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Sexual dysfunction in multiple sclerosis: A 6-year follow-up study

Journal of the Neurological Sciences, Volume 358, Issues 1–2, 15 November

Abstract

Purpose

Sexual dysfunction (SD) is a common but often overlooked and undertreated symptom in multiple sclerosis (MS). The purpose of our longitudinal study was to explore the changes in the level of sexual functioning in MS cohort after a period of 3 and 6 years of follow-up, as well as to investigate the predictors of changes in SD during the period of observation.

Methods

The study population comprise a cohort of 93 patients with MS (McDonald's criteria, 2001) who were assessed at three time points during the study (baseline, and at the 3- and 6-year follow-up). The presence and severity of SD was quantified by Szasz sexual functioning scale. Independent predictors of the ordinal-scaled measure of sexual problems were identified using a generalized linear mixed regression models.

Results

The number of reported SD symptoms increased markedly for both genders during the whole period of observation. Duration of follow-up, age, level of physical disability, depression and fatigue were identified as independent prognostic factors for deterioration of sexual functioning in patients with MS during the 6-year follow-up.

Conclusion

Our study provides insight into dynamics of change in sexual function among patients with MS and predictors of change, over the period of 6 years.

Keywords: Multiple sclerosis, Sexual dysfunction, Cohort study, Predictors, Libido, Gender.

1. Introduction

Sexual dysfunction (SD) is a common and very distressing symptom of multiple sclerosis (MS). Studies on the prevalence of perceived sexual concerns in MS demonstrated that 40–80% of women and 50–90% of men have sexual complaints [1], [2], [3], and [4]. It has also been shown that proportion of SD in MS is greater than in other neurological diseases, and almost five times higher than in the general population [4] and [5]. However, despite this recognized importance of sexual functioning problems in MS, this aspect of illness has been poorly estimated in clinical practice, and, therefore, often remain under-diagnosed and undertreated.

Sexual functioning is a complex process that depends on the neurologic, vascular, and endocrine systems, and is influenced by numerous psychosocial factors. MS can affect sexuality, sexual functions, and expressions of intimacy both directly (referred to as primary SD) and indirectly (referred to as secondary and tertiary SD) [2], [6], [7], and [8]. Primary SD results from demyelinating lesions in the central nervous system that affect the sexual response and/or sexual feelings [9]. Secondary SD stems from MS-related symptoms that are not associated with the neural pathways of the genital system and commonly include fatigue, muscle weakness, spasticity, mobility problems, tremor, urinary dysfunction, pain, cognitive problems and side effects from medications [10]. Tertiary SD refers to disability-related psychosocial, social and cultural issues that may affect sexual functioning [11] and [12].

Over the past two decades there has been an expansion of studies examining the type and frequency of symptoms of SD in patients suffering from MS. [1], [2], [3], [4], [5], [6], [7], [8], [9], [13], and [14] However, majority of these studies had cross-sectional design and the results from longitudinal studies that have dealt with this issue are still remarkably rare. To the best of our knowledge, the changes in sexual function among patients with MS has been followed and analyzed only in two studies [15] and [16]. Additionally, considerably less is known about predictors of changes in MS-related SD symptoms over time.

Therefore, we conducted a longitudinal study in MS cohort to investigate the following items: 1) changes in the level of sexual functioning after a period of the 3- and 6-year follow-up; 2) symptoms of SD which changed over time; and 3) demographic and clinical characteristics of MS patients as potential predictors of changes in SD during the follow-up period.

2. Methods

2.1. Patients

The sampling method and the description of the measurements have been published elsewhere [14]. Briefly, the study comprised 109 MS patients who fulfilled following inclusion criteria: diagnosis of MS according to the McDonald's criteria [17], age 18–60 years, Expanded Disability Status Scale (EDSS) score < 8 [18], and written informed consent. Exclusion criteria were: relapse of the disease in the last month, pre-existing major chronic illness and/or psychiatric disorders, and antidepressive or corticosteroid therapy during the last month.

None of the MS patients received immunomodulatory therapy at the beginning of the study, and during the follow-up period the proportion of treated patients was less than 10%.

