Abstract
Introduction
Inflammatory bowel diseases (IBD) significantly influence sexual function due to their symptoms. The impact of the disease on sexuality and intimacy is a predominant concern for IBD patients, though data on sexual (SD) and erectile dysfunction (ED) and their determinants remain scarce.
Aim
The aim of this study was to evaluate sexual function and identify predictors of SD among patients with IBD during biological treatment.
Material and methods
This prospective study included 135 adult patients with Crohn’s disease (n = 106) and ulcerative colitis (n = 29) who were selected for biological treatment based on established criteria (CD: CDAI > 300; UC: Total Mayo score > 6). Participants completed validated questionnaires on their sexual function: the Female Sexual Function Index (FSFI) and the International Index of Erectile Function-5 (IIEF-5), with a question from the Inflammatory Bowel Disease Questionnaire (IBDQ).
Results
43.7% of patients reported SD, with similar proportions in men and women (p = 0.536). There was no significant correlation between the duration of IBD, type of medication or calprotectin levels and the results of the FSFI and IIEF-5 questionnaires. Self-reported limitations were greater for women compared to men (p < 0.001), with a significant correlation between them and both IIEF-5 and FSFI scores across both disease types (p < 0.001).
Conclusions
SD and ED among patients treated with biologics were associated with psychological factors but not disease severity. The type of medication used to treat the underlying disease did not influence the development of SD. These findings underscore the need for a comprehensive understanding of sexual health and psychological support for IBD patients.
Keywords: sexual dysfunction, erectile dysfunction, sexuality, inflammatory bowel diseases, ulcerative colitis, Crohn disease
Introduction
Crohn’s disease (CD) and ulcerative colitis (UC) are debilitating conditions that profoundly affect patients’ quality of life. Both diseases occur with similar frequency in men and women, with approximately 25% of patients becoming sexually active shortly after diagnosis. This early resumption of sexual activity often leads to numerous questions and challenges in planning their sex lives and future procreation. Furthermore, patients with inflammatory bowel diseases (IBD) are at an increased risk of developing anxiety and depression [1, 2]. During disease flare-ups, an exacerbation of psychological symptoms is typically observed [3, 4], and both psychological symptoms and disease flare-ups are associated with a diminished quality of life [3]. Sexuality is a significant determinant of quality of life, and concerns about the impact of the disease on sexuality and intimacy are prominent among IBD patients. Despite this importance, data on sexual dysfunction (SD) and its determinants in this population remain limited [5, 6].
In empirical research worldwide, the most commonly utilized tools to assess sexual dysfunction are the Female Sexual Function Index (FSFI) for women and the International Index of Erectile Function (IIEF) for men. The FSFI [7] is a 19-item, self-reported inventory designed to evaluate female sexual functioning. This tool has been validated using a clinically diagnosed sample of women with female sexual arousal disorders and encompasses six domains: desire (two items), arousal (four items), lubrication (four items), orgasm, satisfaction, and pain (three items each). The IIEF was initially developed in English and validated to assess the severity of erectile dysfunction (ED). It consists of 15 questions distributed among five categories: erectile function, orgasm, sexual desire, sexual satisfaction, and overall satisfaction. The IIEF scores range from 1 to 75, categorizing erectile function into five subcategories: normal/none, mild, mild/moderate, moderate, and severe. To facilitate the diagnosis of ED, a shortened version known as the IIEF-5 was developed [8]. This streamlined version, comprising only five questions, has been validated as a specific, sensitive, and reliable scale for clinical use [9].
ED is defined as the persistent inability to achieve and maintain an erection sufficient for satisfactory sexual intercourse [10–12]. The incidence and prevalence of ED are considerable, and there is growing awareness that the condition is treatable [10, 13]. Despite the increasing demand for clinical services and the significant impact of ED and other sexual disorders on interpersonal relationships and quality of life, epidemiological data remain relatively scarce [14–16].
The prevalence of ED varies depending on the population under study and the definitions and methods used. Since ED frequently accompanies aging and is associated with chronic illnesses such as diabetes mellitus, heart disease, hypertension, and various neurological diseases, very few studies have specifically addressed the incidence and prevalence of this condition within the IBD population [17, 18].
Aim
The aim of this study was to evaluate sexual function and identify predictors of sexual dysfunction among patients with IBD undergoing biological treatment.
