Dr Margaux Stoppa

Aubert Agostini

Audrey Pivano

Pascale Siles

Lisa Calderon

Antoine Netter
email: antoine.netter@gmail.com

Mild endometriosis of the uterosacral ligaments: a retrospective study of magnetic resonance imaging performance for diagnosis BIOGRAPHY

Keywords:

The identification of minimal changes in the normal appearance of USL should not automatically lead to the conclusion of mild endometriosis at this location. This should not be the sole argument for performing surgery, and the history, intensity of painful symptoms and clinical examination remain paramount in this context.

INTRODUCTION

A lthough it affects approximately 10% of women of reproductive age, the diagnosis of endometriosis is still problematic, often with a long delay that postpones adequate management [START_REF] Ballard | What's the delay? A qualitative study of women's experiences of reaching a diagnosis of endometriosis[END_REF][START_REF] Zondervan | Endometriosis[END_REF]. Magnetic resonance imaging (MRI) is recognized as one of the preferred methods of diagnosis because it allows complete mapping of deep endometriosis lesions to monitor their evolution or to plan excision surgery [START_REF] Gerges | Meta-analysis and systematic review to determine the optimal imaging modality for the detection of uterosacral ligaments/torus uterinus, rectovaginal septum and vaginal deep endometriosis[END_REF][START_REF] Netter | Progression of deep infiltrating rectosigmoid endometriotic nodules[END_REF]. Among the structures that are routinely observed by radiologists, the uterosacral ligaments (USL) are the most frequent location of deep endometriosis [START_REF] Hajati | A review of more than 2000 cases of site-specific pelvic endometriosis rates by MRI: a guide to minimizing under/ overdiagnosis non-invasively[END_REF]. USL connect the posterior surface of the uterine cervix to the anterior surface of the first sacral pieces. Their common origin is behind the uterus, near the isthmus on the midline, where their union forms the torus uterinum [START_REF] Gray | Anatomy of the Human Body[END_REF].

According to the literature, MRI scans have very good diagnostic performance in detecting the presence of deep endometriosis on USL, with high specificity and sensitivity (superior to 0.80 for both) [START_REF] Gerges | Meta-analysis and systematic review to determine the optimal imaging modality for the detection of uterosacral ligaments/torus uterinus, rectovaginal septum and vaginal deep endometriosis[END_REF]. However, this structure, which measures approximately 1 mm in diameter, has not traditionally been observed on MRI in the absence of any lesion. With the advent of more efficient MRI and the generalization of thin sections (2À3 mm) passing specifically in the plane of USL, radiologists can now perceive all subtleties in the shape and size of these organs [START_REF] Bazot | Value of thin-section oblique axial T2-weighted magnetic resonance images to assess uterosacral ligament endometriosis[END_REF]. There are no precise semiological criteria for the description of USL, and it has become difficult to differentiate between variants of normal and mild endometriotic involvement. Confirming the absence of endometriosis is thus particularly problematic, especially when no other lesion is found in the pelvis and the deformities observed on the USL are minimal.

With the high profile of endometriosis in the media over the last decade, the number of pelvic MRI scans requested for suspected endometriosis has dramatically increased [START_REF] Holowka | Mediating pain: navigating endometriosis on social media[END_REF][START_REF] Towne | Health information in the era of social media: an analysis of the nature and accuracy of posts made by public Facebook pages for patients with endometriosis[END_REF]. As a result, cases of women with suggestive symptoms whose MRI reveals only very slight abnormalities have become common [START_REF] Le Moal | Increasing incidence and spatial hotspots of hospitalized endometriosis in France from 2011 to 2017[END_REF]. Radiologists are often forced to describe these abnormalities, which often concern USL, without being able to confirm their pathological nature or the presence of endometriosis. This uncertainty on the part of medical staff often causes additional stress for patients and complicates management decisions, especially regarding surgery.

This study sought to determine the diagnostic value of MRI semiology in identifying mild endometriosis of the USL.

MATERIALS AND METHODS

Study design

This retrospective study was conducted between January 2016 and December 2020 in the Department of Medical Imaging at La Timone Hospital and the Department of Obstetrics and Gynecology at La Conception Hospital, Marseille, France. The study was approved by an independent ethics committee (RGPD/Ap-Hm 2022-63, 22 August 2022).

