Introduction

Sexuality is one of the indicators of quality of life; influencing thoughts, feelings, actions, integrations, and thus, mental and physical health. This is multifactorial and has a complex structure, influenced by biological, psychological, socioeconomic, intellectual, religious and sociocultural factors. This exercise, thus, depends on the integration of all these factors [1, 2].

The treatment of cervical cancer (CC) can cause adverse effects which can significantly affect quality of life and are mainly related to radiotherapy, caused by the action on the healthy tissues and organs adjacent to the tumor. The most affected areas are the vagina, the intestine/rectum and the bladder, which suffer from alterations in the mucus and can evolve into a series of alterations and dysfunctions, mostly sexual, fecal and urinary [3, 4].

Regarding the side effects of the treatment, acute effects generally have good prognosis, disappear in a short time, and improve by the use of medications. Later effects are, however, more severe and difficult to control clinically, and are often irreversible [4].

Sexual dysfunction is the main source of patient suffering post-treatment of CC [5]. Golbasi and Erenel [6] affirmed that female sexuality is most negatively affected by gynecological cancers, in comparison to other types of cancers and chronic diseases, and the adverse physical and psychological effects tend to decrease with time, though the effects on sexual life remain for a longer period.

Around 70 % of CC survivors suffer from sexual dysfunction [3], such as the decrease in vaginal sensitivity, reduction of sexual and orgasmic desire and excitation due to vaginal dryness, soreness and bleeding, dyspareunia and vaginal atrophy following treatment [3, 5, 7–14].

Some studies have evaluated the sexual function of gynecological cancer survivors in general, without restriction to cervical cancer; and those studies that have focused on cervical cancer were restricted to the initial stages of the disease, including in situ carcinoma. This study is focused on using samples from invasive cervical cancer survivors (stages from I to IVA), from patients that have concluded the treatment for at least 3 months. In this way, women included in the study would have developed the later side effects from the treatment during the data collection period. In addition, this study used a questionnaire that considers the multidimensional aspect of the sexual function, which was translated to Portuguese and culturally adapted.

In this context, the aim of this study was to evaluate the sexual function of women diagnosed with invasive cervical cancer that have completed the treatment for at least 3 months; identify the variables associated to sexual function and compare it to a control group composed by women with no cancer history.

Materials and methods

Study design

This study was considered to be an observational, analytical, epidemiological case–control.

Study population

The study group was composed of woman subjected to treatment of invasive cervical cancer (surgery, radiotherapy, chemotherapy—isolated or combined), within the period between 2005 and 2013, in a oncology referral institution located in Juiz de Fora (Minas Gerais, Brazil), and who were being monitored in this institution at the time of data collection. The recruitment process occurred throughout the cancer hospital archive, followed by active search of the cases, during which the phone numbers of the patients were obtained. After many attempts of contacting the patients via phone, a randomized sample selection was inviable due to the outdated information. In this way, eligible women that went to the institution for post-treatment follow-up were invited to join the research. Therefore, the study population was selected by convenience.

Inclusion criteria were: women diagnosed with invasive cervical cancer (CC; stages I to IVA); end of the treatment at least 3 months prior to the interview date—due to the time defined for the beginning of later side effects related to the treatment [3, 4, 15]; age equal or superior to 18 years.

The exclusion criteria were: showing diagnosed psychiatric, mental or neurological disorders with some cognitive deficit; history of other cancer (for cancer group women) or other significant morbidity such as chronic renal insufficiency, cardiac insufficiency, chronic obstructive pulmonary disease or severe musculoskeletal disturbances and disabilities. In the cancer group, women treated for recurring disease were excluded.

Data collection

The data collection was carried out from January to October 2013. Eligible women were invited to join the research, and were properly informed about the procedures, justification and relevance of this study.

Those women that accepted to join the study signed the Statement of Informed Consent. Data were collected in a unique interview performed face-to-face, in an adequate space in the Institution where the research was performed. The instruments used in the research can be observed in the following section:

Sample characterization questionnaire

For the cancer group, the questionnaire was divided into three parts. The first part referenced the disease and treatment characteristics and the diagnosis of other comorbidities, whose data were obtained through searching the records; the second part related to the socioeconomic, demographic, habitual, social/support network and self-reported comorbid characteristics; the third part was composed of alterations relating to the possible adverse effects of treatment. For the control group, the questionnaire was composed of questions referring to the socioeconomic, demographic, habitual, social/support network and self-reported disease symptom characteristics, menopause and sexuality.

