The Role of Hysterosalpingo-Foam Sonography in the Diagnosis of Hydrosalpinx: A Prospective Clinical Study.

Introduction Hydrosalpinx is a major cause of tubal factor infertility. Hysterosalpingography (HSG) is the primary method for assessing tubal patency and hydrosalpinx, but its complications have prompted the use of hysterosalpingo‐foam sonography (HyFoSy). This study aimed to evaluate the diagnostic performance of HyFoSy in detecting hydrosalpinx.

A prospective study was conducted at the Department of Obstetrics and Gynecology, Faculty of Medicine, between June 2020 and January 2022. Twenty patients diagnosed with hydrosalpinx by HSG underwent tubal evaluation using HyFoSy. Intraluminal tubal diameter in the isthmus, ampulla, and infundibulum were measured during the procedure. Laparoscopy (L/S) served as the reference standard. Statistical analyses were performed using SPSS 20.0. Receiver operating characteristic (ROC) curves were used to determine cut‐off values, with area under the curve (AUC), sensitivity, and specificity calculated. Inter‐rater reliability was assessed with Cohen's kappa, and p values < 0.05 were considered significant.

The mean patient age was 33.3 ± 7.9 years. No significant difference was observed in isthmus measurements between hydrosalpinx and non‐hydrosalpinx tubes (p = 0.615), whereas significant differences were found in ampulla and infundibulum measurements (p = 0.023, p < 0.01). For hydrosalpinx diagnosis, HyFoSy demonstrated higher sensitivity (96% vs. 88%) and specificity (80% vs. 73%) than HSG. For tubal patency, HyFoSy also showed higher sensitivity (85% vs. 71%) and specificity (96% vs. 90%).

HyFoSy provides higher diagnostic accuracy than HSG for both tubal patency and hydrosalpinx. It is a reliable and more patient‐friendly alternative for hydrosalpinx evaluation.

fallopian tubes, hydrosalpinx, hysterosalpingographic foam sonography, hysterosalpingography, infertility 1. Introduction About 30%–40% of infertility cases worldwide are due to fallopian tube‐related pathologies [1, 2]. Hydrosalpinges account for 10%–30% of these pathologies [1, 3, 4]. Hydrosalpinx occurs as a result of distal tubal obstruction due to fluid accumulation in the ampullary portion of the fallopian tube [3, 5]. This condition is most commonly associated with pelvic inflammatory disease (PID), particularly infections caused by Chlamydia trachomatis [4, 5]. In addition to PID, other factors such as endometriosis, appendicitis, and previous abdominal‐pelvic surgery also play a role in the development of hydrosalpinx [1, 5]. Clinically, the presence of hydrosalpinx has been associated with poor reproductive outcomes, such as lower implantation and pregnancy rates, both in natural conception and assisted reproductive technologies (ART) [3, 6]. Various techniques are used in the evaluation of the fallopian tubes, including ultrasound (US), hysterosalpingography (HSG), hysterosalpingo‐contrast sonography (HyCoSy), hysterosalpingographic foam sonography (HyFoSy), and laparoscopy (LS) [2, 7]. Among these, LS is still considered the gold standard for evaluating tubal patency; however, its invasive nature and the need for anesthesia significantly limit its routine use in daily clinical practice [7]. In contrast, conventional US has a relatively limited role in evaluating the fallopian tubes and is informative in the presence of peritubal or intraluminal fluid [2]. HSG is one of the most commonly used methods for examining the fallopian tubes and uterine cavity due to its relatively low cost and the fact that it can be performed in an outpatient setting [8]. It has demonstrated good accuracy, particularly in the detection of proximal tubal disease [9]. In fact, it has been reported that it may be associated with increased pregnancy rates after tubal flushing [10]. However, HSG is often painful for patients due to factors such as cervical traction, uterine distension, and the passage of contrast material into the peritoneal cavity [11]. Additionally, the procedure involves exposure to ionizing radiation, and the use of iodinated contrast agents carries a risk of adverse reactions [8]. HyFoSy is a method in which the passage of a foam‐based contrast agent