2.2. Measurements

Information on SD has been collected through face-to-face structured interviews. The two different sets of questions regarding SD were developed to address separately for both genders (Appendix 1). They comprise 13 questions for women and 16 for men and include social and medical sexual issues. The questionnaire consists of questions that are related to the type of SD symptoms, their frequency, and time of onset. Furthermore, questionnaire comprises the questions regarding patient's willingness to talk about sexual problems with the doctor, friends and/or emotional partner. Moreover, this questionnaire includes a set of gender-specific questions concerning presence of certain SD symptoms (total loss of erections, incomplete erections, erections not effective to penetrate, inability to ejaculate, premature ejaculation, orgasmic dysfunction and reduced libido for males; and anorgasmia or hyporgasmia, difficulties in achieving orgasm, decreased vaginal lubrication, changes in vaginal sensation and reduced libido for females). The questionnaire was filled in by a trained physician of the same gender as a patient. The presence and severity of SD was quantified by Szasz sexual functioning scale (Appendix 2) [19]. This evaluation has been performed independently by an investigator according to the results of the questionnaire. No exclusions were made for sexual orientation or sexual partner status.

The neurological impairment was assessed using the EDSS (Appendix 2) [18]. Because of the inter-observer variability in the EDSS scoring, testing was performed by a single experienced observer.

Fatigue symptoms were quantified using the Fatigue Severity Scale (FSS) (Appendix 2) [20].

Severity of depressive symptoms was quantified in all patients using the Hamilton Rating Scale for Depression (HDRS) (Appendix 2) [21].

The study psychiatrist was blinded to the EDSS score. Namely, psychiatrist's interview was performed in the room where the patient was already sitting, so psychiatrist had no chance to assess patient's walking ability. Furthermore, psychiatrist also had no access to the medical documentation related to the degree of patient's physical disability, FSS and SD data.

2.3. Data collection

At three time points during the study (baseline, and at the 3- and 6-year follow-up), the sexual function, EDSS, HDRS, and FSS were assessed. One hundred and nine MS patients were initially enrolled in the study. The attrition rates and the explanations for dropouts were described elsewhere [22]. Twelve (11.0%) MS patients dropped out of the study at 3 years: 4 could not have been reached due to displacement and 8 were not willing to participate (the sample size after the 3-year follow-up was 97 patients). At 6 years, 11 patients (10.1%) from the baseline MS cohort were considered lost to follow-up: 2 patients died, 3 could not have been reached due to displacement, and 6 were not willing to participate. However, 5 patients from the baseline cohort who did not participate at the 3-year examination were reenrolled in the study at 6 years. Four MS patients who were assessed at baseline and at 3 years dropped out at the end of the study. Consequently, the total number of responders after the 6-year follow-up was 98 MS patients. Finally, among all responders initially enrolled in the study, 93 MS patients were examined at each of the 3 time points (at the baseline, and at the 3- and 6-year follow-up). Keeping in mind the fact that mixed regression analyses require group of patients who were assessed at each point of estimation, these 93 patients represented the target cohort for current longitudinal investigation; response rate was 85.3%.

2.4. Statistical analysis

To compare the demographics and clinical characteristics of the MS patients in three time points of assessments Friedman rank test, followed by Wilcoxon signed rank post-hoc test for nonparametric variables and ANOVA with repeated measures, followed by Bonferroni post hoc test for continuous variables were performed.

The importance of overall changes in the presence and severity of SD over the 6-year follow-up is qualified using Friedman rank test followed by paired-sample Wilcoxon signed rank in post-hoc analyses, when it was required. In case that a significant p-value (less than 0.05) is detected by Friedman rank test, the paired-sample Wilcoxon signed rank test is used in post-hoc analyses, in order to detect time points when significant SD-related changes appear.

The Cochran's Q test is applied to compare the changes in the distribution of dichotomous variables during the 6-year follow-up, followed by McNemar test in post-hoc analyses, if necessary.

The differences between males and females according to the proportion of MS patients with active sexual life and number of SD symptoms at each time-point have been explored by employing χ2 test.

Independent predictors of the ordinal-scaled measure of sexual problems (expressed as Szasz sexual functioning scale score) are identified using a generalized linear mixed regression models that are based on the proportional odds assumption and the correlation between the repeated measurements of a subject across time considered. Hence, the generalized linear latent and mixed models (GLLAMM) in STATA 10 are used to fit random-effects multilevel regression models with repeated ordinal measurements [23]. All covariates that are considered significant at level of 0.05 in univariate analysis were further entered in final multivariate (adjusted) model. The results are presented as odds ratio (OR) with corresponding 95% confidence intervals (95% CI).