Study population

Women whose medical cases were discussed during monthly pluridisciplinary endometriosis meetings during the study period were screened for eligibility. To be included in the study, women needed to have undergone laparoscopy for endometriosis when between 18 and 45 years old and also to have undergone an MRI of sufficient quality during the year before surgery. Patients could be included whether endometriosis of the USL was suspected or not (FIGURE 1A and1B). Exclusion criteria were large lesions leaving no doubt as to their endometriotic nature on an MRI (according to two radiologists), an absence of description of the USL on the surgical report, and insufficient quality of the MRI that prohibited the proper assessment of USL implication (FIGURE 1C and1D).

MRI technique and analysis

All MRI were performed at the Women's Health Imaging Department at La Timone Hospital (Marseille, France) no more than a year before surgery. MRI were performed with a Siemens Spectra 3.0T MRI device (Siemens AG, Munich, Germany) according to the guidelines for endometriosis of the European Society of Urogenital Radiology (Bazot et al., 2017). This protocol includes T1-weighted sequences with and without fat saturation, and T2-weighted sequences in the sagittal, axial § coronal planes and a thin section sequence (2 mm) in an axial oblique plane perpendicular to the long axis of the cervix, i.e. the plane of the USL. The protocol also requires digestive preparation and use of an antispasmodic to reduce intestinal peristalsis. The sequences are acquired with anterior and posterior abdominal saturation bands to avoid the signal from s. c. fat.

Every MRI was independently interpreted by two experienced radiologists (LC and MS) who did not have access to any medical files or any information regarding the surgery. In cases of disagreement over the presence of endometriosis of the USL, the MRI in question could be secondarily and jointly read again by two radiologists to reach consensus.

After an exploration of the literature and a discussion with different radiologists at the study unit, six criteria for describing USL were chosen: (i) asymmetry between the two USL (FIGURE 2A), (ii) thickening (FIGURE 2B), (iii) irregularity (FIGURE 2C) and (iv) straightness (FIGURE 2D) on T2-weighted sequences, (v) the presence of a nodule on any sequence (FIGURE 2E) and (vi) the presence of a focal T1 hypersignal (FIGURE 2F). The radiologists were asked to fill a grid with the characteristics of the USL for each side. They also measured the proximal diameter of each ligament on the T2 sequence in the sagittal or axial plane and reported the presence of ovarian endometriomas and superficial or deep lesions of endometriosis, according to previously published criteria [START_REF] Netter | Surgical management of endometriotic women with pregnancy intention in France: a national snapshot of centers performing a high volume of endometriosis procedures[END_REF].

Surgery and histopathology

Surgical and histopathology reports were retrospectively analysed to ascertain the visual presence of endometriosis during surgery and its histological confirmation. All patients underwent laparoscopy in the study unit. Since 2016, standardized surgical reports have been used, including a description of the right and left USL to assess the presence or absence of endometriosis according to the surgeon. Visible lesions are generally resected in their entirety and sent for histopathology to confirm the presence or absence of endometriosis. Occasionally, USL apparently free of endometriosis may also be biopsied, particularly when no other endometriosis lesions are found during exploration of the peritoneal cavity.

Statistical analysis

The number of subjects included was constrained by the duration of the study, dating back to the date of implementation of standardization of the surgical reports for endometriosis (January 2016).

Descriptive data are reported using means § SD or medians (minimumÀmaximum) for quantitative variables and by counts (percentages) for categorical variables. Therefore, the demographic characteristics, symptomatology and clinical examination of the women were described as well as surgical and imaging data.

For each previously defined MRI sign, the agreement between the two radiologists responsible for the review was calculated using Cohen's kappa (k) method and is expressed as k (95% confidence interval [95% CI]). Additionally, the right and left USL were individually considered in this analysis.

The diagnostic performance (primary end-point) of each MRI sign was estimated using the presence or absence of endometriosis from the laparoscopy as the reference. The right and left USL were individually considered for all criteria, except for the asymmetry criterion, which required consideration of both USL. For each sign, the sensitivity, specificity, positive likelihood ratio, negative likelihood ratio, positive predictive value, negative predictive value and accuracy are reported with the 95% CI.

