ORIGINAL STUDY
Sexual Activity and Function in Patients With Gynecological Malignancies After Completed Treatment Donata Grimm, MD,* Annette Hasenburg, MD,Þ Christine Eulenburg, PhD,þ Lisa Steinsiek, MD,* Sebastian Mayer, MD,Þ Stephanie Eltrop, MD,Þ Katharina Prieske, MD,* Fabian Trillsch, MD,* Sven Mahner, MD,* and Linn Woelber, MD*
Objective: Sexual activity (SA) and sexual function (SF) after completion of treatment are central for quality of life (QoL) in women affected by gynecological cancer (GC). The aim of this study was to analyze the sexual outcome and overall QoL of women after treatment for primary GC compared with a healthy control group (CG). Methods: In a multicenter cross-sectional study, 77 women aged 28 to 67 years were surveyed at least 12 months after completion of primary therapy for cervical, endometrial, or vulvar cancer [gynecological cancer group (GCG)]. Data were collected through validated questionnaires (Female Sexual Function Index-d, EORTC Quality of Life Questionnaire-C30, and Sexual Activity Questionnaire) and compared to a control of 60 healthy women (CG). Results: In the GCG, 41.3% were sexually active compared to 78.0% in the CG. Twelve women of the CG and 42 women of the GCG indicated the reasons for their sexual inactivity. The most common reason for sexual inactivity in the GCG was ‘‘the-presence-of-a-physicalproblem’’ [18/42 (42.9%) vs 2/12 (16.7%) in the CG], whereas in the CG, ‘‘because-I-do-nothave-a-partner’’ was most common [6/12 (50.0%) vs 11/42 (26.2%) in the GCG]. Sexually active patients in the GCG had an SF comparable to the CG. In multivariate analysis of the total cohort (n = 137), relationship status [solid partnership vs living alone; odds ratio (OR), 33.82; 95% confidence interval (CI), 4.83Y236.70], smoking (OR, 0.25; 95% CI, 0.06Y1.03), and age (OR, 0.87; 95% CI, 0.79Y0.94) influenced SA significantly. The probability of SA thereby decreased with increasing age. Quality of life and subjective general health status were not significantly different between the GCG and the CG (EORTC Quality of Life Questionnaire-C30 score 68.25 vs 69.67). Conclusions: A high number of patients with GC remain sexually inactive after treatment, indicating that women experience persistent functional problems. However, women who regain SA after completed treatment have a good overall SF and vice versa. Key Words: Gynecological cancer, FSFI, Sexual activity, Sexual function, QoL Received January 23, 2015, and in revised form March 24, 2015. Accepted for publication March 24, 2015. (Int J Gynecol Cancer 2015;25: 1134Y1141)
*Department of Gynecology and Gynecologic Oncology, University Medical Center Hamburg-Eppendorf, Hamburg; †Department of Gynecology and Gynecologic Oncology, University Hospital Freiburg, Freiburg; ‡Department of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Copyright * 2015 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000468
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Address correspondence and reprint requests to Linn Woelber, MD, Department of Gynecology and Gynecologic Oncology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany. E-mail: [email protected]. Supported by internal departmental sources. The authors declare no conflicts of interest. Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal’s Web site (www.ijgc.net).
International Journal of Gynecological Cancer
& Volume 25, Number 6, July 2015
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International Journal of Gynecological Cancer
& Volume 25, Number 6, July 2015
of gynecological cancer (GC) includes, in most Treatment cases, radical surgery, and depending on tumor stage and
additional risk factors, adjuvant chemotherapy (CTX) and/or radiotherapy (RX). These oncologic therapies may cause significant physical adverse effects that can interfere with sexuality1: RX and/or CTX can damage neuronal structures as well as the vaginal tissue and also impair ovarian function in premenopausal women.2 Second, psychological and social factors associated with the diagnosis of cancer are also major factors influencing sexuality. Changes in self-perception with subjective loss of attractiveness are especially important in this context.3 Initially, the goal of GC treatment is to cure or considerably prolong the patients’ life; subsequently, the best possible quality of life (QoL) gets more important. Sexuality, rarely addressed during consultation, is an important dimension of QoL and of great interest for cancer patients and their partners before, during, and after treatment. Many patients with history of GC notice changes in their sexuality compared to the time before diagnosis.4Y8 Sexual dysfunction after GC, characterized by decreased desire or interest, arousal disorder, dyspareunia, and difficulty or inability to achieve orgasm is frequent with rates ranging from 30% to 100% in affected women.1,9Y12 Most women diagnosed with GC are elderly and postmenopausal; however, previous studies have also shown that elderly patients continue sexual relationships after diagnosis of cancer if possible.13,14 Sexuality should therefore be addressed as a central topic during consultation of all patients.15 Ekwall et al observed that openness and communication about sexual issues is often lacking.15,16 Patients and physicians consider sexual health to be a major concern, but deficits in communication are persisting.14,17Y20 A recent survey demonstrated that 40% to 68% of patients with GC and breast cancer felt that it would be helpful to speak with a sexual health expert, but only 7% to 10% had done so.21 Only 10% to 28% of patients with GC received information on sexual function (SF) from medical or paramedical personnel before start of treatment.8,22,23 Besides multiple obstacles, lack of scientific evidence regarding sexual behavior and impairment after treatment of GC especially in patients with endometrial cancer (EC) and vulvar cancer (VC) at least partially explains this communicational deficit. The aim of this multicenter cross-sectional study was to describe and analyze the sexual activity (SA), SF, and QoL of women with a primary diagnosis of cervical cancer (CC), EC, and VC after completed treatment. Results were compared with a healthy control group (CG).
MATERIALS AND METHODS Patients treated at the University Medical Center Hamburg-Eppendorf and the University Clinic of Freiburg between 1997 and 2008 were retrospectively identified to assess SA, SF, and QoL after completion of treatment. Inclusion criteria were as follows: ages 18 to 70 years; primary diagnosis of CC, EC, and VC and Q12 months or more intervals after completion of primary therapy. Exclusion criteria were preexisting depression, untreated thyroid dysfunction, and histologically proven recurrence and/or secondary malignancy. Patients were identified using existing tumor documentation
Sexuality After Treatment of GC
databases at the participating centers, consecutively contacted via telephone and informed about aims and scope of the study. After revision of the inclusion and exclusion criteria, patients were explicitly informed that participation was voluntary and that the data would be held confidential and anonymous. If the patients consented, pseudonymized questionnaires were sent via mail to assure undisturbed self-report. The study protocol was approved by the local ethics committees (leading vote Freiburg; reference number 397/09). The CG consisted of 60 healthy female patients of the University Dental Clinic of Freiburg who were prospectively selected. The questionnaires were handed out to consecutive patients during routine consultation. The criteria for inclusion were ages between 18 and 70 years, no history of cancer or depression, and no surgery during the last 4 weeks. Quality of life, SA, and SF were assessed by a questionnaire which was composed of 3 components from validated questionnaires to limit time and effort for participating patients: the complete Sexual Activity Questionnaire (SAQ), items 11 to 13 of the Female Sexual Function Index (FSFI), and 2 questions regarding general health and QoL of the EORTC Quality of Life Questionnaire (QLQ-C30).24Y26 Information about the patients’ demographics was obtained with an additional questionnaire.
Statistics Data are reported as median and range or mean and SD for continuous variables and as count and percent for categorical variables. Differences between groups were evaluated using Student’s t tests and Chi2 tests. Associations of different variables with SA were tested with multivariate logistic regression. As some variables had missing values, a multiple imputation step was performed before multivariate analysis. Statistical analysis was conducted using SPSS 21.0. The level of significance was 0.05.
RESULTS After prior consultation by telephone, 227 (87.3%) of 260 eligible women agreed to participate in the study and therefore received questionnaires via mailing. One hundred fifty-one women answered via mail (response rate of 66.5%), thereof, 71 with a nonparticipation declaration and 80 with valid questionnaires. Information regarding the patients not willing to participate and reasons given for nonparticipation are provided in Supplemental Table S1, http://links.lww.com/IGC/A297. Three of the 80 questionnaires could not be considered due to violations of inclusion criteria resulting in 77 GC patients. Overall, 137 patients were included in further analyses: 77 patients in the GC group [gynecological cancer group (GCG); CC (n = 38), EC (n = 18), and VC (n = 21)] and 60 healthy female patients of the University Dental Clinic Freiburg as CG.