Material and methods
This prospective, single-center study enrolled a cohort of 135 consecutive adult patients with CD (n = 106) and UC (n = 29) who were undergoing biological treatment due to disease flare-ups. Participants were selected based on uniform inclusion criteria (CD: CDAI > 300; UC: Total Mayo score > 6). Recruitment occurred during outpatient visits to the Department of Gastroenterology and Internal Medicine in Warsaw, Poland, from April 1, 2018, to July 18, 2020. All patients were invited to anonymously complete a validated questionnaire on their sexual function, using either the FSFI or the IIEF-5, along with a question from the Inflammatory Bowel Disease Questionnaire (IBDQ): “To what extent has your bowel problem limited your sexual activity in the last 2 weeks?” Due to the nature of the assessments, female and male patients were evaluated separately. In addition to the questionnaires, medical history and sociodemographic data were collected through an anonymous survey, including age, duration of disease, treatment regimen, calprotectin levels, comorbid conditions, and IBD activity scores (CDAI and Mayo).
Statistical analysis
Statistical analysis was conducted using R version 4.0.5, a programming environment for statistical computing (R Core Team, Vienna, Austria). Nominal variables were presented as percentages, while continuous data were reported as either mean ± SD or median (Q1; Q3). The distribution’s normality was assessed using the Shapiro-Wilk test, skewness, and kurtosis. Group comparisons were performed using the χ2 test or Fisher’s exact test for nominal variables and the t-test or Mann-Whitney U test for continuous variables, as appropriate. Correlations between the IIEF-5/FSFI scores and selected continuous variables were examined using Spearman’s correlation coefficient. All analyses used a p-value of < 0.05 to determine statistical significance.
Results
A total of 135 patients were included in the study, consisting of 68 women and 67 men, with 106 patients diagnosed with CD and 29 with UC. The average duration of the disease since diagnosis was 7.48 years. Steroids were more commonly used among women (35%) compared to men (18%; p = 0.037). Additionally, comorbid conditions such as hypertension, psoriasis, or atopic dermatitis were more frequently reported by women (46% vs. 25%; p = 0.023). Other disease parameters and calprotectin levels did not show significant differences between men and women (Table I).
Table I.
Characteristics of patients
| Parameter | N | Total | Men | Women | P-value | |
|---|---|---|---|---|---|---|
| N | 135 | 67 | 68 | |||
| Age [years] mean ± SD | 135 | 33.44 ±9.62 | 32.31 ±7.86 | 34.54 ±11.04 | 0.178 | |
| Place of living, n (%) | ||||||
| Rural | 135 | 23 (17.0) | 13 (19.4) | 10 (14.7) | 0.619 | |
| Urban | 112 (83.0) | 54 (80.6) | 58 (85.3) | |||
| Disease, n (%) | ||||||
| Crohn’s disease | 135 | 106 (78.5) | 55 (82.1) | 51 (75.0) | 0.428 | |
| Ulcerative colitis | 29 (21.5) | 12 (17.9) | 17 (25.0) | |||
| Disease duration [years] mean ± SD | 133 | 7.48 ±5.33 | 7.99 ±5.57 | 6.96 ±5.05 | 0.268 | |
| Steroids, n (%) | 135 | 36 (26.7) | 12 (17.9) | 24 (35.3) | 0.037 | |
| Immunosuppression, n (%) | 134 | 119 (88.1) | 62 (92.5) | 57 (83.8) | 0.194 | |
| Comorbidities, n (%) | 135 | 48 (35.6) | 17 (25.4) | 31 (45.6) | 0.023 | |
| Calprotectin [mg/kg] median (Q1; Q3) | 120 | 312.90 (100.00; 607.00) | 181.00 (48.30; 685.50) | 350.50 (128.25; 547.50) | 0.130 | |
| CDAI, mean ± SD | 106 | 333.60 ±85.98 | 333.92 ±74.35 | 333.27 ±97.74 | 0.969 | |
| Partial Mayo Score, median (Q1; Q3) | 29 | 1.00 (0.00; 2.00) | 0.00 (0.00; 1.25) | 2.00 (1.00; 2.00) | 0.041 | |
SD were identified in 86 patients, with no statistically significant difference observed between men and women. The mean IIEF-5 score for men was 19.85 ±6.97, with 40% (27 out of 67) experiencing ED. For women, the mean FSFI score was 25.21 ±6.64, with 47% (32 out of 68) reporting sexual dysfunction. Additionally, self-assessed limitations due to the disease were significantly more severe for women (p < 0.001) (Table II).