from the uterine cavity to the fallopian tubes and the peritoneal cavity is monitored by US to assess tubal patency [12, 13]. It is generally better tolerated by patients and is associated with less procedural pain [12, 13, 14]. In addition, it does not involve exposure to ionizing radiation and allows for the simultaneous assessment of both uterine abnormalities and tubal factors during the same examination [15, 16, 17]. In addition to these advantages, HyFoSy offers a brief window for visualizing the contrast transition. Its application and interpretation, however, depend on experience and technical skill [15, 16, 17]. Although studies have indicated that HyFoSy has diagnostic accuracy comparable to that of HSG for tubal patency [7, 14, 15], evidence supporting its reliability and effectiveness, particularly in the diagnosis of hydrosalpinx, is limited. For this reason, in our study, we aimed to investigate the diagnostic performance of HyFoSy for hydrosalpinx in a selected clinical population. 2. Materials and Methods This prospective clinical study was conducted between June 2020 and January 2022 after obtaining approval from the Faculty of Medicine Clinical Research Ethics Committee (Decision No: 20200708/8). Written informed consent was obtained from all participants, and the study was conducted in accordance with the principles of the Declaration of Helsinki and Good Clinical Practice (GCP) guidelines. Women aged 18–45 with complaints of infertility and/or pelvic pain were included in the study if at least one hydrosalpinx was detected on HSG and there was an indication for LS due to infertility or pelvic pain. Patients with pyosalpinx, hematosalpinx, or acute PID, pregnant women, those with adnexal masses, or those with known hypersensitivity to iodinated contrast agents were excluded from the study. During the study, five patients were excluded for refusing LS and three for acute PID, and the study was ultimately completed with 20 patients. The patients' basic demographic data, including age, weight, and body mass index (BMI), were recorded. Additionally, clinical information such as menstrual regularity, PID, history of ectopic pregnancy, history of pelvic or tubal surgery, infertility status, and presence of uterine anomalies was also collected. All patients underwent tubal evaluation consisting of HSG, HyFoSy, and LS, with HyFoSy performed prior to LS. For the HyFoSy procedure, the hysterosalpingo—foam kit (ExEm Gel; GynaecologIQ) was administered into the uterine cavity, and the passage of the echogenic foam through the fallopian tubes was monitored in real time using transvaginal ultrasonography. During the examination, the intraluminal tubal diameter was measured at three anatomical segments of the tube (isthmus, ampulla, and infundibulum). No analgesic, anesthetic, or prophylactic antibiotic was administered prior to the HyFoSy examination. Two patients (10%) experienced transient hypotension during the procedure. All HyFoSy examinations and intraluminal tubal diameter measurements were performed by the same surgical team using a predefined examination and measurement protocol. For the purposes of this study, hydrosalpinx at HyFoSy was defined as the presence of a dilated fallopian tube associated with distal tubal obstruction, with absent or markedly impaired contrast spill into the peritoneal cavity. Segmental intraluminal tubal diameter measurements obtained during HyFoSy were recorded separately and subsequently evaluated as potential diagnostic markers for hydrosalpinx. LS was performed in patients with infertility and/or pelvic pain who had imaging findings suggestive of hydrosalpinx on HSG and/or HyFoSy and for whom surgical evaluation was considered clinically indicated. Patients without a clinical indication for LS were not included in the study. LS served as the reference standard for confirming the presence of hydrosalpinx. During the procedure, both fallopian tubes were systematically examined, and tubal patency was assessed using a 0.25% methylene blue solution administered via a Rubin cannula. Surgical procedures such as fimbrioplasty, salpingectomy, or tubal clipping were performed on the affected tube or tubes. No intraoperative or postoperative complications were observed. 