Sexual Function of Patients with Deep Endometriosis after Surgical Treatment: A Systematic Review

► systematic review ► endometriosis ► sexual health ► surgery ► dyspareunia

Objective To review the current state of knowledge on the impact of the surgical treatment on the sexual function and dyspareunia of deep endometriosis patients. Data Source A systematic review was conducted in accordance with the Meta- Analysis of Observational Studies in Epid emiology (MOOSE) guidelines. We conducted systematic searches in the PubMed, EMBA SE, LILACS, and Web of Science databases from inception until December 2022. The eligi bility criteria were studies including: preoperative and postoperative comparat ive analyses; patients with a diagnosis of deep endometriosis; and questionnaires to measure sexual quality of life. Study Selection Two reviewers screened and reviewed 1,100 full-text articles to analyze sexual function after the surgical treatment for deep endometriosis. The risk of bias was assessed using the Newcastle-Ottawa scale for observational studies and the Cochrane Collaboration ’s tool for randomized controlled trials. The present study was registered at the International Prospective Register of Systematic Reviews (PROSPERO; registration CRD42021289742). Data Collection General variables about the studies, the surgical technique, com- plementary treatments, and questionnaire sw e r ei n s e r t e di na nM i c r o s o f tE x c e l2 0 1 0 (Microsoft Corp., Redmond, WA, United States) spreadsheet. Synthesis of Data We included 20 studies in which the videolaparoscopy technique was used for the excision of deep in filtrating endometriosis. A meta-analysis could not be performed due to the substantial heterogeneity among the studies. Classes III and IV of the revised American Fertility Society classi fication were predominant and multiple received January 11, 2023 accepted May 3, 2023 DOI https://doi.org/ 10.1055/s-0043-1772596. ISSN 0100-7203. © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. This is an open access article published by Thieme under the terms of the 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 THIEME Review Article 729 Article published online: 2023-11-29

Endometriosis is de fined as the presence of endometrial stroma and glands outside the uterine cavity. It is present in 3% to 15% of fertile women,1 and it affects women’s quality of life, causing chronic pelvic pain, dyspareunia, infertility, as well as certain deleterious sexual effects in 67% of the cases. 2 In contrast, deep in filtrating endometriosis (DIE) consists of the penetration of the endometrial tissue more than 5 mm below the peritoneal surface. 3 The literature reports that endometriotic disease is the main cause of dyspareunia, and it affects 60% to 70% of women undergoing surgery. The common presence of DIE on cardinal and uterosacral ligaments, on the pouch of Douglas and on the posterior vaginal fornix represents a nine-old increase in the risk of developing dyspareunia. 2,4 Dyspareunia does not cause only pain: it is also associated with psychological and psychosocial injury. Feelings of fear during intercourse, as well as guilt, are predominant among DIE patients, and they directly and indirectly affect domains of sexual function such as desire, frequency, pleasure and orgasm. 5 The treatment for endometriosis is mainly focused on pain control and quality of life improvement, including, sexual life. Hormonal therapies are effective for pain control during disease progression, but they can also lead to gonadal suppression and reduced sexual response. 6 However, surgi- cal procedures and radical resection of all visible endome- triosis nodules may improve quality of life in up to 85% to 95% of severe to moderate cases. 7 According to international guidelines, endometriosis is a chronic disease that requires a life-long management plan to control pain symptoms and to avoid multiple surgical pro- cedures. 8 Hormonal therapies to achieve a hypoestrogenic status are effective to control pain and disease progression, but they are also associated with gonadal suppression and surgical techniques for the treatment of endometriosis were performed. Standardized and validated questionnaires were applied to evaluate sexual function.

Laparoscopic surgery is a complex procedure that involves multiple organs, and it has been proved to be effective in improving sexual function and dyspareunia in women with deep in filtrating endometriosis. Resumo Objetivo Revisar a literatura publicada sobre o impacto do tratamento cirúrgico na função sexual e na dispareunia de pacientes com endometriose profunda. Fonte de Dados Uma revisão sistemática foi realizada de acordo com as diretrizes Meta-Analysis of Observational Studies in Epidemiology (MOOSE). Realizamos pesqui- sas sistemáticas nas bases de dados PubMed, EMBASE, LILACS e Web of Science desde o início até dezembro de 2022. Os critérios de e legibilidade foram estudos que incluíam: análises comparativas pré- e pós-operatóri as; pacientes com diagnóstico de endome- triose profunda; e a aplicação de questionários para avaliar a função sexual. Seleção dos Estudos Dois revisores selecionaram e revisaram 1.100 artigos para analisar a da função sexual após o tratamento cirúrgico da endometriose profunda. O risco de viés foi calculado usando-se a escala de Newcastle-Ottawa para estudos observacionais e a ferramenta para ensaios clínicos randomizados da Cochrane Collaboration. O estudo foi cadastrado no International Prospective Register of Systematic Reviews (PROSPERO; cadastro CRD42021289742). Coleta de dados Variáveis gerais sobre os estudos, a técnica cirúrgica, os tratamentos complementares e os questionários foram inseridas em uma planilha do Microsoft Excel 2010 (Microsoft Corp., Redmond, WA, Estados Unidos). Síntese dos dados Foram incluídos 20 estudos em que se usou a técnica de videolaparoscopia para a excisão da endometriose profunda. Uma meta-análise não pôde ser realizada devido à heterogeneidade substancial entre os estudos incluídos. As classes III e IV da escala revisada da American Fertility Society foram predominantes, e múltiplas técnicas cirúrgicas foram usadas para o tratamento da endometriose. Questionários padronizados e validados foram aplicados para avaliar a função sexual. Conclusão A cirurgia laparoscópica é um procedimento complexo que envolve múltiplos órgãos, e provou ser e ficaz na melhora da função sexual e da dispareunia em mulheres com endometriose profunda. Palavras-chave ► revisão sistemática ► endometriose ► saúde sexual ► cirurgia ► dispareunia Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al.730 reduced sexual response. 6 The aim of the surgical treatment is the excision of all endometriosis lesions to improve pain and infertility. However, in cases of extensive DIE, surgery is associated with peri- and postoperative complications, as well as a decrease in sexual function. 9 Thus, the present systematic review aims to assess how surgery affects sexual function and dyspareunia in patients undergoing surgical treatment to treat DIE.