Sexual function evaluation questionnaire

To evaluate the sexual function of sexually active participants, the Female Sexual Function Index (FSFI) was used [16]. This questionnaire was translated to Portuguese and culturally adapted, to be considered valid for the evaluation of sexual responses in Brazilian women [17]. From this, the instrument showed strong psychometric properties for evaluating and monitoring sexual function between sexually active women who had survived cancers, including cervical cancer [8, 18].

FSFI, composed of 19 questions, evaluated the female sexual responses for the preceding 4 weeks, categorized as the following phases or components of sexual response: sexual desire, sexual excitation, vaginal lubrication, orgasm, sexual satisfaction and pain [17]. The final scores were varied between 2 and 36, with the higher scores indicating a higher degree of sexual function [16]. Women who presented scores less than or equal to 26 were considered as carriers of sexual dysfunction [6, 18–20].

Ethical considerations

The study was approved by the Research Ethics Committee of the Federal University of Juiz de Fora, approved under opinion No. 131.805/2012. The participants were oriented to the study objectives and the interview was made after the two-way signature of  Statement of Informed Consent.

Statistical analysis

The data was digitally collected, organized and analyzed through utilizing the Statistical Package for Social Sciences (SPSS) software, version 15.0.

The bivariate analysis was conducted in order to ascertain differences between the groups: for the numerical variables the Mann–Whitney test was utilized, for the nominal variables the Chi squared (χ 2) or Fisher’s test was used, when necessary. In order to verify the association between sexual function and the independent variables, the Mann–Whitney test was used. To interpret the findings, statistical significance was considered for values at P < 0.05 and differentiation tendencies at P < 0.10.

According to the distribution of the independent variables in the descriptive analysis, the variables were regrouped into two categories, in order to facilitate bivariate analysis (Table 1).

Table 1 Categorization of independent variables. Juiz de Fora, MG, Brazil, 2005–2013
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To determine the influence of variables related to possible adverse effects on sexual function post-treatment (total FSFI), a multiple linear regression analysis was conducted with  Enter method, for variable entry according to the statistical significance of these and of the final model The variables that reached a level of significance of less than 20 % were included in the bivariate analysis model. Following the multivariate analysis, the variables were maintained in the final model with a 5 % level of significance (P ≤ 0.05).

Results

From the cervical cancer survivors that were followed up in the institution during the data collection period, two did not wish to join the research, three were in recurring treatment, and one had the diagnosis of previous cerebrovascular accident, with motor sequelae.

The total study sample consisted of 74 women divided into two groups: cancer (n = 37) and control (n = 37). The mean age of the participants was 50.88 years and median 51 years, (minimum 24 years, maximum 85 years), with a standard deviation of 12.97 years.

The period after conclusion of the treatment ranged from three to 92 months, with a mean of 36.78 (SD 25.25) months. The majority of the cancer survivors had tumors histologically classified as squamous (82.9 %); diagnosed as Stage IB by FIGO (International Federation of Gynecology and Obstetrics, 40 %); submitted to surgical and adjuvant radiotherapy treatment (45.9 %); and not undergone chemotherapy treatment (51.4 %). From the patients subjected to chemotherapy, 67 % were also treated with radiotherapy, and 33 % were also subjected to surgery and radiotherapy, after chemotherapy. Relating to the post-treatment sexual life, 56.8 % of the cancer group women reported receiving guidance; of these five made use of a vaginal dilator, although this use was not continued and on the data of the interview, none were wearing dilators (Table 2).

Table 2 Description of clinical, therapeutic and medical variables of women in the cancer group. Juiz de Fora, MG, Brazil, 2005–2013
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Both groups had similar distributions of socioeconomic and demographic variables, except for the “conjugal situation” (P = 0.05), in which the control group showed a greater frequency of women living with a partner (Table 3). In relation to the psychosocial variables and habits of life, those “relationships with husband/partner” being considered as “good or very good” was different between the groups (P = 0.02), with the frequency of women in the control group being higher.

Table 3 Description of sociodemographic and economic variables in the studied groups. Juiz de Fora, MG, 2005–2013 (continues)
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No statistically significant differences were observed between the groups for the variables relating to health (smoking, alcohol consumption, systemic arterial hypertension, diabetes mellitus, heart disease, arthritis/rheumatism, other health problems and continued use of medications).

The following variables, which in the cancer group can be associated to adverse effects of treatment, were different between the two groups (P < 0.05), with the greater frequency occurring in the cancer group: menopause; bleeding during or after sexual relations; increase in frequency, urgency, incontinence and retention of urination; increase of diarrhea, urgency and incontinence of feces; anal pain and mucus; intestinal bleeding and lymphedema in lower limbs. The majority of the women in the cancer group (64.9 %) reported menopause as being related to the treatment.

