Breast Cancer Patients’ Experience and Wishes Regarding Communication on Sexual Health: The BEROSE Study

Abstract BEROSE is a single-center observational study, which aimed to determine the proportion of women with breast cancer who received information on sexual health from health professionals throughout their whole care pathway. A total of 318 women with all stages of breast cancer (30% metastatic) and at different time interval from diagnosis (up to 7 years) participated to the survey. Sixty-five percent of women reported that they had not received any information about sexual health over the whole care. Increased awareness among the healthcare professionals and particularly the oncology community is needed to discuss sexual health in women with breast cancer.


Introduction
Breast cancer (BC) is the most common cancer among women in the world (1). Thanks to improved screening programs and systemic and locoregional treatments, the mortality from BC in Western countries is steadily decreasing. In addition, patients with metastatic BC are living longer, by virtue of more effective systemic therapies (2,3). As a result, two million women in Europe currently have a BC history (4). Maintaining a long-term quality of life is therefore a major health concern among women that are being treated for early and advanced BC (5).
Several studies have evaluated the impact of BC on women's sexual health (SH), with 34% to 85% of women reporting sexual problems during and/or after BC treatment (6)(7)(8). Multiple factors and treatment side effects may directly or indirectly affect SH. Body image modification induced by local and systemic therapies, along with weight gain and fertility impairment associated to chemotherapy and endocrine therapy can severely undermine self-confidence (9,10), especially among young women (11,12). In addition, fatigue, pain, vaginal dryness, decreased desire and hot flushes that tend to persist for long time after treatment termination can hinder the recovery of sexual well-being (13)(14)(15). Finally, the psycho-social burden deriving from the diagnosis of BC and treatment side effects, including fear of being sexually unattractive following body changes, fear of cancer recurrence and death, changes in social and work position (16,17) and changes in the couple dynamics (18)(19)(20)(21) are major obstacles to a normal SH (22)(23)(24).
However, the issue of sexuality in women with BC is often underexplored and not adequately addressed (22,25,26). Nevertheless, prior studies showed that 68% of women with BC experience sexual difficulties and 60% sought to receive information on BC-related sexual changes, regardless the stage of the disease (27), even in advanced cancer or palliative care (28,29). Women often do not raise the question as the decline in the quality of sexual life is perceived as a "price to pay" (30) or they do not feel comfortable to discuss sexual concerns with their healthcare providers and would prefer the professionals to initiate the discussion on SH (31,32). However, it is also difficult for healthcare professionals, to address the topic of SH due to lack of adequate training (33), lack of time (34,35), or embarrassment (36).
Healthcare providers play a key role in providing timely information on the sexual consequences of BC diagnosis and treatment and advising women and their partners on the possible solutions. Nevertheless, few studies evaluated patients' perceptions regarding communication on SH with health care providers, at different time points of BC care and follow-up. We therefore conducted a cross-sectional study, among women with all stages of BC from a single large comprehensive cancer center, with the aim of determining the proportion of women who received information from health professionals about SH at any time during their BC care, from diagnosis to follow-up.

Design and setting
The BEROSE study (Breast cancEr patients' expeRience with cOmmunication on Sexual hEalth) was a cross-sectional observational study carried out at the Gustave Roussy Cancer Center (GRCC), a comprehensive cancer center located in a large urban area (Villejuif, France).

Participants
From June 12th to July 31th, 2020 all women !18 years old, with any stage of breast cancer, who had an in-person visit or a teleconsultation in the Breast Cancer Unit at GRCC and were undergoing standard follow-up or receiving anticancer therapy for early or metastatic BC, were asked to fill in a one-time survey. Women were considered ineligible if they had severe cognitive or psychiatric illness or if they were unable to read and/or write French language.

