Article published online: 2021-07-27 THIEME Original Article | Artigo Original 467 Sexuality of Female Spina Bifida Patients: Predictors of a Satisfactory Sexual Function Sexualidade feminina em pacientes com espinha bífida: preditores de uma função sexual satisfatória Guilherme Lang Motta1,2 Anna Bujons3 Yesica Quiróz3 Erika Llorens3 Maira Zancan2,4 Tiago Elias Rosito2,5 1 Surgery Department, Universidade Federal de Santa Maria, Santa Address for correspondence Guilherme Lang Motta, MD, MSc, PhD, Maria, Rio Grande do Sul, RS, Brazil Avenida Roraima 1000, 97105-900, Santa Maria, Rio Grande do Sul, 2 Postgraduate Program in Health Sciences: Gynecology and RS, Brasil (e-mail: glangmotta@gmail.com). Obstetrics, Universidade Federal do Rio Grande do Sul, RS, Brazil 3 Pediatric Urology Department, Fundació Puigvert, Barcelona, Spain 4 Gynecology and Obstetrics Department, Universidade Federal de Santa Maria, Santa Maria, Rio Grande do Sul, RS, Brazil 5 Urology Department, Hospital de Clínicas de Porto Alegre, Porto Alegre, Rio Grande do Sul, RS, Brazil Rev Bras Ginecol Obstet 2021;43(6):467–473. Abstract Objective To assess the sexual function of women with spina bifida (SB), and to verify the factors that influence their sexual function. Methods A cross-sectional study in which a validated female-specific questionnaire was applied to 140 SB female patients from four different cities (Porto Alegre, Brazil; and Barcelona, Madrid, and Málaga, Spain) between 2019 and 2020. The question- naires collected data on the clinical characteristics of SB, and female sexual function was assessed using the 6-item version of the Female Sexual Function Index (FSFI-6) validated to Portuguese and Spanish. Results Half of the patients had had sexual activity at least once in the life, but most (57.1%) did not use any contraception method. Sexual dysfunction was present in most (84.3%) patients, and all sexual function domains were impaired compared those of non-neurogenic women. The presence of urinary and fecal incontinence significantly affected the quality of their sexual activity based on the FSFI-6. Keywords Conclusion The specific clinical aspects of the SB patients, such as urinary and fecal ► sexuality incontinence, should be properly addressed by their doctors, since they are associated ► spina bifida with reduced sexual activity and lower FSFI-6 scores in the overall or specific domains. ► sexual dysfunction There is also a need to improve gynecological care among sexually-active SB patients, ► urinary incontinence since most do not use any contraceptive methods and are at risk of inadvertent ► myelomeningocele pregnancy. received DOI https://doi.org/ © 2021. Federação Brasileira de Ginecologia e Obstetrícia. All rights June 18, 2020 10.1055/s-0041-1732464. reserved. accepted ISSN 0100-7203. This is an open access article published by Thieme under the terms of the May 5, 2021 Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/) Thieme Revinter Publicações Ltda., Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil 468 Sexuality of Female Spina Bifida Patients Motta et al. Resumo Objetivo Analisar a função sexual de pacientes do sexo feminino com espinha bífida (EB), e avaliar quais fatores influenciam na função sexual. Métodos Uma pesquisa transversal em que um questionário validado para mulheres foi aplicado em 140 pacientes com EB de quatro cidades diferentes (Porto Alegre, Brasil; e Barcelona, Madri e Málaga, Espanha) entre 2019 e 2020. Os questionários coletaram dados sobre características clínicas da espinha bífida, e a função sexual feminina foi avaliada com a versão de seis itens do Índice de Funcionamento Sexual Feminino (IFSF-6) nas versões validadas para português e espanhol. Resultados Metade das pacientes havia praticado atividade sexual pelo menos uma vez na vida, mas a maioria (57.1%) não utilizava nenhum método contraceptivo. A disfunção sexual estava presente na maioria das pacientes (84.3%), sendo todos os domínios de função sexual prejudicados em comparação com os de mulheres não neurogênicas. A