Ultrasonography Sliding Sign as a Predictor for Intraabdominal Adhesions in Repeated Cesarean Deliveries: Retrospective Cross Sectional Study.

O.Y. wrote the main manuscript text. C.A., U.A., O.Y., and H.A.A. conducted data collection and analysis. All authors reviewed the manuscript. All authors read and approved the final manuscript.

This study was performed in line with the principles of the Declaration of Helsinki. And this was a retrospective cohort research. All procedures performed were in accordance with the ethical standard of the institutional committee (Name: Izmir Democracy University, Buca Seyfi Demirsoy Training and Research Hospital Ethics Committee, File Number: 2024/225, Date: 31/01/2024).

The authors have nothing to report.

Table  1 was given to demonstrate participants' clinical and demographic details. The median age of Group 1 (31 (19–41)) was older than Group 2 (28.5 (19–41)). This difference was statistically significant ( p  = 0.01). Both pregestational and gestational BMI were similar for both groups ( p  = 0.3; p  = 0.2, respectively). Gravidy and partiy were statistically higher in Group 1 ( p  < 0.0001; p  < 0.0001, respectively). Smoking habit was similar for groups ( p  = 0.2). Previous vaginal delivery was detected at a higher rate in Group 1, but this difference was not statistically significant (9.3% vs. 4.5%; p  = 0.1). Number of previous cesarean section was found as 2 (1–4) in Group 1 and 1 (1, 2) in Group 2 ( p  < 0001). ≥  2 number of previous cesarean section was 71.9% in Group 1 and 30.7% in Group 2 ( p  < 0001). The groups were similar in terms of time passed after last cesarean section ( p  = 0.07). Demographic and clinical characteristics of the patients. Comparison of the surgical results of the groups was shown in Table  2 . The birth weight, gestational age, total operative time were similar between groups ( p  = 0.1; p  = 0.3; p  = 0.3, respectively). The preoperative hemoglobin, postoperative hemoglobin, and hemoglobin drop exhibit no statistically significant difference among the groups ( p  = 0.1; p  = 0.3; p  = 0.3, respectively). Duration of maternal hospitalization was similar between groups ( p  = 0.2). Perioperative surgical complications were detected in three cases in Group 1 (2.8%), including bladder injury in two cases and bowel injury in one case. There were no perioperative complications in Group 2. There is no statistical difference among the groups with regard to perioperative complications. As expected, Nair's Score was detected higher in Group 1 ( p  < 0001). The groups were similar with regard to 1‐min APGAR score, 5‐min APGAR score and necessity of neonatal intensive care unit ( p  = 0.9; p  = 0.9; p  = 0.5, respectively). Comparison of operative results of the groups. The Cohen's Kappa showed that there was an almost‐perfect agreement between observers for ultrasonography sliding sign (90.9%, k  = 0.81.6; p  < 0.001). The diagnostic value of transabdominal ultrasonography sliding sign for detecting the presence of intra‐abdominal adhesion (according to the Nair's Modified Scoring system) was presented in Table  3 , Figures  1 and 2 . The region below ROC curves for the sliding sign was 0.717 (95% CI: 0.645–0.789). The sensitivity was 58.9%, specificity was 84.6%, positive predictive value (PPV) was 81.7%, negative predictive value (NPV) was 63.6%, positive likelihood ratio (LR+) was 3.8, negative likelihood ratio (LR−) was 2, with an overall accuracy of 70% ( p  < 0.0001). Diagnostic value of transabdominal ultrasonography sliding sign according to the presence of intra‐abdominal adhesion (modified Nair's scoring system). ROC analysis of the diagnostic value of transabdominal ultrasonography sliding sign according to the modified Nair's scoring system. STARD diagram to report the flow of participants throughout the study (modified Nair's score). The diagnostic value of transabdominal ultrasonography sliding sign for detecting the presence of intra‐abdominal adhesion (based on scoring system of Nair) was illustrated in Table  4 , Figures  3 and 4 . A Nair's score = 2 was identified as the cut‐off point where the sliding sign finding was statistically significant. The region below ROC curves for the sliding sign was 0.713 (95% CI: 0.640–0.786). The sensitivity was 54%, specificity was 70%, PPV was 73.8%, NPV was 49.2%, LR+ was 1.8, LR− was 1.5, with an overall accuracy of 65% ( p  = 0.03). Diagnostic value of transabdominal ultrasonography sliding sign according to the presence of intra‐abdominal adhesion (Nair's scoring system). ROC analysis of the diagnostic value of transabdominal ultrasonography sliding sign according to the Nair's scoring system. STARD diagram to report the flow of participants throughout the study (Nair's score).