Demographic and Clinical Data Baseline demographic data are displayed in Table 1. Comparing the GCG with the CG, significant differences regarding age, weight, body mass index (BMI), grade of education, alcohol intake, menopausal status, and concurrent medication were noted. Patients in the GCG had a significantly higher median age of 51 years (range, 28Y67 years)
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TABLE 1. Patient characteristics in the GCG (n = 77) and CG (n = 60), P values from Student’s t test for continuous variables, and from Chi2 test or Fisher’s test for categorical variables GCG (n = 77) Variable, median (range) Age, years Height, m Weight, kg BMI, kg/m2 Relationship, n (%) Living alone Married Solid partnership Grade of education, n (%) None Secondary school qualification High school Nicotin, n (%) Nonsmokers Smokers Alcohol (glasses/wk), n (%) 0 G1 1Y2 93 Unknown Menopausal status, n (%) Premenopausal Postmenopausal Unknown Family history of cancer, n (%) Yes No Any concurrent medication, n (%) Yes No
51 1.65 69 25.6
(28Y67) (1.53Y1.82) (48Y115) (18.1Y41.4)
17 (22.1) 47 (61.0) 13 (16. 9)
P
46 (21Y53) 1.68 (1.50Y1.85) 63 (43Y124) 22.5 (17.4Y36.2)
0.001 0.138 0.001 0.001 0.237
7 (11.7) 39 (65.0) 14 (23.3) 0.001
2 (2.6) 30 (39.0) 45 (58.5)
1 (1.7) 17 (28.3) 42 (70) 0.189
54 (70.1) 23 (29.9)
48 (80.0) 12 (20.0)
40 13 10 13 1
12 (20.0) 11 (18.3) 16 (26.7) 21 (35.0) 0 (0.0)
0.001 (51.9) (16.9) (13.0) (16.9) (1.3)
0.001 7 (9.1) 67 (87.0) 3 (3.9)
46 (76.7) 11 (18.3) 3 (5.0) 0.445
36 (46.7) 41 (53.3)
32 (53.3) 28 (46.7)
48 (62.3) 29 (37.7)
24 (40.0) 36 (60.0)
0.009
compared to 46 years (range, 21Y53 years) in the CG (P G 0.001); 87.0% of the patients in the GCG compared to only 18.3% in the CG were postmenopausal (P G 0.001).
Sexual Activity and Function With the SAQ part I, a total of 136 (76 in GCG and 60 in the CG) women provided information about their SA. However, not all questions were answered by each patient; in some cases, single items of the questionnaire remained unanswered. Therefore, the denominators vary for different items and are provided for each question. With regard to the question of SA in the SAQ part I, 78.0% (46/59) of women in the CG were sexually active compared to only 41.3% (31/75) in the GCG. In the SAQ part II, 12 women of the CG and 42 women of the GCG indicated the reasons for their sexual inactivity (Fig. 1).
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CG (n = 60)
The most common reason in the CG was ‘‘because-I-do-nothave-a-partner-at-the-moment’’ (6/12, 50%). ‘‘Other-reasons’’ besides prespecified causes for sexual inactivity in the CG were alienation of the partner and, in 1 case, a rheumatoid arthritis (2/12, 16.7%). The most common reason in the GCG was ‘‘because-I-have-a-physical-problem-which-makes-sexualrelations-difficult-or-uncomfortable’’ (18/42, 42.9%). This reason was most frequent in the group of patients with VC (8/12, 66.6%). Physical problems likely resulting from anticancer therapy in 5 cases, such as incontinence, stoma, and introitus stenosis in the GCG, are subsumed under ‘‘other-reasons,’’ completed by 15/42 (35.7%) patients. ‘‘Decreased-sexualdesire,’’ ‘‘arousal-disorder,’’ and ‘‘not-feeling-like-a-womanany-longer’’ were also named as ‘‘other-reasons’’ in the GCG. ‘‘I-am-not-interested-in-sex’’ and ‘‘I-am-too-tired’’ * 2015 IGCS and ESGO
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Sexuality After Treatment of GC
FIGURE 1. Reasons for sexual inactivity in the CG (n = 12) and the GCG (n = 42) in percent as indicated in the SAQ part 2. were more common in the GCG than the CG [15/42 (35.7%) vs 2/12 (16.7%) and 8/42 (19.0%) vs 0/12 (0%)] (Fig. 1). Answers related to the woman’s partner as the cause of inactivity were comparably expressed in both groups (Fig. 1). In multivariate analysis of the total cohort (n = 137; GCG = 77, CG = 60), age, relationship, and smoking status influenced SA significantly. The probability of SA [odds ratio (OR), 0.87; 95% confidence interval (CI), 0.799Y0.948] decreased with older age in years. Compared to single women, the probability of SA was highly increased in married women (OR, 14.54; 95% CI, 2.79Y75.69) and in women with solid relationships (OR, 33.82; 95% CI, 4.83Y236.70) (Table 2). There were no significant differences between cancer patients and the CG with regard to different tumor entities and SA. Furthermore, the impact of the investigated patient characteristics on SA was not significantly different, comparing GCG and CG. In SAQ part III and FSFI ‘‘orgasm,’’data from 77 (n = 31 GCG, n = 46 CG) sexually active women were available. Means and SDs of the factors ‘‘habit,’’ ‘‘pleasure,’’ ‘‘discomfort,’’ and ‘‘orgasm’’ without significant differences are listed in Table 3.
A total of 99 (GCG, n = 48; CG, n = 51) women estimated their subjective health status and 98 (GCG, n = 48; CG, n = 50) regarding their overall QoL on a 7-point scale from 1 ‘‘very bad’’ to 7 ‘‘excellent.’’ With regard to the health status, we found comparable mean values in the GCG (5.04 vs 5.16) with a median of 5 in both groups (P = 0.09). The QoL was also similar in both groups (5.15 in the GCG vs 5.2) in the CG (P = 0.79). For further evaluation, raw scores from the EORTC QLQ-C30 questionnaire were transformed according to standard methods (range, 0Y100).24 The EORTC QLQ-C30 score at 69.67 in the CG compared to 68.25 in the GCG did not reveal statistical differences. Table 4 displays the applied therapies in the GCG (n = 77), most (55.8%) of the patients underwent solely a surgical treatment. All 38 women with CC had surgery, 27/38 (71.1%) received a radical hysterectomy, 6/38 (15.8%) a conisation or simple hysterectomy, and 5/38 (13.1%) an exenteration. All 18 women with EC underwent a simple hysterectomy with adnexectomy, 5/18 (27.8%) women received additional lymphadenectomy (LAE), and 6/18 (33.3%) women additional LAE and omentectomy. All patients with VC (n = 21)
TABLE 2. Multivariate analysis regarding factors influencing SA in the GCG (n = 77) and the CG (n = 60)
Smoking (yes vs no) Age (continuously per year) BMI (continuously) Any medication vs none Relationship Married vs living alone Solid partnership vs living alone Postmenopausal vs premenopausal Cancer vs control Grade of education None vs high school qualification Secondary school qualification vs high school qualification
P
OR
0.005 0.001 0.857 0.470
0.254 0.870 0.991 1.471
0.001 G0.001 0.058 0.503
14.541 33.824 0.216 1.718
2.793Y75.698 4.833Y236.707 0.044Y1.053 0.352Y8.386
0.490 0.857
4.803 1.107
0.056Y412.535 0.367Y3.344
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95% CI 0.062Y1.030 0.799Y0.948 0.894Y1.097 0.516Y4.190
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TABLE 3. Sexual function in the GCG and the CG, SAQ part 3 + FSFI orgasm. SAQ Part 3 + FSFI Orgasm
GCG
CG
Item (range) and number (GCG/CG)
Mean
SD
Mean
SD
P
Habit (0Y3) (n = 30/n = 46) Pleasure (0Y18) (n = 30/n = 44) Discomfort (0Y6) (n = 31/n = 46) Orgasm (1.2Y6) (n = 30/n = 46)
0.80 11.97 1.55 4.95
0.71 3.84 1.65 1.34
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.563* 0.787* 0.291* 0.770*
*Student’s t test.
had local surgery and 18/21 (85.7%) underwent an additional inguinofemoral LAE [in 15 cases, full dissection (unilateral, n = 2; bilateral, n = 13); in 3 cases, a bilateral sentinel node dissection only; in 3 patients, data were not available]. Ten (47.6%) of 21 received a radical local excision (WLE), 8/21 (38.1%) a partial vulvectomy, and 3/21 (14.3%) a complete vulvectomy. Table 5 shows the SF of sexually active patients compared to the CG with regard to the different tumor entities. No significant differences regarding SF could be demonstrated. The impact of different therapeutic modalities on SA, SF, and QoL was analyzed for patients with CC (n = 38; median age, 43 years) and VC (n = 21; median age, 52 years). Owing to the low response rate for SA and SF (4/18), patients with EC were not included in these calculations. Sixteen (42.1%) of 38 patients with CC were solely treated surgically and 22/38 (57.9%) with additional chemoradiation (RTX) (Table 4). In the group of patients treated with surgery plus adjuvant RTX, SA was substantially lower compared to those undergoing surgery only (38.1% vs 66.7%, Table 6). Likewise, SF was worse (ie, ‘‘pleasure’’ 11.63 vs 13.8, P = 0.180) and overall QoL impaired (EORTC score 67.3 vs 71.2, P = 0.673) without reaching statistical significance. Sixteen (76.2%) of 21 patients with VC were solely treated surgically and 5/21 (23.8%) with surgery plus RX (Table 4). Eight (38.1%) of 21 patients were sexually active (Table 6). Women treated with WLE instead of complete vulvectomy had a higher SA (n = 5/10, 50% vs n = 4/11, 36.4%), better SF [significant for the factor ‘‘orgasm’’ (mean 5.6 vs 2.9, P = 0.041)], as well as in trend better subjective general health
(mean 5.86 vs 4.75, P = 0.213) and QoL (mean 6.29 vs 4.75, P = 0.064) (Table 6). Furthermore, women with preservation of the clitoris [11/21 (52.3%) versus without 10/21 (47.6)] were more often sexually active (6/11, 54.5% vs 3/10, 30%, P = 0.387). The exact time interval between completion of anticancer treatment and response to the questionnaire was known in 76/77 cases (98.7%). Treatment was completed in median 3 years before this study (range, 1Y11 years). To analyze the impact of the time interval between completed therapy and answering of the questionnaire on SA and SF, we further divided the current study population into 2 groups, namely in a short-term cohort (n = 33, 1Y3 years after primary therapy) and a long-term cohort (n = 43, Q4 years after primary therapy). Results are displayed in Supplemental Table S2, http://links.lww.com/IGC/A297. Sexual activity was lower in the short-term cohort (30.3% vs 48.8% in the long-term cohort), whereas SF did not differ between the 2 groups. Subjective health status (median, 5 and 5) and QoL (median, 5.5 and 5) did not also significantly differ.