presença de incontinência urinária e fecal afetou significativamente a qualidade da atividade sexual das pacientes. Palavras-chave Conclusão Aspectos clínicos específicos da EB, como incontinência urinária e fecal, ► sexualidade devem ser adequadamente abordados pelos médicos assistentes, visto que estão ► espinha bífida associados à redução na atividade sexual e piores resultados no IFSF-6. Também é ► disfunção sexual necessário melhorar o atendimento ginecológico das pacientes sexualmente ativas, ► incontinência urinaria uma vez que a maioria não utiliza métodos contraceptivos e corre o risco de gravidez ► mielomeningocele inadvertida. Introduction invited to participate in this study. Only women older than 18 years of age who could read and understand the ques- Spina bifida (SB) is the main neurological birth defect that tionnaire, after informed consent, were enrolled. The surveys occurs due to an impaired closure of the neural tube, leading were administered in person by trained interviewers who to multi-systemic dysfunctions such as neurogenic bladder.1 helped the patients to fulfill them. A non-probability purpo- The life expectancy of SB patients has increased as a result of sive sampling of 210 patients was eligible and invited, with improved medical care; therefore, adult-life issues, such as 140 accepting to participate after reading the informed social life and sexuality, have become growing concerns consent (response rate of 66.6%). among this population.1,2 There is consistent data associat- The questionnaires collected data on demographics, soci- ing the complications of SB, such as urinary incontinence (UI) oeconomics, clinical and gynecological characteristics, and and fecal incontinence, with negative effects on socializa- sexuality. Female sexual function was assessed using the 6- tion.1,3 Sexuality among SB patients is considered an impor- Item Version of the Female Sexual Function Index (FSFI-6) tant topic of discussion, and it lead to many studies on the validated to Spanish and Portuguese.10–12 It consists of a male population.4,5 Studies on female SB patients, however, questionnaire that approaches the following sexual function are limited, and most have small sample sizes, are single- domains: desire, arousal, lubrication, orgasm, satisfaction, institution surveys, or use non-validated questionnaires.6–9 and pain. Each item has a score varying from 0 to 5, whose These studies revealed that women with SB present higher sum provides the final score. A FSFI-6 total score  19 was sexual dysfunction rates than the general female population, considered a positive screening for female sexual dysfunc- and they suggest that some clinical factors, such as spinal- tion (FSD).12 Sexual activity was defined as having a history cord level and UI, could predict their sexual outcomes. The of at least one sexual intercourse. The body mass index (BMI) aim of the present study was to assess the sexual function of was calculated using the patient’s weight in kilograms women with SB and to verify the factors that influence their divided by the square of height in meters, and obesity of sexual function. was defined as a BMI score  30. Fecal incontinence or UI were defined as involuntary leakage of urine or feces. Psy- chological disorders were identified according to the Methods patient’s report, and they included the following conditions: A cross-sectional study was implemented in four different SB depression, anxiety, or mood disorders. centers (Spina Bifida associations inBarcelona, Madrid and The authors followed guidelines of the Strengthening the Málaga, Spain; and the Urology Department at Hospital de Reporting of Observational Studies in Epidemiology Clínicas de Porto Alegre, in Porto Alegre, Brazil). Between (STROBE) statement during the preparation oif the present 2019 and 2020, adult female SB patients who undergoing manuscript.13 The following statistical tests utilized were regular follow-up in the aforementioned centers were used: Chi-squared, Fisher exact, and Mann-Whitney, and Rev Bras Ginecol Obstet Vol. 43 No. 6/2021 © 2021. