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Physician-Patient Communication in Risk-Reducing Salpingo-Oophorectomy Surgery: History
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Contributor: Ana C. Alves-Nogueira , Daniela Melo ,
Carlos Carona
,
Margarida Figueiredo-Dias

Risk-reducing bilateral salpingo-oophorectomy (RRSO) is an effective prophylactic surgery provided to premenopausal women carrying BRCA1 or BRCA2 mutations and presenting an increased risk of developing breast or ovarian cancer. This procedure is related to physiological, sexual, and psychosocial distress, which altogether increase uncertainty and complexity in the clinical decision-making process and post-surgery adaptation. Physician-patient communication (PPC) has been pointed out as a determinant factor in the decision-making to undergo RRSO, and the subsequent adjustment of women. 

  • risk-reducing salpingo-oophorectomy (RRSO)
  • BRCA mutation
  • ovarian cancer
  • breast cancer
  • physician-patient communication (PPC)

1. Introduction

Hereditary breast and/or ovarian cancer are associated with specific genetic variants that greatly increase the lifetime risk of developing these conditions [1][2]. For instance, some rare gene mutations correlate with breast and/or ovarian cancer predisposition syndromes [2][3][4][5]. However, the most common and well-known examples are the pathogenic BRCA1 and BRCA2 genomic variants, present in 1 to 300–500 women and responsible for 5–10% of breast cancers, and 10–15% of ovarian cancers [3][4][6][7][8][9].
As long as BRCA1 and BRCA2 mutations are involved, risk-reducing strategies should be implemented to prevent the risk of cancer, such as risk-reducing salpingo-oophorectomy (RRSO). RRSO is an effective risk-reducing surgery recommended to high-risk premenopausal healthy women carrying these mutations, ideally after the age of 35 or immediately after childbearing is complete [10][11]. It includes the surgical removal of the fallopian tubes and ovaries bilaterally and has proved its effectiveness in preventing ovarian cancer in BRCA1/2 carriers [1][6]. Nevertheless, the removal of apparently healthy organs may have serious physiological, sexual, and psychological consequences and does not ensure the elimination of future cancer risk.
The decision-making process to undergo RRSO is highly challenging for women and depends on multiple variables, such as personal appraisals, medical history, and psychological functioning [12]. Several qualitative studies have analyzed how these variables interact and contribute to the decision-making process (e.g., [13][14]). Even though a solid theoretical framework suggests the synthesis of potential interrelations between determinants, processes, and outcomes, ultimately guiding research and clinical intervention in shared decision-making processes [15], this has been systematically lacking in the aforementioned research.
Additionally, the decision to undergo RRSO is expected to be shared between the woman and her physician/oncologist. In this sense, physician-patient communication (PPC) has been acknowledged as a crucial factor in patient-centered care and associated with positive effects over healthcare outcomes (e.g., [16][17][18]). PPC also appears to be distinctively linked to women’s adaptation outcomes after RRSO [13][19][20][21].

2. Clinical Background for the Recommendation of RRSO

2.1. Genomic Susceptibility to Ovarian/Breast Cancer

Some rare moderately penetrant genes confer an increased risk of developing hereditary breast and/or ovarian cancer, such as MLH1, MSH2 or STK11 [2][3][4][5].
Despite the risk conferred by these rare pathogenic variants, research is still scarce on this topic, preventing the establishment of clinical management protocols for most of them [5].
It is noteworthy that most cases of hereditary breast and/or ovarian cancers are associated with germline mutations in BRCA1 and BRCA2 genes [8]. BRCA1 and BRCA2 mutations are responsible for 5–10% of breast cancers and 10–15% of ovarian cancers [3][4][6][9]. Besides the high cumulative risk at the age of 70–80, women carrying these mutations may already present an increased risk up to 10% for developing ovarian cancer by the age of 50 [4]. The 5-, 10-, and 15-year cumulative risk for BRCA1 carriers is 13.7%, 23.8%, and 36.1%, respectively; and for BRCA2 carriers is 12.0%, 18.7% and 28.5%, respectively [22].
Given the lifetime and cumulative risks of cancer in BRCA germline mutation carriers, after genetic testing disclosure, risk-reducing strategies are usually recommended by clinical practice guidelines [2][7][10][23].