In recent years, the number of cesarean sections performed has skyrocketed. There are regions in the world where the rates of cesarean sections range from 44.3% to 60.0% (Anekpornwattana et al.  2020 ; Boerma et al.  2018 ). In women undergoing repeat cesarean sections, intra‐abdominal adhesions can develop in 46%–83% of cases, potentially resulting in intraoperative or postoperative complications such as bleeding, injuries at bowel and bladder, neonatal morbidity and hysterectomy (Tulandi et al.  2009 ; Morales et al.  2007 ). Few studies have employed ultrasonography to assess the existence of intra‐abdominal adhesion prior to surgery. However, these studies either relied on transvaginal ultrasonography, which may not be universally accessible, or had varying sample sizes that did not adequately showcase the effectiveness of this approach. Additionally, there was inconsistency in the standardization of the evaluation of intra‐abdominal adhesions and inter‐observer ultrasonography assessment among these studies (Baron et al.  2018 ; Sönmez et al.  2023 ; Yosef et al.  2023 ; Charernjiratragul et al.  2023 ; Ayachi et al.  2018 ). Our objective was to evaluate the ultrasonography sliding sign with enhanced reliability using an inter‐observer approach, with the aim of predicting standardized intra‐abdominal adhesions before cesarean section.

The cesarean section rate is currently experiencing a dramatic increase, resulting in heightened complications such as intraperitoneal adhesions, placenta location and invasion anomalies. These complications can occasionally lead to significant challenges during cesarean section, with adverse effects on both neonate and mother. The present study was a retrospective cohort research designed to verify the accuracy of dynamic ultrasonography in identifying intra‐abdominal adhesions in females having multiple cesarean sections. In this current research, the diagnostic value of transabdominal ultrasonography sliding sign for detecting the presence of intra‐abdominal adhesion (according to the modified Nair's scoring system) yielded a 84.6% specificity, 58.9% sensitivity, and an overall 70% accuracy. A Nair's score ≥ 2 was identified as the cut‐off point, with the sliding sign finding being statistically significant, resulting in a 70% specificity, 54% sensitivity, and 65% accuracy. In recent years, ultrasonography has emerged as a viable and noninvasive tool for predicting adhesions, with the “sliding sign” being predominantly utilized to predict adhesions related to pelvic endometriosis. The initial study by Baron et al. introduced the use of the sliding sign to predict adhesions in repeating cesarean sections Baron et al. ( 2018 ). They reported sensitivity and positive predictive value of 76.2% and 84%, respectively. In that research, the proportion of patients having two or more previous cesarean sections was 86.4%, and there was an incidence of severe adhesions in 35.6% of cases. According to the Yosef et al. study, the proportion of patients with two or more previous cesarean sections was 64.2% (Yosef et al.  2023 ). They found that the sliding sign demonstrated a 100% sensitivity and 86.84% specificity in its prognostic capacity to identify intra‐abdominal adhesions in females having recurrent cesarean birth. However, adhesions were not categorized in that study (Yosef et al.  2023 ). In our study, the percentage of patients who had undergone two or more previous cesarean sections was 71.9% in the group with adhesions and 30.7% in the group without adhesions. When considering all patients collectively, this rate was 53%. Additionally, we conducted intraoperative adhesion assessments using both Nair's and modified Nair's scoring systems. When considering all adhesion categories based on the Modified Nair's Score system, the observed