3. Results

The main demographic and clinical characteristics of 93 patients with MS with assessments at baseline, and after 3- and 6-year follow-up, are presented at Table 1.

Table 1 Demographics and clinical characteristics of 93 patients who provided assessments at baseline, and at the 3-year and at the 6-year follow-up.

At baseline At the 3-year follow-up At the 6-year follow-up p value
Gender, No (%)
 Male 27 (29.0) 27 (29.0) 27 (29.0) /a
 Female 66 (71.0) 66 (71.0) 66 (71.0)
Аgе (years)
 Mean ± SD 41.5 ± 8.5 44.6 ± 8.5 47.5 ± 8.4 /b
 Range 20–61 23–64 26–67
Education (years), no (%)
 Primary (1–8) 7 (7.5) 7 (7.5) 7 (7.5) 0.854c
 Secondary (9–12) 64 (68.9) 64 (68.9) 62 (66.7)
 University (13) 22 (23.6) 22 (23.6) 24 (25.8)
Marital status, no (%)
 Single (never married) 20 (21.5) 19 (20.4) 18 (19.4) 0.789c
 Married/cohabiting 65 (69.9) 65 (69.9) 64 (68.8)
 Widowed 2 (2.2) 2 (2.2) 3 (3.2)
 Separated/divorced 6 (6.4) 7 (7.5) 8 (8.6)
Current employment status
 Employed/student 33 (35.5) 34 (36.5) 32 (34.4) 0.752c
 Retired 45 (48.4) 46 (49.5) 48 (51.6)
 Unemployed 15 (16.1) 13 (14.0) 13 (14.0)
Age at onset (years)
 Mean ± SD 32.2 ± 8.4 32.2 ± 8.4 32.2 ± 8.4 /a
 Range 17–50 17–50 17–50
Disease duration (years)
 Mean ± SD 9.2 ± 6.5 12.1 ± 6.4 15.2 ± 6.5 /b
 Range 1–28 4–31 7–34
Current disease course, no (%)
 Relapsing remitting 66 (71.0) 56 (60.2) 42 (45.2) < 0.001c
 Secondary progressive 20 (21.5) 30 (32.3) 44 (47.3)
 Primary progressive 7 (7.5) 7 (7.5) 7 (7.5)
EDSS score
 Mean ± SD 4.2 ± 1.6 4.7 ± 1.8 5.1 ± 2.1 < 0.001d
 Range 1.0–7.5 1.0–9.0 1.0–9.0
HDRS score
 Mean ± SD 12.3 ± 5.5 14.5 ± 6.1 16.0 ± 6.9 < 0.001d
 Range (3–33) (4–32) (5–34)
FSS score
 Mean ± SD 4.7 ± 1.5 5.4 ± 1.9 5.7 ± 2.2 < 0.001d
 Range (1.7–9.0) (1.5–9.0) (1.4–9.0)

a Not applicable, unchangeable variable over time.

b Not applicable, variable gradually increased over time.

c Friedman rank test followed by Wilcoxon signed rank test in post hoc analyses.

d ANOVA with repeated measures followed by Bonferroni post hoc test.

The changes were statistically significant (p < 0.001) between all time-dependent data sets (baseline vs. end of 3-year follow-up; baseline vs. end of 6-year follow-up; end of 3-year follow-up vs. end of 6-year follow-up).

Bold values indicate significance at p-value < 0.05.

The proportion of MS patients still having sexual intercourses (i.e., with a Szasz score less than 3) significantly decreased over time, for both men and women [from 70.4% at baseline to 66.7% after 3-year, and to 51.9% at the 6-year follow-up (Cochran's Q = 7.000; p = 0.030 for males); and from 68.2% at baseline to 63.6% at the 3-year, and to 39.4% at the 6-year follow-up (Cochran's Q = 28.455; p < 0.001 for females)]. Furthermore, at each of the time-points of the estimation, there were no statistically significant difference between men and women in the prevalence of those still having sexual intercourses (χ2 = 0.046, p = 0.836 at baseline; χ2 = 0.077, p = 0.782 at the 3-year; and χ2 = 1.213, p = 0.192 at the 6-year follow-up).