The present systematic review was conducted in accordance with the Meta-Analysis of Observational Studies in Epidemi- ology (MOOSE) guidelines. The study protocol was registered at the at the International Prospective Register of Systematic Reviews (PROSPERO; registration CRD 42021289742) and followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. 10 We performed a search in the following databases: PubMed, EMBASE, Cochrane Library, LILACS, and Web of Science from inception to December 2022. The main key- words used were deep endometriosis , sexual function , resec- tion,a n d shaving. The full search strategy used can be found in ►Chart 1 . Two independent reviewers (GC and DF) were invited to analyze all articles found. Initially, an analysis of the titles and abstracts was performed to screen for potential eligible studies. Later, the reviewers evaluated the fully screened articles to select eligible studies. Disagreements were re- solved by joint review and consensus among reviewers. To comply with the objectives of the present systematic review, the eligibility criteria were as follows: comparative studies on female sexual function before and after surgery for deep endometriosis; studies with women previously diagnosed with deep endometriosis by physical examination or complementary imaging exams submitted to surgery; and studies with the application of standardized questionnaires to assess sexual function and dyspareunia. No clinical treat- ment associated with surgery was established, neither a limited time of follow-up after surgery, nor were there language restrictions during the initial search. The exclusion criteria were: conference abstracts, case reports, case series, reviews, and duplicate studies. In the full-text analysis, articles published in languages other than English, Portu- guese, Italian, Spanish, and French were also excluded. The two reviewers (GC and DF) inserted the data from all the included studies in a Microsoft Excel 2010 (Microsoft Corp., Redmond, WA, United States) spreadsheet. We extracted general variables form the studies, such as author- ship, year of publication, country, type of study, follow-up, surgery performed, age of the patients, and the number of patients included. We also recorded the name of the ques- tionnaire used for the evaluation of sexual function and dyspareunia. The heterogeneity among the studies and ques- tionnaires found in the literature did not enable the perfor- mance of a meta-analysis. The outcome of interest was the assessment of sexual function before and after surgery using a validated question- naire. The presence of dyspareunia before and after the surgery was also evaluated. Chart 1 Searchstrategy for the selection of studies Database Search Strategy Number Of Studies PubMed ( deep endometriosis OR deep infiltrating endometriosis OR endometrioma )A N D(resection OR excision OR nodulectomy OR cystectomy OR shaving OR rectosigmoidectomy )A N D (dyspareunia OR (sexual AND (function OR quality OR behavior) OR (pain OR dysfunction) AND (sexual OR sexual intercourse) 313 EMBASE ( deep endometriosis/exp OR deep endometriosis OR deep in filtrating endometriosis/exp OR deep in filtrating endometriosis OR endometrioma/exp OR endometrioma )A N D( resection/exp OR resection OR excision/exp OR excision OR nodulectomy/exp OR nodulectomy OR cystectomy/exp OR cystectomy OR shaving/exp OR shaving OR rectosigmoidectomy/exp OR rectosigmoidectomy )A N D dyspareunia OR (sexual AND (function OR quality OR sexual behavior) OR (pain OR dysfunction) AND (sexual OR sexual intercourse) AND (article/it OR article in press/it OR review/it) AND [female] 597 Cochrane Library (deep endometriosis OR deep infiltrating endometriosis OR endometrioma )A N D(resection OR excision OR nodulectomy OR cystectomy OR shaving OR rectosigmoidectomy ) AND (dyspareunia OR (sexual AND (function OR quality OR sexual behavior) OR (pain OR dysfunction) AND (sexual OR sexual intercourse) 20 LILACS ( deep endometriosis OR deep infiltrating endometriosis OR endometrioma )A N D(resection OR excision OR nodulectomy OR cystectomy OR shaving OR rectosigmoidectomy )A N D (dyspareunia OR (sexual AND (function OR quality OR sexual behavior) OR (pain OR dysfunction) AND (sexual OR sexual intercourse) 9 Web of Science (deep endometriosis OR deep infiltrating endometriosis OR endometrioma )A N D(resection OR excision OR nodulectomy OR cystectomy OR shaving OR rectosigmoidectomy )A N D (dyspareunia OR (sexual AND (function OR quality OR sexual behavior)) OR (pain OR dysfunction) AND (sexual OR sexual intercourse) 161 Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al. 731 To evaluate the risk of bias in non-randomized studies (such as case-control and cohort studies), we used the Newcastle-Ottawa Scale (NOS), while the risk of bias in randomized controlled trials (RCT) was evaluated using the Cochrane Collaboration ’s tool (RoB-1). 11,12 The NOS is based on a star scoring system in which the observational study is assessed in terms of three broad parameters: selection of the study groups; comparability of the groups; and ascertainment of either the exposure or the outcome of interest for case-control or cohort studies respectively. 11 On the other hand, the RoB-1 covers six domains of the possible biases of RCTs: selection bias, performance bias, detection bias, attrition bias, reporting bias, and other biases. Each domain is classi fied as low, high, or unclear risk of bias. 12

