Intraoperative ultrasound assessment of ureteral patency after uterosacral ligaments apical suspension for prolapse surgical repair: A feasibility study

To prospectively compare power Doppler ultrasound diagnostic performance with reference standard cystoscopy in evaluating ureteral patency in a population at high risk of ureteral lesions.

the best approach could be to return to diagnostics in case of procedures with an "above-average" risk of urinary tract injury.For instance, pelvic organ prolapse repair is considered as a surgery with a high risk of ureteral injury.There is now renewed interest in native-tissue techniques because of their lower costs and lack of mesh-related complications. 5,6][9][10] Among available procedures, uterosacral ligaments (USL) suspension is considered a versatile and effective procedure to suspend the vaginal apex [11][12][13] but involves a risk of ureteral injury up to 10.9%. 14e to the prevalence of ureteral injury, proper intraoperative recognition of this condition is of the utmost importance.Recently, the use of intraoperative ultrasound has been proposed in these patients to identify ureteral kinking, using the power Doppler mode to visualize ureteral jets. 15Ultrasound evaluation of ureteral patency carries some potential advantages compared with intraoperative cystoscopy.Ultrasonography is a widespread diagnostic tool, which can be used with no additional costs and it is very familiar to gynecologists.Moreover, it is a completely non-invasive method, with no risk of iatrogenic damage or infection.Lastly, it does not require specific contrast agents, and urine or saline solutions may be appropriate media for evaluating the ureter-bladder complex.However, there are currently no data on the diagnostic performance of ultrasound in identifying intraoperative ureteral kinking.
As a consequence, with the present study, we aimed to prospectively compare ultrasound diagnostic performance with reference standard cystoscopy in terms of sensitivity, specificity, positive predictive value, and negative predictive value of ureteral kinking in a population at high risk (women undergoing pelvic organ prolapse repair with USL suspension).Moreover, we wished to analyze factors related to errors in binary classification based on ultrasound.

| MATERIAL S AND ME THODS
This was a prospective study.We analyzed 100 consecutive women who underwent pelvic organ prolapse repair between April 2021 and May 2022 through USL suspension, which represents the standard procedure in our institution.Before the start of the current study, we also performed intraoperative cystoscopy as part of our routine practice during this surgical procedure.Preoperative evaluation included medical interviews, clinical examination, and prolapse staging according to the Pelvic Organ Prolapse Quantification system.
Two experienced vaginal surgeons (M.F. and A.C.) carried out all surgery, according to the previously described technique. 16,17Once the hysterectomy was completed, or the Douglas pouch was opened in case of vaginal vault prolapse, a long gauze was placed to pack the small bowel out of the operative field and was lifted by a Breisky-Navratil retractor.An Allis or Kocher clamp grasping the uterosacral stump close to the vaginal rim was placed and gentle traction was applied to identify and palpate the USL path.When technically feasible, the position of the ureter was identified.On each side, the USL was transfixed with three consecutive polydioxanone monofilament long-term absorbable 0 sutures (Assufil monofilamento™; Assut Europe).Each suture was passed ventral to dorsal to reduce the risk of ureteral entrapment.The lowest (first) suture was placed at the level of the ischial spine, whereas the two following sutures were placed 1 cm above the previous one.Additional surgical procedures, such as anterior or posterior vaginal wall prolapse repair, were performed when indicated.
Intravenous administration of 300 mL of saline solution was performed 10-15 min before the end of the procedure.If there were no contraindications, 10 mg of furosemide was also administered.At the end of the procedure, the bladder was filled with 300 mL of mannitol solution.All ultrasound scans were obtained using a convex 3.5-MHz probe, before cystoscopic evaluation.Ultrasound examination of the bladder was performed with suprapubic transverse scans.
Bilateral simultaneous ureteral jet evaluation with power Doppler was performed at the level of the ureterovesical junctions with a pulse repetition frequency set to detect low flow for a maximum time of 3 minutes, as previously described. 18The power Doppler field included the entire posterior wall of the bladder.Ureteral patency tests were evaluated separately on each side and considered negative if the jet was clearly observed, and positive when it was not visualized during the 3 min (Figure 1 Statistical analysis was performed with JMP 7.0 (SAS Institute, Cary, NC, USA).A P value less than 0.05 was considered significant.

| RE SULTS
A total of 100 consecutive women were analyzed, for a total of All women underwent USL suspension.Additional procedures and intraoperative data are reported in Table 2.According to the reference standard urethrocystoscopy, at least one ureter not ejaculating was observed in 6% of patients, for a total of seven ureter jets not visualized.Ultrasound findings in terms of true positive, true negative, false positive, and false negative are reported in Figure 2. Notably, ultrasound was able to correctly categorize 193 out of 200 ureters, and no false-negative results were obtained.
Ultrasound with power Doppler showed 100% sensitivity and 95.9% specificity in detecting the lack of ureteral jet.The negative predictive value was 100%, while the positive predictive value was 46.7%.Risk factor analysis did not find any variables related to errors in binary classification based on ultrasound (Table 3).In particular, the lack of furosemide administration was not a risk factor for misclassification.