The gender-specific distribution of MS patients according to Szasz sexual functioning scale score at baseline and at the 3- and 6-year follow-up are presented in Table 2. The proportion of patients concerning the presence and severity of SD significantly varied across 6-year period for both genders (Friedman Chi-square = 21.288; p < 0.001 for males, and Friedman Chi-square = 47.832; p < 0.001 for females). These changes were statistically significant between all time-dependent data sets [at baseline vs. at the 3-year follow-up (p = 0.004 for males, and p = 0.007 for females); at baseline vs. at the 6-year follow-up (p < 0.001 for both genders); at the 3-year follow-up vs. at the 6-year follow-up (p = 0.019 for males, and p < 0.001 for females)].

Table 2 The gender-specific distribution of MS patients according to Szasz sexual functioning scale score at the baseline and at the 3 and at the 6-year follow-up.

Szasz sexual functioning scale scorea At baseline At the 3-year follow-up At the 6-year follow-up pc
(overall change)
No (%)
Males (n = 27)
0 5 (18.5) 4 (14.8) 2 (7.4)
1 9 (33.3) 3 (11.1) 4 (14.8)
2 5 (18.5) 11 (40.7) 8 (29.6)
3 7 (25.9) 7 (25.9) 8 (29.6)
4 1 (3.7) 2 (7.4) 5 (18.5)
Total 27 (100) 27 (100) 27 (100)
Median (range)
1 (0–4)c 2 (0–4)c 3 (0–4)c < 0.001b
 
Females (n = 66)
0 12 (18.2) 7 (10.6) 3 (4.5)
1 21 (31.8) 17 (25.8) 13 (19.7)
2 12 (18.2) 18 (27.3) 10 (15.2)
3 14 (21.2) 17 (25.8) 26 (39.4)
4 7 (10.6) 7 (10.6) 14 (21.2)
Total 66 (100) 66 (100) 66 (100)
Median (range)
1 (0–4)c 2 (0–4)c 3 (0–4)c < 0.001b

a 0-Sexually active as before and/or not experiencing sexual problems; 1-sexually less active than before and/or now experiencing some sexual problems but not concerned; 2-sexually less active than before and/or now experiencing some sexual problems and concerned; 3-sexually inactive but still concerned; 4-sexually inactive and not concerned.

b Friedman rank test.

c Wilcoxon signed rank test, the changes were statistically significant between all time-dependent data sets at baseline vs. at the 3-year follow-up (p = 0.004 for males and p = 0.007 for females); at baseline vs. at the 6-year follow-up, (p < 0.001 for both genders); at the 3-year follow-up vs. at the 6-year follow-up (p = 0.019 for males and p < 0.001 for females).

The prevalence of SD-related symptoms in males and females with MS during the follow-up are listed in Tables 3 and 4. At each point of assessment, the most common sexual problem among both men and women was reduced libido. All the symptoms of SD have been reported more frequently at each subsequent time-point, but statistical significance was reached after the period of 6 years only for incomplete erections, erections not effective to penetrate, inability to ejaculate and reduced libido for male population, and for anorgasmia, difficulties in achieving orgasm and reduced libido for female population. The only statistically meaningful change after the 3-year period was noticed in women for difficulties in achieving orgasm.

Table 3 The prevalence of symptoms of sexual dysfunction among males with multiple sclerosis (n = 27) at baseline and at the 3-year and at the 6-year follow-up.

Symptoms At baseline At the 3-year follow-up At the 6-year follow-up p a (overall change)
No (%)
Total loss of erections 7 (25.9) 6 (22.2) 8 (29.6) 0.223
Incomplete erections 12 (44.4) 15 (55.6) 18 (66.7) 0.009
Erections not effective to penetrate 6 (22.2) 11 (40.7) 17 (63.0)⁎⁎ < 0.001
Inability to ejaculate 7 (25.9) 8 (29.6) 14 (51.9)⁎⁎ 0.005
Premature ejaculation 11 (40.7) 11 (40.7) 13 (48.1) 0.135
Reduced libido 13 (48.1) 17 (63.0) 19 (70.4) 0.018

a Cochran's Q test.

McNemar test; the changes were significantly different from baseline.

⁎⁎ McNemar test; the changes were significantly different from baseline and the 3-year follow-up.

Table 4 The prevalence of symptoms od sexual dysfunction among females with multiple sclerosis (n = 66) at baseline and at the 3-year and at the 6-year follow-up.