We found 1,100 studies; after removing the duplicates, 831 studies were screened for titles and abstracts by 2 reviewers who selected 108 studies for full-text analyses. Finally, a total of 20 studies ful filled the eligibility criteria and were includ- ed in the present systematic review. A flowchart of the search and selection of studies is summarized in ►Fig. 1 . Observational studies and one RCT were included in the review. Half of the cohort studies (50%) had a score /C21 7 stars on the NOS scale, while 38% had 6 stars, and 2, /C20 5 stars. The RCT had a score of 6 stars on the NOS scale; it was on a comparison of laparoscopic surgeries with and without uterosacral ligament resection, and it presented an unclear risk of bias for random sequence generation and allocation sequence concealment, and a high risk for blinding of the outcome assessment. In total, the studies included evaluated 2,145 patients with follow-ups ranging from 3 to 69 months. The characteristics of the included studies are presented in ►Chart 2 . A comparison of the pre- and postoperative outcomes regarding sexual function and dyspareunia is shown in ►Chart 3 . The predominant surgical technique used to treat DIE patients was laparoscopic surgery. A total of 14 articles used only the laparoscopy technique for DIE excision, while 3 studies associated it with the CO 2 laser technique. 13–15 Two studies performed vaginal surgery associated with the lapa- roscopic procedure, when necessary, 16,17 and one combined laparoscopy with transurethral surgery. 18 In one study,18 transurethral and laparoscopic surgeries to resect bladder endometriosis presented a signi ficancy im- provement in sexual function in all 6 domains of the Female Sexual Function Index (FSFI), with a postoperative score of 28.2 þ//C0 1.7. Setälä et al. 16 and Fritzer et al. 17 performed vaginal surgery associated with videolaparoscopy proce- dures to resect vaginal endometriosis lesions, resulting in a significant increase on sexual comfort and pleasure accord- ing to the modi fied McCoy Female Sexuality Questionnaire (MFSQ). 16 However, the study by Fritzer et al. 17 did not show significant results in the final FSFI score in any of the three population groups compared (DIE, vaginal resection, and peritoneal endometriosis). 17 Sexual function after the CO 2 laser technique was evaluated by two different Fig. 1 Flowchart o the search and selection of studies. Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al.732 Chart 2 Characteristics of the studies selected Author, year Country Type of study N Type of surgery Age in years Sexual function questionnaire Dyspareunia questionnaire Garry et al., 27 2000 United Kingdom Prospective 57 Laparoscopic excision surgery – SAQ NRS Abbot et al., 24 2003 Australia Prospective 254 Laparoscopic excision surgery Median: 31 (range 20–48) SAQ VAS Vercellini et al., 32 2003 Italy Randomized controlled trial 180 Laparoscopic excision surgery Mean 30 /C6 5S S R S V A S Ferrero et al., 26 2007 Italy Prospective 98 Laparoscopic excision surgery Mean 34.6 /C6 3.4 DSFI; GSSI – Ferrero et al., 25 2007 Italy Prospective 73 Laparoscopic excision surgery Mean 34.7 /C6 4.3 DSFI; GSSI VAS Meuleman et al., 15 2009 Belgium Retrospective 56 Laparoscopic excision surgery with CO 2 laser Median:32 (range: 24–42) SAQ VAS Meuleman et al., 13 2012 Belgium Retrospective 45 Laparoscopic excision surgery with CO 2 laser Median 30 (range: 18–42) SAQ VAS Mabrouk et al., 33 2012 Italy Prospective 125 Laparoscopic excision surgery Mean 35.4 /C6 5.5 SHOW-Q VAS Setälä et al., 16 2012 Finland Prospective 22 Laparoscopic excision surgery or combined laparoscopic vaginal surgery Median: 29 (range: 19–40) MFSQ VAS Kossi et al., 21 2013 Finland Prospective 26 Laparoscopic excision surgery Median: 33.5 (range: 22 –46) MFSQ – Van den Broeck et al., 14 2013 Belgium Prospective 203 (total); 76 WB; 127 WOB Laparoscopic excision surgery with CO 2 laser – SSFS – Di Donato et al., 31 2015 Italy Prospective 250 DIE; 250 HG Laparoscopic excision surgery DIE: mean 34 /C6 5 HG: mean 32 /C6 6 SHOW-Q – Fritzer et al., 17 2016 Germany Prospective 96 Laparoscopic excision surgery or combined laparoscopic vaginal surgery Median: 30.8 (range: 18 –45) FSDS; FSFI NRS Pontis et al., 18 2016 Italy Prospective 16 FSFI – (Continued ) Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al. 733 Chart 2 (Continued ) Author, year Country Type of study N Type of surgery Age in years Sexual function questionnaire Dyspareunia questionnaire Combined transurethral and laparoscopicd surgeries Mean: 29.12 /C6 4.33 Riiskjaer et al., 20 2016 Denmark Prospective 128 Laparoscopic excision surgery Mean: 33.8 /C6 5.3 SVQ 1: never; 2: a little; 3: often; 4: very often Uccella et al., 29 2018 Italy Prospective 34 Laparoscopic excision surgery Median 39 (range: 27–51) FSFI – Lermann et al., 19 2019 Germany Retrospective 134 WOB; 113 WB; 100 CG Laparoscopic excision surgery WOB: mean 34.3 /C6 6; WB: mean – 37.7 /C6 6. KFSP – Ianieri et al., 28 2022 Italy Retrospective 100 Laparoscopic Excision Surgery Mediana:38 (32,5 – 43) FSFI VAS Martínez-Zamora et al., 34 2021 Spain Prospective 193 (total); 129 DIE; 64 CG Laparoscopic excision surgery DIE: mean 33.5 /C6 6.04; CG: mean 34.7 /C6 4.5 SQoL-F; FSDS; B- PFSF – Zhang et al., 30 2022 China Retrospective 55 Laparoscopic excision surgery Mean: 30 /C6 3 FSFI – Abbreviations: B-PFSF, Brief Pro file of Female Sexual Function; CG, control group; CO 2, carbon dioxide; DIE, deep in filtrating endometriosis; DSFI, Derogatis Sexual Functioning Inventory; FSDS, Female Sexual Distress Scale, revised; FSFI, Female Sexual Function Index; GSSI, Global Sexual Satisfaction Index; HG, healthy group; KFSP, Kurzfragebogen Sexu alität und Partner-schaft; MFSQ, McCoy Female Sexuality Questionnaire modi fied by Wiklund et al; NRS, Numeric Rating Scale; SAQ, Sexual Activity Questionnaire; SSFS, Short Sexual Functioning Scale; SHOW-Q, Sexual Health Outc omes in Women Questionnaire; SQoL-F, Sexual Quality of Life /C0 Female Questionnaire; SQV, Sexual Function-Vaginal Changes Questionnaire; SSRS, Sabbatsberg Sexual Rating Scale; VAS, Visual Analogue Scale; WB , with bowel resection; WOB, without bowel resection. Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al.734 Chart 3 Preoperative and postoperative comparison of sexual function and dyspareunia according to the questionnaires applied Sexual Function Dyspareunia Autor, year Follow-up (months) Preoperatively Postoperatively Significance Preoperatively Postoperatively Significance Questionnaire: SAQ Garry et al., 27 2000 4 Pleasure: 11 (6 /C6 13) Pleasure: 13 (9 /C6 16) Pleasure: 0.002 7 (5.5 /C6 9) 0 (0 /C6 4) 0.0001 Discomfort: 3 (1.5 /C6 5) Discomfort: 1 (0 /C6 3) Discomfort: < 0.05 Habit:1 (0 /C6 1) Habit:1 (1 /C6 2) Habit: < 0.002 Abbott, et al., 24 2003 60 Pleasure:10 (5 /C6 12) Pleasure:12 (9 /C6 16) Pleasure: 0.001 Median: 6.0 (0.0–9.0) 0.0 (0.0 –4.0) < 0.001 Discomfort: 3 (1 /C6 5) Discomfort: 2( 1 . 5/C6 3) Discomfort: < 0.012 Habit:1 (0 /C6 1) Habit:1(1 /C6 1) Habit:0.001 Meuleman et al., 15 2009 29 –– Pleasure: < 0.0001 5 (0 –10) 1 (0 –10) < 0.0001 Discomfort: < 0.0001 Habit< 0.0001 Meuleman et al., 13 2012 27 –– Pleasure: 0.009 28 (0 –95) 1 (0 –63) < 0.0001 Discomfort: 0.026 Habit: 0.0003 Questionnaire: FSFI Pontis et al., 18 2016 12 26 /C6 2.5 28 /C6 1.7 < 0.001 ––– Uccella et al., 29 2018 6 19.1 (1.2 –28.9) 22.7 (12.2 –31) 0.004 ––– Ianieri et al., 28 2022 3 P: 19.4 /C6 9.8 P: 21.6 /C6 10.8 0.34 P: 5.2 /C6 3.6 P: 0.9 /C6 2.2 < 0.001 NP 23.8 /C6 3.7 NP: 23.7 /C6 8.1 NP: 3.7 /C6 3.5 NP: 0.1 /C6 0.5 Zhang et al., 30 2022 26 26.1 /C6 32 6 . 8 /C6 3 0.25 ––– Questionnaire: FSFI and FSDS Fritzer et al., 17 2016 10 FSFI –– DIE: 0.21 DIE: 6.18 DIE: 2.49 < 0.001 Vaginal: 0.98 Peritoneal: 0.11 Vaginal: 6.64 Vaginal: 2.18 < 0.001 FSDS –– DIE: 0.04 Vaginal: 0.25 Peritoneal: 5.05 Peritoneal: 2.85 < 0.001 Peritoneal: 0.34 Questionnaire: SHOW-Q Mabrouk et al., 33 2012 6 Satisfaction: 51 Satisfaction: 65 < 0.0005 7 /C6 31 /C6 3 < 0.0001 Orgasm: 57 Orgasm: 59 0.7 Desire: 55 Desire: 64 < 0.0004 (Continued ) Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al. 735 Chart 3 (Continued ) Sexual Function Dyspareunia Autor, year Follow-up (months) Preoperatively Postoperatively Significance Preoperatively Postoperatively Significance Di Donato et al., 31 2015 12 Satisfaction: 50 Satisfaction: 75 < 0.001 ––– Orgasm:63 Orgasm:62 Not signi ficant Desire: 58 Desire: 72 < 0.001 Questionnaire: DSFI and GSSI Ferrero et al., 26 2007 3 DSFI Frequency with USL: 1.3 /C6 0.7; without USLE: 1.6 /C6 0.7 Frequency with USL: 2.3 /C6 0.7; without USL: 2.2 /C6 0.8 Frequency ith USL: < 0.001; without USL: 0.004 ––– 3 DSFI Orgasm with USL: 2.3 /C6 1.0; without USL: 2.9 /C6 1.0 Orgasm with USL: 4.4 /C6 1.1; without USL: 3.1 /C6 1.5 Orgasm with USL: 0.001; without USL: 0.003 3 GSSI With USL: 3.4 /C6 1.7; without USL: 4.1 þ//C0 1.7 With USL: 5.5 /C6 1.9; without USL: 5.3 þ//C0 1.8 With USL: 0.001; without USL: 0.003 Ferrero et al., 25 2007 6 DSFI Frequency with USL: 1.1 /C6 0.6; without USL: 1.3 /C6 0.9 Frequency with USL: 1.8 /C6 0.8; without USL: 2.2 /C6 1.1 Frequency with USL: < 0.001; without USL: < 0.001 With USL: 7.6 /C6 1.1; without USL: 7.1 /C6 1.0 With USL: 2.8 /C6 1.9; without USL: 2.4 /C6 1.8 < 0.001 6 DSFI Orgasm with USL: 2.3 /C6 