Table II.
Sexual disorders in the study group
| Parameter | N | Total | Men | Women | P-value |
|---|---|---|---|---|---|
| Self-assessed limitation due to disease, median (IBDQ) | 133 | 6.00 (3.00; 7.00) | 7.00 (5.00; 7.00) | 3.00 (2.00; 7.00) | < 0.001 |
| IIEF-5, mean ± SD | 67 | 19.85 ±6.97 | – | – | |
| FSFI, mean ± SD | 68 | – | 25.21 ±6.64 | – | |
| Sexual disorders, n (%) | 135 | 59 (43.7) | 27 (40.3) | 32 (47.1) | 0.536 |
The IIEF-5 score showed no significant correlation with either the duration of disease or calprotectin levels. However, a significant positive correlation was observed between the IIEF-5 score and self-assessed disease limitation (p < 0.05), confirmed across both disease types: higher IIEF-5 scores were associated with better self-reported disease management (Table III).
Table III.
Correlation between degree of erectile dysfunction and selected factors in men
| Parameter | Men (IIEF-5) | ||
|---|---|---|---|
| r | P-value | ||
| All patients | |||
| Disease duration | 0.06 | 0.634 | |
| Calprotectin | –0.08 | 0.566 | |
| Self-assessed limitation due to disease (IBDQ) | 0.42 | < 0.001 | |
| Crohn’s disease patients | |||
| Disease duration | 0.10 | 0.457 | |
| Calprotectin | –0.10 | 0.474 | |
| Self-assessed limitation due to disease (IBDQ) | 0.38 | 0.004 | |
| Ulcerative colitis patients | |||
| Disease duration | 0.17 | 0.596 | |
| Calprotectin | 0.31 | 0.684 | |
| Self-assessed limitation due to disease (IBDQ) | 0.67 | 0.017 | |
r – Spearman’s correlation coefficient.
Similarly, the FSFI score did not exhibit significant correlations with disease duration or calprotectin levels. A significant positive correlation was noted between the FSFI score and self-assessed disease limitation (p < 0.05), confirmed in both disease types: improved FSFI scores correlated with better self-assessment of disease limitation (Table IV).
Table IV.
Correlation between degree of sexual dysfunction and selected factors in women
| Parameter | Women (FSFI) | ||
|---|---|---|---|
| r | P-value | ||
| All patients | |||
| Disease duration | 0.02 | 0.905 | |
| Calprotectin | –0.05 | 0.684 | |
| Self-assessed limitation due to disease (IBDQ) | 0.72 | < 0.001 | |
| Crohn’s disease patients | |||
| Disease duration | 0.02 | 0.901 | |
| Calprotectin | –0.04 | 0.791 | |
| Self-assessed limitation due to disease (IBDQ) | 0.78 | < 0.001 | |
| Ulcerative colitis patients | |||
| Disease duration | –0.05 | 0.849 | |
| Calprotectin | –0.12 | 0.682 | |
| Self-assessed limitation due to disease (IBDQ) | 0.56 | 0.019 | |
r – Spearman’s correlation coefficient.
The analysis comparing patients with and without SD did not reveal any correlations with the use of steroids, immunosuppression, or type of disease. Additionally, no significant differences were observed in disease duration or calprotectin levels between patients with and without SD (Table V).
Table V.
