Hydrosalpinx treatment before in‐vitro fertilization: systematic review and network meta‐analysis

F Pérez‐Milán; M Caballero‐Campo; M Carrera‐Roig; E Moratalla‐Bartolomé; J A Domínguez‐Arroyo; J L Alcázar‐Zambrano; L Alonso‐Pacheco; J A Carugno; the Spanish Fertility Society Special Interest Group on Organic Reproductive Disorders

doi:10.1002/uog.27697

. 2025 Jan 26;65(4):414–426. doi: 10.1002/uog.27697

Hydrosalpinx treatment before in‐vitro fertilization: systematic review and network meta‐analysis

F Pérez‐Milán ^1,^2,^3,^#,^✉, M Caballero‐Campo ^1,^2,^#, M Carrera‐Roig ⁴, E Moratalla‐Bartolomé ⁵, J A Domínguez‐Arroyo ^6,⁷, J L Alcázar‐Zambrano ^8,⁹, L Alonso‐Pacheco ¹⁰, J A Carugno ¹¹; the Spanish Fertility Society Special Interest Group on Organic Reproductive Disorders

PMCID: PMC11961103 PMID: 38764191

ABSTRACT

Objective

To compare the safety and effectiveness of different methods, both ablative and non‐ablative, to treat hydrosalpinx in infertile patients before in‐vitro fertilization embryo transfer (IVF‐ET) via a systematic review and network meta‐analysis (NMA).

Methods

A structured literature search was conducted in common citation databases. Eligibility criteria included peer‐reviewed randomized controlled trials (RCTs) or cohort studies comparing the effectiveness and/or safety of different hydrosalpinx treatments, including salpingectomy, laparoscopic proximal tubal occlusion (LTO), insertion of an intratubal device (ITD), ultrasound‐guided aspiration, sclerotherapy and expectant management. Primary outcomes were live birth, ongoing pregnancy and clinical pregnancy. Miscarriage, ectopic pregnancy and procedural complications were considered as secondary outcomes. The main NMA included only RCTs, while observational studies were included in a secondary aggregate NMA. Pooled effects were summarized as odds ratios (ORs) with 95% CI for direct and indirect comparisons, derived from random‐effects models. Imprecision of NMA estimates was assessed by comparison of their 95% CIs with predefined thresholds for effect size considered to represent clinical relevance (OR < 0.9 or >1.1). Heterogeneity for NMA findings was estimated using the variance of the distribution of the underlying treatment effects (τ²), expressed as a 95% prediction interval. Surface under the cumulative ranking curve (SUCRA) was used to predict relative treatment rankings for each outcome.

Results

The main analysis included nine RCTs, while an additional 17 observational studies were incorporated into the aggregate analysis. The NMA of RCTs revealed no significant differences in live birth rate between hydrosalpinx treatment methods, with LTO achieving the highest SUCRA value (0.9). Salpingectomy and ultrasound‐guided aspiration significantly increased the ongoing pregnancy rate compared with no treatment (OR, 4.35 (95% CI, 1.70–11.14) and 2.80 (95% CI, 1.03–7.58), respectively), with salpingectomy having the highest SUCRA value (0.9). Clinical pregnancy rate was significantly higher following salpingectomy (OR, 2.24 (95% CI, 1.30–3.86)) and LTO (OR, 2.55 (95% CI, 1.20–5.51)) compared with no treatment, despite some heterogeneity; LTO had the highest SUCRA value (0.8). NMA showed no significant differences in secondary outcomes between treatments. Aggregate NMA indicated that sclerotherapy significantly increased the live birth rate compared with no treatment. Higher ongoing pregnancy rate was observed in patients treated with salpingectomy, ultrasound‐guided aspiration and LTO compared to untreated patients, with salpingectomy having the highest SUCRA value (0.9). Except for ITD insertion, all interventions increased the clinical pregnancy rate compared with no treatment. LTO had a greater effect on clinical pregnancy rate compared to ultrasound‐guided aspiration, with no significant differences in other pairwise comparisons. NMA ranked LTO as the most effective treatment for increasing the clinical pregnancy rate and reducing the miscarriage rate, while sclerotherapy was deemed safer with regard to the ovarian response to IVF stimulation.