adhesion rate was 54%. The sensitivity of the sliding sign was determined to be 58.9%, with a specificity of 84.6%. In the evaluation of adhesion analysis as a numerical value according to Nair's score system, we identified the cut‐off point of Nair's score as 2, indicating a statistically significant sensitivity of 54% and specificity of 70%. Consequently, the proportion of patients with a Nair score ≥ 2 was 37.3%. According to the results of our study, patients with a Nair's score of 2 were categorized into the mild group according to the Modified Nair's score classification. This indicates that the threshold at which the sensitivity and specificity of the Nair score become statistically significant pertains to cases that have not yet advanced to the severe adhesion group. In the research of Charernjiratragul K. et al. the relationship between negative sliding sign and intraoperative adhesion was examined (Charernjiratragul et al.  2023 ). In this study, the number of two or more previous cesarean sections was 19%. Similar to the cut‐off point in our study, the diagnostic performance of the sliding sign was highest in medium to thick adhesions (only Grade 2, any site), with a 60.6% sensitivity and a 91.9% specificity. Sensitivity was lower for all degrees of adhesion, but specificity for any site of adhesion remained high. However, we point out that we did not evaluate adhesions as a subgroup based on location in our study. According to our study, the median age of patients in the adhesion group was higher. Concurrently, gravidy and parity were also higher in the adhesion group. This observation can be attributed to the association between increased gravidity, parity, and the number of cesarean sections with advancing age. Total operative time, hemoglobin drop, and duration of maternal hospitalization did not exhibit differences between the study groups categorized based on the presence of adhesion. The perioperative surgical complication rate was 2.8% in the adhesion group. Both groups demonstrated similarity in terms of 1‐ and 5‐min APGAR scores. In Group 2, the need for hospitalization to the newborn intensive care unit was 1.5 times greater. The presence of a sliding sign finding on ultrasonography is significant in predicting the obstetric and neonatal parameters assessed above before the operation. It serves to alert anesthesiologists, surgical teams, and pediatricians regarding potential higher risks of complications during preoperative preparations. Cohen's Kappa analysis demonstrated an almost‐perfect agreement between observers for the ultrasonography sliding sign applied with a standardized method in our study (90.9%, k  = 0.816). This agreement rate was similar to the inter‐observer correlation rate reported in Drukker et al.'s study (0.87) (Drukker et al.  2018 ). Conversely, it surpassed the correlation rates of 0.58 in Bukar M. et al.'s study and 0.52 in Baron et al.'s study (Baron et al.  2018 ; Bukar et al.  2022 ). Baron et al. proved a 0.77 intraobserver variability correlation (Baron et al.  2018 ). However, the absence of intraobserver variability analysis in our study posed a limitation. Another limitation was the retrospective structure of the research. The strengths of our study encompass the inclusion of both qualitative and quantitative assessments. Additionally, the study achieved triple masking: both sonographers were unaware of the surgical findings, the surgeon remained unaware of the ultrasound findings, and the data analyst was unaware of both sonographic and surgical findings. Furthermore, the strict inclusion of causes that may lead to intra‐abdominal adhesion among the exclusion criteria of the study enhances the homogeneity and purity of our study group.

The authors have nothing to report.

The authors declare no conflicts of interest.