Comparison of patients with and without sexual dysfunction. Groups compared with χ2 test or Fisher’s exact test for nominal variables and with t-test or Mann-Whitney U test for continuous variables. Both with 95% CI (confidence interval)
| Parameter | Sexual disorders | OR/MD (95% CI) | P-value | ||
|---|---|---|---|---|---|
| No | Yes | ||||
| Men | |||||
| n | 40 | 27 | |||
| Steroids, n (%) | 8 (20.0) | 4 (14.8) | 0.70 (0.19; 2.59) | 0.827 | |
| Immunosuppression, n (%) | 36 (90.0) | 26 (96.3) | 2.89 (0.30; 27.37) | 0.886 | |
| Disease type, n (%) | |||||
| Crohn’s disease | 31 (77.5) | 24 (88.9) | 2.32 (0.57; 9.52) | 0.386 | |
| Ulcerative colitis | 9 (22.5) | 3 (11.1) | |||
| Disease duration [years] mean ± SD | 8.30 ±5.21 | 7.52 ±6.14 | –0.78 (–3.67; 2.11) | 0.589 | |
| Calprotectin [mg/kg] median (range) | 169.00 (5.00; 2410.00) | 229.00 (0.00; 2160.00) | 60.00 (–152.00; 158.00) | 0.934 | |
| Women | |||||
| n | 36 | 32 | |||
| Steroids, n (%) | 13 (36.1) | 11 (34.4) | 0.93 (0.34; 2.51) | > 0.999 | |
| Immunosuppression, n (%) | 31 (86.1) | 26 (81.3) | 0.70 (0.19; 2.56) | 0.831 | |
| Disease type, n (%) | |||||
| Crohn’s disease | 26 (72.2) | 25 (78.1) | 1.37 (0.45; 4.17) | 0.779 | |
| Ulcerative colitis | 10 (27.8) | 7 (21.9) | |||
| Disease duration [years] mean ± SD | 7.12 ±5.49 | 6.77 ±4.56 | –0.35 (–2.82; 2.12) | 0.777 | |
| Calprotectin [mg/kg], median (range) | 337.50 (8.20; 1760.00) | 409.00 (30.9; 1260.00) | 71.50 (–113.00; 218.00) | 0.712 | |
OR – odds ratio, MD – mean/median difference.
Statistical analysis revealed significant differences in IIEF-5 scores between men with UC (22.42 ±3.70) and those with CD (19.29 ±7.41; mean difference = –3.13, 95% CI [–6.10; –0.15]; p = 0.040) (Table VI). However, no similar differences were identified among women (Table VII). The presence of steroids or immunosuppression did not affect the IIEF-5 or FSFI scores (Tables VI and VII).
Table VI.
Comparison of IIEF-5 score with steroids, immunosuppression and disease type. Groups compared with t-test
| Parameter | Men | |||
|---|---|---|---|---|
| IIEF-5 (mean ± SD) | MD (95% CI) | P-value | ||
| Steroids | ||||
| No | 19.65 ±7.23 | 1.10 (–2.97; 5.17) | 0.580 | |
| Yes | 20.75 ±5.83 | |||
| Immunosuppression | ||||
| No | 19.75 ±10.50 | 0.04 (–16.40; 16.48) | 0.994 | |
| Yes | 19.79 ±6.85 | |||
| Disease type | ||||
| Ulcerative colitis | 22.42 ±3.70 | –3.13 (–6.10; –0.15) | 0.040 | |
| Crohn’s disease | 19.29 ±7.41 | |||
MD – mean difference with 95% CI (confidence interval).
Table VII.
Comparison of FSFI score with steroids, immunosuppression and disease type. Groups compared with t-test. MD – mean difference with 95% CI (confidence interval)
| Parameter | Women | |||
|---|---|---|---|---|
| FSFI (mean ± SD) | MD | P-value | ||
| Steroids | ||||
| No | 24.77 ±7.38 | 1.24 (–1.79; 4.27) | 0.417 | |
| Yes | 26.01 ±5.05 | |||
| Immunosuppression | ||||
| No | 22.28 ±9.69 | 3.50 (–3.12; 10.11) | 0.271 | |
| Yes | 25.78 ±5.83 | |||
| Disease type | ||||
| Ulcerative colitis | 26.89 ±2.91 | –2.24 (–4.75; 0.26) | 0.078 | |
| Crohn’s disease | 24.65 ±7.42 | |||
Discussion
As defined by the World Health Organization, sexual health is a state of physical, emotional, mental, and social well-being in relation to sexuality; it is not merely the absence of disease, dysfunction, or infirmity [19]. Sexual health, along with one’s body image, plays a critical role in psychosocial functioning and significantly impacts overall quality of life [20]. IBD can alter patients’ physical appearance due to scarring from surgery or the presence of stomas, fistulas, or abscesses, potentially increasing the risk of a disturbed body image, especially among women and postoperative patients. Studies indicate that a depressed mood is the most prevalent and significant risk factor for sexual impairment in IBD patients, with 35% to 58% reporting sexual disorders associated with their diagnosis [21, 22]. The frequency of sexual dysfunction is generally higher in IBD patients compared to healthy controls.