2.1. Statistical Analysis All statistical analyses were performed using SPSS for Windows (version 20.0). Categorical variables were expressed as numbers and percentages, while continuous variables were summarized as mean ± standard deviation or median with interquartile range (IQR) or minimum‐maximum values, depending on the distribution of the data. The normality of continuous variables was assessed using the Shapiro–Wilk test. Depending on the distribution pattern, parametric or non‐parametric statistical methods were selected. The differences between the two independent groups were examined using the independent samples t‐test for normally distributed variables and the Mann–Whitney U test for non‐normally distributed variables. To investigate diagnostic performance, receiver operating characteristic (ROC) curve analysis was performed to determine optimal cut‐off values, and the corresponding sensitivity and specificity values were calculated. The agreement between diagnostic techniques was assessed using Cohen's kappa coefficient. A p value less than 0.05 was considered to indicate statistical significance. 3. Results The demographic and clinical characteristics of the patients are shown in Table 1. The average age of the women included in the study was 33.3 ± 7.9 years, and the median body mass index (BMI) was 24.7 kg/m2 (IQR: 22.9–28.1). TABLE 1. | Parameter | N = 20 | |---|---| | Age | 33.3 ± 7.9 | | BMI (kg/m2) | 24.7 [22.9–28.1] | | Gravida | 0 [0–1] | | Parity | 0 [0–1] | | Irreguler periods n (%) | 4 (20%) | | History of PID n (%) | 2 (10%) | | History of Ectopic pregnancy n (%) | 1 (5%) | | History of pelvic surgery n (%) | 4 (20%) | | History of IVF | 4 (20%) | | Infertility | 1 (5%) | | Pelvic pain | 4 (20%) | | Infertility+ pelvic pain | 15 (75%) | During HyFoSy, the median (range) intraluminal tubal diameter values were 1.3 mm (1.2–1.9) in the isthmus, 1.7 mm (1.5–1.8) in the ampulla, and 2.1 mm (1.7–2.6) in the infundibulum. The intraluminal diameter at the isthmus was similar in tubes with and without hydrosalpinx and did not differ significantly (p = 0.615). In contrast, the intraluminal diameters measured at both the ampullary and infundibular segments were significantly greater in tubes with hydrosalpinx than in those without hydrosalpinx (p = 0.023 and p < 0.01, respectively) (Table 2). TABLE 2. | Variable | Cut‐off | Area under the curve (AUC) | p | Sensitivity | Specificity | |---|---|---|---|---|---| | Isthmus | 1.990 | 0.452 | 0.615 | 12.00% | 100.00% | | Ampulla | 1.845 | 0.717 | 0.023 | 68.00% | 80.00% | | Infundibulum | 2.740 | 0.908 | < 0.001 | 100.00% | 80.00% | Note: Statistically significant p values are shown in bold (p < 0.05). ROC curve analysis demonstrated that the infundibular segment had the highest diagnostic performance for predicting hydrosalpinx (AUC = 0.908), followed by the ampullary segment (AUC = 0.717), whereas the isthmus showed poor discriminatory performance (AUC = 0.452) (Figure 1). The diagnostic performance of HSG and HyFoSy for detecting hydrosalpinx compared with laparoscopic findings is summarized in Tables 3 and 4. HSG demonstrated 88% sensitivity and 73% specificity for the diagnosis of hydrosalpinx, with positive predictive value (PPV) and negative predictive value (NPV) of 84% and 78%, respectively. HyFoSy demonstrated superior diagnostic performance, with 96% sensitivity and 80% specificity, while the PPV and NPV were 88% and 92%, respectively. TABLE 3. | HSG | Hydrosalpinx at laparoscopy | No hydrosalpinx at laparoscopy | Total | |---|---|---|---| | Hydrosalpinx (+) | 22 | 4 | 26 | | Hydrosalpinx (−) | 3 | 11 | 14 | | Total | 25 | 15 | 40 a | Total of 40 tubes evaluated in 20 patients. TABLE 4. | HyFoSy | Hydrosalpinx at laparoscopy | No hydrosalpinx at laparoscopy | Total | |---|---|---|---| | Hydrosalpinx (+) | 24 | 3 | 27 | | Hydrosalpinx (−) | 1 | 12 | 13 | | Total | 25 | 15 | 40 a | Total of 40 tubes evaluated in 20 patients. Agreement with LS was stronger for HyFoSy (κ = 0.78) than for HSG (κ = 0.62), indicating substantial agreement for both techniques but better concordance for HyFoSy. The false‐positive and false‐negative rates were 15% and 21% for HSG