This was a retrospective cross‐sectional research carried out at a secondary care center. All procedures performed were in accordance with the ethical standard of the institutional committee (File Number: 2024/225, Date: 31/01/2024) and with the Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent to participate was obtained from all of the participants in the study. Between January 2022 and January 2024, 350 individuals who had cesarean section were accepted in the research. The exclusion criteria were: elective primary cesarean section, urgent cesarean section, history of urgent cesarean section, vaginal delivery, urgent or elective cesarean section between 24th and 36th (0–6 days) weeks due to maternal or fetal indications, intrauterine fetal death, gestational body mass index > 35%, history or presence of placental location and invasion anomalies, closing the uterine layers other than the single‐layer continuous locking technique in a previous cesarean section, perioperative intra‐abdominal antiadhesive therapy in previous cesarean section, history of pelvic inflammatory disease or tuba‐ovarian abscess, cesarean incision other than Pfannenstiel, history of endometriosis, history of pelvic surgery (myomectomy, ectopic pregnancy etc.), connective tissue disorders (marfan, lichen sclerosis, etc.). Data of 198 patients were analyzed. Demographic data (body mass index (BMI), age, weight, height, smoking habit, etc. of patient), obstetric history (gravida, parity, number of previous cesarean section, etc.), gynecological history (history of pelvic surgery or endometriosis) of the patients were documented. To assess sliding signs, all pregnant participants received transabdominal ultrasonography utilizing GE Medical Systems' VolusonP6 ultrasonography equipment and a 2‐ to 5.5‐MHz convex probe. The sonographic examinations were conducted by two obstetricians with 12 and 10 years of experience in obstetric ultrasonography, who were unaware of each other's findings. In case of discrepancies, a third obstetrician with 10 years of experience ensured consensus. The ultrasonographic evaluations were performed within 1 week before the scheduled cesarean section. A separate obstetrician within the team recorded the findings. Ultrasonography evaluation was performed based on sliding sign description in the literature (Baron et al.  2018 ). The uterus could be seen slipping caudally under the fascia transversalis and parietal peritoneum when the probe was positioned near the transverse skin scar and the participant was instructed to inhale deeply. When the uterus was seen sliding against the abdominal wall, the sliding sign was said to be present. The sliding indication was deemed missing when there were no visible movements of the uterus beneath the fascia. Intervisceral adhesions and adhesions between the viscera and peritoneal surfaces were graded based on the scoring system of Nair; Grade 0: 0 adhesion, Grade 1 adhesions involving a single band connecting viscera or from one viscus to the abdominal wall. Grade 2 adhesions consisting of 2 bands between abdominal wall and the viscera. Grade 3 adhesions entail more than 2 bands between viscera and the abdominal wall or between viscera. Grade 4 adhesions indicating viscera directly attached to the abdominal wall, with no regard to the quantity or size of adhesive bands (Nair et al.  1974 ). In the modified scoring system of Nair, Nair's scores were classified. According to this classification; Grade 0: 0 adhesion, Grade 1, 2: mild adhesions, Grade 3, 4: severe adhesions. All cesarean section procedures were performed by a surgeon unaware of the results of the ultrasonographic sliding sign evaluation. The surgeon used the modified Nair classification system to examine every single individual for intra‐abdominal adhesion. According to the Nair's modified scoring system, the cases were classified as Group 1 (adhesions present [Grade ≥ 1]; n  = 107, 54%) and Group 2 (no adhesions [Grade 0]; n  = 91, 46%). Analyzes were made with SPSS 26.0 (IBM Inc., Chicago, IL, USA). Kolmogorov‐Smirnov test was taken as the base for the Normality analysis. The Mann–Whitney U test was employed to assess variables that were not normally distributed. These outcomes were expressed as median (min‐max) numbers for each group. Chi‐square test and Fisher precision test were employed in the categorical data analysis. These were presented as counts and percentages (%). An inter‐rater reliability analysis was performed for ultrasonography sliding sign finding. For this purpose, the Cohen's Kappa was calculated. Receiver operating characteristic (ROC) analysis was used to determine the area under the curve (AUC), which indicates the average sensitivity of ultrasonography sliding sign finding. It was determined what the proper cut‐off value was, which was the total of the highest values for sensitivity and specificity. There was a 95% confidence interval (CI) for the results. A p value of less than 0.05 was deemed statistically significant. The sample size was determined using the “Statistics and Sample Size Pro” MS Excel Sample Size Calculator for Diagnostic Test Studies. The calculation was based on the following parameters: an expected sensitivity of 76.0%, an expected specificity of 92.0%, an anticipated prevalence of cesarean section (CS) of 38.0% (corresponding to the CS rate at our center), a desired precision of 12.0%, and a 95% confidence interval. Accordingly, the required sample size was calculated to be 129 participants.