| DISCUSS ION
Ureteral kinking is considered the main pitfall of USL suspension during prolapse repair.Its recognition during the procedure is of the utmost importance to avoid long-term sequelae.However, the opportunity to perform universal cystoscopy is under debate due to costs, invasiveness, and lack of training.With this study, we aimed to compare, for the first time, ultrasound diagnostic performance with reference standard cystoscopy in evaluating ureteral patency after USL suspension.Our experience suggests that ultrasound with power Doppler can be an excellent triage test to greatly reduce the use of cystoscopy.In particular, ultrasound was able to properly de-  effects such as hypokalemia.However, our series showed that this is not an indispensable step for visualizing ureteral jets.Hence, in elderly and frail patients it can be omitted or replaced by either increased intravenous fluid administration or longer ultrasound observation time.
To the best of our knowledge, this is the first study evaluating the diagnostic performance of ultrasound power Doppler in identifying ureteral kinking during prolapse repair with USL suspension.
Ultrasound with power Doppler represents an effective and reliable non-invasive screening test to exclude ureteral kinking and reduce the need for intraoperative cystoscopy in gynecologic procedures at medium-high risk for ureteral injury.
). Laterality was defined based on the emergence of the jet from the left or right side of the posterior bladder wall.Ultrasound test results were noted and diagnostic cystoscopy was then performed as the reference standard to evaluate ureteral patency (negative: ureteral jet visualized; positive: ureteral jet not visualized).Operators have standard general gynecologic ultrasound skills and advanced pelvic floor ultrasound skills.Before the start of the study, all operators performed 5-10 bladder scans in the outpatient setting to gain familiarity with power Doppler observation of ureteral jets, without the use of any bladder medium.The study was approved by the Institutional Review Board of San Gerardo Hospital in Monza, Italy (Protocol US-URETERS, no.392, 22/03/2021).Informed consent was acquired before the start of the study from all the patients.Data were entered into a dedicated database by one author and double-checked by one other author.Descriptive statistics were calculated as absolute numbers with percentages for categorical variables and as median (interquartile range) for continuous variables.Diagnostic performance of ultrasound compared with reference standard endoscopy was expressed in terms of sensitivity, specificity, and positive and negative predictive values.Risk factor analysis was performed using Student t test for continuous parametric variables, the Wilcoxon test for continuous non-parametric variables, and χ 2 test for non-continuous variables.

aa
fine the patency of 192 out of 200 ureters, with no false-negative and only eight false-positive results.The diagnostic performance of the test resulted in 100% sensitivity and 95.9% specificity compared with the reference standard.The negative predictive value was 100% and the positive predictive value was 46.7%.These F I G U R E 1 Demonstration of ureteral jet with power Doppler.(a) Lack of ureteral jet; (b, c) right and left ureteral jets; (d) simultaneous bilateral ureteral jets.TA B L E 1 Population characteristics.Data are given as absolute numbers with percentages for categorical variables and as median (interquartile range) for continuous variables.b Body mass index is calculated as weight in kilograms divided by the square of height in meters.Data are given as absolute numbers with percentages for categorical variables and as median (interquartile range) for continuous variables.performance indices make ultrasound an excellent screening test to exclude ureteral kinking, with no risk of missing ureteral complications.According to our data, cystoscopy may be avoided in 94% of patients following ultrasound.Obviously, in the case of the lack of visualization of ureteral jets, it is mandatory to perform cystoscopy before trying any surgical management, because of the low positive predictive value.Interestingly, ultrasound tests seem to perform well irrespective of patient characteristics, including body mass index and contraindications to diuretic stimulus, as demonstrated by the risk factor analysis.Despite the absence of studies about the use of ultrasound to assess ureteral patency, this was already performed in other settings, in particular in the emergency room as part of the evaluation of renal colic.A previous study has demonstrated ureteral jet asymmetry oncolor Doppler in the case of obstruction and has been proposed as a non-invasive alternative to computed tomography.18More recently, power Doppler mode has been used to visualize ureteral jets in patients with symptoms of renal colic.19Compared with color Doppler, power Doppler has some advantages-it is characterized by enhanced sensitivity and specificity, and clearer visualization of body fluid movements.In gynecology, power Doppler ultrasound has been proposed to evaluate ureteral patency in high-risk procedures for ureteral injuries, such as hysterectomy or pelvic floor reconstructive surgery,15 but until now no data were available.The ultrasound ureteral patency test is easy, requires only minimal equipment with no additional cost, and carries no risk of iatrogenic urethra/bladder injury for the patients.Moreover, ultrasonography may be a much more familiar tool to gynecologists compared with cystoscopy.This test can be particularly attractive for physicians dealing with procedures with a high risk of ureteral injuries, such as pelvic floor surgeons.A limitation that must be acknowledged is the lack of an interobserver variability analysis.However, both operators performed the minimum required training.A further limitation is the impossibility of performing a direct visualization of bladder integrity.However, saline leakage outside the bladder as well as free fluid in the Douglas pouch can be visualized as sonographic signs of bladder wall injury.Another limitation can be the use of furosemide to enhance diuretic stimulus, which may carry a small risk of pharmacologic adverse F I G U R E 2 Results of ultrasound test on 200 ureters.FN, false negative; FP, false positive; TN, true negative; TP, true positive.TA B L E 3 Risk factors analysis for errors in classification based on ultrasound.a