DISCUSSION The aim of this study was to analyze the SA, SF, and QoL of women with completed treatment for primary GC compared with a healthy control. Additionally, information about the association between radicality as well as treatment modality and SF was assessed. We observed that 41.3% of the cancer patients were sexually active compared to 78.0% of women in the CG. The most common reason for sexual inactivity in the GCG was
TABLE 4. Primary therapy of all GC patients (GCG, n = 77) with regard to the different tumor entities [CC (n = 38), EC (n = 18), and VC (n = 21)] Tumorentity CC (n = 38)
Total
EC (n = 18)
VC (n = 21)
Therapy
Number
%
Number
%
Number
%
Number
%
S S + CTX S + RX S + RTX
16 0 0 22
42.1 0 0 57.9
11 1 5 1
61.1 5.6 27.8 5.6
16 0 5 0
76.2 0 23.8 0
43 1 10 23
55.8 1.3 13.0 29.9
S, Surgery, CTX, Chemotherapy, RX, Radiotherapy, RTX, Chemoradiation.
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International Journal of Gynecological Cancer
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Sexuality After Treatment of GC
TABLE 5. Sexual function of patients in the GCG compared to the CG with regard to different tumor entities SAQ Part 3 + FSFI Orgasm Item (range) and number (GCG and CG) CC (n = 18) Habit (0Y3) (n = 18/n = 46) Pleasure (0Y18) (n = 18/n = 44) Discomfort (0Y6) (n = 18/n = 46) Orgasm (1.2Y6) (n = 18/n = 46) EC (n = 4) Habit (0Y3) (n = 4/n = 46) Pleasure (0Y18) (n = 4/n = 44) Discomfort (0Y6) (n = 4/n = 46) Orgasm (1.2Y6) (n = 4/n = 46) VC (n = 8) Habit (0Y3) (n = 8/n = 46) Pleasure (0Y18) (n = 8/n = 44) Discomfort (0Y6) (n = 8/n = 46) Orgasm (1.2Y6) (n = 8/n = 46)
GCG
CG
Mean
SD
Mean
SD
P
0.83 12.83 1.89 5.24
0.62 3.37 1.81 0.99
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.719* 0.241* 0.123* 0.188*
1.25 8.75 0.75 5
1.26 2.50 0.96 0.95
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.323* 0.118* 0.648* 0.762*
0.5 11.63 1.22 4.25
0.54 4.78 1.48 1.98
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.098* 0.973* 0.900* 0.305*
*Student’s t test.
‘‘the-presence-of-a-physical-problem’’ (42.9%) and ‘‘becauseI-don’t-have-a-partner’’ in the CG (50.0%). Previous studies identified the lack of a partner not only as the most common reason for sexual inactivity in healthy cohorts but also in cohorts of patients with CC or ovarian cancer.5,26,27 In contrast to our study, presence of a ‘‘physical-problem’’ was less often identified in previous studies using the SAQ: in patients with primary CC, Wenzel et al27 and Greimel et al28 reported a physical problem with a frequency of 13.2% [treatment: surgery with or without CTX and/or RX, 1Y11 years after treatment, median age 47.8 (surgery alone), 42.6 (surgery and CTX), 46.2 (surgery and RX) -years)] and 13.0% (no information on mode of treatment, initial diagnosis 5Y10 years ago, mean age 37 years). Consistent with previous data from healthy cohorts, SA decreased with higher median age in our study.29,30 Multivariate analysis showed consistent results with age, relationship status, and smoking habits influencing SA significantly. Patients in the GCG of our study were, however, 5 years older (median 51 vs 46 years in the CG) and almost all postmenopausal (87.0% vs 18.3% in the CG). Furthermore, the lack of a partner was more frequent in the GCG (22.1% vs 11.7% in the CG). The discrepancies between ages and postmenopausal status of the CG and the GCG are a making interpretation of the statistically significant difference in SA observed between the groups difficult. However, opposite to the CG, the most common reason for inactivity in the GCG was ‘‘the-presence-of-aphysical-problem’’ with 42.9%. These results confirm that at least to some extent lower SA in the GCG originated from the earlier illness. Despite limited comparability, SF, QoL, and subjective general health were not significantly different between the GCG and CG and similar to populations without cancer.26 These results show that although far fewer women in the GCG were sexually active, the SF of patients actually active
was not different from that seen in healthy women. Even more, sexual ‘‘pleasure’’ in the GCG was in trend greater although the degree of ‘‘discomfort’’ during intercourse was higher. This effect was pronounced in the group of patients with CC with a better comparability to the CG (median age 43 vs 46 years in the CG and SA 50.0% vs 78.0% in the CG): sexually active patients after CC had a higher score for sexual ‘‘pleasure’’ and ‘‘orgasm’’ than women in the CG although more ‘‘discomfort’’ during intercourse was reported [mean 1.89 vs 1.13 (P = 0.123)]. This is in line with a recent review showing that CC survivors are at risk for sexual pain disorders, whereas sexual satisfaction is not impaired.31 Regarding different therapy modalities in CC, our analysis showed less SA (38.1% vs 66.7%), worse SF, and overall QoL in patients treated with surgery and adjuvant RTX in contrast to those solely treated surgically, in line with previously published data.28,32Y34 Especially pain disorders are negatively influenced by RX.31 Patients with VC had a lower sexual frequency compared to the CG [‘‘habit’’ mean 0.5 vs 0.89 (P = 0.098)]. Differences between sexually active VC patients and the CG regarding ‘‘discomfort,’’ ‘‘pleasure,’’ and ‘‘orgasm’’ were, however, of minor importance. Previous studies on VC have shown higher rates of sexual dysfunction, in particular concerning ‘‘arousal’’ and ‘‘orgasm’’ difficulties.35Y38 However, in these studies, the time intervals from therapy to interview were inhomogeneous and the number of cases was very small.32 In our study, sexually active VC patients treated with radical local excision instead of vulvectomy had a better SF with significantly higher values for the factor ‘‘orgasm.’’ Patients with preserved clitoris had significantly higher values for the factor ‘‘pleasure’’ than those after resection of the clitoris. Nevertheless, 66.7% of the patients with VC were sexually inactive because of a physical problem. Likes et al39 demonstrated
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TABLE 6. Results of the SAQ, FSFI, and EORTC QLQ-C30 of patients with VC and CC with regard to the applied treatment modalities CC (n = 38) Therapy
Surgery
Surgery + RTX
Number
16
22
10/15 (66.7%)
8/21 (38.1%)
Sexually active Item (Range) and Number (S/SR)
Mean
SD
Mean
SD
P*
Habit (0Y3) (n = 10/n = 8) Pleasure (0Y18) (n = 10/n = 8) Discomfort (0Y6) (n = 10/n = 8) Orgasm (1.2Y6) (n = 10/n = 8) QoL (n = 11/n = 13) Subjective health (n = 11/n = 13)
0.90 13.8 1.80 5.40 5.27 5.27
0.74 3.12 2.20 0.87 1.55 1.35
0.75 11.63 2.00 5.05 5.00 5.08
0.46 3.46 1.31 1.15 1.35 1.32
0.624 0.180 0.824 0.472 0.650 0.723
VC (n = 21) Therapy
Wide Local Excision
Vulvectomy
Number
10
11
5/10 (50.0%)
4/11 (36.4%)
Sexually active Item (Range) and Number (WLE/V)
Mean
SD
Mean
SD
P*
Habit (0Y3) (n = 4/n = 4) Pleasure (0Y18) (n = 4/n = 4) Discomfort (0Y6) (n = 5/n = 4) Orgasm (1.2Y6) (n = 4/n = 4) QoL (n = 7/n = 4) Subjective health (n = 7/n = 4)
0.75 15.0 0.6 5.6 6.29 5.86
0.50 2.16 1.34 0.80 0.76 1.07
0.25 8.25 2.0 2.9 4.75 4.75
0.50 4.27 1.41 1.91 1.71 1.71
0.207 0.030 0.172 0.041 0.064 0.213
*Student’s t test. S, Surgery; SR, surgery + RTX; V, vulvectomy; WLE, wide local excision.
