Adenomyosis: A potential cause of surgical failure in treating dyspareunia in rectovaginal septum endometriosis

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Abstract

OBJECTIVE: Dyspareunia can severely impact the quality of life of patients with endometriosis. This symptom is often linked to a specific form of deep infiltrating endometriosis, such as rectovaginal septum endometriosis. Despite the radicality of surgery, persistence and recurrence of symptoms post-surgery are not uncommon. The aim of the present study was to determine whether adenomyosis contributes to the failure of surgical interventions for dyspareunia in these patients. METHODS: A retrospective single-cohort study was conducted at the at tertiary care gynecologic center of the University Federico II of Naples, using medical records from January 2020 to July 2023. The study included patients who underwent surgery for dyspareunia associated with rectovaginal endometriosis and had a definitive histologic diagnosis. Pain and sexual quality of life were assessed using the visual analog scale (VAS) and the sexual quality of life-female (SQoL-F) questionnaire, both before and 6 months after surgery. Patients with isolated rectovaginal endometriosis were compared to those with concurrent adenomyosis. RESULTS: A total of 94 patients were included: thirty-five in group A (endometriosis with adenomyosis) and 59 in group B (isolated rectovaginal endometriosis). Histology confirmed deep infiltrating endometriosis (DIE) in all patients. Clinical characteristics such as age, BMI, abnormal uterine bleeding, and infertility, showed no significant differences between the groups. Multiparity was more common in group A (20%) compared to group B (5.1%) (P < 0.001). Pain VAS scores decreased significantly in both groups: from 7.11 to 5.40 in group A and from 7.34 to 3.31 in group B (both P < 0.001). Sexual quality of life (SQoL) scores improved significantly: from 42 to 57 in group A and from 41 to 66 in group B (both P < 0.001). Patients in group B showed a more significant improvement. Adjusted linear regression showed no significant association between parity and the severity of dyspareunia or sexual quality of life. CONCLUSION: Adenomyosis appears to reduce the effectiveness of surgical treatment for dyspareunia in patients with rectovaginal septum endometriosis. Comprehensive preoperative screening for adenomyosis is recommended to improve surgical outcomes and provide appropriate counseling. Future research should further explore the impact of adenomyosis on dyspareunia and the potential benefits of adjunctive medical therapies.
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Author

Antonio Mercorio : Conceptualization, methods, validation, investigation, data analysis, writing original draft preparation, writing—review and editing, visualization, and project administration. Luigi Della Corte : Methods, writing—review and editing, and supervision. Pierluigi Giampaolino : Investigation, writing—review and editing. Michela Dell'Aquila : Writing—review and editing. Daniela Pacella : Conceptualization, methods, data analysis. Giuseppe Bifulco : Writing—review and editing, and supervision.

Funding

This research has not received any funding from public, commercial, or non‐profit organizations, nor has it received any financial support from the institution.

Results

A total of 94 patients were included the analysis. Of these, 35 belonged to group A, characterized by endometriosis of the rectovaginal septum with concurrent adenomyosis, while 59 were in group B, which comprised patients with isolated endometriosis of the rectovaginal septum, as abovementioned (Figure  1 ). The histology confirmed in all patients the diagnosis of DIE. Flow chart of the retrospective study population. The clinical characteristics of all patients are shown in Table  1 . No statistically significant difference was found in terms of age, body mass index (BMI, calculated as weight in kilograms divided by the square of height in meters), abnormal uterine bleeding and infertility. Multiparity was significantly more common in patients with associated adenomyosis (7/35, 20%) compared to those with isolated endometriosis (3/59, 5.1%) ( P  < 0.001). No statistical difference in nodule dimension was found between the two groups. Study population characteristics. Abbreviations: AUB, abnormal uterine bleeding; BMI, body mass index; SD, standard deviation. Bowel perforation during surgery was encountered in 2% of patients (3/94). In all cases, the bowel was sutured during surgery and no intra‐ or postsurgical unfavorable outcomes occurred. No conversion to laparotomy as well as no delayed complication were registered. The mean baseline VAS score for pain decreased from 7.11 ± 0.72 to 5.40 ± 0.98 in group A ( P  < 0.001), and from 7.34 ± 0.94 to 3.31 ± 1.04 in group B ( P  < 0.001) (Figure  2 ). Similarly, there was a significant improvement in the SQoL score: the mean baseline score increased from 42 ± 4.6 to 57 ± 5 in group A ( P  < 0.001), and from 41 ± 5.8 to 66 ± 20 in group B ( P  < 0.001) (Figure  3 ). However, patients with isolated rectovaginal nodules showed a more significant improvement and pronounced benefit from surgery (Table  2 ). Evaluation of the visual analogue scale (VAS) score at baseline and at the 6‐month follow up in group A (rectovaginal endometriosis associated with adenomyosis) and group B (isolated rectovaginal endometriosis). Evaluation of the sexual quality of life‐female (SQoL‐F) score at baseline and at the 6‐month follow up in group A (rectovaginal endometriosis associated with adenomyosis) and group B (isolated rectovaginal endometriosis). Mean of the differences between post‐ and preoperative VAS and SQoL‐F values. Abbreviations: SQoL‐F, sexual quality of life‐female; VAS, visual analog scale. Adjusted linear regression models were used to assess the potential impact of parity on the VAS score and SQoL‐F. Regarding the VAS score, the adjusted linear regression analysis indicated an adjusted beta coefficient for parity of −0.06, with a 95% confidence interval ranging from −0.48 to 0.36, and a P value of 0.785, showing no statistically significant association between parity and the severity of dyspareunia. Similarly, the influence of parity on dyspareunia and sexual quality of life, as measured by the SQoL‐F, was examined, showing the same result (Tables  S1 and S2 ).