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexuality of Female Spina Bifida Patients Motta et al. 469 they were analyzed using the Statistical Package for the Table 1 Gynecological care and sexuality characteristics of Social Sciences (IBM SPSS Statistics for Windows, IBM spina bifida patients Corp., Armonk, NY, US) software, version 25.0. A Poisson logistic regression model was created to assess both sexual Characteristic n (%) activity or dysfunction, and in each model we included the Gynecological examination variables that presented significance of association (p < 0.05) Irregular visits 95(67.9) or a trend to association (p < 0.2) in the bivariate analysis: Regular visits 25(17.9) BMI, UI and fecal incontinence. The present study was approved by each local institutional ethics committee under Has never undergone a gynecological 20(14.3) examination registration number (CAAE 96636518.3.0000.5327). Sexual activity No 70(50) Results Yes 70(50) In the present study, we analyzed 140 adult female SB Contraceptive methoda,b patients, with a mean age of 27 (range: 18 to 42) years and No 40(57.1) a mean BMI of 26.2 (range: 18 to 43) Kg/m2, who were interviewed in Spain (89.3%) and Brazil (10.7%). Most Yes 30(42.9) patients were single (85%) women living with their Pregnancy parents/family (82.1%) who economically-dependent on No 134(95.7) them (66.4%). Their level of schooling was most commonly Yes 6(4.3) Elementary School (61.4%). Myelomeningocele at lower lev- a Sexual dysfunction els (91.4%) associated with hydrocephalus (82.9%) was the No 11(15.7) most common SB presentation at birth. Approximately 77.1% presented mobility without the need of aids, while 22.9% Yes 59(84.3) were wheelchair-dependent. In total, UI occurred in 83.6% of a Notes: Assessed only among sexually-active women; includes hor- b the patients, fecal incontinence was present in 64.3%, and monal and non-hormonal contraceptives. 16.4% claimed a history of psychological disorder. Regular annual gynecological (GO) follow-up was a rou- tine for 17.9% of the patients, irregular previous GO con- sexual dysfunction (p ¼ 0.004) in the regression analysis was sultations occurred in 67.9%, and 14.3% had never had a UI. Patients who suffered from UI presented a prevalence single GO evaluation. Half of the patients had had sexual ratio of 1.46 (95% confidence interval [95%CI]: 1.21–1.76) of activity at least once in their life, and most (85%) were single sexual dysfunction, and a prevalence ratio of 0.78 (95%CI: women. Among those sexually active, most (57.1%) did not 0.67–0.9) of sexual activity. use any contraception method. Gestational history was The sexual-function domains were also analyzed quanti- present in 6 (4.3%) patients, all of them subitted to deliveries tatively. Obesity, type of SB, and deambulation status did not by cesarean section without complications (►Table 1). Sex- influence the scores of any sexual function domain. Those ual dysfunction was present in 84.3% of the sexually-active without hydrocephalus had better scores only in the orgasm patients, with a median FSFI-6 total score of 14.5 (range: 4 to domain. Fecal incontinence and UI were significantly associ- 26). The scores on specific domains of the FSFI-6 were also ated with lower scores in all domains, except for pain analyzed among the sexually-active women (►Fig. 1). (►Table 3). The clinical characteristics of the patients were compared with their sexual activity and the presence of sexual dys- function (FSFI-6 overall score > 19). The type of SB, spinal cord level, hydrocephalus, use of wheelchair, psychological disorder, and fecal incontinence were not statistically asso- ciated with differences in the rates of sexual activity or dysfunction. Obesity (BMI  30) had a significant association with sexual dysfunction (p ¼ 0.004; Fisher exact test), but no differences regarding sexual-activity rates (p ¼ 0.572). The presence of UI was associated with significant lower rates of sexual activity (continent: 78.3% versus