservation on sexuality, although they did not employ the mastectomy patients [26–28]. In this study, despite the use of the FSFI as a metric of measurement [23]. greatest opportunity for retaining their baseline appearance, There are several limitations of the present study. This the NSM group did not have superior body image or sexual secondary analysis is based on a small subset of a larger function outcomes when compared to SSM or TMRM. The cohort of surveyed patients that included both breast con- NSM patients were on average younger, more likely to be servation and mastectomy without reconstruction. There- premenopausal, and had the lowest rate of receipt of fore, the failure to detect a difference between some chemotherapy and radiation, with chemotherapy previously responses may quite possibly be due to the small sample correlated with sexual dysfunction in survivorship, and size. Second, the investigator-generated questions used radiation’s independent role less clear [14, 19]. Despite this have not been validated, even though they are similar to the favorable constellation, along with retention of the native questions in prior studies. Moreover, by combining patients nipple-areolar complex (NAC), this group’s median total who underwent simple and modified radical mastectomy, FSFI score met criteria for sexual dysfunction. NSM we were unable to investigate the effect of axillary dis- patients also had the lowest sexual desire scores. There was section on sexual function, if one exists. a trend for this group to also be least satisfied with their Critically, patients were evaluated at a single point in postoperative appearance. While the chest was more fre- time and therefore we cannot comment on how parameters quently involved in sexual activity for NSM, 40% reported changed over time. Furthermore, patients were solicited to caress of the breast as unpleasant. Though NSM leaves the participate in this survey during surveillance visits in sur- total overlying skin envelope intact, complete sensory vivorship, rather than a unique venue. As such, many preservation is rarely achieved. potential participants may have had competing diagnosis- Our results were somewhat different than those reported related issues commanding attention and understandably by Didier et al. who used a novel questionnaire of 56 items precluding survey participation. Finally, with less than a investigating post-surgical body image satisfaction and 60% response rate, we cannot comment on the

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Table 3 Parameters of intimacy among mastectomy type

Total, n (row %) TMRM SSM NSM p-value pcr-value 16 36 8

Q1. Satisfied w/appearance of chest Satisfied 11 (68.8) 24 (66.7) 4 (50.0) 0.6 0.1 Q2. Comfortable w/partner seeing chest Comfortable 13 (81.3) 27 (75.0) 6 (75.0) Equal 1 (6.3) 1 (2.8) 0 (0.0) 0.8 0.5 Uncomfortable 2 (12.5) 8 (22.2) 2 (25.0) Q4. Importance of role of chest in intimacy (before surgery) Important 15 (93.8) 33 (91.7) 8 (100.0) 1.0 0.5 Not important 1 (6.3) 3 (8.3) 0 (0.0) Q3. Importance of role of chest in intimacy (after surgery) Important 12 (75.0) 28 (77.8) 6 (75.0) 1.0 0.06 Not important 4 (25.0) 8 (22.2) 2 (25.0) Change in importance of role of chest in intimacya Same 10 (62.5) 25 (69.4) 4 (50.0) 0.5 0.3 Less important 6 (37.5) 11 (30.6) 4 (50.0) Q5. In the past 4 weeks, how OFTEN was chest (n = 13) (n = 27) caressed or stimulated during sexual activity?b Often 2 (15.4) 13 (48.2) 4 (66.7) 0.06 0.04 Q6 How MUCH is treated breast part of intimacy? (n = 11) (n = 33) (n = 8) 0.3 0.3 Much 8 (72.7) 16 (48.5) 6 (75.0) Not much 3 (27.3) 17 (51.5) 2 (25.0) Q7. How pleasurable is it to have breast stimulated?c (n = 10) (n = 33) Unpleasant 0 (0.0) 8 (24.2) 3 (37.5) 0.1 0.3 pcr = regression model adjusting for both receipt of chemotherapy and/or radiation a Change in importance of role of chest in intimacy is an combined analysis of Q3 and Q4, it was not a question in the survey tool b Often (almost always, most times) c Unpleasant (moderately unpleasant, very unpleasant) generalizability of our results. Theoretically, a greater preoperative sexual function to be assessed. As skin and proportion of NSM with sexual dissatisfaction could have nipple-sparing mastectomy becomes more widely adopted, chosen to participate. a greater number of patients undergoing these types of Strengths of our study include that patients were queried mastectomy will be available to participate in such a study. at least a year from primary treatment, as sexual dysfunc- Evaluating a larger nipple-sparing mastectomy cohort may tion can persist and worsen with time [10]. Additionally, also further clarify the trends that our present study sug- this is the first study that has combined the use of the FSFI gests regarding this population’s inferior postoperative and questions specific to breast sensuality, persistence of sexual function and body image outcomes. Surprisingly, the role of the breast in intimacy after breast cancer sur- the intuitive advantages of NSM in the aspects of satis- gery, and the perception of stimulation of the treated and faction with appearance, comfort, and pleasure during reconstructed breast. Given that the literature presents intimacy, and persistence of the role of the breast in sex- mixed results regarding an effect of reconstruction after uality were not confirmed in our study, and this should be mastectomy on sexual function, we chose to analyze the explored in future studies. Prior publications have shown data excluding those not reconstructed, and therefore these factors are better preserved with breast conservation eliminating the absence of reconstruction as a potential and support the ongoing recommendation for breast con- confounder [29, 30]. servation over nipple- or skin-sparing mastectomy in eli- With the increasing number of skin envelope-sparing gible patients [21]. Finally, it is imperative to provide a mastectomies being performed in both the prophylactic and comprehensive review of the consequences of mastectomy, therapeutic setting, a prospective study may better capture during preoperative counseling, and educational tools to changes in sexual function after mastectomy allowing for help clinicians describe realistic expectations for both

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