Conclusions

This NMA fails to support the effectiveness of any hydrosalpinx treatment to improve the live birth rate following IVF‐ET, although the beneficial effect of salpingectomy and ultrasound‐guided aspiration on ongoing pregnancy rate and of salpingectomy and LTO on clinical pregnancy rate reinforces current recommendations. Based on the aggregated analysis, sclerotherapy could be an effective alternative to conventional laparoscopic techniques, with a favorable safety profile. © 2024 The Author(s). Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.

Keywords: aspiration, Fallopian tube, hydrosalpinx, infertility, interventional ultrasonography, in‐vitro fertilization, IVF, salpingectomy, sclerotherapy, tubal obstruction, tubal occlusion

INTRODUCTION

Hydrosalpinx is a pathological condition of the Fallopian tubes resulting from an inflammatory condition or pelvic adhesions. It is characterized by a transmural tubal lesion accompanied by metaplastic changes of the endosalpinx, stromal fibrosis, sclerosis, formation of serosal adhesions, fimbrial agglutination and accumulation of serous fluid in the tubal lumen ¹ . These changes transform the Fallopian tube into a fusiform or folded sack, which often communicates with the uterine cavity, with spillage of intratubal fluid.

The presence of sonographically detectable hydrosalpinx decreases the success rate of in‐vitro fertilization (IVF) ² , ³ , ⁴ , ⁵ . This effect may be mediated by pro‐inflammatory substances released from the lesion ⁶ , which have an embryotoxic effect ⁷ , ⁸ , ⁹ . Moreover, hydrosalpinx fluid in the endometrial cavity may decrease endometrial receptivity and impair embryo implantation via a mechanical flushing effect ¹⁰ .

Salpingectomy was the first treatment with proven effectiveness to minimize the negative effects of hydrosalpinx on reproductive outcome ¹¹ , ¹² . Concerns about the risk of compromising ovarian vascularization have been raised, especially in cases of complex resection ¹³ , ¹⁴ , ¹⁵ . Furthermore, salpingectomy incurs a risk of surgical injury to other pelvic organs or may not be feasible to perform, particularly in cases with distorted anatomy due to extensive pelvic adhesions or other surgical comorbidity. These limitations generated interest in finding safer alternatives to salpingectomy, such as laparoscopic proximal tubal occlusion (LTO), which requires a less extensive, shorter and safer surgical intervention, and has a similar beneficial effect on IVF outcome ¹⁶ , ¹⁷ , ¹⁸ . A number of non‐ablative procedures have also been developed in recent years, including hysteroscopic insertion of an intratubal device (ITD) ¹⁹ , ²⁰ , ²¹ , ²² and ultrasound‐guided aspiration of hydrosalpinx fluid, with or without chemical sclerotherapy ²³ , ²⁴ , ²⁵ . These approaches have the potential advantages of being safer, less invasive, better tolerated and more cost‐effective, although studies to support their use in clinical practice are scarce, poorly designed and statistically underpowered.

The aim of this study was to update the knowledge base on the treatment of infertile women diagnosed with hydrosalpinx before undergoing IVF embryo transfer (ET) ²⁶ , considering recent evidence from randomized controlled trials (RCTs) and observational studies, which have started to include less invasive and potentially safer procedures. We applied network meta‐analysis (NMA) methodology to obtain new evidence on the impact of treatment methods on reproductive outcome based on complementary, indirect comparisons not provided by available studies.

METHODS

This was a systematic review and NMA of the effect of hydrosalpinx treatments on reproductive outcome following IVF‐ET. The study protocol was registered in the PROSPERO database (registration number: CRD42021227983).

Eligibility criteria

We included studies that satisfied the following criteria: (1) peer‐reviewed RCT or cohort study (prospective or retrospective); (2) study population consisting of infertile women undergoing IVF‐ET; (3) comparison of effectiveness and/or safety of different hydrosalpinx treatments (salpingectomy, LTO, ITD insertion, ultrasound‐guided sclerotherapy and/or ultrasound‐guided aspiration) or between a treatment and expectant management; (4) reported results for at least one of our outcomes of interest; (5) low or moderate risk of bias for observational studies according to validated assessment scales (any risk of bias was permitted for RCTs); (6) results expressed in the appropriate terms to be summarized in a quantitative synthesis; (7) follow‐up time of sufficient length to detect the assessed outcomes; and (8) articles published in English, French, German or Spanish.