2.2. Risk-Reducing Measures and RRSO

Various strategies can be used to reduce cancer risk, morbidity, and mortality in women with an increased risk of hereditary breast and ovarian cancer [5], within a multidisciplinary approach [3].
Regarding the screening methods, mammography seems to be the only effective imaging strategy in reducing breast cancer mortality. However, it presents lower detection sensitivity in BRCA mutation carriers in comparison to the general population, particularly in women under 40 years old and carrying a BRCA1 variant. It is noteworthy that breast MRI is reported as the most sensitive screening exam for BRCA mutation carriers. Still, data are missing about the effectiveness of this strategy in reducing long-term mortality in these women [24]. On the other hand, compared to breast cancer screening, ovarian cancer screening methods are largely ineffective, with no reported benefit in reducing ovarian cancer mortality [3][25]. Specifically, in a 2007 observational, follow-up study in the general population, annual screening with combined CA125 and transvaginal ultrasound failed to detect early-stage cancer. In fact, there were women diagnosed with stage III/IV cancers, while having a normal screening 3 to 10 months before diagnosis [6].
The evidence of the effect of oral contraception on breast cancer risk among BRCA1/2 mutation carriers is still controversial. Although a few case-control studies have reported a modest increase in breast cancer risk [8], at least two meta-analyses showed no increased risk of breast cancer in women with BRCA1/2 mutation taking oral contraception [1][3][6][26]. 
The use of tamoxifen and aromatase inhibitors (AI) as chemoprevention strategies has shown efficacy in reducing the risk of invasive breast cancer in high-risk postmenopausal women. However, there are no prospective studies evaluating the risk-reduction effect of tamoxifen in women with BRCA mutations.
Women carrying BRCA1 and 2 mutations have a breast cancer risk reduction of at least 90% when undergoing risk-reducing mastectomy (RRM) [2][3][8][25][26][27][28]. This risk reduction also translates in a 90% decrease in cancer-related mortality [25]. In addition, RRM is associated with low rates of postoperative complications and reduced rates of surgery-related mortality, even though the risk of developing breast cancer is not fully eliminated [8]. 
As for RRSO, surgical removal of both ovaries and fallopian tubes in premenopausal women significantly reduces the levels of circulating hormones, which may lead to a reduced risk of developing estrogen-dependent breast cancer. Some authors continue to argue that RRSO leads to a 40–70% risk reduction of developing breast cancer [1][2][3][4][6][22][27][28][29][30]. However, hereditary breast cancer is often triple-negative, so hormonal mechanisms alone are not enough to cause breast cancer [31]. In addition, a prospective multicenter cohort study reported that RRSO significantly reduced the risk of breast cancer for BRCA2 pathogenic variant carriers but not for BRCA1 carriers [28]. In turn, when performed in premenopausal women carrying BRCA1/2 mutations, RRSO reduced the risk of ovarian cancer by 80–96% [1][2][4][6][7][8][26][29][32], as well as the mortality rate associated with ovarian cancer by 94% [29].

2.3. Physiological Implications of RRSO

Despite being considered a safe surgical procedure [6], RRSO has several physiological implications, mainly related to the surgical removal of the ovaries. Indeed, RRSO will lead to a surgical menopause, associated with a sudden decrease in estrogen levels and, consequently, with the onset of menopausal distress, including vasomotor symptoms, genitourinary syndrome, sleep disturbances, mood swings, and sexual dysfunction (e.g., decreased libido, vaginal dryness, and dyspareunia). These symptoms are generally more severe than in natural, gradual menopause [1][3][7][33].
Bilateral RRSO has also been associated with an increased non-cancer-related morbidity, such as increased risk of osteoporosis, cardiovascular disease, and metabolic syndrome, even though further studies are warranted [1][4][6][33]. First, bone mineral density decreases by up to 6.7% in premenopausal women at 12 months after an oophorectomy, which is much higher than the rate observed in natural menopause [34]. Second, despite the absence of prospective data, cohort studies show a slightly increased risk of cardiovascular disease in premenopausal women undergoing RRSO [35]. Third, these women may experience negative changes in lipid profile, with subsequent development of atherosclerosis [36].
Additionally, the recommendation to offer a RRSO from the age of 35 also limits the fertility window and could represent a major concern, especially in developed countries where the mean age of the first pregnancy is postponed [37].
Recently, and considering the existing evidence that many ovarian cancers originate in the fallopian tubes, it has been suggested that a risk-reducing salpingectomy alone, or followed by an oophorectomy close to the age of natural menopause, might postpone the onset of early menopause symptoms and allow an extended fertility window. However, the level of risk reduction achieved through this strategy is unknown, and data regarding the efficacy of this approach are lacking [1][6][7][8][26][28].
Hormone replacement therapy (HRT) (i.e., the exogenous administration of estrogens) has been recommended to women without a personal history of breast cancer, in the absence of counterindications, and until the natural age of menopause, in order to reduce menopausal distress following RRSO [1][2][8][33][38]. According to a systematic review evaluating the risks and benefits of HRT, this therapy was associated with improved quality of life, better sexual functioning and bone health, less menopausal distress, and reduced risk of cardiovascular disease after RRSO [1][2][3][6][7][33]. Although concerns have been raised about a possible increase in risk of breast cancer with the use of HRT, a large meta-analysis of 1100 women with pathogenic BRCA1/2 variants undergoing RRSO found no increased risk of breast cancer with short-term use of HRT (HR 0.98; 95% CI (0.63–1.52)) [1]. Nevertheless, large, controlled trials are urgently needed, and women should be informed that the existing data are limited [7][8][33].