and 11% and 7% for HyFoSy, respectively (Figure 2). When tubal patency was evaluated using laparoscopic findings as the reference standard, HSG achieved 71% sensitivity and 90% specificity, whereas HyFoSy demonstrated higher sensitivity (85%) and specificity (96%). The PPV and NPV for HSG were 62% and 93%, respectively, while those for HyFoSy were 85% and 96%, respectively. Diagnostic agreement with LS was also higher for HyFoSy (κ = 0.82) than for HSG (κ = 0.60), reflecting near‐perfect agreement for HyFoSy and substantial agreement for HSG. 4. Discussion In infertility practice, both HSG and HyFoSy are commonly used to evaluate tubal patency, and comparable diagnostic performance has been reported for these two methods [15]. However, for hydrosalpinx, the evidence available in the HyFoSy assessment remains limited [16, 17]. In our prospective cohort, we performed HyFoSy prior to LS as the reference standard in patients diagnosed with hydrosalpinx using HSG and produced preliminary data showing that HyFoSy can reliably identify hydrosalpinx and may serve as a practical alternative to HSG. Large‐scale evidence has shown that HSG provides only moderate diagnostic accuracy in evaluating tubal patency. For example, a meta‐analysis of 20 studies involving 4179 patients reported a sensitivity of 65% and a specificity of 83% for HSG [9]. Similarly, an individual patient data meta‐analysis including seven studies and 4521 women reported a pooled sensitivity of 53% and specificity of 87% for HSG in the detection of tubal pathology. The authors further demonstrated that the diagnostic sensitivity of HSG was higher in women with risk factors for tubal disease than in those without such risk factors [18]. Studies investigating the concordance between HSG and LS have reported a significant degree of agreement for some tubal pathologies; kappa values reached 0.89 for proximal tubal obstruction and remained at a moderate to high level for distal tubal obstruction, hydrosalpinx, and peritubal adhesions (κ = 0.72, 0.68, and 0.65, respectively) [7]. Consistent with these findings, the performance of HSG in our cohort (sensitivity 71%, specificity 90%, κ = 0.60) is in line with values reported in the literature. Several studies have shown that HyFoSy is suitable as a first‐line test for evaluating tubal patency, reporting diagnostic sensitivity and specificity values of up to 87.5% and 100%, respectively [13, 17]. Furthermore, numerous studies have demonstrated that the overall accuracy and effectiveness of HyFoSy are comparable to those of HSG and, in some cases, even superior [15]. The current literature increasingly presents HyFoSy as a robust alternative to HSG in terms of diagnostic accuracy and clinical feasibility [13, 16, 17]. In our study, HyFoSy achieved sensitivity and specificity values of 85% and 96%, respectively, and demonstrated almost perfect agreement with LS (κ = 0.82). These results are highly consistent with previously reported data [15]. The rationale for evaluating the isthmic, ampullary, and infundibular segments separately was based on the known anatomical heterogeneity of the fallopian tube and the tendency of distal tubal obstruction to produce more pronounced dilatation in the ampullary and infundibular regions [2, 3, 5]. To our knowledge, segmental intraluminal tubal diameter measurements obtained during HyFoSy have not previously been systematically evaluated as potential diagnostic markers of hydrosalpinx. Unlike previous studies, our study focused not only on evaluating tubal patency but also on investigating the potential role of HyFoSy in the diagnosis of hydrosalpinx. In addition, we explored whether segmental intraluminal tubal diameter measurements obtained during HyFoSy could help discriminate between tubes with and without hydrosalpinx. We observed that intraluminal tubal diameters measured at the infundibular and ampullary segments were significantly greater in women with hydrosalpinx than in those without hydrosalpinx, whereas measurements at the isthmus level were similar between the two groups (1.31 mm vs. 1.32 mm, p = 0.61; 2.17 mm vs. 1.67 mm, p = 0.02; and 4.83 mm vs. 2.09 mm, p < 0.01, respectively). Based on these measurements, exploratory