Furthermore, the cancer group presented worse results for the variables related to sexual function (Table 4). It is worth noting that the majority (59.5 %) of the CC survivors reported that the diagnosis and/or treatment interfered with their sexual function. The sexual frequency between the sexually active women was similar between the two groups, with the majority reporting frequencies between once and three times per week.

Table 4 Description of variables related to sexual function in the studied groups. Juiz de Fora, MG, Brazil, 2005–2013
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The total FSFI score varied between 9.60 and 35.10 in the cancer group and 23.90 and 36.00 in the control group (data not presented). In Table 3, the means of the cancer group can be observed as being statistically inferior to those of the control group in all the FSFI criteria and also in the total instrument score (P < 0.05). In both groups, the “desire” mean was the lowest and the “satisfaction” the highest. The total FSFI score mean was 21.72 in the cancer group, classified as sexual dysfunction because the cutoff point was considered as being below 26 (Table 5).

Table 5 Comparison between the groups relating to sexual function. Juiz de Fora, MG, Brazil, 2005–2013
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Table 6 shows the independent variables analyzed which presented a statistical association (P ≤ 0.05) or tendency to associate (0.05 < P < 0.10).

Table 6 Factors associated to sexual function. Juiz de Fora, MG, Brazil, 2005–2013 (continues)
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The final multiple linear regression model presented an R2 coefficient of 0.83 and a value of P < 0.01. Table 7 shows the variables which related to possible adverse effects of treatment that remained in the final model. Of these, only “bleeding during/after sexual relations”, “hematuria” and “diarrhea” were not significant (P > 0.05).

Table 7 Multivariate linear regression (final model): influence of related variables on possible adverse post-treatment effects on sexual function (total FSFI). Juiz de Fora, MG, Brazil, 2005-2013
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Discussion

The sexual function of cervical cancer survivors was inferior when compared with the control group in all FSFI domains and the total FSFI score, pointing towards a potentially negative impact of treatment on the sexuality of these women. This highlights the possibility of the aforementioned negative impact with the lack of orientation and adequate support of professional assistance, referring to the early approach of potentially adverse effects of disease treatments. Furthermore, the impact of the occurrence of a natural gynecologic cancer on patients’ quality of life should be taken into consideration, especially in the sexual sphere, as the organ involved is very symbolically important to the female sex and extremely connected to sexual activity [7].

Higher education showed a positive impact on sexual function. Huguet et al. [21] also constituted this association in samples of women subjected to treatment for breast cancer. According to these authors, a possible justification is the fact that women with greater education show more internal resources for dealing with the disease and a closer idea to the extent of the disease.

In relation to the psychosocial variables, 36.8 % of the women from the cancer group classified their conjugal relationship as poor or regular and only 32.4 % mentioned their partner as a source of family support. This can be associated with the fact that a large part of the women in the cancer group did not have a partner (48.6 %). Another factor that can also be related to this finding refers to the impact of the treatment on sexual function. Sexual dysfunction, observed in 80 % of the sexually active survivors, negatively affected couple relations and may even result in the abandonment of the woman by her husband or partner [7, 9].

According to Lara et al. [22], the importance of sexual health is instantly recognized for the longevity of effective relations and as a part of overall health and well-being of the individual. Currently, independent of gender, the satisfying aspect of sex has demonstrated greater important than their reproductive purposes.

In a study by Bernardo et al. [7], a higher frequency of sexual abstinence (73.6 %) was found in women affected by the disease in comparison to the present study. Abandonment by partners, separation or divorce following cancer diagnosis or treatment and the lack of medical orientation were the main motives highlighted [7].

Despite a large part of the women in the cancer group reporting vaginal stenosis/shortening and considering that the cancer and/or treatment interfered in their sexual life, no difference was seen in the frequency of sexual activity when compared to the control group. Within this context, according to White [14], for many women sexual frequency is determined more by the sexual interest of the partner and by the motivation in maintaining sexual relations, despite the absence of desire, looking to preserve the harmony and reduce the possibility of separation.

Similar to the results of the present research, Rodrigues et al. [23] observed prejudice mostly in the “desire” of sexual function, evaluated by the FSFI. The “satisfaction” domain already presented a higher mean score, which may demonstrate a tendency for women to adapt to sexual relation, in order to become satisfactory to the method which connects pleasure to the partner, even with little or no desire and before all the difficulties.

The impact of CC treatment on sexual function is also observed in diverse studies. White [14] noted sexual difficulties post-treatment, showing prevalence between 50 and 80 %. Bernardo et al. [7], however, found a frequency of 70 % sexual dysfunction. Lalos et al. [24] also verified that the majority of CC survivors showed sexual disturbances, primarily dyspareunia and reduction of sexual desire 1 year post-treatment. From this, the majority agreed that the treatment had a negative impact on women’s sexual health. In a longitudinal study by Jensen et al. [25], it was observed that in the two-year period ´post-treatment, 50 % of cervical cancer survivors reported vaginal stenosis, 85 % had low or no sexual interest and 30 % were unsatisfied with their sexual life.