A receiver operating characteristic (ROC) curve was used to evaluate the ability of the measurement of USL thickness from the MRI to predict the presence or absence of endometriosis based on laparoscopy. A cut-off value for USL thickness measurement was examined using the Youden index (sensitivity + specificity À 1) to find the best compromise between specificity and sensitivity.

All statistical analyses were two-sided, and the results were considered statistically significant when the P-value was <0.05. These analyses were performed using SPSS Statistics for Windows, Version 20.0 (IBM Corp., Armonk, NY, USA).

RESULTS

Population and surgery

Between January 2016 and December 2020, 539 medical files were presented during the monthly endometriosis multidisciplinary team meetings. After applying exclusion criteria, 77 patients were included in the retrospective analysis (FIGURE 3). The women's characteristics are summarized in

MRI analysis

The MRI characteristics of the women are reported in A ROC curve (FIGURE 4) was used to determine the predictive value of the USL diameter, and the area under the curve was 0.588 (95% CI 0.464À0.703). The best cut-off value for the prediction of endometriosis was found at a diameter of 3.85 mm, which was associated with a sensitivity of 0.46 and a specificity of 0.83 (Youden index 0.293).

The inter-observer agreement was assessed for each criterion and the diameter of the USL (TABLE 5). Agreement between the radiologists were excellent for 'straightness' (Cohen's k = 0.827 [95% CI

DISCUSSION

This is the first study to specifically address the MRI description of mild USL endometriosis. The study population was largely selected to keep only the most subtle and doubtful cases, which are challenging for radiologists. The study suggests that MRI is an imperfect examination in cases of mild USL endometriosis and that even experienced radiologists will have difficulty stating with certainty the presence or absence of endometriosis in these specific cases. Six criteria were listed, and one MRI measurement; their values for detecting the presence of endometriosis were precisely reported. None of the reported criteria has sufficient diagnostic performance to be used alone, and when considered together, they lose all specificity. Asymmetry and thickening were the most sensitive morphological criteria but were associated with moderate specificities, while the presence of a nodule, a hypersignal T1 spot or the The diagnostic performance of each MRI sign was estimated by using the presence or absence of endometriosis from the laparoscopy as the reference.

The right and left USL were individually considered for all criteria, except for the asymmetry criterion, which required consideration of both USL. CI were calculated using the ClopperÀPearson exact method. a For statistical reasons an involvement of both USL (bilateral) is also counted in right and left. CI = confidence interval; MRI = magnetic resonance imaging; USL = uterosacral ligament.

irregular appearance of USL appeared to have good specificities but low sensitivities in this population. Concerning the diameter measurement, the threshold value reported has good specificity but low sensitivity and is therefore of little use in most cases (when the diameter is below the threshold). Furthermore, apart from the criteria 'thickening' and 'straightness' and the diameter measurement, the other criteria remain subject to moderate to low agreement between observers.