UI: 44%; p ¼ 0.003; Chi-squared test) and higher rates of sexual dysfunction (continent: 50% versus UI: 96.2%; p < 0.001; Fisher exact test) (►Table 2). A Poisson logistic regression model using BMI, UI and fecal Fig. 1 Median total score and scores for the domains of the six-item incontinence was created to assess both sexual activity and version of the Female Sexual Function Index (FSFI-6) among sexually- dysfunction. The only clinical variable that demonstrated active women with spina bifida. Data are presented as medians (25th significance with lower sexual activity (p ¼ 0.006) and more percentile––75th percentile). Rev Bras Ginecol Obstet Vol. 43 No. 6/2021 © 2021. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. 470 Sexuality of Female Spina Bifida Patients Motta et al. Table 2 Clinical characteristics and sexual outcomes Sexual activity Sexual dysfunction n ¼ 140 n ¼ 70 No Yes No Yes 2 Body mass index (Kg/m )  20 4(50) 4(50) 3(75) 1(25%) 20–25 18(41.9) 25(58.1) 1(4) 24(96%) 25–30 35(52.2) 32 (47.8) 6(18.8) 26(81.2%)  30 13(59.1) 9(40.9) 1(11.1) 8(88.9) a b p-value 0.572 0.004 Myelomeningocele 64(50) 64 (50) 11(17.2) 53(82.8) Meningocele/Others (includes spina bifida occulta) 6(50) 6(50) 0(0) 6(100) p-value 1a 0.580b Spinal cord level Lumbar or lumbosacral 64(50) 64(50) 10(15.6) 54(84.4) Thoracic or Thoracolumbar 6(50) 6(50) 1(16.7) 5(83.3) p-value 1a 1b Hydrocephalus No 13(54.2) 11(45.8) 2(18.2) 9(81.8) Yes 57(49.1) 59(50.9) 9(15.3) 50(84.7) a b p-value 0.654 1 Deambulation Deambulates 52(48.1) 56(51.9) 9(16.1) 47(83.9) Wheelchair 18(56.3) 14(43.7) 2(14.3) 12(85.7) p-value 0.421a 1b Urinary incontinence No 5(21.7) 18(78.3) 9(50) 9(50) Yes 65(55.6) 52(44.4) 2(3.8) 50(96.2) a b p-value 0.003 < 0.001 Fecal incontinence No 23(46) 27(54) 7(25.9) 20(74.1) Yes 47(52.2) 43(47.8) 4(9.3) 39(90.7) a b p-value 0.480 0.092 Psychological disorder No 59(50.4) 58(49.6) 8(13.8) 50(86.2) Yes 11(47.8) 12(52.%) 3(25) 9(75) p-value 0.820a 0.386b Notes: aChi-squared test; bFisher exact test; female sexual dysfunction was assessed only among sexually-active women. Discussion A sexual activity rate of 50% among the SB patients in the present study is concordant with previous research6–8,14 that Spina bifida is a complex group of anatomical changes reported rates of sexual activity among women with the characterized by impaired fusion of the vertebral arches in same condition ranging from 32% to 68%. This demonstrates the first 28 days of the embryo, and it is considered the main important differences compared with the general female neurological birth defect.1 Traditionally considered a condi- population from the countries involved in the study – Brazil tion of the pediatric population, SB has undergone major and Spain –,which presented sexual intercourse rates rang- changes due to better medical care, and, nowadays, most ing from 83.6% to 85.3%.15,16 Also, the prevalence of sexual patients reach adulthood.2 Thus, the increase in life expec- dysfunction in the present study (84.3%), compared with a tancy leads to a rising importance of sexuality among this large Brazilian sample of non-SB women with dysfunction population. rates of 49%, highlights the need to improve sexual care in Rev Bras Ginecol Obstet Vol. 43 No. 6/2021 © 2021. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexuality of Female Spina Bifida Patients Motta et al. 471 Table 3 Clinical characteristics and specific domains of the 6-item version of the Female Sexual Function Index (FSFI-6) among sexually-active female spina bifida patients. Data are presented as medians (25th percentile–75th percentile) Desire Arousal Lubrication Orgasm Satisfaction Pain Overall Type of lesion Myelomeningocele 3(2–3) 2(1–3) 2(2–3) 2(1–3) 2(1–3) 4(3–4) 14.5(11.25–18) Meningocele/Others 2(2–3) 2(1.75–3.25) 2(1.75–3.25) 2(1.75–3) 1.5(1–2.25) 4.5(3–5) 15.5(11.75–17.5) (includes spina bifida occulta) p-value 0.542 0.655 0.786 0.761 0.345 0.247 0.891 Spinal cord level Lumbar or lumbosacral 3(2–3) 2(1–3) 2(2–3) 2(1–3) 2(1–3) 4(3–4) 15(11.25–18) Thoracic or 1.5(1–4) 