Discussion

In our study, we investigated whether the coexistence of adenomyosis with rectovaginal septum endometriosis impacts the surgical outcome in treating dyspareunia. Our findings, at the 6‐month post‐surgery follow‐up, suggest that the simultaneous presence of adenomyosis diminishes the efficacy of surgical interventions aimed at alleviating dyspareunia and enhancing sexual quality of life. The current literature presents substantial evidence highlighting the improvement in sexual function and dyspareunia following surgical intervention in patients with DIE. However, it is imperative to acknowledge that surgical intervention does not guarantee symptomatic relief 26 and some evidence has documented instances where patients persistently experience symptoms postoperatively. 27 , 28 Radical surgery is essential to achieve successful outcomes, yet it requires a careful balance with the risks of potential iatrogenic comorbidities in these otherwise healthy and young women. The established correlation between adenomyosis and endometriosis has been extensively documented in scientific literature. Recent studies have indicated a notably high prevalence of adenomyosis, diagnosed via ultrasound, in women with endometriosis, with reported rates reaching up to 89.4%. 29 , 30 , 31 While it is well known that deep endometriosis can impair sexual function, on the other hand, adenomyosis has been typically associated with abnormal uterine bleeding, subfertility, dysmenorrhea, and chronic pelvic pain. 15 To date, there is a noticeable lack of evidence concerning the evaluation of the quality of sexual life and dyspareunia in patients with adenomyosis. 32 A recent study suggests that adenomyosis, even when isolated, negatively impacts sexual quality of life and contributes to dyspareunia. 33 Alcalde et al. found that women with isolated adenomyosis had similar sexual quality of life to those with DIE, and lower compared to controls, highlighting its effect on dyspareunia. 34 Adenomyosis has been recognized also a significant factor in symptom persistence after surgery. A retrospective study that evaluated symptoms and transvaginal ultrasound (TVUS) features in patients who underwent laparoscopic segmental rectosigmoid resection for DIE found that persistent symptoms, including dyspareunia in 88% of cases, were often associated with adenomyosis. 35 Although the pathogenesis of endometriosis and adenomyosis remains debatable, shared molecular deregulations observed in these pathologies could explain their strong clinical connection. 36 , 37 Particular interest has focused on the association between focal adenomyosis of the outer myometrium (FAOM) and DIE. In a cross‐sectional study of 292 patients with preoperative MRIs, researchers investigated the presence of diffuse adenomyosis or FAOM in relation to different endometriosis phenotypes, including superficial endometriosis, ovarian endometrioma, and DIE. FAOM showed a strong correlation with the DIE phenotype, observed in 66.3% of cases ( P  < 0.001), whereas diffuse adenomyosis did not show significant correlation ( P  = 0.068). 38 FAOM is associated not only with the disease phenotype but also with its severity. In a cross‐sectional study, patients with symptomatic DIE and FAOM had a higher mean number of DIE lesions compared to those without FAOM. 13 There is a hypothesis that ectopic endometriotic cells could infiltrate the posterior uterine wall, forming a posterior focal adenomyotic nodule, which may explain both prevalence and symptom similarities like dyspareunia. 39 However, due to the retrospective nature of this study and the lack of information on the specific type of adenomyosis in this cohort, we were unable to investigate the association between FAOM and DIE. Parity has been identified as a significant risk factor for adenomyosis, with epidemiologic data showing a strong correlation between adenomyosis and multiparity. In our cohort, we observed a higher percentage of multiparous women with coexistent adenomyosis compared to those with isolated endometriosis. However, after adjusting for other variables using linear regression models, parity showed no statistically significant impact on dyspareunia severity in patients with rectovaginal endometriosis associated with adenomyosis or isolated rectovaginal endometriosis. Our study has many strengths. Patient selection was meticulously conducted using the Enzian scoring system, a tool specifically devised for classifying DIE with a focus on retroperitoneal structures. In our study, we focused our analysis on a specific subgroup of patients with isolated rectovaginal septum nodules. This type of DIE localization has been particularly associated with deep dyspareunia. 40 Therefore, we specifically focused our attention on these lesions and the shaving surgical procedure. Indeed, other procedures, such as colorectal resection, might lead to a more complex postoperative recovery and some postoperative dysfunction, which could potentially bias the results, particularly in terms of their impact on sexual activity. Another important aspect of our study was the evaluation of sexual dysfunction. To gain comprehensive clinical insights into the efficacy of the surgical intervention, we extended our analysis beyond the VAS score for dyspareunia. We utilized a specific questionnaire, developed to assess the impact of female sexual dysfunction (FSD) on women's sexual quality of life. 24 This tool has proven to be useful in various clinical populations, including patients with adenomyosis and endometriosis. 34 Our study has certain limitations. First, the use of questionnaires to determine sexual function presents shortcomings, particularly due to the lack of standardized instruments that can fully capture the complexity of DIE and its association with female sexual function. Another aspect concerns its retrospective design, which might have influenced the sensitivity of our findings. Moreover, the small study population size, although necessary to exclude patients on hormonal therapy, with multiple or varied endometriosis lesions, or who had undergone other eradication interventions, might limit the generalization of our results. Finally, our study design did not entirely eliminate the possibility of misdiagnosing rectovaginal endometriosis or overlooking milder, unrecognized deep lesions in some women.