supporting results: older age and a more extensive vulvar excision were associated with poor SF and QoL. So far, there are very limited data on the time course and changes in SA and SF after GC treatment. In our study, SA was a little lower in the short-term cohort (1Y3 years after primary therapy) in patients with GC (30.3 % vs 48.8% Q4 years after primary therapy) but SF did not differ. In a study by Jensen et al,33 173 women with early-stage CC were interviewed within the first 2 years after primary therapy at specific time intervals. Within these 2 years, a decline in sexual inactivity was noted (25% after 3 months to 11% after 24 months). Sexual satisfaction, level of discomfort, and orgasm ability during intercourse did not change. Although direct comparison to our results is difficult, similar trends can be observed: fewer women are sexually active shortly after therapy. Women who regain SA have a good overall SF. A possible limitation of our study is the nonresponder rate. It remains unclear whether nonresponders had more or less physical problems and were therefore less motivated to answer questions about their SA. We tried to minimize this possible selection bias by initial telephone contact and the
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option to complete a nonparticipation declaration. Strength of the study is the high response rate of 66.5%, resulting in 77 patients included. Taken together, the impact of a GC diagnosis and subsequent treatment on women’s sexuality is profound.40 A high number of patients with GC remain sexually inactive, indicating that women may experience persistent functional problems especially after multimodal treatment or extensive surgery. However, women who regain SA after completed treatment have a good overall SF and vice versa. Gynecologic oncologists should therefore find effective communication strategies to support their patients improve their SA. Instead of focusing on resuming vaginal intercourse, counseling for avoiding pain might be more important. To confirm the results obtained with this study, larger longitudinal studies are desirable.
REFERENCES 1. Abbott-Anderson K, Kwekkeboom KL. A systematic review of sexual concerns reported by gynecological cancer survivors. Gynecol Oncol. 2012;124:477Y489. * 2015 IGCS and ESGO
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2. Alder J, Bitzer J. [Gynecological cancer and sexuality]. Ther Umsch. 2011;68:581Y586. 3. Pilger A, Richter R, Fotopoulou C, et al. Quality of life and sexuality of patients after treatment for gynaecological malignancies: results of a prospective study in 55 patients. Anticancer Res. 2012;32:5045Y5049. 4. Liavaag AH, Dorum A, Bjoro T, et al. A controlled study of sexual activity and functioning in epithelial ovarian cancer survivors. A therapeutic approach. Gynecol Oncol. 2008;108:348Y354. 5. Taylor KL, Shelby R, Gelmann E, et al. Quality of life and trial adherence among participants in the prostate, lung, colorectal, and ovarian cancer screening trial. J Natl Cancer Inst. 2004;96:1083Y1094. 6. Donovan KA, Small BJ, Andrykowski MA, et al. Utility of a cognitive-behavioral model to predict fatigue following breast cancer treatment. Health Psychol. 2007;26:464Y472. 7. Juraskova I, Butow P, Robertson R, et al. Post-treatment sexual adjustment following cervical and endometrial cancer: a qualitative insight. Psychooncology. 2003;12:267Y279. 8. Tangjitgamol S, Manusirivithaya S, Hanprasertpong J, et al. Sexual dysfunction in Thai women with early-stage cervical cancer after radical hysterectomy. Int J Gynecol Cancer. 2007;17:1104Y1112. 9. Anderson B. Quality of life in progressive ovarian cancer. Gynecol Oncol. 1994;55:S151YS155. 10. Bodurka DC, Sun CC. Sexual function after gynecologic cancer. Obstet Gynecol Clin North Am. 2006;33:621Y630, ix. 11. Brotto LA, Yule M, Breckon E. Psychological interventions for the sexual sequelae of cancer: a review of the literature. J Cancer Surviv. 2010;4:346Y360. 12. Audette C, Waterman J. The sexual health of women after gynecologic malignancy. J Midwifery Womens Health. 2010;55:357Y362. 13. Shell JA, Smith CK. Sexuality and the older person with cancer. Oncol Nurs Forum. 1994;21:553Y558. 14. Carter J, Stabile C, Gunn A, et al. The physical consequences of gynecologic cancer surgery and their impact on sexual, emotional, and quality of life issues. J Sex Med. 2013; 10 Suppl 1:21Y34. 15. Stead ML. Sexual function after treatment for gynecological malignancy. Curr Opin Oncol. 2004;16:492Y495. 16. Ekwall E, Ternestedt BM, Sorbe B. Important aspects of health care for women with gynecologic cancer. Oncol Nurs Forum. 2003;30:313Y319. 17. Lindau ST, Gavrilova N, Anderson D. Sexual morbidity in very long term survivors of vaginal and cervical cancer: a comparison to national norms. Gynecol Oncol. 2007;106:413Y418. 18. Carter J, Goldfrank D, Schover LR. Simple strategies for vaginal health promotion in cancer survivors. J Sex Med. 2011;8:549Y559. 19. Quinn GP, Vadaparampil ST, Lee JH, et al. Physician referral for fertility preservation in oncology patients: a national study of practice behaviors. J Clin Oncol. 2009;27:5952Y5957. 20. Rogers M, Todd C. Information exchange in oncology outpatient clinics: source, valence and uncertainty. Psychooncology. 2002;11:336Y345. 21. Hill EK, Sandbo S, Abramsohn E, et al. Assessing gynecologic and breast cancer survivors’ sexual health care needs. Cancer. 2011;117:2643Y2651.
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22. Tsai TY, Chen SY, Tsai MH, et al. Prevalence and associated factors of sexual dysfunction in cervical cancer patients. J Sex Med. 2011;8:1789Y1796. 23. Stead ML, Brown JM, Fallowfield L, et al. Lack of communication between healthcare professionals and women with ovarian cancer about sexual issues. Br J Cancer. 2003;88:666Y671. 24. Aaronson NK, Ahmedzai S, Bergman B, et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst. 1993;85:365Y376. 25. Rosen R, Brown C, Heiman J, et al. The Female Sexual Function Index (FSFI): a multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther. 2000;26:191Y208. 26. Thirlaway K, Fallowfield L, Cuzick J. The Sexual Activity Questionnaire: a measure of women’s sexual functioning. Qual Life Res. 1996;5:81Y90. 27. Wenzel L, DeAlba I, Habbal R, et al. Quality of life in long-term cervical cancer survivors. Gynecol Oncol. 2005;97:310Y317. 28. Greimel ER, Winter R, Kapp KS, et al. Quality of life and sexual functioning after cervical cancer treatment: a long-term follow-up study. Psychooncology. 2009;18:476Y482. 29. Chedraui P, Perez-Lopez FR, San Miguel G, et al. Assessment of sexuality among middle-aged women using the Female Sexual Function Index. Climacteric. 2009;12:213Y221. 30. Lindau ST, Schumm LP, Laumann EO, et al. A study of sexuality and health among older adults in the United States. N Engl J Med. 2007;357:762Y774. 31. Lammerink EA, de Bock GH, Pras E, et al. Sexual functioning of cervical cancer survivors: a review with a female perspective. Maturitas. 2012;72:296Y304. 32. Frumovitz M, Sun CC, Schover LR, et al. Quality of life and sexual functioning in cervical cancer survivors. J Clin Oncol. 2005;23:7428Y7436. 33. Jensen PT, Groenvold M, Klee MC, et al. Longitudinal study of sexual function and vaginal changes after radiotherapy for cervical cancer. Int J Radiat Oncol Biol Phys. 2003;56:937Y949. 34. Park SY, Bae DS, Nam JH, et al. Quality of life and sexual problems in disease-free survivors of cervical cancer compared with the general population. Cancer. 2007;110:2716Y2725. 35. van de Wiel HB, Schultz WC, Hallensleben A, et al. Sexual functioning following treatment of cervical carcinoma. Eur J Gynaecol Oncol. 1988;9:275Y281. 36. Green MS, Naumann RW, Elliot M, et al. Sexual dysfunction following vulvectomy. Gynecol Oncol. 2000;77:73Y77. 37. Weijmar Schultz WC, van de Wiel HB, Bouma J, et al. Psychosexual functioning after the treatment of cancer of the vulva. A longitudinal study. Cancer. 1990;66:402Y407. 38. Aerts L, Enzlin P, Vergote I, et al. Sexual, psychological, and relational functioning in women after surgical treatment for vulvar malignancy: a literature review. J Sex Med. 2012;9:361Y371. 39. Likes WM, Stegbauer C, Tillmanns T, et al. Correlates of sexual function following vulvar excision. Gynecol Oncol. 2007;105:600Y603. 40. Barbera L, Fitch M, Adams L, et al. Improving care for women after gynecological cancer: the development of a sexuality clinic. Menopause. 2011;18:1327Y1333.