Exclusion criteria were: (1) non‐comparative studies; (2) studies analyzing non‐infertile patients; (3) studies assessing hydrosalpinx treatment options in patients undergoing assisted reproductive techniques aside from IVF; (4) observational studies deemed to have a high risk of bias; and (5) studies without complete data for analysis.

Literature search and selection of studies

A systematic review of primary studies was carried out in the following databases: MEDLINE, EMBASE, Web of Science, Cochrane Central Register of Controlled Trials (CENTRAL) and ClinicalTrials.gov. The search strategy (Appendix S1) was adapted to the syntax requirements for each database. No time restrictions were applied for the literature search. Reference lists of the identified studies were searched manually to identify additional papers not detected by the structured searches.

Identified studies were screened initially by title and abstract by two different authors. Disagreements regarding suitability for full‐text review were resolved by discussion with a third author. Prespecified eligibility criteria were applied to the studies selected for full‐text evaluation. Risk of bias in RCTs was assessed using the Cochrane Collaboration RoB 2 tool ²⁷ . For cohort studies, risk of bias was assessed using the Newcastle–Ottawa Scale ²⁸ and qualified according to the standards of the United States Agency for Healthcare Research and Quality (AHRQ). All RCTs, and observational studies scoring ≥6 on the Newcastle–Ottawa Scale and corresponding to good or fair quality according to AHRQ standards, were included. The study selection process was conducted in accordance with the PRISMA extension statement for NMA ²⁹ .

Data collection

Data extracted from the selected studies included the first author, year of publication, study design, study period and setting, inclusion and exclusion criteria, definitions and numbers of exposed and control patients, outcomes considered, absolute frequencies of events and controlling for confounders. The data extraction process was performed by one author using a predefined form and reviewed by a second author. Results were inputted into the data extraction form as published; if necessary, additional calculations were performed using the data provided in the study. Disagreements regarding data extraction were resolved by consensus between all authors. In the case of overlapping samples between more than one study, the study with the largest number of observations was included.

We considered the following management options: salpingectomy, LTO, ITD insertion, ultrasound‐guided aspiration, ultrasound‐guided sclerotherapy and expectant management. Unilateral and bilateral procedures were considered. Our primary outcomes were live birth rate, clinical pregnancy rate and ongoing pregnancy rate, defined according to the International Glossary on Infertility and Fertility Care ³⁰ . Secondary outcomes included miscarriage rate and ectopic pregnancy rate (reproductive outcomes), in addition to the number of retrieved oocytes, gonadotropin dose used during ovarian stimulation, variation in serum level of anti‐Müllerian hormone (AMH) (before vs after procedure) and procedural complications (abdominal wall or pelvic infection, fluid re‐accumulation, ITD migration and need for repeat intervention or additional surgery).

Network geometry

Network diagrams were constructed for all outcomes, in which treatment techniques and expectant management were represented by nodes and head‐to‐head comparisons were represented by connecting axes. The color of the sectors within the nodes represents the distribution by risk of bias of the contributing studies. The diameter of the nodes and the thickness of the connecting axes between the nodes were proportional to the number of patients and studies, respectively, in each comparison. The connectivity of each network diagram was described qualitatively.

Assessment of transitivity

The comparability of study populations and treatments was assessed qualitatively on the basis of the characteristics of the patients and procedures reported by the studies (Table S1). If transitivity could not be assumed, it was assessed by statistical comparisons of potential effect modifiers, if five or more direct comparisons were available.

Statistical analysis

The main analysis considered only RCTs. The effects of network comparisons were summarized as odds ratio (OR) with 95% CI for binary outcomes and as standardized mean difference (SMD) with 95% CI for continuous outcomes. The imprecision of NMA estimates for primary outcomes was determined by comparison of the 95% CI with predefined thresholds for effect size considered to represent clinical relevance (OR < 0.9 or > 1.1 for dichotomous variables and 1 SMD for continuous variables). Based on these comparisons, concern about imprecision was classified as low, intermediate or high using the Confidence in Network Meta‐Analysis (CINeMA) tool ³¹ , ³² .