Conclusions

Our study highlights the potential impact of adenomyosis in reducing the effectiveness of surgical interventions for dyspareunia in patients with endometriosis. Based on our findings, we recommend thorough screening for adenomyosis in patients with deep infiltrating endometriosis (DIE), given its high prevalence in such cases. This screening could significantly influence both clinical and surgical management, making it essential for proper preoperative counseling in DIE patients with adenomyosis who are seeking relief from dyspareunia. Future research should focus on determining whether specific adenomyosis localizations are more strongly associated with persistent dyspareunia, as well as exploring the potential role of adjuvant medical therapies. Conducting future studies to delve deeper into this issue is crucial in order to enhance our clinical strategies and improve outcomes for patients affected by endometriosis.

Introduction

Endometriosis is a benign yet progressive and chronic condition, affecting 50%–70% of women experiencing pelvic pain symptoms during their reproductive years. 1 A prevalent symptom associated with endometriosis is deep dyspareunia, which is pain experienced during deep penetration. Compared to the general female population, women with endometriosis face a nine‐fold increased risk of experiencing dyspareunia. 2 This condition significantly impacts the quality of a woman's life, not only causing severe pain but also adversely affecting intimate relationships and self‐esteem. Deep dyspareunia has been frequently associated with rectovaginal septum endometriosis, a subtype of deep infiltrating endometriosis (DIE), characterized by the subperitoneal invasion of endometriotic lesions that extend more than 5 mm in depth. In this particular condition, pain during intercourse in endometriosis can be triggered by the traction of scarred and non‐elastic endometriotic tissue or by mechanical pressure on the lesion during coitus. 3 The efficacy of medical treatment is often limited in cases of DIE associated with dyspareunia. 4 Surgery has shown globally better outcomes compared to medical therapy. However, some studies indicate that persistence and recurrence of symptoms are common post‐surgery. 5 , 6 For these reasons, dyspareunia and sexual dysfunctions associated with endometriosis represent major clinical challenges. Adenomyosis is a chronic, benign gynecologic condition affecting 20%–35% of women during their reproductive years. 7 It is characterized by the infiltration of endometrial tissue, including glands and stroma, into the myometrium. Commonly associated symptoms include pain, abnormal uterine bleeding, and infertility. 8 , 9 A significant correlation between endometriosis and adenomyosis, has been reported in several studies. 9 , 10 In particular, adenomyosis has been notably associated with DIE. 11 , 12 Recent research found adenomyosis in 56.7% of patients with DIE. 13 The mechanisms underlying the pain caused by deep endometriosis nodules remain poorly understood. While female dyspareunia and sexual dysfunction are significant societal concerns, these issues have not been extensively investigated. Although some studies have identified impairments in sexual function among endometriosis patients, 14 , 15 particularly in those with DIE, 16 , 17 research specifically addressing sexual dysfunction in patients with adenomyosis, either as an isolated condition or in combination with rectovaginal septum endometriosis, remains scarce. 18 In light of the above, in the present study we investigated the possible role of adenomyosis in diminishing the success of surgical interventions for dyspareunia in patients with rectovaginal septum endometriosis, a specific subtype of DIE.