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Sexual Activity and Function in Patients With Gynecological Malignancies After Completed Treatment Donata Grimm, MD,* Annette Hasenburg, MD,Þ Christine Eulenburg, PhD,þ Lisa Steinsiek, MD,* Sebastian Mayer, MD,Þ Stephanie Eltrop, MD,Þ Katharina Prieske, MD,* Fabian Trillsch, MD,* Sven Mahner, MD,* and Linn Woelber, MD*
Objective: Sexual activity (SA) and sexual function (SF) after completion of treatment are central for quality of life (QoL) in women affected by gynecological cancer (GC). The aim of this study was to analyze the sexual outcome and overall QoL of women after treatment for primary GC compared with a healthy control group (CG). Methods: In a multicenter cross-sectional study, 77 women aged 28 to 67 years were surveyed at least 12 months after completion of primary therapy for cervical, endometrial, or vulvar cancer [gynecological cancer group (GCG)]. Data were collected through validated questionnaires (Female Sexual Function Index-d, EORTC Quality of Life Questionnaire-C30, and Sexual Activity Questionnaire) and compared to a control of 60 healthy women (CG). Results: In the GCG, 41.3% were sexually active compared to 78.0% in the CG. Twelve women of the CG and 42 women of the GCG indicated the reasons for their sexual inactivity. The most common reason for sexual inactivity in the GCG was ‘‘the-presence-of-a-physicalproblem’’ [18/42 (42.9%) vs 2/12 (16.7%) in the CG], whereas in the CG, ‘‘because-I-do-nothave-a-partner’’ was most common [6/12 (50.0%) vs 11/42 (26.2%) in the GCG]. Sexually active patients in the GCG had an SF comparable to the CG. In multivariate analysis of the total cohort (n = 137), relationship status [solid partnership vs living alone; odds ratio (OR), 33.82; 95% confidence interval (CI), 4.83Y236.70], smoking (OR, 0.25; 95% CI, 0.06Y1.03), and age (OR, 0.87; 95% CI, 0.79Y0.94) influenced SA significantly. The probability of SA thereby decreased with increasing age. Quality of life and subjective general health status were not significantly different between the GCG and the CG (EORTC Quality of Life Questionnaire-C30 score 68.25 vs 69.67). Conclusions: A high number of patients with GC remain sexually inactive after treatment, indicating that women experience persistent functional problems. However, women who regain SA after completed treatment have a good overall SF and vice versa. Key Words: Gynecological cancer, FSFI, Sexual activity, Sexual function, QoL Received January 23, 2015, and in revised form March 24, 2015. Accepted for publication March 24, 2015. (Int J Gynecol Cancer 2015;25: 1134Y1141)
*Department of Gynecology and Gynecologic Oncology, University Medical Center Hamburg-Eppendorf, Hamburg; †Department of Gynecology and Gynecologic Oncology, University Hospital Freiburg, Freiburg; ‡Department of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Copyright * 2015 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000468
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Address correspondence and reprint requests to Linn Woelber, MD, Department of Gynecology and Gynecologic Oncology, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246 Hamburg, Germany. E-mail: [email protected]. Supported by internal departmental sources. The authors declare no conflicts of interest. Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal’s Web site (www.ijgc.net).
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& Volume 25, Number 6, July 2015
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& Volume 25, Number 6, July 2015
of gynecological cancer (GC) includes, in most Treatment cases, radical surgery, and depending on tumor stage and
additional risk factors, adjuvant chemotherapy (CTX) and/or radiotherapy (RX). These oncologic therapies may cause significant physical adverse effects that can interfere with sexuality1: RX and/or CTX can damage neuronal structures as well as the vaginal tissue and also impair ovarian function in premenopausal women.2 Second, psychological and social factors associated with the diagnosis of cancer are also major factors influencing sexuality. Changes in self-perception with subjective loss of attractiveness are especially important in this context.3 Initially, the goal of GC treatment is to cure or considerably prolong the patients’ life; subsequently, the best possible quality of life (QoL) gets more important. Sexuality, rarely addressed during consultation, is an important dimension of QoL and of great interest for cancer patients and their partners before, during, and after treatment. Many patients with history of GC notice changes in their sexuality compared to the time before diagnosis.4Y8 Sexual dysfunction after GC, characterized by decreased desire or interest, arousal disorder, dyspareunia, and difficulty or inability to achieve orgasm is frequent with rates ranging from 30% to 100% in affected women.1,9Y12 Most women diagnosed with GC are elderly and postmenopausal; however, previous studies have also shown that elderly patients continue sexual relationships after diagnosis of cancer if possible.13,14 Sexuality should therefore be addressed as a central topic during consultation of all patients.15 Ekwall et al observed that openness and communication about sexual issues is often lacking.15,16 Patients and physicians consider sexual health to be a major concern, but deficits in communication are persisting.14,17Y20 A recent survey demonstrated that 40% to 68% of patients with GC and breast cancer felt that it would be helpful to speak with a sexual health expert, but only 7% to 10% had done so.21 Only 10% to 28% of patients with GC received information on sexual function (SF) from medical or paramedical personnel before start of treatment.8,22,23 Besides multiple obstacles, lack of scientific evidence regarding sexual behavior and impairment after treatment of GC especially in patients with endometrial cancer (EC) and vulvar cancer (VC) at least partially explains this communicational deficit. The aim of this multicenter cross-sectional study was to describe and analyze the sexual activity (SA), SF, and QoL of women with a primary diagnosis of cervical cancer (CC), EC, and VC after completed treatment. Results were compared with a healthy control group (CG).
MATERIALS AND METHODS Patients treated at the University Medical Center Hamburg-Eppendorf and the University Clinic of Freiburg between 1997 and 2008 were retrospectively identified to assess SA, SF, and QoL after completion of treatment. Inclusion criteria were as follows: ages 18 to 70 years; primary diagnosis of CC, EC, and VC and Q12 months or more intervals after completion of primary therapy. Exclusion criteria were preexisting depression, untreated thyroid dysfunction, and histologically proven recurrence and/or secondary malignancy. Patients were identified using existing tumor documentation
Sexuality After Treatment of GC
databases at the participating centers, consecutively contacted via telephone and informed about aims and scope of the study. After revision of the inclusion and exclusion criteria, patients were explicitly informed that participation was voluntary and that the data would be held confidential and anonymous. If the patients consented, pseudonymized questionnaires were sent via mail to assure undisturbed self-report. The study protocol was approved by the local ethics committees (leading vote Freiburg; reference number 397/09). The CG consisted of 60 healthy female patients of the University Dental Clinic of Freiburg who were prospectively selected. The questionnaires were handed out to consecutive patients during routine consultation. The criteria for inclusion were ages between 18 and 70 years, no history of cancer or depression, and no surgery during the last 4 weeks. Quality of life, SA, and SF were assessed by a questionnaire which was composed of 3 components from validated questionnaires to limit time and effort for participating patients: the complete Sexual Activity Questionnaire (SAQ), items 11 to 13 of the Female Sexual Function Index (FSFI), and 2 questions regarding general health and QoL of the EORTC Quality of Life Questionnaire (QLQ-C30).24Y26 Information about the patients’ demographics was obtained with an additional questionnaire.
Statistics Data are reported as median and range or mean and SD for continuous variables and as count and percent for categorical variables. Differences between groups were evaluated using Student’s t tests and Chi2 tests. Associations of different variables with SA were tested with multivariate logistic regression. As some variables had missing values, a multiple imputation step was performed before multivariate analysis. Statistical analysis was conducted using SPSS 21.0. The level of significance was 0.05.
RESULTS After prior consultation by telephone, 227 (87.3%) of 260 eligible women agreed to participate in the study and therefore received questionnaires via mailing. One hundred fifty-one women answered via mail (response rate of 66.5%), thereof, 71 with a nonparticipation declaration and 80 with valid questionnaires. Information regarding the patients not willing to participate and reasons given for nonparticipation are provided in Supplemental Table S1, http://links.lww.com/IGC/A297. Three of the 80 questionnaires could not be considered due to violations of inclusion criteria resulting in 77 GC patients. Overall, 137 patients were included in further analyses: 77 patients in the GC group [gynecological cancer group (GCG); CC (n = 38), EC (n = 18), and VC (n = 21)] and 60 healthy female patients of the University Dental Clinic Freiburg as CG.