Conventional pairwise meta‐analysis based on a random‐effects model was performed to assess direct comparisons between treatments. We also fitted a random‐effects model to estimate the OR or SMD, as appropriate, from NMA comparisons. League tables were used to obtain the results of NMA comparisons for each outcome. Surface under the cumulative ranking curve (SUCRA) values were used to rank competing treatments. SUCRA expresses the estimated likelihood for each intervention to be the best procedure with regard to the analyzed outcome.

Inconsistency between direct and indirect comparisons was analyzed at two levels. An overall analysis was performed by means of a specific multivariate meta‐analysis based on a random‐effects model, providing a chi‐square value to test the null hypothesis of consistency. Secondly, per‐comparison inconsistency analysis was performed by testing the significance of the difference between direct and indirect estimations of effect size in each comparison loop.

Bias across the studies was summarized for NMA using the CINeMA framework ³¹ , ³² , based on a combination of individual judgment of risk of bias and its relative contribution to NMA estimates. Cohort studies with a score of 6 or 7 on the Newcastle–Ottawa Scale and RCTs classified as having some concern of bias by the RoB 2 tool were considered by the CINeMA tool to have a moderate risk of bias ³¹ , ³² . STATA software version 17.0 (StataCorp, College Station, TX, USA), supplemented with the mvmeta package ³³ , was used for NMA analysis, while the free software Review Manager version 5.3 from the Cochrane Collaboration ³⁴ provided the direct comparisons.

Reporting bias and small‐study effects were assessed by analyzing the symmetry of per‐comparison funnel plots, in which the x‐axis represents the estimated size of effect (on a logarithmic scale) and the y‐axis expresses the difference between standard error for each study and the standard error of the pooled estimate. The network graphs package for STATA ³⁵ , ³⁶ was used to generate graphical representations of bias analysis. These risks were classified as low, intermediate or high for each outcome. The risk of bias caused by indirect contributions from the NMA was analyzed using the CINeMA framework approach, which combines the individual score on indirectness of each study with its relative contribution to each comparison ³¹ , ³² .

For the direct‐comparison meta‐analysis, statistical heterogeneity was estimated using the I ² statistic, which was graded according to Higgins' criteria ³⁷ . Heterogeneity for NMA findings was estimated using the variance of the distribution of the underlying treatment effects (τ²), expressed as a 95% prediction interval, which shows where the true effect of a theoretical new study similar to the available studies is expected to lie. The judgment about the heterogeneity of NMA estimates was made by considering the extension of the 95% prediction interval into predefined intervals for a clinically relevant effect size.

According to CINeMA methodology, assessment of within‐study bias, reporting bias, indirectness, imprecision, heterogeneity and incoherence (as an expression of inconsistency) was summarized in a synoptic table designed according to the Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach. This table also contained the final judgment on the confidence rating of the estimates.

Additional analyses aggregating the findings of RCTs and observational studies were performed, applying the same methodology as that described for the main analysis.

RESULTS

Study selection

The process of study identification and selection is summarized in Figure 1. Of 43 full‐text articles retrieved from databases/registers that were assessed, 26 ¹¹ , ¹⁴ , ¹⁶ , ¹⁸ , ²³ , ²⁴ , ³⁸ , ³⁹ , ⁴⁰ , ⁴¹ , ⁴² , ⁴³ , ⁴⁴ , ⁴⁵ , ⁴⁶ , ⁴⁷ , ⁴⁸ , ⁴⁹ , ⁵⁰ , ⁵¹ , ⁵² , ⁵³ , ⁵⁴ , ⁵⁵ , ⁵⁶ , ⁵⁷ studies were included and 17 ¹⁷ , ²⁵ , ⁵⁸ , ⁵⁹ , ⁶⁰ , ⁶¹ , ⁶² , ⁶³ , ⁶⁴ , ⁶⁵ , ⁶⁶ , ⁶⁷ , ⁶⁸ , ⁶⁹ , ⁷⁰ , ⁷¹ , ⁷² were excluded. The main characteristics of the included studies are summarized in Table S1. Excluded studies and reasons for exclusion are detailed in Table S2. Assessment of the risk of bias for RCTs and observational studies using the RoB 2 tool and Newcastle–Ottawa Scale, respectively, is presented in Appendix S2.