Symptoms At baseline At the 3-year follow-up At the 6-year follow-up pa (overall change)
No (%)
Anorgasmia 8 (12.1) 13 (19.7) 19 (28.8)⁎⁎ 0.001
Difficulties in achieving orgasm 27 (40.9) 36 (54.5) 48 (72.7)⁎⁎ < 0.001
Decreased vaginal lubrication 27 (40.9) 30 (45.5) 31 (47.0) 0.039
Changes in vaginal sensation 18 (27.3) 20 (30.3) 17 (25.8) 0.497
Reduced libido 47 (71.2) 49 (74.2) 56 (84.8)⁎⁎ 0.006

a Cochran's Q test.

McNemar test; the changes were significantly different from baseline.

⁎⁎ McNemar test; the changes were significantly different from baseline and the 3-year follow-up.

The proportion of patients with SD (Szasz score > than 0) tended to raise for both genders during the whole follow-up, but this increasing tendency reached statistical significance only for female population [from 77.8% at baseline to 81.5% at the 3-year, and to 88.9% at the 6-year follow-up, for males (Cochran's Q = 4.667; p = 0.097); and from 72.7% at baseline to 77.3% at the 3-year, and to 87.9% at the 6-year follow-up, for females (Cochran's Q = 11.286; p = 0.004)]. Additionally, the number of reported SD symptoms increased markedly (Friedman rank test < 0.001) for both genders during the whole follow-up period (Table 5). There were no statistically significant differences between males and females in relation to the number of SD symptoms at each of the points of estimation (χ2 = 1.545, p = 0.672 at baseline; χ2 = 0.720, p = 0.868 at the 3-year; and χ2 = 2.862, p = 0.413 at the 6-year).

Table 5 The distribution of MS patients according to number of symptoms of sexual dysfunction at baseline and at the 3-year and at the 6-year follow-up.

Number of symptoms of sexual dysfunction At baseline At the 3-year
follow-up
At the 6-year
follow-up
pa
(overall change)
No (%)
Males (n = 27)
0 6 (22.2) 5 (18.5) 3 (11.1)
1 5 (18.5) 2 (7.4) 1 (3.7)
2 4 (14.8) 4 (14.8) 4 (14.8) 0.001a
> 2 12 (44.5) 16 (59.3) 19 (70.4)
p (post-hoc analyses) b 0.024 0.006
 
Females (n = 66)
0 18 (27.3) 15 (22.7) 8 (12.1)
1 8 (12.1) 7 (7.6) 7 (10.6)
2 15 (22.7) 13 (19.7) 13 (19.7) < 0.001a
> 2 25 (37.9) 33 (50.0) 38 (57.6)
p (post-hoc analyses) b 0.018 < 0.001⁎⁎

a Friedman rank test.

b Wilcoxon signed rank test.

The changes were significantly different from baseline.

⁎⁎ The changes were significantly different from baseline and the 3-year follow-up.

The proportions of MS patients who were willing to talk about sexual problems with doctors and friends did not significantly change over the follow-up, in both men and women (Table 6). Moreover, the chance of discussing sexual issues with partners increased markedly at the 6-year follow-up, for both genders (from 22.2% at baseline to 33.3% at the 6-year follow-up, p = 0.049 for males, and from 22.7% at baseline to 30.3% at the 6-year follow-up, p = 0.048 for females).

Table 6 The gender-specific proportion of MS patients who were willing to discuss sexual issues.

Persons discussing sexual issues At baseline At the 3-year follow-up At the 6-year follow-up pa
(overall change)
No (%)
Males (n = 27)
Doctor 1 (3.7) 2 (7.4) 2 (7.4) 0.368
Friend 1 (3.7) 3 (11.1) 2 (7.4) 0.223
Emotional partner 6 (22.2) 7 (25.9) 9 (33.3) 0.049
 
Females (n = 66)
Doctor 1 (3.0) 3 (4.5) 3 (4.5) 0.264
Friend 4 (6.1) 3 (4.5) 4 (6.1) 0.368
Emotional partner 15 (22.7) 18 (27.3) 20 (30.3) 0.048

a Cochran's Q test.

McNemar test; the changes were significantly different from baseline.

Bold values indicate significance at p-value < 0.05.