Demographic and Clinical Data Baseline demographic data are displayed in Table 1. Comparing the GCG with the CG, significant differences regarding age, weight, body mass index (BMI), grade of education, alcohol intake, menopausal status, and concurrent medication were noted. Patients in the GCG had a significantly higher median age of 51 years (range, 28Y67 years)
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TABLE 1. Patient characteristics in the GCG (n = 77) and CG (n = 60), P values from Student’s t test for continuous variables, and from Chi2 test or Fisher’s test for categorical variables GCG (n = 77) Variable, median (range) Age, years Height, m Weight, kg BMI, kg/m2 Relationship, n (%) Living alone Married Solid partnership Grade of education, n (%) None Secondary school qualification High school Nicotin, n (%) Nonsmokers Smokers Alcohol (glasses/wk), n (%) 0 G1 1Y2 93 Unknown Menopausal status, n (%) Premenopausal Postmenopausal Unknown Family history of cancer, n (%) Yes No Any concurrent medication, n (%) Yes No
51 1.65 69 25.6
(28Y67) (1.53Y1.82) (48Y115) (18.1Y41.4)
17 (22.1) 47 (61.0) 13 (16. 9)
P
46 (21Y53) 1.68 (1.50Y1.85) 63 (43Y124) 22.5 (17.4Y36.2)
0.001 0.138 0.001 0.001 0.237
7 (11.7) 39 (65.0) 14 (23.3) 0.001
2 (2.6) 30 (39.0) 45 (58.5)
1 (1.7) 17 (28.3) 42 (70) 0.189
54 (70.1) 23 (29.9)
48 (80.0) 12 (20.0)
40 13 10 13 1
12 (20.0) 11 (18.3) 16 (26.7) 21 (35.0) 0 (0.0)
0.001 (51.9) (16.9) (13.0) (16.9) (1.3)
0.001 7 (9.1) 67 (87.0) 3 (3.9)
46 (76.7) 11 (18.3) 3 (5.0) 0.445
36 (46.7) 41 (53.3)
32 (53.3) 28 (46.7)
48 (62.3) 29 (37.7)
24 (40.0) 36 (60.0)
0.009
compared to 46 years (range, 21Y53 years) in the CG (P G 0.001); 87.0% of the patients in the GCG compared to only 18.3% in the CG were postmenopausal (P G 0.001).
Sexual Activity and Function With the SAQ part I, a total of 136 (76 in GCG and 60 in the CG) women provided information about their SA. However, not all questions were answered by each patient; in some cases, single items of the questionnaire remained unanswered. Therefore, the denominators vary for different items and are provided for each question. With regard to the question of SA in the SAQ part I, 78.0% (46/59) of women in the CG were sexually active compared to only 41.3% (31/75) in the GCG. In the SAQ part II, 12 women of the CG and 42 women of the GCG indicated the reasons for their sexual inactivity (Fig. 1).
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CG (n = 60)
The most common reason in the CG was ‘‘because-I-do-nothave-a-partner-at-the-moment’’ (6/12, 50%). ‘‘Other-reasons’’ besides prespecified causes for sexual inactivity in the CG were alienation of the partner and, in 1 case, a rheumatoid arthritis (2/12, 16.7%). The most common reason in the GCG was ‘‘because-I-have-a-physical-problem-which-makes-sexualrelations-difficult-or-uncomfortable’’ (18/42, 42.9%). This reason was most frequent in the group of patients with VC (8/12, 66.6%). Physical problems likely resulting from anticancer therapy in 5 cases, such as incontinence, stoma, and introitus stenosis in the GCG, are subsumed under ‘‘other-reasons,’’ completed by 15/42 (35.7%) patients. ‘‘Decreased-sexualdesire,’’ ‘‘arousal-disorder,’’ and ‘‘not-feeling-like-a-womanany-longer’’ were also named as ‘‘other-reasons’’ in the GCG. ‘‘I-am-not-interested-in-sex’’ and ‘‘I-am-too-tired’’ * 2015 IGCS and ESGO
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Sexuality After Treatment of GC
FIGURE 1. Reasons for sexual inactivity in the CG (n = 12) and the GCG (n = 42) in percent as indicated in the SAQ part 2. were more common in the GCG than the CG [15/42 (35.7%) vs 2/12 (16.7%) and 8/42 (19.0%) vs 0/12 (0%)] (Fig. 1). Answers related to the woman’s partner as the cause of inactivity were comparably expressed in both groups (Fig. 1). In multivariate analysis of the total cohort (n = 137; GCG = 77, CG = 60), age, relationship, and smoking status influenced SA significantly. The probability of SA [odds ratio (OR), 0.87; 95% confidence interval (CI), 0.799Y0.948] decreased with older age in years. Compared to single women, the probability of SA was highly increased in married women (OR, 14.54; 95% CI, 2.79Y75.69) and in women with solid relationships (OR, 33.82; 95% CI, 4.83Y236.70) (Table 2). There were no significant differences between cancer patients and the CG with regard to different tumor entities and SA. Furthermore, the impact of the investigated patient characteristics on SA was not significantly different, comparing GCG and CG. In SAQ part III and FSFI ‘‘orgasm,’’data from 77 (n = 31 GCG, n = 46 CG) sexually active women were available. Means and SDs of the factors ‘‘habit,’’ ‘‘pleasure,’’ ‘‘discomfort,’’ and ‘‘orgasm’’ without significant differences are listed in Table 3.
A total of 99 (GCG, n = 48; CG, n = 51) women estimated their subjective health status and 98 (GCG, n = 48; CG, n = 50) regarding their overall QoL on a 7-point scale from 1 ‘‘very bad’’ to 7 ‘‘excellent.’’ With regard to the health status, we found comparable mean values in the GCG (5.04 vs 5.16) with a median of 5 in both groups (P = 0.09). The QoL was also similar in both groups (5.15 in the GCG vs 5.2) in the CG (P = 0.79). For further evaluation, raw scores from the EORTC QLQ-C30 questionnaire were transformed according to standard methods (range, 0Y100).24 The EORTC QLQ-C30 score at 69.67 in the CG compared to 68.25 in the GCG did not reveal statistical differences. Table 4 displays the applied therapies in the GCG (n = 77), most (55.8%) of the patients underwent solely a surgical treatment. All 38 women with CC had surgery, 27/38 (71.1%) received a radical hysterectomy, 6/38 (15.8%) a conisation or simple hysterectomy, and 5/38 (13.1%) an exenteration. All 18 women with EC underwent a simple hysterectomy with adnexectomy, 5/18 (27.8%) women received additional lymphadenectomy (LAE), and 6/18 (33.3%) women additional LAE and omentectomy. All patients with VC (n = 21)
TABLE 2. Multivariate analysis regarding factors influencing SA in the GCG (n = 77) and the CG (n = 60)
Smoking (yes vs no) Age (continuously per year) BMI (continuously) Any medication vs none Relationship Married vs living alone Solid partnership vs living alone Postmenopausal vs premenopausal Cancer vs control Grade of education None vs high school qualification Secondary school qualification vs high school qualification
P
OR
0.005 0.001 0.857 0.470
0.254 0.870 0.991 1.471
0.001 G0.001 0.058 0.503
14.541 33.824 0.216 1.718
2.793Y75.698 4.833Y236.707 0.044Y1.053 0.352Y8.386
0.490 0.857
4.803 1.107
0.056Y412.535 0.367Y3.344
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95% CI 0.062Y1.030 0.799Y0.948 0.894Y1.097 0.516Y4.190
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TABLE 3. Sexual function in the GCG and the CG, SAQ part 3 + FSFI orgasm. SAQ Part 3 + FSFI Orgasm
GCG
CG
Item (range) and number (GCG/CG)
Mean
SD
Mean
SD
P
Habit (0Y3) (n = 30/n = 46) Pleasure (0Y18) (n = 30/n = 44) Discomfort (0Y6) (n = 31/n = 46) Orgasm (1.2Y6) (n = 30/n = 46)
0.80 11.97 1.55 4.95
0.71 3.84 1.65 1.34
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.563* 0.787* 0.291* 0.770*
*Student’s t test.
had local surgery and 18/21 (85.7%) underwent an additional inguinofemoral LAE [in 15 cases, full dissection (unilateral, n = 2; bilateral, n = 13); in 3 cases, a bilateral sentinel node dissection only; in 3 patients, data were not available]. Ten (47.6%) of 21 received a radical local excision (WLE), 8/21 (38.1%) a partial vulvectomy, and 3/21 (14.3%) a complete vulvectomy. Table 5 shows the SF of sexually active patients compared to the CG with regard to the different tumor entities. No significant differences regarding SF could be demonstrated. The impact of different therapeutic modalities on SA, SF, and QoL was analyzed for patients with CC (n = 38; median age, 43 years) and VC (n = 21; median age, 52 years). Owing to the low response rate for SA and SF (4/18), patients with EC were not included in these calculations. Sixteen (42.1%) of 38 patients with CC were solely treated surgically and 22/38 (57.9%) with additional chemoradiation (RTX) (Table 4). In the group of patients treated with surgery plus adjuvant RTX, SA was substantially lower compared to those undergoing surgery only (38.1% vs 66.7%, Table 6). Likewise, SF was worse (ie, ‘‘pleasure’’ 11.63 vs 13.8, P = 0.180) and overall QoL impaired (EORTC score 67.3 vs 71.2, P = 0.673) without reaching statistical significance. Sixteen (76.2%) of 21 patients with VC were solely treated surgically and 5/21 (23.8%) with surgery plus RX (Table 4). Eight (38.1%) of 21 patients were sexually active (Table 6). Women treated with WLE instead of complete vulvectomy had a higher SA (n = 5/10, 50% vs n = 4/11, 36.4%), better SF [significant for the factor ‘‘orgasm’’ (mean 5.6 vs 2.9, P = 0.041)], as well as in trend better subjective general health
(mean 5.86 vs 4.75, P = 0.213) and QoL (mean 6.29 vs 4.75, P = 0.064) (Table 6). Furthermore, women with preservation of the clitoris [11/21 (52.3%) versus without 10/21 (47.6)] were more often sexually active (6/11, 54.5% vs 3/10, 30%, P = 0.387). The exact time interval between completion of anticancer treatment and response to the questionnaire was known in 76/77 cases (98.7%). Treatment was completed in median 3 years before this study (range, 1Y11 years). To analyze the impact of the time interval between completed therapy and answering of the questionnaire on SA and SF, we further divided the current study population into 2 groups, namely in a short-term cohort (n = 33, 1Y3 years after primary therapy) and a long-term cohort (n = 43, Q4 years after primary therapy). Results are displayed in Supplemental Table S2, http://links.lww.com/IGC/A297. Sexual activity was lower in the short-term cohort (30.3% vs 48.8% in the long-term cohort), whereas SF did not differ between the 2 groups. Subjective health status (median, 5 and 5) and QoL (median, 5.5 and 5) did not also significantly differ.