Flowchart summarizing selection of studies for systematic review and network meta‐analysis. *Only articles published in English, French, German or Spanish were included.

The primary analysis included nine RCTs ¹⁸ , ³⁸ , ³⁹ , ⁴⁰ , ⁴¹ , ⁴² , ⁴³ , ⁴⁴ , ⁴⁵ . The results of individual RCTs for each outcome are presented in Appendix S3. The additional analyses also included 14 retrospective cohort studies ¹¹ , ¹⁴ , ¹⁶ , ²³ , ²⁴ , ⁴⁶ , ⁴⁷ , ⁴⁸ , ⁴⁹ , ⁵⁰ , ⁵¹ , ⁵² , ⁵³ , ⁵⁴ and three prospective cohort studies ⁵⁵ , ⁵⁶ , ⁵⁷ .

Network geometry

Direct comparison of treatments with regard to live birth rate was reported by only four RCTs ³⁹ , ⁴³ , ⁴⁴ , ⁴⁵ and included pairwise comparisons of salpingectomy with LTO, ITD insertion and no treatment, which formed a network with low connectivity (Figure 2a). Ongoing pregnancy was analyzed by five RCTs ¹⁸ , ³⁸ , ⁴¹ , ⁴² , ⁴³ . The network for this outcome is made up of six direct pairwise comparisons, four of which involve salpingectomy, and includes only two comparisons for ultrasound‐guided aspiration and none for sclerotherapy (Figure 2b). NMA provided indirect estimates for four pairwise comparisons not analyzed directly for ongoing pregnancy. For clinical pregnancy, salpingectomy was again the most frequently compared treatment in the included RCTs ¹⁸ , ³⁸ , ³⁹ , ⁴⁰ , ⁴¹ , ⁴² , ⁴³ , ⁴⁴ , ⁴⁵ . Ultrasound‐guided treatments were represented only by ultrasound‐guided aspiration, which was compared with salpingectomy ⁴² and with no treatment ⁴⁰ , ⁴¹ (Figure 2c). For this outcome, NMA generated four indirect estimations of comparative treatment effects not analyzed directly by available studies. Network maps for secondary outcomes are presented in Appendix S4.

Network diagrams for comparisons between treatment techniques for hydrosalpinx with regard to reproductive outcome following *in‐vitro* fertilization embryo transfer: (a) live birth; (b) ongoing pregnancy; and (c) clinical pregnancy. Color of sectors within nodes represents distribution by risk of bias of included studies (red, high risk; yellow, moderate risk; green, low risk). Diameter of nodes is proportional to pooled sample size. Thickness of connecting axes is proportional to the number of studies in each comparison. ITD, intratubal device; LTO, laparoscopic proximal tubal occlusion; No treat, no treatment; Salp, salpingectomy; US asp, ultrasound‐guided aspiration.

Assessment of transitivity

Transitivity of the included studies was assumed considering the similarity of the study characteristics, populations and applied interventions.

Risk of bias within studies

Risk‐of‐bias assessment of the included RCTs using the RoB 2 tool is shown in Appendix S2. Risk of bias was rated as low in two studies ⁴⁰ , ⁴¹ , moderate in five studies ¹⁸ , ³⁸ , ³⁹ , ⁴³ , ⁴⁴ and high in two studies ⁴² , ⁴⁵ . The contribution of studies with a moderate risk of bias to NMA estimates for live birth was >70% for all NMA comparisons (Appendix S5). For ongoing pregnancy, studies with a low risk of bias contributed the majority of data only for the comparison of ultrasound‐guided aspiration vs no treatment, while studies with a high risk of bias contributed >70% of data to the comparison of salpingectomy vs ultrasound‐guided aspiration. For clinical pregnancy, most of the NMA comparisons were based on data from studies with a moderate risk of bias, with two exceptions: the comparison of salpingectomy vs ultrasound‐guided aspiration, for which studies with a high risk of bias contributed >50%, and the comparison of ultrasound‐guided aspiration vs no treatment, for which studies with a low risk of bias contributed >50%.