2(2–3.5) 2(1–4) 2(2–2.5) 1(1–3.5) 4(3.75–5) 14.3(11.75–20.75) thoracolumbar p-value 0.322 0.349 0.761 0.573 0.430 0.221 0.908 Hydrocephalus No 2(1–3) 2(1–3) 2(2–3) 3(2–4) 1(1–2) 4(4–5) 15(12–18) Yes 3(2–3) 2(1–3) 2(2–3) 1(1–3) 2(1–3) 4(3–4) 14(11–18) p-value 0.303 0.802 0.701 0.015 0.328 0.241 0.703 Deambulation Deambulates 2.5(2–3) 2(1–3) 2(2–3) 2(1.25–3) 2(1–3) 4(3–4) 15(11.25–18) Wheelchair 3(2–4) 2(0.75–3) 2.5(1.5–3) 1(0.75–2.25) 2(1–3.25) 4(2.25–4) 13.5(11.5–16.25) p-value 0.067 0.843 0.524 0.136 0.062 0.232 0.534 Urinary incontinence No 3.5(3–4) 3(3–3.25) 4(3–4) 3(2–3) 3.5(3–4) 4(3–4) 19.5(18–23) Yes 2(1.25–3) 2(1–2) 2(1.25–3) 2(1–3) 1.5(1–2) 4(3–4) 13(11–15.75)  p-value < 0.001 < 0.001 < 0.001 0.037 < 0.001 0.381 < 0.001 Fecal incontinence No 3(2–4) 3(2–3) 3(2–4) 3(2–3) 3(2–4) 4(3–4) 18(13–21) Yes 2(1–3) 2(1–2) 2(2–3) 2(1–2) 2(1–2) 4(3–5) 13(11–16) p-value 0.007 0.009 0.017 0.006 0.004 0.065 0.003 Psychological disorder No 3(2–3) 2(1–3) 2(2–3) 2(1–3) 2(1–3) 4(3–4) 14.5(11.75–18) Yes 3(2–3) 2(2–3) 2(2–3) 3(1.25–3) 2(1–3.75) 4(3–4.75) 15.5(11.5–21.75) p-value 0.802 0.374 0.866 0.194 0.903 0.993 0.547  Note: Mann-Whitney non-parametric test. SB.17 The weak median scores found in the overall and inferior compared with non-neurogenic female sexually- specific-domains of the FSFI-6 among our patients are similar active patients who attended the gynecology outpatient to the scores found in previous studies that quantitatively clinic of the Brazilian institution in the present study (SB assessed sexuality in a quantitative matter.8,18 Lee et al.18 patients: 42.9%; regular patients: 91.9%), revealing the risk of found lower overall and specific-domain scores in the FSFI of inadvertent pregnancy among the population with SB.19 SB patients when compared with non-SB women who also Other studies7,9 have already demonstrated a lack of contra- suffered from sexual dysfunction, showing that these neu- ception in these patients, which is believed to be related to rologic patients demand more attention to their sexual life inadequate sex education and unfamiliarity with the avail- than regular patients.18 able options. Other factors that may contribute are the high To comprehend the sexuality of female patients, it is rates of latex allergy and comorbidities associated with SB important to assess their GO aspects. Our study demonstrat- that restrict the use of contraceptives (such as epilepsy and ed that only 17.9% of the SB patients had regular annual GO the use of anticonvulsants; and reduced mobility and throm- follow-up, meanwhile almost 15% had never undergone a boembolic events).20,21 The physiological process of preg- single GO evaluation. Also, the prevalence of contraceptive nancy and the effects of fetal growth can exacerbate the methods used by sexually-active SB patients was much manifestations of SB, such as bone abnormalities (mainly in Rev Bras Ginecol Obstet Vol. 43 No. 6/2021 © 2021. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. 472 Sexuality of Female Spina Bifida Patients Motta et al. the spine and hips), which could restrict mobility, cause pain, Conclusion make vaginal delivery difficult, and hinder epidural analge- sia.20,22 Spina bifida patients have been encouraged to The clinical aspects of SB patients, such as UI and fecal perform vaginal deliveries and follow the obstetric indica- incontinence, should be properly addressed by their doctors, tions for cesarean section respecting their orthopedic limi- since they are associated with reduced sexual activity and tations (auch as narrow pelvis or severe scoliosis).20,23 lower FSFI-6 scores in the overall or specific domains. There Despite these recommendations, SB patients are still most is also a need to improve GO care among sexually-active SB often submitted to cesarean sections when compared with patients, since most do not use any contraceptive methods, the general population.23 In the present study, in spite of the and are at risk of inadvertent pregnancy. low rates of contraception, only 4.3% had a history of pregnancy, and there