Bazot and Daraï (2017) describe USL involvement as basically a spiculated nodule or irregular thickening with hyposignal on T2-weighted sequences and where asymmetry would be strongly suggestive of the diagnosis; this highlights the importance of comparing the two ligaments. Histologically, hypointense lesions on T2-weighted sequences reflect fibromuscular hyperplasia lesions, and focal T1-weighted hypersignals correspond to haemorrhagic implants as observed in other endometriosis locations [START_REF] Anaf | Smooth muscles are frequent components of endometriotic lesions[END_REF]. The straightness aspect of USL is not described in the literature, but this criterion showed very good specificity and good inter-observer correlation in the current study. It is possible that this aspect reflects an incipient rigid fibrous infiltration in endometriosis of the ligaments at a lesser stage than for the 'arciform' aspect classically described by authors in the case of severe bilateral involvement [START_REF] Bazot | Diagnosis of deep endometriosis: clinical examination, ultrasonography, magnetic resonance imaging, and other techniques[END_REF]. However, the criterion of 'thickening' of the USL, which is cited in several reference publications as a sign of endometriosis, appears to be of little relevance in this study population, with insufficient sensitivity and specificity [START_REF] Bazot | Diagnosis of deep endometriosis: clinical examination, ultrasonography, magnetic resonance imaging, and other techniques[END_REF][START_REF] Coutinho | MR imaging in deep pelvic endometriosis: a pictorial essay[END_REF]. To refine this notion of thickening, several authors have already attempted to determine a threshold for measuring the diameter of the USL to evoke the diagnosis of endometriosis, i.e. >9 mm for [START_REF] Kinkel | Magnetic resonance imaging characteristics of deep endometriosis[END_REF] or >3 mm for [START_REF] Bazot | Diagnosis of deep endometriosis: clinical examination, ultrasonography, magnetic resonance imaging, and other techniques[END_REF]. In the current study population, the diameter measurement was moderately correlated with the presence of an endometriotic lesion (area under the curve 0.59) with cases of ligaments measured at less than 3 mm even though they were pathological at laparoscopy. Some studies also suggest that healthy USL may have a thickened appearance and postulated that pathological ligaments may be thin in the 'fibrous' phase of the disease and that the ligaments may be more voluminous in the active inflammatory phase of endometriosis [START_REF] Ohba | Evaluation of endometriosis in uterosacral ligaments by transrectal ultrasonography[END_REF]. Furthermore, measurement of the diameter of the USL is not always feasible as analysis of this area may be limited by uterine retroflexion and the presence of myoma or endometrioma within the pouch of Douglas [START_REF] Bazot | Value of thin-section oblique axial T2-weighted magnetic resonance images to assess uterosacral ligament endometriosis[END_REF].

Gerges et al. (2021) conducted a systematic review and meta-analysis to determine the optimal modality for the detection of USL. They included four MRI studies with a total of 440 women and found high sensitivity (81% [66À90%]) and specificity (83 [62À94%]) [START_REF] Alborzi | Diagnostic accuracy of magnetic resonance imaging, transvaginal, and transrectal ultrasonography in deep infiltrating endometriosis[END_REF][START_REF] Bazot | Comparison of 3D and 2D FSE T2-weighted MRI in the diagnosis of deep pelvic endometriosis: preliminary results[END_REF][START_REF] Fiaschetti | Deeply infiltrating endometriosis: evaluation of retro-cervical space on MRI after vaginal opacification[END_REF][START_REF] Manganaro | The role of 3.0T MRI in the assessment of deep endometriosis located on the uterosacral ligaments[END_REF]. Other previous meta-analyses reported similar results [START_REF] Guerriero | Transvaginal ultrasound vs magnetic resonance imaging for diagnosing deep infiltrating endometriosis: systematic review and metaanalysis[END_REF][START_REF] Nisenblat | Imagingmodalities for thenon-invasivediagnosisofendometriosis[END_REF][START_REF] Noventa | Imaging modalities for diagnosis of deep pelvic endometriosis: comparison between transvaginal sonography, rectal endoscopy sonography and magnetic resonance imaging. A head-to-head meta-analysis[END_REF]). These differences are not surprising, as the populations included in these studies used broader selection than in the current study and included women for whom the presence of USL endometriosis was obvious on MRI. Indeed, almost half of the current study population had minimal to moderate endometriosis with a median rASRM score of 12, and for 9.1% of patients, no endometriosis lesions were ultimately found during laparoscopy. In this sense, this study specifically addresses the issue of cases that radiologists are likely to misidentify as endometriosis.

The main weakness of the present study is its retrospective nature, which systematically raises the question of data quality. There are no such concerns regarding the data in this study because the consultations and operative reports were standardized for endometriosis patients throughout the study period. Thus, the description of USL was systematically reported and often associated with laparoscopic images for all procedures. Additionally, the retrospective nature of the study has no impact on the interpretation of the MRI scans as they were reviewed as part of the study. Some might argue that the sample is too small to draw conclusions. This is due to the very restrictive exclusion criteria that were used to retain only the most dubious cases, which were truly challenging for radiologists. Moreover, the sample size is comparable to that of other studies dealing with the recognition of USL in MRI.

Another criticism is the creation of criteria that are not justified by a sound literary basis. To our knowledge, there are no other studies or data in the literature concerning the MRI description of anatomical variations of USL or mild endometriosis at this location. Six distinct criteria were provided, which are used in current practice and whose iconographies will inevitably evoke subtle deformities that radiologists have already encountered. Although these criteria can also be reused for scientific or practical purposes, they are primarily useful in this study as they demonstrate that mild USL deformities are not necessarily indicative of endometriosis.