Marin et al. observed that sexual desire and satisfaction deteriorated in half of the women and one-third of the men following an IBD diagnosis. All patients with IBD in their study had significantly lower scores on sexual function indexes compared to controls, with a higher prevalence of sexual dysfunction noted among women. In our study, 43.7% of participants were confirmed to have sexual dysfunction, although no significant differences were noted between men and women (p = 0.536). Independent predictors of sexual dysfunction among IBD patients, according to Marin et al., included the use of corticosteroids in women and the use of biological agents, depression, and diabetes in men [22]. However, our results did not reveal any correlation between sexual dysfunction and the use of steroids, immunosuppression, or disease type.
In a study by Riviere et al., 54% of women and 43% of men with IBD reported experiencing sexual dysfunction and erectile dysfunction, respectively. There was no significant difference in the prevalence of sexual dysfunction between patients with active or inactive disease (for women: 53.2% vs. 61.2%, p = 0.66; for men: 26.3% vs. 15.5%, p = 0.11). Notably, sexual dysfunction and erectile dysfunction were significantly associated with age older than 50 years. These rates were considerably higher than those observed in control groups and were primarily influenced by psychological factors; disease severity did not have a significant impact [23]. Our findings also confirmed that disease severity did not affect sexual or erectile dysfunction.
Bel et al. evaluated 168 female and 119 male IBD patients and found no differences in the prevalence of sexual dysfunction (SD) between patients and controls. However, participants with active disease had significantly lower scores on the IIEF-5 and FSFI compared to controls and patients in remission. According to their data, statistically significant correlations were identified between disease activity, fatigue, depressive mood, quality of life, and sexual function for both genders. Depression emerged as the most crucial determinant of impaired sexual function in IBD [24]. In our study, all participants were experiencing a flare of IBD and were undergoing biological treatment. We did not inquire about additional factors that might affect sexual functioning, such as quality of life or fatigue.
Muller et al. investigated whether female gender was an independent predictor of impaired body image (OR = 3.246, p < 0.05), decreased libido (OR = 3.574, p < 0.05), and infrequent sexual activity (OR = 3.895, p < 0.05) [25]. Our findings indicated a significant positive correlation between the IIEF-5/FSFI scores and self-assessed disease limitations (p < 0.05) for both men and women across both disease types.
Our study has several limitations. It was conducted at a single center and was observational in nature. Additionally, we did not include specific questions regarding the impact of surgery, perianal disease, or psychological support on patients with sexual dysfunction and impaired body image.
Conclusions
Sexual and erectile dysfunction among patients treated with biologics were predominantly associated with psychological factors; disease severity showed no significant influence. Additionally, the type of medications used to manage Crohn’s disease and ulcerative colitis did not impact the development of sexual dysfunction. Self-assessed limitations due to the disease were significantly more severe for women, and there was a significant positive correlation between IIEF-5 and FSFI scores and the assessment of limitations. Women also had a higher prevalence of comorbidities such as hypertension, psoriasis, or atopic dermatitis (46% vs. 25%; p = 0.023), which might have influenced these scores. A deeper understanding of the roles of sexual functioning and body image in the quality of life of IBD patients is essential, as these factors highlight the need for psychological support alongside medical treatment.
Funding
No external funding.
Ethical approval
Not applicable.
Conflict of interest
The authors declare no conflict of interest.