The predictors of change of Szasz sexual functioning scale score over the 6-year follow-up period that were identified using mixed-effects regression models with repeated ordinal measurements are illustrated in Table 7. After testing for variables interaction and controlling the effect of potential confounders, the multivariate adjusted model has revealed that following variables had independent prognostic value for deterioration of sexual functioning in patients with MS at the 6-year follow-up: duration of follow-up, age, EDSS, HDRS and FSS scores. Namely, this analysis showed that with each follow-up year, the risk of transition from lower to higher Szasz sexual functioning scale score increased for 31%, while with each additional year of age this risk raised for 15%. Additionally, this predictive model also demonstrated that with one-unit increase in EDSS score, the risk for decline in sexual functioning measured by Szasz sexual functioning scale increased about 4 times over the studied period. Moreover, it was also observed that worsening in HDRS and FSS scores for one unit increased the risk for deterioration in SD for 29% and 9%, respectively.

Table 7 Mixed-effects regression models with repeated ordinal measurements showing the predictors of change of Szasz sexual functioning scale score over the 6-year follow-up.

Unadjusted models Adjusted model
OR 95% CI p OR 95% CI p
Time (years) 1.69 1.47–1.95 < 0.001 1.31 1.13–1.52 < 0.001
Gender 1.46 0.30–7.21 0.639
Age (years) 1.15 1.06–1.26 0.001 1.15 1.01–1.31 0.030
Marital status (married/cohabiting) 0.09 0.02–0.44 0.003 1.09 0.26–4.53 0.901
Education (years) 0.93 0.68–1.27 0.646
Current employment status
 Employed/student Reference
 Unemployed 1.13 0.14–9.55 0.907 3.85 0.27–53.99 0.318
 Retired 5.61 1.17–26.92 0.031 0.60 0.09–3.78 0.583
Disease duration (years) 1.22 1.09–1.36 < 0.001 1.09 0.95–1.25 0.201
Current disease course
 Relapsing remitting Reference
 Secondary progression 30.04 1.83–493.09 0.017 0.45 0.02–11.56 0.627
 Primary progression 72.49 22.55–233.02 < 0.001 0.94 0.20–4.43 0.934
EDSS score 11.33 6.05–21.23 < 0.001 4.12 2.05–8.28 < 0.001
HDRS score 1.61 1.43–1.81 < 0.001 1.29 1.12–1.49 < 0.001
FSS score 1.22 1.17–1.28 < 0.001 1.09 1.03–1.16 0.003

OR, odds ratio; CI, confidence interval; EDSS, Expanded Disability rating Scale; HDRS, Hamilton Depression Rating Scale.

Bold values indicate significance at p-value < 0.05.

4. Discussion

This survey provides the results of longitudinal evaluation of sexual function among persons with MS during the period of 6 years. The prevalence of MS patients still having sexual intercourses significantly decreased at the 6-year follow-up. This finding is in accordance with those obtained in the Italian MS cohort, in which the proportion of patients with active sexual life slightly declined over the period of 2 years [15]. Furthermore, the results of our study also showed increasing risk for the development of SD in patients with MS over the period of 6 years, for both genders. This is in line with results obtained in the two longitudinal studies dealing with sexual issues in MS. [15] and [16] Namely, the percentage of patients with at least one symptom of SD in our investigation increased from 77.8% to 88.9% in males, and from 72.7% to 87.9% in females, at the 6-year follow-up. Furthermore, numerous studies with cross-sectional design dealing with sexual issues in MS have shown that the prevalence of SD in patients with this neurological disorder varies significantly, ranging from 40% to 90% [1], [2], [3], [5], [6], [7], [8], and [9]. We assume that these differences in the proportion of MS patients with SD in various MS populations might be due to the different MS cohort-specific demographic and clinical characteristics. Additionally, although the majority of the studies which investigate gender differences in MS underline that SD were more common among males [6], the results of our study did not confirm this finding. The absence of any significant gender-specific difference regarding sexual functioning in our MS cohort might be partially explained by small sample size of males and rigid social and cultural background regarding sexuality, especially for females, in Serbian society.

