Factors of sexual quality of life in gynaecological cancers: a systematic literature review

Background The impact of cancer diagnosis and treatment on sexual quality of life (SQoL) is a well-established survivorship issue for gynaecological cancer survivors (GCS), yet little is known on how to intervene. Purpose The aim of this systematic review was to identify the factors explaining the variability in SQoL for GCS. Methods We used the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) framework and the software Covidence. Electronic databases Scopus, Web of Science, PUBMED and CINAHL were searched for original research on GCS published between 2002 and 2018. We performed a two-stage screening process against selection criteria and quality assessment of individual studies. The Salutogenic Theory and the PRECEDE–PROCEED model were used as theoretical frameworks to identify and categorise factors. Results The initial search yielded 3,505 articles resulting in a total of 46 studies used to examine the association between factors of SQoL and gynaecological cancers. Our findings suggested that SQoL varies across subgroups based on age, menopausal status, relationship status, and treatment modality. Protective factors included clinicians’ knowledge and confidence, preventive medical approach, risk and needs assessment, patient–clinician communication, relationship quality, psychosocial support, symptom management, accessibility of psychosexual care, and self-efficacy in the rediscovery of sexuality. Conclusion Despite the high incidence and long-term impact of sexual health issues on quality of life, supportive care needs are not being met. A better understanding of the evidence base around the factors of SQoL can help health professionals take steps to protect and improve SQoL in GCS.


SQoL as a key survivorship issue for GCS
Although survival rates for women diagnosed with gynaecological cancers are improving, the quality of life (QoL) for those women and their families often suffer as a result [1][2][3]. The World Health Organization (WHO) and the literature have characterised sexuality as a human right and a key component of QoL [2,[4][5][6]. In 2012, an estimated three million women worldwide were living with gynaecological cancers, with more than half experiencing sexual difficulties [2,7]. High rates of sexual dysfunction, sexual inactivity and sexual morbidity in this population have been shown to greatly impact QoL [3,5,7,8]. The term "sexual quality of life" (SQoL) emphasises this link between sexuality and QoL [7][8][9][10][11].
Despite sexuality being recognised as a key survivorship issue for gynaecological cancer survivors (GCS) [12,13], little is known on how best to support SQoL in this population [8,14]. This is an important public health issue considering that cancer treatment can extend life expectancy by 25-30 years [15]. Furthermore, there is growing evidence for the need to integrate sexuality as part of routine care in gynaecological cancer recovery given current unmet needs [3,16]. Consequently, further investigation was warranted to understand the factors that are amenable to public health action to protect and improve SQoL.

Defining SQoL-beyond sexual dysfunction
Beckjord and Campas [11] defined SQoL for female cancer survivors as a broad concept covering sexual attractiveness, interest, participation and function. Interestingly, McCallum et al. [14] found that the meaning of healthy sexuality for GCS includes concepts of emotional intimacy, body image, sexual self-schema, and sexual response. They also discovered that sexuality is shaped by the interplay of physical, psychological, and interpersonal experiences. Similarly, WHO recognises sexuality as being "influenced by the interaction of biological, psychological, social, economic, political, cultural, legal, historical, religious and spiritual factors." [6] As such, WHO defines sexual health as "a state of physical, emotional, mental, and social well-being in relation to sexuality; it is not merely the absence of disease, dysfunction or infirmity" [6].
The literature on sexuality and gynaecological cancers has predominantly focused on sexual dysfunction and sexual inactivity-at the expense of a more salutogenic approach to SQoL [2,12,17,18]. Contrary to the disease orientation, salutogenesis [19] promotes the creation of health. To maximise health outcomes, it is imperative to go beyond common complaints of sexual dysfunction or lack of desire [2] and acknowledge the complex interplay of individual, social and environmental factors. Consequently, this review used the Salutogenic Theory [19] and the WHO definition of sexual health to explore how to move GCS towards greater SQoL by understanding the factors that relate to all aspects of the person-rather than merely sexual dysfunction. The aim of this systematic review was to identify the risk and protective factors that have been studied as explanations of variability in the SQoL of GCS. Our research question was: what are the risk and protective factors of SQoL in GCS?

Search strategy
We used the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) framework and the software Covidence in this systematic review [20,21]. The search for eligible studies was conducted in four electronic databases, Scopus, Web of Science, PUBMED, and CINAHL for articles published in English between 2002 and 2018. The search strategy was developed with input from a health librarian with expertise in systematic review searching. Search terms, such as "sexual quality of life", "sexual health", and "sexual wellbeing", were combined with terms such as "factor", "predictor", and "cause" for each gynaecological cancer. Two reviewers performed a two-stage screening process (abstract and title, then full text) against selection criteria and a third investigator solved any discrepancy. All voting was blinded, meaning that contributors were unable to see each other's votes until they casted their own.