References
- 1.Costal AL, Chaves EC. Stress coping strategies and depressive symptoms among ulcerative colitis patients. Rev Esc Enferm USP 2006; 40: 507-14. [DOI] [PubMed] [Google Scholar]
- 2.Walker EA, Gelfand MD, Gelfand AN, et al. The relationship of current psychiatric disorder to functional disability and distress in patients with inflammatory bowel disease. Gen Hosp Psychiatry 1996; 18: 220-9. [DOI] [PubMed] [Google Scholar]
- 3.Pizzi LT, Weston CM, Goldfarb NI, et al. Impact of chronic conditions on quality of life in patients with inflammatory bowel disease. Inflamm Bowel Dis 2006; 12: 47-52. [DOI] [PubMed] [Google Scholar]
- 4.Kunzendorf S, Jantschek G, Straubinger K, et al. The Luebeck interview for psychosocial screening in patients with inflammatory bowel disease. Inflamm Bowel Dis 2007; 13: 33-41. [DOI] [PubMed] [Google Scholar]
- 5.Buvat J, Glasser D, Neves RCS, et al. Sexual problems and associated help-seeking behavior patterns: results of a population-based survey in France. Int J Urol 2009; 16: 632-8. [DOI] [PubMed] [Google Scholar]
- 6.Ghosh S, Louis E, Beaugerie L, et al. Development of the IBD disk: a visual self-administered tool for assessing disability in inflammatory bowel diseases. Inflamm Bowel Dis 2017; 23: 333-40. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.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: 191-208. [DOI] [PubMed] [Google Scholar]
- 8.Rosen RC, Cappelleri JC, Smith MD, et al. Development and evaluation of an abridged, 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res 1999; 11: 319-26. [DOI] [PubMed] [Google Scholar]
- 9.Cappelleri JC, Rosen RC. Reply to ‘The sexual health inventory for men (IIEF-5)’ by Ja Vroege. Int J Impot Res 1999; 11: 353-4. [DOI] [PubMed] [Google Scholar]
- 10.NIH Consensus Development Panel on Impotence . Impotence JAMA 1993; 270: 83-90. [PubMed] [Google Scholar]
- 11.Feldman HA, Goldstein I, Hatzichristou DG, et al. Impotence and its medical and psychosocial correlates: results of the Massachusetts Male Aging Study. J Urol 1994; 151: 54-61. [DOI] [PubMed] [Google Scholar]
- 12.Morley JE. Impotence. Am J Med 1986; 80: 897-905. [DOI] [PubMed] [Google Scholar]
- 13.Goldstein I, Lue TF, Padma-Nathan H, et al. Oral sildenafil in the treatment of erectile dysfunction. N Engl J Med 1998; 338: 1397-404. [DOI] [PubMed] [Google Scholar]
- 14.Jonler M, Moon T, Brannan W, et al. The effect of age, ethnicity and geographical location on impotence and quality of life. Br J Urol 1995; 75: 651-5. [DOI] [PubMed] [Google Scholar]
- 15.Laumann EO, Paik A, Rosen RC. Sexual dysfunction in the United States: prevalence and predictors. JAMA 1999; 281: 537-44. [DOI] [PubMed] [Google Scholar]
- 16.Kirby RS. Impotence: diagnosis and management of male erectile dysfunction. Br Med J 1994; 308: 957-61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Wagner G, Saenz de Tejada I. Update on male erectile dysfunction Br Med J 1998; 316: 678-82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Szydlarska D, Jakubowska A, Rydzewska G. Assessment of sexual dysfunction in patients with inflammatory bowel disease. Gastroenterology Rev 2019; 14: 104-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.World Health Organization . Defining Sexual Health; Report of a Technical Consultation on Sexual Health. Geneva: World Health Organization, 2002. [Google Scholar]
- 20.Knowles SR, Gass C, Macrae F. Illness perceptions in IBD influence psychological status, sexual health and satisfaction, body image and relational functioning: a preliminary exploration using Structural Equation Modeling. J Crohns Colitis 2013; 7: e344-50. [DOI] [PubMed] [Google Scholar]
- 21.Moody GA, Mayberry JF. Perceived sexual dysfunction amongst patients with inflammatory bowel disease. Digestion 1993; 54: 256-60. [DOI] [PubMed] [Google Scholar]
- 22.Marin L, Manosa M, Garcia-Planella E, et al. Sexual function and patients’ perceptions in inflammatory bowel disease: a case-control survey. J Gastroenterol 2013; 48: 713-20. [DOI] [PubMed] [Google Scholar]
- 23.Rivière P, Zallot C, Desobry P, et al. Frequency of and factors associated with sexual dysfunction in patients with inflammatory bowel disease. J Crohns Colitis 2017; 11: 1347-52. [DOI] [PubMed] [Google Scholar]
- 24.Bel LG, Vollebregt AM, Van der Meulen-de Jong, et al. Sexual dysfunctions in men and women with inflammatory bowel disease: the influence of IBD-related clinical factors and depression on sexual function. J Sex Med 2015; 12: 1557-67. [DOI] [PubMed] [Google Scholar]
- 25.Muller KR, Prosser R, Bampton P, et al. Female gender and surgery impair relationships, body image, and sexuality in inflammatory bowel disease: patient perceptions. Inflamm Bowel Dis 2010; 16: 657-63. [DOI] [PubMed] [Google Scholar]