1.2; without USL: 3.1 /C6 1.0 Orgasm with USL: 1.3 /C6 0.9; without USL: 4.2 /C6 1.3 Orgasm with USL: < 0.001; without ULSE: < 0.003 6 GSSI With USL: 3.2; without USL: 3 With USL: 5; without USL: 5.8 < 0.001 < 0.001 12 DSFI Frequency with USL: 1.1 /C6 0.6; without USL: 1.3 /C6 0.9 Frequency with USL: 1.9 /C6 0.7; without USL: 2.2 /C6 1.1 Frequency with USL: < 0.001; without USL: < 0.027 With USL: 7.6 /C6 1.1; without USL: 7.1 /C6 1.0 With USL: 2.8 /C6 2.2; without USL: 2.2 /C6 1.8 < 0.001 12 DSFI Orgasm with USL: 2.3 /C6 1.2; without USL: 3.1 /C6 1.0 Orgasm with USL: 1.9 /C6 0.7; without USL: 4.0 /C6 1.0 Orgasm with USL: < 0.001; without USL: < 0.118 12 GSSI With USL: 3.2; without USL: 3 With USL: 5.2; without USL: 5.6 < 0.001 < 0.001 Questionnaire: MFSQ Setälä et al., 16 2012 12 Sexual satisfaction: 21.1 Sexual satisfaction: 2.1 < 0.05 4.3 1.7 < 0.05 Sexual problem: 6.3 Sexual problem: 1.4 < 0.05 Partner satisfaction: 12.1 Partner satisfaction: 0.8 Not signi ficant Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al.736 Chart 3 (Continued ) Sexual Function Dyspareunia Autor, year Follow-up (months) Preoperatively Postoperatively Significance Preoperatively Postoperatively Significance Kossi et al., 21 2013 12 Sexual satisfaction: 20.1 Sexual satisfaction: 2.8 < 0.01 ––– Sexual problem: 7 Sexual problem: 1.1 < 0.10 Partner satisfaction: 12.1 Partner satisfaction: 0.7 < 0.10 Questionnaire: KFSP Lermann et al., 19 2019 69 WB: 24 WB: 25 0.416 ––– WOB: 27.5 WOB: 19.5 0.001 Questionnaires: SQOL, FSDS and B-PFSF Martínez-Zamora et al., 34 2021 36 SQOL-F: 70 SQOL-F: 77 < 0.001 ––– FSDS: 17 FSDS: 10 < 0.001 B-PFSF: 18 B-PFSF: 25 < 0.001 Questionnaire: SQV Riiskjaer et al., 20 2016 12 Satisfaction: 3 (1 –7) Satisfaction: 4 (1 –7) 0.0001 3 (1 –4) 2 (1 –4) < 0.0001 Frequency: 2 (1 –5) Frequency: 3(1 –5) 0.0004 Desire: 2 (1 –4) Desire: 2 (1 –4) 0.0003 Questionnaire: SFSS Van den Broeck et al., 14 2013 6 Orgasm – WB:10.5%; WOB:16.3% Orgasm – WB: 0%; WOB: 10% 0.05 Excitation – WB:21.6%; WOB:11.5% Excitation – WB:7.4%; WOB:13%% > 0.05 Desire – WB:31.7%; WOB: 28.4% Desire – WB:9.4%; WOB:19.4% > 0.05 18 Orgasm – WB:16.3%; WOB:10,5% Orgasm – WB: 6.3%; WOB: 2.9% > 0.05 WB: 44.8%; WOB: 31.3% WB: 6.3%; WOB: 20% > 0.05 Excitation – WB: 21.6%; WOB: 11.5% Excitation – WB: 6.3%; WOB: 2.9% > 0.05 Desire – WB: 28.4%; WOB: 31.7% Desire – WB: 12.1%; WOB: 5.7% > 0.05 (Continued ) Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al. 737 questionnaires.13–15 The Sexual Activity Questionnaire (SAQ) showed signi ficant postoperative improvement on the following pillars of sexual function: pleasure, habit 13,15 and discomfort. 15 The Short Sexual Function Scale (SSFS) only presented signi ficant improvement in the pillar of orgasm after surgery. 14 Other articles also evaluated sexual function and DIE of the bowel. A comparative study 19 analyzed sexual function for the following sixty-nine months after DIE surgery with and without bowel resection. Postoperatively, the patients without bowel resection improved signi ficantly in all cate- gories on the Kurzfragebogen Sexualität und Partner-schaft (KFSP) questionnaire. Not only no signi ficant postoperative improvement was observed in the patients in the bowel endometriosis group, but this group had signi ficantly poorer scores in comparison with the control group. 19 Riiskjaer et al. 20 performed laparoscopy for DIE of the bowel and observed positive results on the Sexual Function-Vagi- nal Changes Questionnaire (SQV) after one year of follow- up: there was a signi ficant increase in vaginal changes, general sexual satisfaction, desire for sexual intercourse, and frequency of sexual intercourse. Laparoscopic resection for bowel endometriosis also resulted in an increase in sexual satisfaction on the overall MFSQ score one year after surgery in one study. 21 Sexual problems and satisfaction with partner scores did not change signi ficantly in another study.22 The surgical data related to the female sexual function response in the studies analyzed were collected and pre- sented in ►Chart 4 . The extension of the endometriosis was ascertained intra- operatively using the revised American Fertility Society (rAFS) 22 and the Enzian scale 23 in 13 studies. 13–17,19,24–30 In the evaluated articles, 45.32% of the patients were classi fied as rAFS class IV (severe), followed by 27.67% as class III (moder- ate),13.65% as class II (mild), and 13.40% as class I (minimal). The most common pelvic sites of DIE involvement were: the uterosacral ligaments (51.24%), the bowel (31.56%), the vagina (14.45%), the rectovaginal septum (8.89%) and the retrocer- vical nodule (6.46%). 