In our study the most common sexual problem was reduced libido, with the prevalence varying during the follow-up period from 48.1% to 70.4% in males, and from 71.2% to 84.8% in females. This finding is in line with numerous published investigations which pointed out that lack of sexual desire is the most frequent sexual complaint in patients with MS. Nevertheless, the rates of decreased libido in our MS group were within the upper range or even over the range (from 31.4% to 68.6%) demonstrated in reports by the majority of the other authors [2], [3], [4], [15], and [16]. However, the high frequency (80.5%) of decreased sexual desire is also recorded in Turkish MS cohort [7]. The higher frequencies of SD detected in our investigation, in comparison to other studies, might be partially explained by the fact that a very small proportion (< 5%) of our MS patients have been treated with antidepressants [24]. It can be hypothesized that among our patients due to cultural reasons there is higher frequency of non-treated depression, and recently it has been demonstrated that SD in patients with MS could be partly related to depressive symptoms [25]. However, these findings might be also attributed to specific socio-cultural background of the Serbian society with a lack of psycho-social support to MS patients. Thus, the influence of cultural tradition cannot be ignored in this context. The results of our study also implicate that all the symptoms of SD have been reported more frequently at each of the subsequent time-points. However, statistical significance was reached only at the 6-year follow-up for incomplete erections, erections not effective to penetrate, inability to ejaculate and reduced libido for male population, and for anorgasmia, difficulties in achieving orgasm and reduced libido for female population. Our results are in accordance with those observed in the 5-year longitudinal study related to the observed increasing tendency of reported SD symptoms in MS patients across time [16]. On the other hand, after the 2-year follow-up, in the Italian MS cohort there were no meaningful changes in prevalence of any of SD symptoms in women, while the statistically significant alteration was observed for frequency of inability to ejaculate and for orgasmic dysfunction in men [15].

Sexuality has been recognized as a very sensitive issue in almost every culture. Thus, the majority of the people hesitate to discuss about their sexual problems and intimacy. In our study, the proportions of MS patients who were willing to talk about sexual problems with doctors and friends are very low, for both men and women (ranging from 3.0% to 7.4% at different time-points of assessments), without significant increase over the 6-year period. However, the chance of discussing sexual issues with partners increased markedly during the follow-up, for both genders (from 22.2% at baseline to 33.3% at the 6-year follow-up for males, and from 22.7% at baseline to 30.3% for females). In the Italian cohort of MS patients, during the 2-year follow-up, the probability of talking about sexual complaints with friends and partners did not increase significantly (from 15.7% to 21.1%, and from 40.7% to 48.5%, respectively), whereas the possibility to discuss with doctors had risen considerably (from 7.4% to 28.4). The low proportion of persons with MS who were ready to talk about their sexual problems in our study might be attributed to the specific social and cultural characteristics of Serbian society. In line with this finding, in the Serbian validation study of the MSQoL-54 questionnaire, the disease-specific instrument for measuring quality of life in patients with MS, it has been already revealed that the highest percentage of missing data was noticed for items concerning sexual function and satisfaction for sexual function (both 20%) [26]. Persons with MS in Serbia probably found sex-related questions as highly distressing or too private to be answered to, based on rigid cultural tradition regarding sexuality in our country. Although sexual functioning is recognized as one of the major determinant of the quality of life in MS, only a minority of MS patients discuss sexual issues with health professionals [2], [4], and [13]. On the other hand, the result from several studies pointed out that the majority of MS patients took advantage of well-informed sexual counseling with their doctors [15] and [27]. These findings highlighted the fact that there was a large discrepancy between the needs and desires of MS patients in terms of discussing sexual problems with their doctors in the physician's office. Furthermore, it has to be emphasized that health-care professionals identified several barriers in managing sexual dysfunction of their patients [28]. The most commonly mentioned difficulties included personal embarrassment, time pressures, lack of appropriate training and concerns related to inability to cope with the issues raised [28]. Additionally, insufficient attention of neurologists, regarding the problems of sexual functioning in MS, could be due, at least partially, to the heterogeneity of numerous MS clinical manifestations [13].

There are many studies facing sexual issues in MS, but only a very few of them have examined predictors of SD changes over time. To our best knowledge, in this survey, mixed-effects regression models have been used for the first time to assess predictor of change of sexual functioning in persons with MS over longer follow-up. The main advantage of this regression model is that it handles time-dependent covariates, in order to provide a clearer picture of the factors that precede changes of the dependent variable. Therefore, by using this regression model, we wanted to explore how individual differences in the change of covariates (i.e. potential predictors) which had been measured over time could explain individual difference in change of dependent variable (Szasz sexual functioning scale score), across the time. The results of our study showed that with each year of the follow-up, the risk of deterioration in sexual functioning increased for 31%, while with each additional year of observation this risk raised for 15%. Our results support the notion that the risk of developing SD and its severity increase significantly as a function of time. This is consistent with a common finding for a higher prevalence of SD in older people who are healthy as well as in persons with various diseases [29] and [30]. Therefore, our result could be partly explained by aging. However, in several MS studies with cross-sectional design it was demonstrated that age correlated with sexual functioning [6], [7], [31], and [32], while, on the other hand, in the remaining, age was not found to be contributing factor when other variables were controlled [33] and [34]. The contradictory findings were also displayed in two longitudinal surveys. Namely, in the 2-year follow-up study, age was identified as significant predictor for changes in sexual function in patients with MS over time [15], whereas in the 5-year longitudinal study SD was not age-dependent [16].