Thus, the current results suggest that the identification of minimal changes in the normal appearance of USL should not automatically lead to the conclusion of mild endometriosis at this location. More importantly, this should not be the sole argument for performing surgery, and the history, intensity of painful symptoms and clinical examination remain paramount in this context.

FIGURE 1

 1 FIGURE 1 Normal uterosacral ligaments (USL) and examples of situations that do not allow proper visualization of USL from the MRI. 1A and 1B: Axial and sagittal T2-weighted sections showing normal USL (arrows) with no lesions found during laparoscopy. 1C: The T2-weighted axial section; endometrioma of the right ovary (star) interfering with visualization of the right USL. 1D: The T2-weighted sagittal section; retroverted retroflexed uterus hindering the visualization of the USL. MRI = magnetic resonance imaging; USL = uterosacral ligament.

FIGURE 2

 2 FIGURE 2 Morphological criteria for the description of uterosacral ligaments (USL) on the MRI. 2A: The axial T2-weighted section showing asymmetry of the USL with a 2 mm nodular thickening of the right USL (arrows). 2B: The axial T2-weighted section with vaginal tagging showing thickening of the left USL (arrows). 2C: The axial T2-weighted section showing an irregular aspect of the right USL (arrows). 2D: The axial section in T2 weighting; the straightness of the right and left USL (arrows). 2E: The T2-weighted axial section; the right USL nodule measured at 6 mm (arrows). 2F: T1-weighted axial section; the haemorrhagic spot (arrows) at the origin of the right USL. Endometrioma of the left ovary. MRI = magnetic resonance imaging; USL = uterosacral ligament.

FIGURE 3 A

 3 FIGURE3A flow chart summarizing the population included in this study.

FIGURE 4

 4 FIGURE 4The receiving operative characteristic curve for the prediction of endometriosis assessment during laparoscopy according to the uterosacral ligament diameter in the magnetic resonance imaging scan. Area under the curve 0.588 (95% confidence interval 0.464À0.703); P = 0.132. The maximum Youden index was calculated at 0.293 for a 3.85 mm measurement with a sensitivity of 0.46 and a specificity of 0.83.

TABLE 1 .

 1 The mean age was 30.5 § 7.0 years, and the vast majority of patients underwent surgery for pain symptoms (73/77, 94.8%).

	The surgical characteristics are reported in
	TABLE 2. Almost half of the included women
	had minimal or moderate endometriosis
	according to the American Society for
	Reproductive Medicine's revised

TABLE 3

 3

		0.62 [95% CI 0.50À0.72], respectively).
		Conversely, 'irregularity', 'nodule',
		'straightness' and 'hypersignal T1 spot'
		were associated with high specificities (0.81
		[95% CI 0.70À0.89], 0.96 [95% CI
		0.89À0.99], 0.95 [95% CI 0.87À0.99] and
		0.99 [95% CI 0.93À1.00], respectively) but
		poor sensitivities (0.22 [95% CI
		0.14À0.33], 0.12 [95% CI 0.06À0.21], 0.08
		[95% CI 0.03À0.16] and 0.08 [95% CI
		0.03À0.16], respectively). The presence of
		at least one criterion for the description of
		the USL was associated with good
		sensitivity (0.80 [95% CI 0.66À0.89]) but
	. The most frequently	poor specificity (0.35 [95% CI 0.16À0.57]).
	reported criteria for the description of USL
	by the radiologists were 'thickening' (54/77
	women [70.1%]), followed by 'asymmetry'
	(48/77 [62.3%]), 'irregularity' (28/77
	[36.4%]), 'nodule' (10/77 [13.0%]),
	'hypersignal T1 spot' (7/77 [9.1%]) and
	'straightness' (5/77 [6.5%]).
	The diagnostic performance of each MRI
	criterion for the surgical confirmation of
	USL endometriosis is presented in TABLE 4.
	Among these criteria, 'asymmetry' and
	'thickening' had the highest sensitivities
	(0.69 [95% CI 0.54À0.80] and 0.51 [95%
	CI 0.40À0.63], respectively) but moderate
	specificities (0.52 [95% CI 0.31À0.73] and