Assessment of inconsistency

Inconsistency could not be statistically tested for the live birth NMA, as there were no sources of inconsistency. Statistical tests for overall and per‐comparison inconsistency for ongoing and clinical pregnancy were not significant (Table 1). Results of inconsistency analysis for secondary outcomes were not significant, with the exception of ectopic pregnancy, for which inconsistency analysis was unfeasible due to there being no sources of inconsistency, and gonadotropin dose, for which inconsistency analysis was significant (Table S3).

Table 1.

Direct comparisons and indirect comparisons estimated by network meta‐analysis of hydrosalpinx treatment effects for primary outcomes reported by nine randomized controlled trials

					Network meta‐analysis
	Direct comparison				Test for inconsistency
Outcome/comparison	Studies (n)	OR (95% CI)	Events/total (per treatment)	I ² (%)	Overall	Per comparison	OR (95% CI)
Live birth^*					NA
Salpingectomy vs:
No treatment	1	1.82 (0.89–3.71)	30/110 vs 14/82	—		NA	1.82 (0.89–3.71)
LTO	2	0.76 (0.43–1.33)	32/112 vs 39/113	—		NA	0.76 (0.43–1.33)
ITD	1	2.37 (0.81–6.98)	16/32 vs 8/27	—		NA	2.38 (0.81–6.98)
US aspiration	0	—	—	—		—	—
Sclerotherapy	0	—	—	—		—	—
LTO vs:
No treatment	0	—	—	—		—	2.40 (0.97–5.97)
ITD	0	—	—	—		—	3.13 (0.92–10.59)
US aspiration	0	—	—	—		—	—
Sclerotherapy	0	—	—	—		—	—
ITD vs:
No treatment	0	—	—	—		—	0.76 (0.21–2.79)
US aspiration	0	—	—	—		—	—
Sclerotherapy	0	—	—	—		—	—
US aspiration vs:
No treatment	0	—	—	—		—	—
Sclerotherapy	0	—	—	—		—	—
Sclerotherapy vs:
No treatment	0	—	—	—		—	—
Ongoing pregnancy^*					NS
Salpingectomy vs:
No treatment	2	4.19 (0.80–21.90)	36/87 vs 7/47	52		NS	4.35 (1.70–11.14)
LTO	1	1.61 (0.71–3.65)	23/49 vs 17/48	—		NS	1.42 (0.49–4.16)
ITD	1	2.92 (1.00–8.49)	19/22 vs 9/27	—		NS	2.92 (0.80–10.66)
US aspiration	1	1.83 (0.92–3.63)	20/80 vs 19/80	—		NS	1.55 (0.65–3.71)
Sclerotherapy	0	—	—	—		—	—
LTO vs:
No treatment	1	7.68 (0.93–63.53)	17/48 vs 1/15	—		NS	3.05 (0.79–11.75)
ITD	0	—	—	—		—	2.05 (0.38–10.99)
US aspiration	0	—	—	—		—	1.09 (0.28–4.21)
Sclerotherapy	0	—	—	—		—	—
ITD vs:
No treatment	0	—	—	—		—	1.49 (0.30–7.37)
US aspiration	0	—	—	—		—	0.53 (0.11–2.53)
Sclerotherapy	0	—	—	—		—	—
US aspiration vs:
No treatment	1	3.69 (1.23–11.06)	15/54 vs 5/53	—		NS	2.80 (1.03–7.58)
Sclerotherapy	0	—	—	—		—	—
Sclerotherapy vs:
No treatment	0	—	—	—		—	—
Clinical pregnancy^*					NS
Salpingectomy vs:
No treatment	3	2.01 (0.97–4.17)	78/218 vs 31/146	40		NS	2.24 (1.30–3.86)
LTO	3	0.93 (0.54–1.60)	58/161 vs 61/161	26		NS	0.88 (0.50–1.52)
ITD	1	2.42 (0.85–6.92)	20/32 vs 11/24	—		NS	2.42 (0.75–7.83)
US aspiration	1	1.76 (0.90–3.41)	32/80 vs 22/80	—		NS	1.23 (0.64–2.36)
Sclerotherapy	0	—	—	—		—	—
LTO vs:
No treatment	1	4.64 (0.94–22.89)	28/48 vs 2/15	—		NS	2.55 (1.20–5.51)
ITD	0	—	—	—		NS	2.76 (0.75–10.07)
US aspiration	0	—	—	—		NS	1.40 (0.60–3.26)
Sclerotherapy	0	—	—	—		—	—
ITD vs:
No treatment	0	—	—	—		NS	0.92 (0.25–3.37)
US aspiration	0	—	—	—		NS	0.50 (0.13–1.94)
Sclerotherapy	0	—	—	—		—	—
US aspiration vs:
No treatment	2	2.60 (1.23–5.50)	27/86 vs 13/87	0		NS	1.82 (0.95–3.50)
Sclerotherapy	0	—	—	—		—	—
Sclerotherapy vs:
No treatment	0	—	—	—		—	—