Procedures
Participants who came to GRCC for an in-person visit could choose between a paper or digital survey. The latter was administered using a SurveyMonkey link (http://www.SurveyMonkey. com), accessible through a QRcode. Given the COVID-19 pandemic, some follow-up consultations were conducted via teleconsultation. Women who had teleconsultations received an email containing the link and the corresponding QRcode. Women who had multiple consultations during the study period were invited to fill in the survey only once. The questionnaire was completely anonymous and no personal information was collected from participants. Neither reminders nor second invitations were sent to any of the participants. The survey did not allow to identify the person indirectly, accordingly to the French legislation [Jarde's law, November 2016] and the EU General Data Protection Rules. The study was approved by the Institutional Review Board (IRB) on April 28 th , 2020 and was internally validated by the data protection officer. The first page of the questionnaire contained a letter informing patients that, by completing the questionnaire, they gave their consent to participate in the study and included a box to be checked in case of refusal to participate.

Questionnaire
Because validated questionnaires evaluating communication between women with BC and health-care professionals about SH do not exist, we created an ad hoc questionnaire, building on published studies about SH. The questionnaire was reviewed and validated by a panel of diverse healthcare professionals at GRCC including medical oncologists, nurses, gynecologists and psychologists with long-term experience in BC and by patient advocacy groups. The final version was reviewed by the research team, tested on a small sample of volunteer patients, and modified according to their comments. The final questionnaire (Supplementary Figure 1S available in Supplemental material) comprises 30 questions divided into 3 main sections: general information (10 questions) including age range, education, family composition, menopausal status, comorbidities, and co-medications; information on BC and treatments (5 questions) such as early or metastatic BC, treatments received and ongoing; and questions on women's SH (15 questions) including: current satisfaction with sexual life compared to sexual life before BC diagnosis, communication on SH with health-care professionals after the diagnosis of BC, how to approach the topic of SH, who initiated the communication and when, patients' preferences and barriers on communication about SH.

Primary and secondary outcomes
The primary outcome was to determine the proportion of women who received information from health professionals about SH at any time during their BC care, from diagnosis to followup, whether the subject is addressed by themselves or by the professional. The proposition was: "The topic of sexuality was addressed in the consultation: Yes by the doctor/nurse/other health professional(s) of Gustave Roussy Institute; Yes by my gynecologist or my general practitioner; Yes by myself; No". The secondary outcomes were (1) to describe the main characteristics of such communication on SH, (2) to assess the perceived impact of BC/its treatments on sexual satisfaction, and (3) to explore factors associated to women's satisfaction with SH and to communication on SH after BC diagnosis.

Statistical analysis
Descriptive statistics were used to describe patients' characteristics (age range, education, family composition, menopausal status, comorbidities and co-medications), BC characteristics (stage and type of treatments), satisfaction with SH and communication on SH.
The primary outcome was computed as the proportion of women who received at least one communication on SH after the diagnosis of BC.
Continuous variables were expressed using medians and ranges. Categorical variables were summarized using absolute count and percentages.
Current sexual satisfaction was compared retrospectively to the sexual satisfaction diagnosis and/or before treatment using a McNemar test.
We also explored the association between the single following variables: women's age range, tumour stage and ongoing treatment and the items: (1) women reported satisfaction with sexuality before BC diagnosis and at time of survey (2) perceived importance of addressing sexuality during BC follow-up.
Associations were tested using Kendall's correlation tests for ordinal variables, Cochran-Armitage trend tests, or Chi-square or Fisher's exact tests when appropriate.
As these latter analyses were exploratory, pvalues were not corrected for test multiplicity so they should be interpreted with caution.
All analyses were performed using R (version 4.0.3) and the "tidyverse" packages (37,38) with a significance level of 5% for 2-sided tests.

Evaluable questionnaires
A total of 580 women were given the paper questionnaire, while 62 were invited to fill the questionnaire in digital form after their teleconsultation; a total of 348 (54%) women completed and returned the survey of whom 329/ 580 (57%) filled the paper questionnaire and 19/ 62 (31%) the online questionnaire. After removing incomplete questionnaires (n ¼ 25, 7.5%) and overt refusals to participate in the study (n ¼ 5, 1.5%), 318 (50%) questionnaires were assessable for our analysis (94% in paper format and 6% in digital version; Figure 1).