Inclusion and exclusion criteria
The inclusion criteria included peer-reviewed studies reporting the factors of SQoL for adult women diagnosed with gynaecological cancer. Gynaecological cancers were defined as those affecting a woman's reproductive system: ovarian, uterine, cervical, vulvar, and vaginal cancers [22,23]. In addition, cancers of the placenta and fallopian tubes were included. Studies of women for pre-cancerous or other health conditions were excluded. Studies addressing both gynaecological and non-gynaecological cancers (e.g., studies of ovarian and breast cancers) were included if gynaecological cancer data were reported separately. No study design was imposed on the original search. We included randomised control trials, qualitative studies, cohort studies, and case-control studies published in English. Studies were excluded if they contained data from other sources than original full-text publications (i.e., reviews, meta-analyses), but reference lists were scrutinised for completeness. Finally, studies were excluded if they did not report at least one factor explaining the association between SQoL and one or more of the gynaecological cancers studied.

Quality assessment and data extraction
Two investigators, one of whom was not involved in article screening and selection, completed quality assessment and preliminary data extraction of individual studies independently. The process was blinded and Critical Appraisal Skills Programme (CASP) checklists [24] were used as standardised tools to critically appraise articles. To be retained for inclusion, studies had to clearly answer the research question and reach a minimum quality score of 50%. Conflicts were resolved by consensus. Studies' general characteristics (author, year of publication, aim, number of participants, country, design, outcome measures, tools, and theoretical frameworks), as well as the clinical characteristics of the patients or survivors (age, FIGO stage, cancer site, etc.) were extracted and tabulated along with factors and recommendations to perform a thematic analysis. All data in this review were obtained from previously published and publicly available studies.

Data analysis
The Salutogenic Theory and the PRECEDE-PROCEED planning model [25,26] were used as theoretical frameworks to identify and categorise factors. Hence, classification of protective factors was performed using predisposing, enabling and reinforcing factors. Predisposing factors are involved at the cognitive level such as knowledge, attitudes, and self-efficacy of GCS in SQoL. Enabling factors are the conditions that help SQoL to occur (e.g., availability of resources, funding or guidelines). Reinforcing factors are those helping to support SQoL in a community and thus involving partners, peers, health providers, etc.
This study revealed the risk and protective factors of SQoL. By risk factors, we refer to the factors that may increase the likelihood of an impaired SQoL in GCS. For example, single irradiated women may be more at risk of an impaired SQoL. In comparison, protective factors may decrease the likelihood of an impaired SQoL. For instance, patient-clinician communication may help protect and improve SQoL.

Results
A total of 3505 articles were identified by our search strategy. Figure 1 shows the PRISMA diagram for the different phases of the systematic review process, which resulted in the inclusion of 46 studies.

Risk factors of SQoL
Our findings suggest that the SQoL of GCS varies across subgroups based on age, menopausal status, relationship status, and treatment modality ( Table 2). To a lesser extent, variations in SQoL have been attributed to cancer site [27], tumour stage [28], BMI [29], education [30][31][32][33], and unemployment [30]. Due to space constraints, we will report only on the factors with the strongest evidence.
GCS aged over 50 may be more likely to suffer from orgasmic disorders and less likely to discuss sexual concerns due to shyness and stigma [14]. Whereas, their younger counterparts have reported feelings of aloneness [27], relationship dissatisfaction [35], distress about long-term sexual problems [39], and concerns about how they feel cancer changed their body [30,39].
Overall, young age was associated with worst adaptation on a range of SQoL measures ranging from the number of sexual problems to the severity of psychosexual distress [39]. In fact, women aged less than 55 years requested help to deal with sexual and psychological complications [34,39], but stated practical considerations and emotional avoidance as barriers to access services [14]. Although sexual problems, such as the lack of sexual desire, were discussed among both groups [14, 29-31, 33, 35, 38]. Corrêa et al. [31], Segal et al.   Qualitative-semi-structured interviews. Demographic and treatment data previously collected and medical records      [29] and Wang et al. [33] have established older age as a predictor of decreased sexual function. Despite this, premenopausal GCS may be particularly at risk of feeling the loss of feminity or developing a fear their partner might leave them [14,30,35]. Menopausal status can also be altered by cancer treatment and affect sexual response [35].