DISCUSSION The aim of this study was to analyze the SA, SF, and QoL of women with completed treatment for primary GC compared with a healthy control. Additionally, information about the association between radicality as well as treatment modality and SF was assessed. We observed that 41.3% of the cancer patients were sexually active compared to 78.0% of women in the CG. The most common reason for sexual inactivity in the GCG was
TABLE 4. Primary therapy of all GC patients (GCG, n = 77) with regard to the different tumor entities [CC (n = 38), EC (n = 18), and VC (n = 21)] Tumorentity CC (n = 38)
Total
EC (n = 18)
VC (n = 21)
Therapy
Number
%
Number
%
Number
%
Number
%
S S + CTX S + RX S + RTX
16 0 0 22
42.1 0 0 57.9
11 1 5 1
61.1 5.6 27.8 5.6
16 0 5 0
76.2 0 23.8 0
43 1 10 23
55.8 1.3 13.0 29.9
S, Surgery, CTX, Chemotherapy, RX, Radiotherapy, RTX, Chemoradiation.
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& Volume 25, Number 6, July 2015
Sexuality After Treatment of GC
TABLE 5. Sexual function of patients in the GCG compared to the CG with regard to different tumor entities SAQ Part 3 + FSFI Orgasm Item (range) and number (GCG and CG) CC (n = 18) Habit (0Y3) (n = 18/n = 46) Pleasure (0Y18) (n = 18/n = 44) Discomfort (0Y6) (n = 18/n = 46) Orgasm (1.2Y6) (n = 18/n = 46) EC (n = 4) Habit (0Y3) (n = 4/n = 46) Pleasure (0Y18) (n = 4/n = 44) Discomfort (0Y6) (n = 4/n = 46) Orgasm (1.2Y6) (n = 4/n = 46) VC (n = 8) Habit (0Y3) (n = 8/n = 46) Pleasure (0Y18) (n = 8/n = 44) Discomfort (0Y6) (n = 8/n = 46) Orgasm (1.2Y6) (n = 8/n = 46)
GCG
CG
Mean
SD
Mean
SD
P
0.83 12.83 1.89 5.24
0.62 3.37 1.81 0.99
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.719* 0.241* 0.123* 0.188*
1.25 8.75 0.75 5
1.26 2.50 0.96 0.95
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.323* 0.118* 0.648* 0.762*
0.5 11.63 1.22 4.25
0.54 4.78 1.48 1.98
0.89 11.73 1.13 4.86
0.64 3.64 1.72 1.18
0.098* 0.973* 0.900* 0.305*
*Student’s t test.
‘‘the-presence-of-a-physical-problem’’ (42.9%) and ‘‘becauseI-don’t-have-a-partner’’ in the CG (50.0%). Previous studies identified the lack of a partner not only as the most common reason for sexual inactivity in healthy cohorts but also in cohorts of patients with CC or ovarian cancer.5,26,27 In contrast to our study, presence of a ‘‘physical-problem’’ was less often identified in previous studies using the SAQ: in patients with primary CC, Wenzel et al27 and Greimel et al28 reported a physical problem with a frequency of 13.2% [treatment: surgery with or without CTX and/or RX, 1Y11 years after treatment, median age 47.8 (surgery alone), 42.6 (surgery and CTX), 46.2 (surgery and RX) -years)] and 13.0% (no information on mode of treatment, initial diagnosis 5Y10 years ago, mean age 37 years). Consistent with previous data from healthy cohorts, SA decreased with higher median age in our study.29,30 Multivariate analysis showed consistent results with age, relationship status, and smoking habits influencing SA significantly. Patients in the GCG of our study were, however, 5 years older (median 51 vs 46 years in the CG) and almost all postmenopausal (87.0% vs 18.3% in the CG). Furthermore, the lack of a partner was more frequent in the GCG (22.1% vs 11.7% in the CG). The discrepancies between ages and postmenopausal status of the CG and the GCG are a making interpretation of the statistically significant difference in SA observed between the groups difficult. However, opposite to the CG, the most common reason for inactivity in the GCG was ‘‘the-presence-of-aphysical-problem’’ with 42.9%. These results confirm that at least to some extent lower SA in the GCG originated from the earlier illness. Despite limited comparability, SF, QoL, and subjective general health were not significantly different between the GCG and CG and similar to populations without cancer.26 These results show that although far fewer women in the GCG were sexually active, the SF of patients actually active
was not different from that seen in healthy women. Even more, sexual ‘‘pleasure’’ in the GCG was in trend greater although the degree of ‘‘discomfort’’ during intercourse was higher. This effect was pronounced in the group of patients with CC with a better comparability to the CG (median age 43 vs 46 years in the CG and SA 50.0% vs 78.0% in the CG): sexually active patients after CC had a higher score for sexual ‘‘pleasure’’ and ‘‘orgasm’’ than women in the CG although more ‘‘discomfort’’ during intercourse was reported [mean 1.89 vs 1.13 (P = 0.123)]. This is in line with a recent review showing that CC survivors are at risk for sexual pain disorders, whereas sexual satisfaction is not impaired.31 Regarding different therapy modalities in CC, our analysis showed less SA (38.1% vs 66.7%), worse SF, and overall QoL in patients treated with surgery and adjuvant RTX in contrast to those solely treated surgically, in line with previously published data.28,32Y34 Especially pain disorders are negatively influenced by RX.31 Patients with VC had a lower sexual frequency compared to the CG [‘‘habit’’ mean 0.5 vs 0.89 (P = 0.098)]. Differences between sexually active VC patients and the CG regarding ‘‘discomfort,’’ ‘‘pleasure,’’ and ‘‘orgasm’’ were, however, of minor importance. Previous studies on VC have shown higher rates of sexual dysfunction, in particular concerning ‘‘arousal’’ and ‘‘orgasm’’ difficulties.35Y38 However, in these studies, the time intervals from therapy to interview were inhomogeneous and the number of cases was very small.32 In our study, sexually active VC patients treated with radical local excision instead of vulvectomy had a better SF with significantly higher values for the factor ‘‘orgasm.’’ Patients with preserved clitoris had significantly higher values for the factor ‘‘pleasure’’ than those after resection of the clitoris. Nevertheless, 66.7% of the patients with VC were sexually inactive because of a physical problem. Likes et al39 demonstrated
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International Journal of Gynecological Cancer
Grimm et al
& Volume 25, Number 6, July 2015
TABLE 6. Results of the SAQ, FSFI, and EORTC QLQ-C30 of patients with VC and CC with regard to the applied treatment modalities CC (n = 38) Therapy
Surgery
Surgery + RTX
Number
16
22
10/15 (66.7%)
8/21 (38.1%)
Sexually active Item (Range) and Number (S/SR)
Mean
SD
Mean
SD
P*
Habit (0Y3) (n = 10/n = 8) Pleasure (0Y18) (n = 10/n = 8) Discomfort (0Y6) (n = 10/n = 8) Orgasm (1.2Y6) (n = 10/n = 8) QoL (n = 11/n = 13) Subjective health (n = 11/n = 13)
0.90 13.8 1.80 5.40 5.27 5.27
0.74 3.12 2.20 0.87 1.55 1.35
0.75 11.63 2.00 5.05 5.00 5.08
0.46 3.46 1.31 1.15 1.35 1.32
0.624 0.180 0.824 0.472 0.650 0.723
VC (n = 21) Therapy
Wide Local Excision
Vulvectomy
Number
10
11
5/10 (50.0%)
4/11 (36.4%)
Sexually active Item (Range) and Number (WLE/V)
Mean
SD
Mean
SD
P*
Habit (0Y3) (n = 4/n = 4) Pleasure (0Y18) (n = 4/n = 4) Discomfort (0Y6) (n = 5/n = 4) Orgasm (1.2Y6) (n = 4/n = 4) QoL (n = 7/n = 4) Subjective health (n = 7/n = 4)
0.75 15.0 0.6 5.6 6.29 5.86
0.50 2.16 1.34 0.80 0.76 1.07
0.25 8.25 2.0 2.9 4.75 4.75
0.50 4.27 1.41 1.91 1.71 1.71
0.207 0.030 0.172 0.041 0.064 0.213
*Student’s t test. S, Surgery; SR, surgery + RTX; V, vulvectomy; WLE, wide local excision.