Participant characteristics
Main participant characteristics are summarized in Table 1. Sixty-one percent of women were older than 50 (n ¼ 194). Almost 80% were married/partnered (n ¼ 253) and 86% (n ¼ 275)had at least one child. The majority (n ¼ 166, 52.2%) had a university-level academic education. Forty percent (n ¼ 128) of women were postmenopausal before their diagnosis of BC and treatment initiation, 79% at the time of the survey. Sixty-five percent (n ¼ 206) of women declared to have a localized BC. The majority of patients were currently receiving chemotherapy or hormone therapy (n ¼ 83, 26% and n ¼ 118, 37% respectively, Table 2). The median time since the BC diagnosis was 3 years [range, 1 À 7].
Communication on sexual health after breast cancer diagnosis Overall, 65% (n ¼ 207) of women reported that they did not have any conversation with any  healthcare provider regarding their SH ( Figure 2). Fourteen percent of women (n ¼ 45/318) had a discussion about this topic because they had brought it up on their own. Finally, the topic was discussed by a Gustave Roussy healthcare provider for 11% of the women and by a gynecologist for 9.7% of them. Two-thirds of women (n ¼ 218, 69%) reported that they considered important to discuss sexual issues during the visits planned for their BC treatment, and for 31% (n ¼ 100) of them, would have preferred health-care professionals, rather oncologists or gynecologists, to initiate the discussion on the impact of BC diagnosis and treatment on SH. When sexual consequences were discussed, it was mainly in terms of adverse effects that treatments could have on sexuality: the health-care provider informed the patient of their possible occurrence (n ¼ 32) or asked if the patient had noted such adverse effects (n ¼ 39). Sexual well-being was directly addressed in only 4.1% (n ¼ 13) of cases (Supplementary Table 1S available in Supplemental material).
When they were asked the most appropriate time for such communication, 45% (n ¼ 145) of women replied "along the whole care pathway". The majority also would have liked to discuss their sexual concerns in the presence of their partner (n ¼ 277, 87%). Participants reported that their preferred physician for such discussion was their oncologist (n ¼ 161, 51%), their gynecologist (n ¼ 129, 41%) or a sex therapist (n ¼ 81, 26%). Finally, the majority of women wished to discuss sexual consequences of BC in an in-person consultation (n ¼ 218; 69%) or, to receive information through a specific leaflet or website (n ¼ 117, 37% and n ¼ 49, 15% respectively).

Sexual health after breast cancer diagnosis
Women were questioned a posteriori on their satisfaction with their sexuality before the diagnosis and/or treatment of BC and then at the time of the survey (Supplementary Table 1S available in Supplemental material). The majority of women reported they were satisfied with their sexuality before the BC diagnosis (166, 52%; Figure 3) or even very satisfied (98, 31%). At the time of survey completion, satisfaction with sexual life had significantly decreased (p < 0.0001) and only 30% of women stated they were satisfied or very satisfied with their sexuality (76, 24% and 18, 6% respectively). Two-thirds of women (n ¼ 213, 67%) perceived a negative impact of cancer and its treatments on their sexuality (Supplementary  Table 1S available in Supplemental material), mainly due to increased vaginal dryness (n ¼ 134/ 213, 63%), decreased desire (n ¼ 121/213, 57%) and a change in body image (n ¼ 86/213, 40%). For 42% (n ¼ 90/213; 24% single and 76% partnered) of women, sexuality was not a priority at the time of the study. Almost a fifth of them reported a positive impact of cancer on their sexuality (n ¼ 60, 19%), mostly in virtue of an improved communication with their partner (n ¼ 26/60, 43%).