Relationship status
Nine studies established a link between relationship status and SQoL [28, 30,32,34,36,37,[40][41][42]. Single women (i.e., unmarried, not in a stable relationship or not living with a significant other) may feel more vulnerable in new relationships [41], be at risk of an impaired body image [28], and have higher rehabilitation needs [34]. According to Barlow et al. [40], intimacy and relationship status are more closely linked to sexual satisfaction than physical arousal. Not surprisingly, relationship status was associated with sexual activity [28,42] and it is also a predictor of sexual function and sexual interest [32,37]. Finally, Pinar et al. [30] found that couples in an arranged marriage or those married for more than 30 years suffer from lower sexual interest and sexual dysfunction.

Treatment modality
The impact of cancer treatment on SQoL is significant, with 25 studies reporting an association with SQoL. As such, Table 2 shows common complaints among GCS after radiotherapy, chemotherapy, and surgery. For example, pelvic radiation may alter vaginal conditions and cause frequent and intense dyspareunia, which in turn can lead to a fear of sexual contact and impact all aspects of sexual response (desire, arousal, orgasm, and resolution), sexual activity, and sexual satisfaction [28,29,[43][44][45][46][47][48][49]. Surgeries to the reproductive organs, such as radical hysterectomy, can not only affect sexual response, but also lead to psychosocial distress due to feelings of grief (e.g., loss of womanhood) or issues with marital cohesion [33,35,48,50]. Furthermore, certain treatments can induce conditions such as lymphedema or menopause, which can impact on sexual desire, sexual intercourse, and overall QoL [34,35,48,48]. Finally, health professionals should be aware that treatment affect women differently. In a study from Stead et al. [35], most women did not have sex during chemotherapy, while others felt it helped them maintain a sense of normality, protect their feminine identity,

Protective factors of SQoL
In line with the Salutogenic Theory [19], this review identified the need for a holistic, patient-centric and multidisciplinary approach to SQoL. This section covers the protective factors of SQoL (Table 3) and the role of the healthcare system, policy makers, and partners of GCS in preventing and reducing the negative consequences of gynaecological cancers.

Clinician's knowledge and confidence
Eleven studies recommended that health professionals should build knowledge and confidence required to address SQoL. First, seven studies [29,34,42,46,49,52,53] revealed the importance of developing an awareness of the risk factors and adverse effects of diagnosis and treatment on SQoL. In fact, Vaz et al. [49] suggested that knowledge of the frequency, duration, and interference of the adverse effects of radiotherapy may facilitate early intervention and reduce the burden of treatment sequelae. Second, four studies [54][55][56][57] emphasised the need to provide training and support to grow confidence and communication skills among nurses and clinicians. Furthermore, Molassiotis et al. [52] encouraged healthcare providers to develop an awareness of cultural views of health and sexuality to support the delivery of culturally sensitive care.

Preventive medical approach
Traditionally, the emphasis of gynaecological cancer treatment has been on improving survival rates. Besides adding years to life, there is now a growing appreciation for the need to improve the quality of those years. As such, four studies [29,42,51,58] reported on preventive measures that address the modifiable risk factors for pelvic floor disorders, menopause, and lymphedema. For instance, identifying patients at high risk of lower lymph lymphedema may help avoid unnecessary lymphadenectomy and bilateral adnexectomy [42,42]. Procedures such as nerve-sparing surgery, ovary preservation, or the extension of the vagina may also help lessen the negative effects of treatment, although more research is needed [33].

Risk and needs assessment
Twelve studies [14, 31, 34, 42, 46, 49-51, 54, 57, 59, 60] supported interdisciplinary efforts in the assessment of risks and early identification of needs for SQoL. Findings from McCallum et al. [14] indicated that understanding patients' long-term needs, desire for help, and barriers to access can help health professionals support GGS in achieving a healthy sexuality. Finally, Juraskova et al. [57] concluded that the quality of sexual relations is the best predictor of sexual function, and sexual function is the best predictor of QoL.

Patient-clinician communication
Seven studies [30,40,47,50,54,57,59] supported the positive effect of ongoing communication on the impact of diagnosis and treatment on SQoL. Furthermore, three studies [14,52,59] recommended giving written information for women embarrassed to raise sexual concerns. This recommendation strengthens the case for communication training to help remove clinicians' barriers and ensure women's concerns are addressed [54][55][56][57]. To this effect, Jensen et al. [47] suggested the PLISSIT model (Permission, Limited Information, Specific Suggestion, Intensive Therapy) as a useful guide to initiate the patient-clinician dialogue.