TABLE 2

 2

	SURGICAL AND
	HISTOPATHOLOGICAL DATA
	Palpation of USL lesion by clinical examination
	under anaesthesia
	Total	25/42 (59.5)
	Bilateral a	8/42 (19.0)
	Right	17/42 (40.5)
	Left	16/42 (38.1)
	Endometriosis lesion of a USL visualized
	laparoscopically
	Total	54/77 (70.1)
	Bilateral a	21/77 (27.3)
	Right	37/77 (48.1)
	Left	38/77 (49.4)
	USL resection
	Total	57/77 (74.0)
	Bilateral a	22/77 (28.6)
	Right	40/77 (51.9)
	Left	39/77 (50.6)
	Other endometriosis lesion visualized by
	laparoscopy
	Endometrioma	22/77 (28.6)
	Superficial	53/77 (68.8)
	peritoneal
	endometriosis
	Absence of endometriosis	7/77 (9.1)
	lesion at laparoscopy
	rASRM score
	Median (minimumÀmaximum)	12 (0À108)
	Minimal (I) or moderate (II)	28/58 (48.3)
	Moderate (III) or severe (IV)	30/58 (51.7)
	Histological confirmation of USL endometriosis
	Total	39/57 (68.4)
	Bilateral a	14/22 (63.6)
	Right	27/40 (67.5)
	Left	26/39 (66.7)
	Histological confirmation of	44/53 (83.0)
	other endometriosis location
	Data are presented as n/N (%) unless otherwise stated.
	rASRM = revised American Society for Reproductive
	Medicine classification of endometriosis;
	USL = uterosacral ligament.
	a For statistical reasons an involvement of both USL
	(bilateral) is also counted in right and left.

TABLE 3

 3

	MRI CHARACTERISTICS OF
	THE USL
	Characteristic	n = 77
	Asymmetry	48/77 (62.3)
	Thickening
	Total	54/77 (70.1)
	Bilateral a	15/77 (19.5)
	Right	36/77 (46.8)
	Left	33/77 (42.9)
	Irregularity
	Total	28/77 (36.4)
	Bilateral a	4/77 (5.2)
	Right	19/77 (24.7)
	Left	13/77 (16.9)
	Nodule
	Total	10/77 (13.0)
	Bilateral a	2/77 (2.6)
	Right	5/77 (6.5)
	Left	7/77 (9.1)
	Straightness
	Total	5/77 (6.5)
	Bilateral a	5/77 (6.5)
	Right	5/77 (6.5)
	Left	5/77 (6.5)
	Hypersignal T1 spot
	Total	7/77 (9.1)
	Bilateral a	1/77 (1.3)
	Right	5/77 (6.5)
	Left	2/77 (2.6)
	USL diameter (mm), mean § SD
	Right	3.3 § 2.3
	Left	3.5 § 2.0
	Other endometriosis lesion
	Total	46/77 (59.7)
	Ovary	36/77 (46.8)
	Data are presented as n/N (%) unless otherwise stated.

TABLE 5

 5

	INTER-OBSERVER AGREEMENT FOR USL ANALYSIS
	Characteristic	Cohen's kappa (95% CI)	P-value
	Diameter, mm	0.609 (0.462À0.723)	<0.001
	Asymmetry	0.593 (0.411À0.775)	<0.001
	Thickening	0.633 (0.510À0.756)	<0.001
	Irregularity	0.465 (0.285À0.645)	<0.001
	Straightness	0.827 (0.592À1.062)	<0.001
	Nodule	0.386 (0.098À0.674)	<0.001
	Hypersignal T1 spot	0.319 (0.157À0.795)	<0.001

CI = confidence interval; USL = uterosacral ligament.

DATA AVAILABILITY

Data will be made available on request.