14,19–21,25,26,28–31 Three comparative studies 25,26,32 evaluated sexual func - tion after resection of the uterosacral ligament. In two of them, 25,26 the authors used the Derogatis Sexual Func - tioning Inventory (DSFI) and Global Sexual Satisfaction Index (GSSI) to analyze sexual function 6 and 12 months postoperatively, and found a signi ficant increase in sexual function up to 6 months. Frequency and orgasm on the DSFI were not signi ficant at the 12-month follow- up.25,26 Similar results were presented by Vercellini et al. 32 after 18 months of follow-up, with no signi ficant improve- ment in sexual function on the Sabbatsberg Sexual Rating Scale (SSRS). An improvement in sexual function was also observed on FSFI scores after resection of bladder endometriosis, 18 as well as a signi ficant improvement in sexual satisfaction and intercourse pain on the MFSQ after twelve months of surgery in a group of women with DIE submitted to vaginal nodule resection.16 Chart 3 (Continued ) Sexual Function Dyspareunia Autor, year Follow-up (months) Preoperatively Postoperatively Significance Preoperatively Postoperatively Significance Questionnaire: SSRS Vercellini et al., 32 2003 18 USL:45.4 /C6 19.9 USL:53.8 /C6 18.8 0.763 USL: 58 (45 –72) USL: 22 (0 –35) 0.0001 CG: 44.7 /C6 20.8 CG: 55.4 /C6 15.6 CG: 54 (26 –67) CG: 18 (0 –30) 0.0001 Abbreviations: B-PFSF, Brief Pro file of Female Sexual Function; CG, control group; DIE, deep in filtrating endometriosis; DSFI, Derogatis Sexual Functioning Inventory; FSDS, Female Sexual Distress Scale, revised; FSFI, Female Sexual Function Index; GSSI, Global Sexual Satisfaction Index; KFSP, Kurzfragebogen Sexualität und Partner-schaft; MFSQ, McCoy Fema le Sexuality Questionnaire modi fied by Wiklund et al; NP, no parametrial group; P, parametrial group; SAQ, Sexual Activity Questionnaire; SFSS, Short Sexual Functioning Scale; SHOW-Q, Sexual Health Outcome s in Women Questionnaire; SQoL-F, Sexual Quality of Life /C0 Female Questionnaire; SQV, Sexual Function-Vaginal Changes Questionnaire; SSRS, Sabbatsberg Sexual Rating Scale; USL, uterosacral ligament; WB , with bowel resection; WOB, without bowel resection. Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al.738 Chart 4 Surgical data as reported by the studies selected Author, year Histological analysis Endometriosis classification Intraoperative classification Nerve-sparing technique Procedures Other endometriosis location (%) Retro cervical (%) USL (%) Rectovaginal septum (%) Vagina (%) Bowel (%) Garry et al., 27 2000 No rAFS III: 63.2% No Complication: 1,9% – bruises Ovaries: 40.3%; total pouch of Douglas obliteration: 30.4%; partial pouch of Douglas obliteration: 33.3% 33.3% No Speci fics i d e : 77.2% 59.6% 38.52% 56.1% Abbot et al., 24 2003 Yes rAFS I:14%; II: 28%; III: 17%; IV: 41% No Complication: 0.3% – iatrogenic bowel injury; 0.6% – transfusion; 0.3% –vaginal deiscense Total pouch of Douglas obliteration: 32%; partial pouch of Douglas obliteration: 18%; bilateral endometrioma: 12%; right: 18%; left: 12% – Unilateral 88%; bilateral: 57% – 6% – Vercellini et al., 32 2003 No rAFS I: 39%; II: 22%; III: 20%; IV: 19% No ––– No speci fic side: 100% –– – Ferrero et al., 26 2007 Yes –– No ––– No speci fic side: 65.3% –– – Ferrero et al., 26 2007 Yes rAFS IV-III: 86.9%; II-I: 12.32% No ––– No speci fic side: 64.7% –– – Meuleman et al., 15 2009 Yes rAFS II: 2.22%; III: 4.44%; IV: 95% Yes Oophorectomy: 9%; appendectomy: 14%; salpingectomy: 30%; cystectomy: 39%; ureterolysis: 86%; adhesiolysis: 100%; complication: 3.5% – vascular anastomosis; 5.3% – compartmental syndrome – 11% –– – Anterior bowel resection: 36%; sigmoid resection: 39% Meuleman et al., 13 2012 Yes rAFS III: 2%; IV: 98% Yes Oophorectomy 2%; bladder suture: 7%; appendectomy: 9%; salpingectomy: 38%; cystectomy: 42%; ureterolysis: 91%; complication: 2.2% – transitory urinary retention – 16% –– – Sigmoid resection: 90% Mabrouk et al., 33 2012 Yes –– Yes Complications: 0.8% – vascular injury; 1.6% –transfusion; 4% – transitory urinary retention; 1.6% – retovaginal fistula; 0.8% – ureterovaginal fistula 55% – 72% – 25% Sigmoid resection: 17%; shaving: 30% Setälä et al., 16 2012 No rAFS – No Appendicectomy: 14%; urinary bladder resection: 14%; salpingectomy: 14%; adhesiolysis: 100%; complications: 14% – transitory urinary retention; 4.5% – anemia; 4% – vaginal deiscense Pouch of Douglas obstruction 7%; peritoneal lesions: 68% 95% 14% 86% 100% 50% (Continued ) Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al. 739 Chart 4 (Continued ) Author, year Histological analysis Endometriosis classification Intraoperative classification Nerve-sparing technique Procedures Other endometriosis location (%) Retro cervical (%) USL (%) Rectovaginal septum (%) Vagina (%) Bowel (%) Kossi et al., 21 2013 Yes –– No Resection of urinary bladder: 7%; appendectomymy: 11%; salpingectomy: 26%; ureterolysis 80%; adhesiolysis: 100%; complications:11.5% – transitory urinary retention; 3.8% – bowel bleeding Peritoneal lesions: 53% – No speci fic side: 88% – 61% 100% Van den Broeck et al., 14 2013 Yes rAFS III: 33%; IV: 66% Yes ––– – – – 100% Di Donato et al., 31 2015 Yes –– No ––– – – – – Fritzer et al., 17 2016 Yes rAFS I: 28%; II: 21%; III: 