Coi Statement

No conflict of interest has been declared by the authors.

Materials And Methods

This retrospective cohort study was conducted at the DAI Materno Infantile of Azienda Ospedaliera Universitaria Federico II in Naples. It involved reviewing the medical records of patients from our endometriosis clinic. The study is reported following the STROBE guidelines. 19 Written informed consent was obtained for all data used in this study, as for all patients who access our Institution. The study was approved by the local ethical committee of the University of Naples Federico II—AORN A. Cardarelli (no. 09/23 of 12/10/2023). All sexually active women, who underwent therapeutic surgery for dyspareunia associated with rectovaginal endometriosis unresponsive to medical therapy, and with a definitive histologic diagnosis of endometriosis, from January 2020 to July 2023, were considered for inclusion in the analysis. The study specifically targeted patients with isolated rectovaginal endometriosis with a nodule no larger than 3 cm in diameter (A1–A2 Enzian score) or coexistent with adenomyosis. 20 We excluded patients with potential confounding factors such as psychiatric disorders, rheumatologic or autoimmune diseases, myofascial syndrome, fibromyalgia, interstitial cystitis, previous surgery for endometriosis and diagnosis of cancer. Only patients who had not undergo hormonal therapy in the 3 months before and 6 months after the surgery were included. According to our protocol, the patients underwent rectovaginal shaving surgery, all performed by the same surgeon who was experienced in this procedure (PG). According to our internal protocol, vaginal and rectal examination together with transvaginal ultrasound and magnetic resonance imaging (MRI) were performed in all patients to identify features of pelvic endometriosis 21 and to detect any signs of associated adenomyosis according to the recent morphologic uterus sonographic assessment (MUSA) features of adenomyosis. 21 In order to evaluate the characteristics of dyspareunia both preoperatively and at the 6‐month post‐surgical follow‐up, patients rated their pain using a 10‐cm VAS 23 ranging from no pain (right extreme) to the worst pain imaginable (left extreme). Additionally, the sexual quality of life‐female (SQoL‐F) questionnaire, an 18‐item survey scored on a Likert scale, was administered: this scale spans from “completely agree” to “completely disagree,” yielding a total score ranging from 18 to 108, where higher scores denote a better quality of sexual life. 24 Shaving procedure was performed using the “reverse technique”: the resection starts from the posterior vaginal fornix; the lesion is separated from the retrocervical area, leaving the disease attached to the anterior surface of the rectum; the lesion is then shaved off the anterior rectal wall through the use of bipolar energy. In this technique, the separation of the nodule from the rectal wall is performed at the end of the surgery, unlike the traditional method where it is done at the beginning. This approach allows the surgeon to perform a more precise dissection of the endometriotic nodule due to the increased mobility of the bowel. 25 A comparative analysis on dyspareunia was conducted between patients with isolated rectovaginal endometriosis (group A) and patients with rectovaginal endometriosis associated with adenomyosis (group B). As the primary outcome, we considered the comparison of the two groups in the mean VAS differences before and after surgery. A total sample size of 94, with 35 in group A and 49 in group B achieved >99% power, which corresponds to a Cohen's D of 1.74. A student's t‐ test for independent populations was considered with a significance level of α  = 0.05. Data are summarized as mean and standard deviation for continuous variables and as absolute frequency and percentage for categorical variables. A student's t ‐test or Mann–Whitney U test, as appropriate, was used to investigate the difference between means for continuous variables. Chi‐squared or Fisher exact test, as appropriate, was used to investigate the difference between groups for categorical variables. Adjusted linear regression model was used to investigate the association between group and individual VAS or SQoL‐F variations. For all analyses, a P value less than 0.05 was considered as the threshold for statistical significance. R software version 4.3.0 was used for the analyses.

Supplementary Material

Data S1.

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Outcome instruments

VAS-pain MUSA Enzian

Condition tags

mesh:D004414mesh:D004715endometriosisadenomyosisdie_deep_infiltratingbowel_endometriosisdyspareuniainfertility

MeSH descriptors

Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis Adenomyosis

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