supporting results: older age and a more extensive vulvar excision were associated with poor SF and QoL. So far, there are very limited data on the time course and changes in SA and SF after GC treatment. In our study, SA was a little lower in the short-term cohort (1Y3 years after primary therapy) in patients with GC (30.3 % vs 48.8% Q4 years after primary therapy) but SF did not differ. In a study by Jensen et al,33 173 women with early-stage CC were interviewed within the first 2 years after primary therapy at specific time intervals. Within these 2 years, a decline in sexual inactivity was noted (25% after 3 months to 11% after 24 months). Sexual satisfaction, level of discomfort, and orgasm ability during intercourse did not change. Although direct comparison to our results is difficult, similar trends can be observed: fewer women are sexually active shortly after therapy. Women who regain SA have a good overall SF. A possible limitation of our study is the nonresponder rate. It remains unclear whether nonresponders had more or less physical problems and were therefore less motivated to answer questions about their SA. We tried to minimize this possible selection bias by initial telephone contact and the
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option to complete a nonparticipation declaration. Strength of the study is the high response rate of 66.5%, resulting in 77 patients included. Taken together, the impact of a GC diagnosis and subsequent treatment on women’s sexuality is profound.40 A high number of patients with GC remain sexually inactive, indicating that women may experience persistent functional problems especially after multimodal treatment or extensive surgery. However, women who regain SA after completed treatment have a good overall SF and vice versa. Gynecologic oncologists should therefore find effective communication strategies to support their patients improve their SA. Instead of focusing on resuming vaginal intercourse, counseling for avoiding pain might be more important. To confirm the results obtained with this study, larger longitudinal studies are desirable.
REFERENCES 1. Abbott-Anderson K, Kwekkeboom KL. A systematic review of sexual concerns reported by gynecological cancer survivors. Gynecol Oncol. 2012;124:477Y489. * 2015 IGCS and ESGO
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& Volume 25, Number 6, July 2015
2. Alder J, Bitzer J. [Gynecological cancer and sexuality]. Ther Umsch. 2011;68:581Y586. 3. Pilger A, Richter R, Fotopoulou C, et al. Quality of life and sexuality of patients after treatment for gynaecological malignancies: results of a prospective study in 55 patients. Anticancer Res. 2012;32:5045Y5049. 4. Liavaag AH, Dorum A, Bjoro T, et al. A controlled study of sexual activity and functioning in epithelial ovarian cancer survivors. A therapeutic approach. Gynecol Oncol. 2008;108:348Y354. 5. Taylor KL, Shelby R, Gelmann E, et al. Quality of life and trial adherence among participants in the prostate, lung, colorectal, and ovarian cancer screening trial. J Natl Cancer Inst. 2004;96:1083Y1094. 6. Donovan KA, Small BJ, Andrykowski MA, et al. Utility of a cognitive-behavioral model to predict fatigue following breast cancer treatment. Health Psychol. 2007;26:464Y472. 7. Juraskova I, Butow P, Robertson R, et al. Post-treatment sexual adjustment following cervical and endometrial cancer: a qualitative insight. Psychooncology. 2003;12:267Y279. 8. Tangjitgamol S, Manusirivithaya S, Hanprasertpong J, et al. Sexual dysfunction in Thai women with early-stage cervical cancer after radical hysterectomy. Int J Gynecol Cancer. 2007;17:1104Y1112. 9. Anderson B. Quality of life in progressive ovarian cancer. Gynecol Oncol. 1994;55:S151YS155. 10. Bodurka DC, Sun CC. Sexual function after gynecologic cancer. Obstet Gynecol Clin North Am. 2006;33:621Y630, ix. 11. Brotto LA, Yule M, Breckon E. Psychological interventions for the sexual sequelae of cancer: a review of the literature. J Cancer Surviv. 2010;4:346Y360. 12. Audette C, Waterman J. The sexual health of women after gynecologic malignancy. J Midwifery Womens Health. 2010;55:357Y362. 13. Shell JA, Smith CK. Sexuality and the older person with cancer. Oncol Nurs Forum. 1994;21:553Y558. 14. Carter J, Stabile C, Gunn A, et al. The physical consequences of gynecologic cancer surgery and their impact on sexual, emotional, and quality of life issues. J Sex Med. 2013; 10 Suppl 1:21Y34. 15. Stead ML. Sexual function after treatment for gynecological malignancy. Curr Opin Oncol. 2004;16:492Y495. 16. Ekwall E, Ternestedt BM, Sorbe B. Important aspects of health care for women with gynecologic cancer. Oncol Nurs Forum. 2003;30:313Y319. 17. Lindau ST, Gavrilova N, Anderson D. Sexual morbidity in very long term survivors of vaginal and cervical cancer: a comparison to national norms. Gynecol Oncol. 2007;106:413Y418. 18. Carter J, Goldfrank D, Schover LR. Simple strategies for vaginal health promotion in cancer survivors. J Sex Med. 2011;8:549Y559. 19. Quinn GP, Vadaparampil ST, Lee JH, et al. Physician referral for fertility preservation in oncology patients: a national study of practice behaviors. J Clin Oncol. 2009;27:5952Y5957. 20. Rogers M, Todd C. Information exchange in oncology outpatient clinics: source, valence and uncertainty. Psychooncology. 2002;11:336Y345. 21. Hill EK, Sandbo S, Abramsohn E, et al. Assessing gynecologic and breast cancer survivors’ sexual health care needs. Cancer. 2011;117:2643Y2651.
Sexuality After Treatment of GC
22. Tsai TY, Chen SY, Tsai MH, et al. Prevalence and associated factors of sexual dysfunction in cervical cancer patients. J Sex Med. 2011;8:1789Y1796. 23. Stead ML, Brown JM, Fallowfield L, et al. Lack of communication between healthcare professionals and women with ovarian cancer about sexual issues. Br J Cancer. 2003;88:666Y671. 24. Aaronson NK, Ahmedzai S, Bergman B, et al. The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst. 1993;85:365Y376. 25. Rosen R, Brown C, Heiman J, et al. The Female Sexual Function Index (FSFI): a multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther. 2000;26:191Y208. 26. Thirlaway K, Fallowfield L, Cuzick J. The Sexual Activity Questionnaire: a measure of women’s sexual functioning. Qual Life Res. 1996;5:81Y90. 27. Wenzel L, DeAlba I, Habbal R, et al. Quality of life in long-term cervical cancer survivors. Gynecol Oncol. 2005;97:310Y317. 28. Greimel ER, Winter R, Kapp KS, et al. Quality of life and sexual functioning after cervical cancer treatment: a long-term follow-up study. Psychooncology. 2009;18:476Y482. 29. Chedraui P, Perez-Lopez FR, San Miguel G, et al. Assessment of sexuality among middle-aged women using the Female Sexual Function Index. Climacteric. 2009;12:213Y221. 30. Lindau ST, Schumm LP, Laumann EO, et al. A study of sexuality and health among older adults in the United States. N Engl J Med. 2007;357:762Y774. 31. Lammerink EA, de Bock GH, Pras E, et al. Sexual functioning of cervical cancer survivors: a review with a female perspective. Maturitas. 2012;72:296Y304. 32. Frumovitz M, Sun CC, Schover LR, et al. Quality of life and sexual functioning in cervical cancer survivors. J Clin Oncol. 2005;23:7428Y7436. 33. Jensen PT, Groenvold M, Klee MC, et al. Longitudinal study of sexual function and vaginal changes after radiotherapy for cervical cancer. Int J Radiat Oncol Biol Phys. 2003;56:937Y949. 34. Park SY, Bae DS, Nam JH, et al. Quality of life and sexual problems in disease-free survivors of cervical cancer compared with the general population. Cancer. 2007;110:2716Y2725. 35. van de Wiel HB, Schultz WC, Hallensleben A, et al. Sexual functioning following treatment of cervical carcinoma. Eur J Gynaecol Oncol. 1988;9:275Y281. 36. Green MS, Naumann RW, Elliot M, et al. Sexual dysfunction following vulvectomy. Gynecol Oncol. 2000;77:73Y77. 37. Weijmar Schultz WC, van de Wiel HB, Bouma J, et al. Psychosexual functioning after the treatment of cancer of the vulva. A longitudinal study. Cancer. 1990;66:402Y407. 38. Aerts L, Enzlin P, Vergote I, et al. Sexual, psychological, and relational functioning in women after surgical treatment for vulvar malignancy: a literature review. J Sex Med. 2012;9:361Y371. 39. Likes WM, Stegbauer C, Tillmanns T, et al. Correlates of sexual function following vulvar excision. Gynecol Oncol. 2007;105:600Y603. 40. Barbera L, Fitch M, Adams L, et al. Improving care for women after gynecological cancer: the development of a sexuality clinic. Menopause. 2011;18:1327Y1333.
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