26%; IV: 25% No – Peritoneal lesions: 41%; DIE: 59% –– – 37% – Pontis et al., 18 2016 Yes –– No – Bladder: 100% –– – – – Riiskjaer et al., 20 2016 No –– No ––– – – – 100% Uccella et al., 29 2018 No Enzian A1 B2 C3 (20.6%); A2 B2 C3 (26.5%); A3 B1 C1 (2.9%); A3 B2 C1 (5.9%); A3 B3 C1 (2.9%); A3 B3 C2 (5.9%); A3 B1 C0 FB (5.9%); A0 B3 C2 FA (5.9%); A3 B1 C1 FA (17.6%); A3 B1 C2 FA (2.9%); A3 B1 C1 FO (2.9%) Yes Bilateral adnexectomy/castration: 8.8%; ureterolysis: 100%; complications: 17.6% – transitory urinary retention –– – – 50% 47.1% Lermann et al., 19 2019 No Enzian – No – WOB: 75.3%; WB: 72.4% – Unilateral – WOB: 48.3%; WB:8%; bilateral – WOB: 27%; WB: 24.1% WOB: 89.9%; WB:87.4% WOB: 41.6%; WB: 75.9% WB: 74.33% Ianieri et al., 28 2022 Yes rAFS II: 2.9%; III: 43.5%; IV: 53.6% Yes Complications: 1% – hemoperitoneum; 2% – iatrogenic bowel injury – 48% –– 15% 64% Martínez-Zamora et al., 34 2021 Yes –– No – Endometriomas – bilateral: 11.62%; left: 24.8%; right: 13.95%; ureter (no speci fic side): 24%; bladder: 28.68%; peritoneal lesions: 76% 47.28% No speci fic side: 68.99% 11.62% 8.52% 39.53% Zhang et al., 30 2022 Yes rAFS I þ II: 20%; III þ IV: 35% No ––– No speci fic side: 25.45% 43.63% – 18% Abbreviations: DIE, deep in filtrating endometriosis; rAFS, revised American Fertility Society classi fication; USL, uterosacral ligament; WO, with bowel resection; WOB, without bowel resection. Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Brasileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al.740 The nerve-sparing surgical technique for DIE excision was described as necessary in six articles, 13–15,28,29,33 in which different results were found: two studies 15,29 showed a significant improvement on the SAQ and the FSFI ’s global sexual function score; two other studies13,33 reported partial improvement in some domains on the FSFI and on the Sexual Health Outcomes in Women Questionnaire (SHOW-Q); and the two remaining studies 14,28 reported no difference in sexual response after the nerve-sparing surgery. Only one article28 aimed to evaluate the functional results after nerve- sparing posterolateral parametrial surgery, and the authors observed an increased risk of postoperative dyspareunia and sexual dysfunction. The FSFI sexual function score improved in the group without parametrial surgery, but not significantly. 28 The diagnosis of endometriosis was confirmed by histolog- ical examination of specimens removed during surgery in 15 studies. 13–15,17,18,20,21,24–26,28,30,31,33,34 Complementary sur- gical procedures for the treatment of endometriosis, including ureterolysis, adhesiolysis, salpingectomy and appendicecto- my, were performed in ten articles. 13–16,21,24,27–29,33 Intra- operative or postoperative complications were reported in nine studies,13,15,16,21,24,27–29,33 and the most common find- ings were transfusions caused by bleeding, transitory urinary retention, and bowel iatrogenic injury. Despite the complica- tion rates reported, only one study28 did not show a significant increase in sexual function after surgery. The clinical treatment was an important point observed on this review. Some articles did not establish inclusion or exclusion criteria regarding the use of hormonal drug treat- ment associated with the procedure, but six stud- ies 13,17,25,26,32–34 defined these criteria as In five studies,17,25,26,32,34 hormonal treatment with gonadotro- pin-releasing hormone (GnRH) analogues and combined or isolated contraceptives were discontinued six months before the procedure, and two studies 25,32 did not reintroduce any type of hormonal treatment postoperatively. All studies presented an increase on sexual function, except, the one by Vercellini et al., 32 which did not show positive results on the SSRS after surgery. One study 13 included a GnRH analogue preoperatively, and other studies included combined contraceptives preop- eratively31,33 and postoperatively. 33 Despite the differences regarding the hormonal treatment, the sexual function score on the SAQ and SHOW-Q improved postoperatively in two of these studies. 31,33 Dyspareunia, also called by some authors deep dyspar- eunia (DD) or pain during sexual intercourse, was assessed in 12 articles, 13–17,20,24,26–28,32,33 mainly through the Visual Analogue Scale (VAS) and the Numeric Rating Scale (NRS). Only Riiskjaer et al. 20 observed dyspareunia as an isolated finding, and evaluated it with its speci fic scale. Three studies 17,27,34 identified a signi ficant decrease in dyspareunia according to the NRS scale in all groups in the pre and postoperative comparison. The VAS was applied by the other articles to evaluate dyspareunia after surgery, and all articles reported a significant improvement in pain during intercourse after surgery, including progressive improve- ment in dyspareunia over time. Only one study 14 did not report a decrease in dyspareunia after 18 months of follow- up.