cut‐off values for hydrosalpinx were identified as 1.84 mm for the ampulla and 2.74 mm for the infundibulum (p = 0.02, and p < 0.001, respectively). These findings are consistent with what is known about the pathophysiology of hydrosalpinx, where distal tubal obstruction leads to progressive dilation of the tube, most prominently in the infundibulum, followed by the ampulla, with the isthmus generally being less affected [3, 5]. However, these values should be interpreted with caution, as they were derived from a relatively small and highly selected patient cohort and therefore should be considered hypothesis‐generating rather than definitive diagnostic thresholds. In our study, HyFoSy has demonstrated a high sensitivity of 96% and moderate specificity of 80% for detecting hydrosalpinx and has shown significant agreement with LS (κ = 0.78). Overall, our findings suggest that HyFoSy may have a potential role not only in the assessment of tubal patency but also in the diagnosis of hydrosalpinx. HyFoSy may be particularly useful in subtle or sonographically occult hydrosalpinx cases that may not be clearly visualized with conventional B‐mode ultrasonography. Future studies directly comparing conventional ultrasonography and HyFoSy may further clarify the incremental diagnostic value of HyFoSy in hydrosalpinx detection. Among the limitations of our study is the inclusion of a relatively small and pre‐selected group of patients diagnosed with hydrosalpinx on HSG who subsequently underwent LS. This may have introduced selection bias and influenced the estimated diagnostic performance of HyFoSy. Furthermore, although all HyFoSy examinations and intraluminal tubal diameter measurements were performed by the same surgical team using a standardized protocol, the reproducibility of these measurements across different observers remains to be established. Despite these limitations, laparoscopic confirmation was available for all patients, providing a uniform reference standard and strengthening the diagnostic comparisons performed in this study. HyFoSy appears to be a practical, well‐tolerated, and radiation‐free method for the evaluation of hydrosalpinx in women undergoing infertility assessment. The findings of this prospective study support the potential utility of HyFoSy in the diagnosis of hydrosalpinx and suggest that segmental intraluminal tubal diameter measurements may provide additional diagnostic information. However, given the relatively small and selected study population, larger prospective studies are needed to validate these findings and to determine their applicability in routine clinical practice. Author Contributions Müge Keskin: data curation, writing – original draft. Sevim Dinçer Cengiz: methodology, supervision. Didem Demir: conceptualization, methodology, data curation, writing – original draft. Ayşe Gizem Yıldız: writing – original draft, conceptualization. Aslı Yarcı Gürsoy: data curation. Recai Pabuçcu: data curation, supervision. Gamze Sinem Yücel: writing – review and editing, conceptualization, methodology, supervision. Funding The authors have nothing to report. Disclosure The authors have nothing to report. Ethics Statement The study protocol was approved by the Ufuk University Faculty of Medicine Clinical Research Ethics Committee (Decision No: 20200708/8). Consent Written informed consent was obtained from all participants included in the study. Conflicts of Interest The authors declare no conflicts of interest. Data Availability Statement Due to institutional regulations and ethical considerations, the data generated and/or analyzed during this study are not publicly available in order to protect participants' privacy and confidentiality. In addition, participants did not provide consent for public data sharing. Data may be available from the corresponding author upon reasonable request, provided that appropriate permission is obtained from the relevant institutional authority and ethics committee.

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Data may be available from the corresponding author upon reasonable request, provided that appropriate permission is obtained from the relevant institutional authority and ethics committee.