were no major complications during Contributors deliveries, which were all cesarean sections. All authors contributed to the writing of the article, The clinical characteristics of SB and the sexual outcomes relevant revision of the intellectual content, and approved have been analyzed qualitatively and quantitatively. The UI the final version submitted for publication. status was the most relevant factor, since it impaired either sexual activity rates and worsened the overall and specific- Conflict of Interests domain scores on the FSFI-6. The only aspect that did not The authors have no conflict of interests to declare. suffer significant influence from the UI was the pain domain. These findings are consonant with those of previous studies, References including the specific data from Gamé et al.,6 who also 1 Copp AJ, Adzick NS, Chitty LS, Fletcher JM, Holmbeck GN, Shaw observed that the desire, arousal and lubrication domains GM. Spina bifida. Nat Rev Dis Primers. 2015;1:15007. Doi: suffered negative effects from UI among SB patients.6–8 Other 10.1038/nrdp.2015.7 non-neurogenic conditions that caused UI also showed that 2 Sawin KJ, Liu T, Ward E, et al; NSBPR Coordinating Committee. The it has major impact in female sexual life, mainly due to the National Spina Bifida Patient Registry: profile of a large cohort of fear of unpredictable incontinence during sex. Urinary in- participants from the first 10 clinics. J Pediatr. 2015;166(02): 444–50.e1. Doi: 10.1016/j.jpeds.2014.09.039 continence impairs the self-esteem and promotes anxiety, 3 Vu Minh Arnell M, Abrahamsson K. Urinary continence appears to which could contribute to these findings.24,25 Although fecal enhance social participation and intimate relations in adolescents incontinence did not promote significant differences in the with myelomeningocele. J Pediatr Urol. 2019;15(01):33.e1–33.e6. rates of sexual activity, we found that it influenced negative- Doi: 10.1016/j.jpurol.2018.08.008 ly, in a similar manner to that of UI, in all sexual-function 4 Wiener JS, Frimberger DC, Wood H. Spina bifida healthcare guidelines for men’s health. Urology. 2018;116:218–226. Doi: domains but pain. Few studies26,27 assessed fecal inconti- 10.1016/j.urology.2018.01.005 nence and sexuality, with a limited inference that it could 5 Shiomi T, Hirayama A, Fujimoto K, Hirao Y. Sexuality and seeking impair the social life and sexual perception of the SB medical help for erectile dysfunction in young adults with spina patients.26,27 Neurological characteristics (type of SB, spinal bifida. Int J Urol. 2006;13(10):1323–1326. Doi: 10.1111/j.1442- cord level, hydrocephalus, walking ability, and the presence 2042.2006.01559.x of concomitant psychological disorders) showed little influ- 6 Gamé X, Moscovici J, Guillotreau J, Roumiguié M, Rischmann P, Malavaud B. Sexual function of young women with myelome- ence in the sexual outcomes. The only significant finding is ningocele. J Pediatr Urol. 2014;10(03):418–423. Doi: 10.1016/j. that those without hydrocephalus had better scores on the jpurol.2013.07.016 orgasm domain of the FSFI-6. Two previous studies9,28 have 7 Gatti C, Del Rossi C, Ferrari A, Casolari E, Casadio G, Scire G. described that SB patients with hydrocephalus demonstrat- Predictors of successful sexual partnering of adults with spina ed inferior sexual activity, fewer sexual partners, and more bifida. J Urol. 2009;182(4, Suppl):1911–1916. Doi: 10.1016/j. sexual dysfunction. The fact that hydrocephalus is caused by juro.2009.02.065 8 Choi EK, Kim SW, Ji Y, Lim SW, Han SW. Sexual function and Arnold-Chiari type-2 cerebellar malformation could explain qualify of life in women with spina bifida: Are the women with the orgasm interference, since the cerebellum demonstrated spina bifida satisfied with their sexual activity? Neurourol Uro- increased activity during orgasm in functional magnetic dyn. 2018;37(05):1785–1793. Doi: 10.1002/nau.23525 resonance imaging studies.29 9 Verhoef M, Barf HA, Vroege JA, et al. 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