Despite the literature highlighting the high impact of treatment with radiotherapy on sexual function compared to surgery [5–9, 26–28], this was not observed in the present study, most likely due to the reduced number of women subjected to only the surgical treatment, while the prevalence of sexual dysfunction increased with age [22, 29]. This association was also not found because the cancer and control groups did not differ in relation to this variable, most likely indicating that in this sample the negative impact observed on sexual function was more related to the treatment for CC.

In the population studied, the relationship with the partner showed association with the sexual function (total score and “orgasm” and “pain” domains). Within this context, Fernandes and Kimura [30] affirmed that for CC survivors, the presence of a sexual partner is very important to create a healthy environment. However, it should be recognized that a good relationship post-diagnosis is more probable in women that already had a healthy relationship pre-diagnosis [9].

From this, health professionals can comprehend the role of partners as providers of affection and physical, emotional and social support, as being essential for a good quality of life and sexual function [30]. Also, the social support factors and the counseling about the disease and sexuality offered to the woman and to her partner, seeking better care for patients can be further stimulated [6, 30]. Through the approach of sexual questions, the couple can develop acceptance and adaptation to alterations caused by the cancer and the sequences of its treatment [31].

In this perspective, Iavazzo et al. [32] evaluated the value of the Gynecological Advice Clinic from the Christie Hospital in Manchester, England. The service was instituted aiming to increase the support offered to the patients during treatments of gynecological cancer, as well as to prepare them to the potential consequences of the treatment. The study emphasizes the positive impact of offering information, advice and solutions to the psychosexual preoccupations of these patients in a context of multiprofessional assistance.

Despite such an approach being extremely important, negligence is observed from the majority of health professionals in the accompaniment routine post-treatment [7, 11, 13, 14, 33, 34]. This negligence can be a reflection of a fragmented vision on the part of some medical teams involved in treating the oncology patients, concentrating more on the health compromising aspects such as the presence of a residual or relapsing tumor, and leaving the sexuality as an afterthought despite its importance to the patients’ qualities of life [7].

Tozo et al. [1] affirmed that the women generally understood the unease in taking their sexual difficulties to the doctor, because the cultural context continues to marginalize female sexuality. Conversely, when complaining, some professionals demonstrate a lack of interest, as sexuality is not considered as an indispensible component of life quality and consequently of health. A large part of professionals in the health area are not found to be adequately prepared for the approach of sexual complaints. This can be related to the low knowledge, due to the lack of disciplines in curricular grades of graduation courses which approach human sexuality as not only limited to reproductive function. From this, there is no necessary support in academic training [1], reflected in a fragmented treatment which does not approach all the necessities of patients.

Variables relating to the possible adverse effects of treatments show negative impacts on sexual function. This shows the importance of a complete investigation, involving these alterations and the necessity of multi-professional assistance in accompanying these cancer patients post-treatment [35].

Through the multiple linear regression analysis, variables relating to the adverse effects of treatments could be observed, such as the interference in sexual life, the presence of stenosis/shortening, alteration of urination frequency, presence of urinary incontinence, rectal bleeding and tenesmus, are factors inversely related to the total FSFI score or can contribute to worse sexual function when present. These findings reinforce the need to create an interdisciplinary assistance model with focused actions for the detection and early intervention of adverse effects of treatment during the follow-ups, as well as orientation and post-discharge reference institutions. This conduct permits a proportionally improved quality of life post-cancer, as sexual function constitutes one of the two indices through which the level of life quality is measured [7].

As the main limitation of this research, the difficulty of recruiting cancer survivors is highlighted; this mostly occurred due to the outdated medical records and abandonment of tracking. From this, as there was no prior review, it could not be affirmed as certain that the observed alterations in the cancer group were exclusively caused by the treatment. Despite the small sample size, the hypothesis that the women subjected to the CC treatment presented a negatively impacted sexual function can be demonstrated with statistical significance, which should, thus, be the focus of interventions.

Against the present findings, it can be perceived that the main objective of follow-up consultations post-treatment of cervical cancer should not only be to evaluate the cure or monitor the relapse of tumors. The investigation of sexual function should also be considered, along with the factors that influence it, as it is an important component of life quality, even prior to therapeutic intervention. Visits are essential to facilitate the adoption of strategies which can make more comprehensive care, direct to the patients’ needs, possible in clinical practice, through a multi- and inter-disciplinary team.