Due to its diverse origin, endometriosis presents great het- erogeneity in terms of anatomical presentation and clinical manifestations, especially if associated with the complexity of multifactorial sexual aspects. Qualitative and quantitative studies have shown that symptomatic endometriosis negatively affects female sexual function, causing discomfort, and they have analyzed these

through global scores. The isolated analysis of the domains of sexual function is unclear, and it is often not the main objective of studies, which limits a comprehensive assessment of sexual functioning. Therefore, the evidence in the literature lacks quality in terms of research design, diagnostic instruments, power of the study, or adjustment for confounding factors. The present review helped expand the knowledge on the types of surgery performed to treat deep endometriosis, and we systematically analyzed the techniques used according to the location and staging of the disease, histopathological confirmation, nerve preservation, and the types of proce- dures performed for lesion resection. The improvement in sexual function and dyspareunia after the surgical treatment in DIE patients was duly expressed by the authors of the studies reviewed. The laparoscopic surgery technique showed precision to treat DIE, in addition to the surgeons’ experience. This statement is corroborated when there are positive results after surgeries, in addition to the correlation with other types of drug treatments. All groups of patients classi fied according to the rAFS showed improvement in the quality of sexual life, especially those in classes IV and III; however it was not possible to identify the statistical relevance of the improvement in sexual function correlated with each group separately. 35,36 Autonomic, sympathetic, and parasympathetic nerves control the vessels in the genital region, and they are responsible for sexual satisfaction and lubrication. The nerve-sparing surgery for DIE is recommended to reduce patient morbidity. 37 However, 73.68% of the studies in this review did not perform the nerve-sparing surgery, neither did they find a direct correlation with female sexual function, as the literature. 29,38 The presence of DIE in the vagina and uterosacral liga- ments is associated with impaired sexual function and dyspareunia. 39 The present review showed an improvement in female sexual function and postoperative dyspareunia despite the location of the endometriosis lesions, disease severity, and surgical treatment performed. We believe that the excision of in flammatory and angiogenic factors caused by DIE during surgery is the main factor for pain relief during sexual intercourse. Getting rid of feelings of fear and anguish caused by pain are also related to the improvement on other factors of sexual function. Rev Bras Ginecol Obstet Vol. 45 No. 11/2023 © 2023. Federação Bras ileira de Ginecologia e Obstetrícia. All rights reserved. Sexual Function after Surgery for Deep Endometriosis Cervantes et al. 741 In addition, the analysis related to deep dyspareunia still needs to be better developed, since the use of the NRS or probing alone is very simplistic compared with the psycho- logical tests to distinguish deep dyspareunia from vulvody- nia or vaginismus, which can also be triggered by chronic pelvic pain. The lack of standardization among the questionnaires used to assess sexual function was a limiting factor in the present review, and it is due to the absence of an instrument capable of encompassing the complexity of DIE and its association with female sexual function. However, we were able to oppose some limiting factors found in the literature, such as follow-up time and questionnaire results. 40 We evaluated some studies with a follow-up longer than one year and with sexual function results demonstrated through the analysis of the domains involved in sexual response, such as arousal, satisfaction, pleasure and others.

Highly-complex surgical approaches for the treatment of endometriosis have always been associated with the risk of complications arising from the excision of deep endometri- otic lesions located mainly in the posterior vaginal fornix, rectal muscular layer, and inferior hypogastric plexus, which could worsen the patient ’s sexual quality of life and pain symptoms. Despite this, the present review demonstrated that radical surgeries for the treatment of DIE improved dyspareunia and sexual function, and they should be provid- ed to women as a treatment alternative. Healthcare profes- sionals should address the topic of sexual health in consultations with women with endometriosis because improvements following surgery can be expected. The pres- ent study not only demonstrates a signi ficant reduction in dyspareunia symptoms, but it also shows that the resection of both minimal and extensive endometriotic disease causes major positive changes in sexual function. Conflict of Interests The authors have no con flict of interests to declare.

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