It is well known that the degree of physical disability deeply influence sexual life of patients living with neurological disorder due to multiple psychological, biological and social aspects of disease-related physical incapacity [3], [6], and [35]. Additionally, it is also noted that the higher level of physical disability leads to the fear of rejection, reduced self-image, lack of confidence, and higher level of stress in relationship between patients and their sexual partners which may affect their emotional and sexual functioning [7] and [14]. Our study confirmed that the level of physical disability and its changes over time had been the crucial predictor of changes of sexual functioning in patients with MS over the period of 6 years. However, the results from previous studies implicate that the contribution of MS-induced physical disability to sexual functioning is still controversial. Although, several studies verified this association [3], [6], [7], and [14], others did not [36]. Furthermore, two longitudinal investigations have not identified the level of physical activity in MS as an independent prognostic factor for change in sexual functioning over time [15] and [16]. The differences between our findings and those from other cohort studies [15] and [16] might be, at least partially, the consequence of the longer period of follow-up and more sensitive statistical approach in our investigation.

Our study also demonstrate that the level of depression and fatigue represent independent prognostic factors for change in sexual function over 6 years. Moreover, it is noted that worsening in HDRS and FSS scores for single unit increased the risk for deterioration in SD for 29% and 9%, respectively. These findings are in accordance with previous studies establishing depression and fatigue as very common symptoms in MS with profound influence on patient's sexual life [2], [7], [14], and [31]. It has been highlighted that SD are not linked only to MS-related physical changes, but also to the patient's psychological and socio-cultural background [2] and [32]. Namely, MS-induced changes in interpersonal relationship and family roles, low self-esteem, depressive mood and demoralization may significantly interfere with sexual feeling and sexual response.

Some limitations of the present study need to be kept in mind during interpretation of the results. First, there were only three assessment points and a 3-year year hiatus between them. Therefore, there is no additional information about variation of investigated covariates and dependent variable that potentially occurred during these mean-time intervals. It is clear that more frequent monitoring during the period of follow-up would provide more information about fluctuation in SD changes and their relationship with changes of selected demographic and clinical variables over time. Second, the information bias must be considered because all data related to both, the presence and severity of SD symptoms are self-reported. Finally, the main drawback of our study lies in the fact that we have used Szasz sexual functioning scale, previously proposed in the study of Zorzon et al.[4] and [15], which has not been validated. Therefore, the comparison of our results with other studies is very difficult and complex. However, this scale offered clear picture about the presence and severity of SD in MS patients and its variations over time in our cohort, which is relatively large, with low dropout rates and detailed assessment of predictors of sexual function changes.

5. Conclusions

In conclusion, our results confirmed remarkable frequency of SD in patients with MS. Moreover, this study provides insight into dynamics of change in sexual function and predictors of change among patients with MS, over the period of 6 years. These findings could address clinicians to a more careful and sensitive approach when assessing the influence of MS-related symptoms in order to increase the focus on sexual issues. Nevertheless, an emerging awareness of the importance of estimating the sexual functioning in this neurological disorder leads to the fact that the screening of SD in MS could be considered as one of the indicators of comprehensive clinical assessment of the MS burden.

Conflict of interest

None.

Acknowledgement

This work was supported by the Ministry of Education and Science of the Republic of Serbia (grant numbers 175031 and 175087).

Appendix A. Supplementary data

[locator:mmc1] (link type not set)

Supplementary material 1

[locator:mmc2] (link type not set)

Supplementary material 2

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Footnotes

a Institute of Epidemiology, Faculty of Medicine, University of Belgrade, Belgrade 11000, Serbia

b Institute of Medical Statistics and Informatics, Faculty of Medicine, University of Belgrade, Belgrade 11000, Serbia

c Clinic of Neurology, Clinical Center of Serbia, Faculty of Medicine, University of Belgrade, Belgrade 11000, Serbia

Corresponding author at: Clinic of Neurology CCS, Dr Subotica 6, Belgrade 11000, Serbia.


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