3. The Psychological Process of Deciding to Undergo RRSO

3.1. The Psychosocial Impact of Undergoing RRSO

As for the psychological impact of having the surgery per se, the available studies report mixed results. On the one hand, some researchers have found the levels of overall post-surgery quality of life to be comparable to those of the general population, along with a significant decrease in cancer-related worry (e.g., [39][40][41]). On the other hand, there is also evidence for impaired sexual functioning, persistent physiological symptoms derived from surgical menopause and hormonal changes (e.g., vaginal dryness, hot flashes, decreased libido), and reduced body image satisfaction in women who underwent RRSO [20][42][43]. Moreover, it has been reported that around 20% of these women continue to present cancer-specific distress after surgery [39][44][45], and increased depressive and anxiety symptoms that tend to persist during one-year post-surgery [46]. Considering the holistic nature of potential consequences of RRSO (i.e., physical, psychological, relational, social), a multidisciplinary approach would be desirable to manage the deleterious effects of the surgery and support BRCA carriers in their decision-making process and post-surgery adaptation. However, even though clinical guidelines often recommend this approach, it is not always reflected in clinical practice, due to economic and organizational factors, which might contribute to the pervasiveness of the negative consequences of surgical menopause [6][8][26][32][47].
Undergoing RRSO surgery tends to be emotionally challenging, with serious physical and psychosocial consequences that may conflict with its primary purpose, and thus impair the decision-making process for women who carry a BRCA mutation. However, little is known about the role of modifiable psychosocial mechanisms that seem to shape the decision-making process, and women’s subsequent adaptation to its outcomes [14][48]. Notably, physician-patient communication has been increasingly acknowledged as a crucial modifiable variable that appears to be uniquely linked to women’s adaptation outcomes, following their decision to (not) undergo RRSO (e.g., [13][19][20][21]).

3.2. The Role of Physician-Patient Communication in the Decision-Making Process and in Post-Surgery Adaptation

Shared decision-making (SDM) consists of joint participation from both physician and patient in making a health decision, through the discussion of the available options and their benefits and harms, while considering the patient’s values, preferences, and circumstances [49]. There are several SDM models used in healthcare practice [50], with some of them specifically developed for oncology care (e.g., [51][52]). Even though no specific model has yet been examined in the context of the decision to undergo prophylactic surgery in mutation carriers, it is possible to establish a connection between the SDM model suggested by Shay and Lafata (2014) and the previously described HBM model. According to this SDM model, heavily drawn from the patients’ perspective, making a health decision depends on the interaction of several factors, such as: patient self-advocacy; open-mindedness and mutual respect between physician and patient; a physician’s personalized recommendation; and mutual information exchange. These factors occur in the context of the relationship and communication between physician and patient [53]. Considering the aforementioned HBM model, physician-patient communication may, therefore, be considered one of the modifying factors that uniquely shapes the women’s subjective appraisals that lead them to make the decision for RRSO.
Physician-patient communication (PPC), and particularly physicians’ empathic communication skills, are at the core of patient-centered healthcare and of medical practice [54][55]. Research has highlighted the positive effects of PPC on patients’ physical and emotional health improvements (e.g., [16][56]), treatment adherence [17][57], and overall well-being [18][58] across several healthcare settings, including cancer care [59].
In the context of decision-making for RRSO in women carrying a BRCA mutation, there are a few studies where the impact of PPC on women’s adjustment was examined. Some qualitative studies commented that even though women were frequently satisfied with their surgery decision, there was also dissatisfaction with the information provided by their physicians before the surgery, which could ultimately worsen the women’s ability to cope with deleterious post-surgery effects. Typically, these clinical information topics relate to possible treatment alternatives, negative impacts of menopausal symptoms, or the potential changes on sexuality and sexual functioning [21][43][60][61]. In a recent qualitative study describing the psychological experiences of women who underwent RRSO, it was found that, in the majority of cases, physicians failed to provide complete information, showed low levels of empathy and respect for the women’s values, preferences, and individuality, and adopted a disease-focused posture (i.e., focusing on organ health or exclusive disease prevention, and disregarding organism-context interactions and health promotion). Following these clinical attitudes, women experienced an increased psychological burden in the decision-making process, sought other professionals, or unwillingly delayed the surgery [14].

This entry is adapted from the peer-reviewed paper 10.3390/curroncol30020185

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