Antoine Netter
email: antoine.netter@gmail.com

Charlotte Litaudon

Claire Tourette

Laura Miquel

Blandine Courbiere

Aubert Agostini

Robot

Keywords:

published or not. The documents may come

Introduction

Five to 20% of women regret having a tubal ligation, of which 1 -2% request a reversal of sterilization. [START_REF] Van Seeters | Tubal anastomosis after previous sterilization: a systematic review[END_REF]. These women are generally otherwise fertile and have a better chance of pregnancy than other patients experiencing infertility, whether by in vitro fertilization (IVF) or after tubal surgery [START_REF] Berger | Effectiveness of bilateral tubotubal anastomosis in a large outpatient population[END_REF][START_REF] Malacova | Live delivery outcome after tubal sterilization reversal: a population-based study[END_REF]. The choice between the two techniques must take into account the patient's age, the date of the last pregnancy, the ovarian reserve and the partner's semen quality [START_REF]Practice Committee of the American Society for Reproductive Medicine. Electronic address: aSRM@asrm.org. Role of tubal surgery in the era of assisted reproductive technology: a committee opinion[END_REF]. Historically, tubal anastomosis surgery has long been performed by microsurgery through laparotomy, which provided very high precision but was associated with some degree of morbidity [START_REF] Patel | Robotic tubal anastomosis: surgical technique and cost effectiveness[END_REF]. The parallel development of in vitro fertilization and laparoscopy have contributed to reducing the indications for tubal surgery. The laparoscopic approach is challenging because of the number and precision of the sutures needed [START_REF] Estes | Tubal anastomosis: once in a blue moon?[END_REF]. The robot-assisted laparoscopic approach may reduce the surgical difficulty and improve the accessibility of this technique [START_REF] Guan | Robotic single-site tubal reanastomosis: the robotic factor[END_REF].

The objective of the present work was to describe the technique of robot-assisted laparoscopic tubo-tubal reanastomosis after sterilization in 10 steps and assess its value.

Case presentation

We present the case of a 36-year-old woman, gravida 3 para 3 (3 cesarean sections), with a history of tubal ligation during her last cesarean section three years before who presented for pregnancy intention. After receiving comprehensive information, the patient opted for tubo-tubal reanastomosis as a first-line procedure rather than in vitro fertilization.

Operative settings

Step 1: Robot installation: The procedure is performed using robotassisted laparoscopy with the Da Vinci Xi four-arm surgical system (Intuitive Surgical, Sunnyvale, California, USA). The patient is positioned in low dorsal lithotomy position with her arms alongside the body. The robot is installed to the right of the patient at an angle of approximately 45°. Four 8 mm robotic ports and one 5 mm assistant port are inserted on a horizontal line at the umbilical level.

Step 2: Assessment of feasibility: The feasibility of the procedure is verified. A sufficient length of healthy tube is required on at least one side. If the tube is too damaged, it may be better to forego the operation in favor of in vitro fertilization.

Step 3: Initial dye test: This step dilates the proximal portion of the tube, which improves the differentiation of the mucosa and thus facilitates the suture.

Contents lists available at ScienceDirect

Journal of Gynecology Obstetrics and Human Reproduction journal homepage: www.elsevier.com

Step 4: cutting the tube: The tube is cut on both sides of the ligature without the use of energy to preserve the vascularization and improve the anastomosis.

Step 5: Opening of the mesosalpinx: The ligated portion of the tube is excised by coagulating the adjacent mesosalpinx with monopolar energy. After this step, the proximal and distal portions of the anastomosis can be placed face to face to identify the mucosal and serosal planes on both sides.

Step 6: Suture of the mucosa: Four mucosal interrupted sutures are performed with a 6-0 absorbable monofilament. It is important to start with the deepest point towards the mesosalpinx as it will soon become inaccessible. For this step, it is necessary to take care to position the knot outside the tube lumen by making the first entry from the outside to the inside and the second entry from the inside to the outside. Also, as far as possible, the tube should not be grasped from inside the lumen or crushed. Either the serosa or the mesosalpinx can be gently grasped.

Step 7: Suture of the serosa: Four serosal interrupted sutures are performed with a 6-0 absorbable monofilament. This step seals the anastomosis to prevent leakage and can resolve bleeding. No energy should be used for coagulation. It is important to selectively grasp the serosa to completely cover the anastomosis. The suture should be handled very gently without applying excessive tension so that it does not break. The knots should be tightened gradually.