Exploratory factors associated to sexual health satisfaction and communication on sexual health
We also evaluated the association between age range, tumor stage and ongoing treatment (especially chemotherapy and hormone therapy versus other treatments) with current and pre-diagnosis satisfaction with sexuality and communication on SH.
Age was not associated with satisfaction with sexuality before BC (p ¼ 0.22) or at the time of the survey (p ¼ 0.49). Communication on SH was of less importance to women with older age (p ¼ 0.03); however, 64% of the patients in the oldest group (>70 years) still considered this topic important (supplementary Figure 2S available in Supplemental material).
Tumor stage was significantly associated with satisfaction with current sexuality, a lower satisfaction being more frequent in patients with metastatic tumors (p ¼ 0.005; supplementary Figure 3S available in Supplemental material).
Ongoing treatment was not significantly associated with current satisfaction with sexuality (p ¼ 0.16; supplementary Figure 4S available in Supplemental material).

Discussion
Although SH is an important dimension of quality of life and BC diagnosis and therapies are associated with a high risk of developing transient or permanent sexual disruptions, very few women obtain information or have access to an appropriate counseling focused on sexual issues.
Our study confirms the lack of communication between patients and health-care professionals on SH in women with BC. Consistent with prior data (26,39), our results confirm that nearly 4 out of 5 women do not receive information from health professionals.
Furthermore, we found a significant deterioration in women's self-rated satisfaction with the quality of their sexual life compared to their prediagnosis satisfaction levels (25). It is also interesting to note that almost one in five women was not satisfied with her SH before BC was diagnosed. These figures are consistent with those carried out by Lammerink et al in 2017 on 521 sexually active and healthy women in the Dutch general population: more than a quarter of which had a sexual dysfunction (40).
Women preferred to receive information on SH throughout their treatment plan, starting as soon as the diagnosis, as recommended by the American Society of Clinical Oncology (ASCO, (41)) and by national societies, such as the French Association of Supportive Oncological Care (AFSOS, (24)). Participation of the partner in the discussion on SH was essential for most of participants (20). Despite the lack of training of oncologists in SH, they were the preferred interlocutors for women, likely due to the relationship of trust that can develop throughout the whole BC care journey (39). Thus, oncologists are expected to initiate the discussion (25,32) on the impact of BC on SH, preferably during inperson consultations, with a clear and inclusive language that make the women and their partners comfortable enough to raise specific questions on this topic.
In our exploratory analyses, as already shown in other studies (33), age did not affect sexual satisfaction, although SH seemed to be a little less essential to discuss for older women.
Metastatic status appeared to be more associated with poorer quality of sexual life (28), but SH issues was as important to discuss as for women with early BC.
Although analysis of sexual satisfaction according to oncological treatment was only exploratory, we did not find any significant difference among patients receiving endocrine therapy and chemotherapy. This differs from the study of Ganz et al. (10) in which a greater deterioration of sexual functioning was associated with chemotherapy. This lack of association can depend upon the measure used to define sexual dysfunction but also on the impact of symptoms of both treatment modalities on patient's sexual health. Chemotherapy can have side effects that directly impact intimacy such as nausea, vomiting, fatigue, but also induce symptoms of chemoinduced menopause. Endocrine therapy, on the other hand, can have more direct adverse effects on the sexual sphere and intimacy, often with vulvo-vaginal dryness that can be associated with pain during sexual intercourse, hot flashes or weight changes that can affect body image (42). These two treatments can therefore impact sexual satisfaction in different ways, so justifying the absence of difference between our two groups of current treatments.
Better management of SH has the potential to increase adherence to treatments (43,44), to reduce certain symptoms such as anxiety or depression associated with BC therapy and to improve communication within the couple and in the family (18,(45)(46)(47), with a significant positive effect on the daily well-being.
The first step is to inform the patients about the consequences of the disease and its treatments on SH and provide advice on the possible remedies for the woman and the couple. Regardless of age (48), disease curability (32) and phase of treatment (26), early and regular support on SH must be offered to all women facing BC diagnosis and treatments, in full respect of women's sexual preferences, cultural diversities and feelings (49).