Relationship quality
Thirteen studies [14,35,36,40,45,47,52,56,59,[61][62][63][64] stated the partner's role in SQoL and the importance of the quality of the partner's relationship. According to Carta et al. [45] and Barlow et al. [40], relational and psychological factors may have a greater impact on sexuality than the physical side effects of cancer treatment. In fact, women who are in a committed and supportive relationship, and create emotional intimacy with their partner, may find it easier to resume and maintain a satisfying sexual relationship [40,45,55,65]. Health practitioners can create a supportive environment for couples by involving partners in care planning and taking their emotional needs and perspectives into account [52,56,59,61].

Symptom management
Eleven studies [14,33,42,43,46,47,49,56,64,68,69] examined the accessibility of patient-centric support for pain and symptom management. According to McCallum et al. [14], many GCS said they would have a healthy sexual life if they could manage the pain and symptoms post-treatment. Moreover, Ferrandina et al. [42] and Jones et al. [64] proposed referrals to specialist clinics dedicated to lymphedema and sexual health to improve SQoL. Finally, four studies [43,56,47,33] covered the role of lubricant and regular, long-term vaginal dilation in sexual recovery. Evidence suggested that interventions aimed at improving both nurses' and patients' self-efficacy in vaginal dilation may improve compliance [43,56,47].

Self-efficacy in the rediscovery of sexuality
Healthy sexuality concepts such as body image (how a woman feels about her body) and sexual self-schema (how a woman sees herself sexually) may be affected throughout the cancer journey [14,30,70]

Discussion
This systematic review included 46 studies that examined the association between factors of SQoL and gynaecological cancers. Our findings suggested that SQoL varies across subgroups based on age, menopausal status, relationship status, and treatment modality. Key protective factors included clinicians' knowledge and confidence, preventive medical approach, risk and needs assessment, patient-clinician communication, relationship quality, psychosocial support, symptom management, accessibility of psychosexual care, and self-efficacy in the rediscovery of sexuality. The included studies provided an understanding of how the major causes of SQoL can help clinicians and policy makers target at-risk individuals through risk reduction (risk factors) and prevention strategies (protective factors). The findings indicated that a holistic, patient-centric and multidisciplinary approach to SQoL is supportive of SQoL among GCS. Subsequently, the first step in addressing SQoL is for all health professionals involved in patients' care to understand who is most at risk of an impaired SQoL and how different treatment modalities may impact on SQoL based on patients' personal characteristics or circumstances. To this effect, William et al. [54] recommended establishing clear practice guidelines, promote shared responsibility and offer training to medical staff for the integration of sexuality in standard care.

Strengths and limitations
The strengths of this review included the use of a systematic, blinded and peer-reviewed process to assess the selection and quality of individual studies. One limitation was that although a number of included studies discussed the impact of gynaecological cancer treatment, they did not provide specifics about the treatment modalities, which made it difficult to ascertain their relative impact on SQoL. Some studies also failed to account for potential confounders in the analysis that could have explained variations in SQoL. Finally, another limiting factor in performing this review was the lack of a clear definition on SQoL for GCS. Although an extensive search strategy mitigated that risk, developing a clear working definition of SQoL for GCS would help inform future research and evidence-based practice.

Conclusion
When it comes to SQoL, a common mistake is to wait until the treatment has taken place to discuss sexual complaints. To reduce the burden of gynaecological cancers, this review identified the factors of SQoL to inform the steps health practitioners can take to support a proactive approach to SQoL. First, conduct risk and needs assessments while providing education to GCS and their partners on the impact of different treatment options on SQoL. This process should start in the initial consultations and include an exploration of preventative surgeries. Second, keep the patient-clinician dialogue open to evaluate treatment outcomes and sexual health needs during routine clinical assessments. Third, provide strategies to improve pain and symptom management or referrals to specialist clinics. Finally, consider the needs of partnered and single women in the provision of psychosexual care and psychosocial support.
Finally, our findings indicated that young single women who were premenopausal at diagnosis and underwent radiotherapy or radical surgeries of the reproductive system have an increased risk for severe sexual dysfunction and psychosexual distress. Although the evidence suggests that YGGS want help in dealing with psychosexual distress, more research is needed to inform intervention design. Consequently, the authors of this study are currently undertaking a qualitative study to explore the strategies that are acceptable in protecting and improving SQoL among YGCS.