Step 8: Suture of the mesosalpinx: The mesosalpinx adjacent to the anastomosis is closed with two interrupted sutures performed with a 2-0 absorbable polyfilament. This step indirectly solidifies the anastomosis by avoiding tensions and prevents incarceration of a bowel loop.

Step 9: Final dye test: A final dye test is performed to assess the patency of the tube and confirm the absence of leakage around the anastomosis.

Step 10: anti-adherent agent: anti-adherent agent is applied near the anastomosis to prevent the formation of adhesions.

Discussion

This video article shows the feasibility of tubal anastomosis in robot-assisted laparoscopy and provides a standardized 10-step technique.

A systematic review of the literature on tubal anastomosis surgery was conducted by Van Seeters et al. in 2017 [START_REF] Van Seeters | Tubal anastomosis after previous sterilization: a systematic review[END_REF]. Although the comparative studies were mostly retrospective and limited in size, the pregnancy rates after surgery seemed to be similar between the different techniques: 68% (95% CI: 58-71%) for laparotomic microsurgery, 65% (95% CI: 61-74%) for laparoscopy and 65% (95% CI: 59 -72%) for robot-assisted laparoscopy. Likewise, the rates of ectopic pregnancies appeared to be similar for the different techniques (between 5.6% and 15%). Only 4 studies specifically focused on the robotic approach [START_REF] Patel | Robotic tubal anastomosis: surgical technique and cost effectiveness[END_REF][START_REF] Rodgers | Tubal anastomosis by robotic compared with outpatient minilaparotomy[END_REF][START_REF] Caillet | Robotically assisted laparoscopic microsurgical tubal reanastomosis: a retrospective study[END_REF][START_REF] Goldberg | Laparoscopic microsurgical tubal anastomosis with and without robotic assistance[END_REF]. Two studies compared the robotic approach with open surgery and have shown similar results in terms of viable intrauterine pregnancies [START_REF] Patel | Robotic tubal anastomosis: surgical technique and cost effectiveness[END_REF][START_REF] Rodgers | Tubal anastomosis by robotic compared with outpatient minilaparotomy[END_REF]. The robot-assisted approach was associated with a shorter recovery time but longer operative time and higher costs. One study of 25 patients compared conventional laparoscopy and robot-assisted laparoscopy and found no difference in pregnancy rates but showed a significant increase in operative time for robot-assisted laparoscopy [START_REF] Goldberg | Laparoscopic microsurgical tubal anastomosis with and without robotic assistance[END_REF]. No study compared the robotic approach with IVF. A study of 84 patients comparing the laparotomic microsurgical approach and IVF found no significant difference in pregnancy rates and suggested a lower cost for the surgical approach [START_REF] Boeckxstaens | Getting pregnant after tubal sterilization: surgical reversal or IVF?[END_REF]. Overall, these data are insufficient to conclude that one technique is superior to another in cases of regret following tubal ligation. The surgical approach nevertheless seems to be a reasonable alternative to IVF [START_REF] Estes | Tubal anastomosis: once in a blue moon?[END_REF]. In particular, the robotic approach combines the advantages of minimally invasive surgery while avoiding the difficulties inherent in laparoscopic suturing and could therefore improve the accessibility of this surgery for patients. There are no studies that formally identify the criteria for selecting patients who would have a better chance of pregnancy after surgery rather than IVF (apart from obvious additional infertility factors, particularly in relation to semen analysis) [START_REF] Van Seeters | Tubal anastomosis after previous sterilization: a systematic review[END_REF]. In case of failure to achieve pregnancy after tubal anastomosis surgery, IVF can be offered to patients. A 2016 study by Berger et al. reported pregnancy rates of 41% (95% CI: 40-42%) 6 months after laparotomy surgery and 58% [95% CI: 57-59%] after one year [START_REF] Berger | Effectiveness of bilateral tubotubal anastomosis in a large outpatient population[END_REF]. This suggests that a delay of at least one year may be allowed before considering IVF.

Conclusion

We have described the technique of tubo-tubal reanastomosis after sterilization with robot-assisted laparoscopy in 10 steps and discussed its value.

Acknowledgement

N/A

Funding

This study received no funding

Declaration of Competing Interest

The authors declare no conflict of interest.

Supplementary materials

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.jogoh.2023.102605.