To this purpose, health professionals should receive adequate training to discuss sexual disorders with their patients and to provide them with appropriate counseling (50).
Our study has some limitations. First, because we aimed to draw an overall picture on SH communication in women with breast cancer, we allowed the inclusion of women with all breast cancer stages and presenting with a wide range of clinical conditions. We acknowledge that the population heterogeneity hampers the possibility of drawing solid conclusions from the information collected through the survey. However, our findings underline that sexual issues require further evaluation also in patients with advanced breast cancer. Secondly, this study was conducted in a single large cancer center to which are frequently referred patients with more complex or advanced BC or at younger age, who may require a highly specialized multidisciplinary approach. Indeed, since the majority of women in our sample are highly educated, it is likely that many of them voluntarily chose a highly specialized center. However, in our study, women were coming from various geographic areas, making our results more generalizable. Furthermore, the age structure of our sample is fairly representative of that of women with BC in France (51). Thirdly, to ensure the provision of total anonymity to the participants, all data concerning their disease and treatments and overall clinical conditions, were self-reported. We acknowledge that due to selfreporting, many clinical data may be inaccurate and incomplete. However, because of the highly sensitive nature of the survey topic, we preferred to rely on self-reported data with the purpose of avoiding patient embarrassment. Fourthly, information regarding SH before BC were collected retrospectively, so a recall bias has to be considered in their interpretation. In addition, to limit the number of questions to the main objectives of the study, we could not capture specific data on gender identity and sexual preferences. Fifth, because our study was based on the response to a questionnaire that was collected only once over the BC care pathway, we were not able to assess the longitudinal evolution of sexual quality of life over treatment and follow-up. Furthermore, we cannot use a validated questionnaire, as to our knowledge a questionnaire validated to evaluate communication on SH in patients with cancer does not exist. Moreover, since sexuality is multidimensional and not just physical (52), we have not found a validated questionnaire that explores these different domains in a comprehensive way. However, our questionnaire was created after a large literature review, coordinated and reviewed by a multidisciplinary team. Finally, in creating this questionnaire and in order to focus on the key professionals in the patient's care pathway, we proposed only two types of health professionals to address the topic; a gynecologist or a healthcare provider from Gustave Roussy Cancer Center, which could constitute a slight limitation. One last important fact to remember is the context of the global COVID-19 pandemic, which also had an impact on the response to our survey, sometimes leading to missed appointments, resulting in virtual rather than face-to-face consultations. However, trying to reduce the impact of this event on our sample, we sent our survey questionnaire by email to all women seen in teleconsultation during the period of our study. Finally, we were not able to accurately assess the rate of refusal to participate due to the multiple channels used (e-mails, posters, distribution of paper questionnaires, etc.) to address the women, nor the reasons for this refusal (good sexual health or, on the contrary, significant sexual problems, taboo subject or women not concerned by the problem). Indeed, we expected a higher recruitment that it is. Likely, it was not reached because of multiple reasons, such as the heavy emotional context faced by patients consulting for BC, the content of the survey as well as the major perturbations in outpatient visits due to the COVID-19 pandemic. Undoubtedly, this low recruitment undermines BEROSE study's potential of identifying the multiple factors associated to SH after BC diagnosis and to the likelihood of communicating on this topic.
In conclusion, although SH is recognized as a central component of quality of life, it remains in general -and in particular in the oncological field -a theme that is rarely mentioned. Our study clearly underlined that all patients, regardless of age, BC stages and ongoing treatment, are concerned about the possible impact of BC treatments on sexual function and are interested in maintaining a good sex life (24,41). Increased awareness among the healthcare professionals and particularly the oncology community is needed to discuss sexual health and the potential impact of the proposed treatments in women with breast cancer.

Funding
The author(s) reported there is no funding associated with the work featured in this article. Data availability statement All data generated and analyzed during this study are available from the corresponding author upon reasonable request.