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Per cycle. ITD, intratubal device; LTO, laparoscopic proximal tubal occlusion; NA, estimation not available because there is no source of inconsistency for this comparison; NS, not significant; OR, odds ratio; US, ultrasound‐guided.

Synthesis of results

Main analysis: primary outcomes

Live birth. No significant differences were observed in the effect of hydrosalpinx treatments on the live birth rate, either by direct comparison or by NMA estimation, although NMA was not conclusive because inconsistency testing was not feasible (Table 1 and Figure 3a). The heterogeneity of the NMA comparisons could not be calculated for the same reason. The rankogram found LTO to be the treatment method with the highest SUCRA value (0.9; mean rank, 1.2) (Figure 4a).

Estimated effect size for comparisons between treatment techniques for hydrosalpinx with regard to reproductive outcome following *in‐vitro* fertilization embryo transfer: (a) live birth; (b) ongoing pregnancy; and (c) clinical pregnancy. Plots show pooled odds ratios (OR, ) with 95% CI () and 95% prediction intervals (95% PI, ), and red dashed vertical lines show the limits of the predefined range for clinically relevant effect (defined as OR < 0.9 or > 1.1). ITD, intratubal device; LTO, laparoscopic proximal tubal occlusion; No treat, no treatment; Salp, salpingectomy; US asp, ultrasound‐guided aspiration.

Inline graphic — Estimated effect size for comparisons between treatment techniques for hydrosalpinx with regard to reproductive outcome following *in‐vitro* fertilization embryo transfer: (a) live birth; (b) ongoing pregnancy; and (c) clinical pregnancy. Plots show pooled odds ratios (OR, ) with 95% CI () and 95% prediction intervals (95% PI, ), and red dashed vertical lines show the limits of the predefined range for clinically relevant effect (defined as OR < 0.9 or > 1.1). ITD, intratubal device; LTO, laparoscopic proximal tubal occlusion; No treat, no treatment; Salp, salpingectomy; US asp, ultrasound‐guided aspiration.

Rankograms, with values for estimated surface under cumulative ranking curve (SUCRA) and mean rank, for treatment methods for hydrosalpinx with regard to reproductive outcome following *in‐vitro* fertilization embryo transfer: (a) live birth; (b) ongoing pregnancy; and (c) clinical pregnancy. ITD, intratubal device; LTO, laparoscopic proximal tubal occlusion; No treat, no treatment; Salp, salpingectomy; US asp, ultrasound‐guided aspiration.

Ongoing pregnancy. The comparison of ultrasound‐guided aspiration vs no treatment was the only direct comparison to show a significant difference in their effects on ongoing pregnancy rate. According to NMA, salpingectomy and ultrasound‐guided aspiration were associated with a significantly higher rate of ongoing pregnancy compared to no treatment (OR, 4.35 (95% CI, 1.70–11.14) and 2.80 (95% CI, 1.03–7.58), respectively) (Table 1 and Figure 3b). Salpingectomy was the treatment method with the highest SUCRA value (0.9; mean rank, 1.4) (Figure 4b). It was only possible to estimate the heterogeneity of direct comparisons for the comparison of salpingectomy vs no treatment (I ² = 52%). Heterogeneity of NMA comparisons was low because the confidence and prediction intervals extended in the same direction beyond the limits of the interval representing a clinically relevant effect on both sides, with the exception of ultrasound‐guided aspiration vs no treatment, for which there were major concerns about heterogeneity (Figure 3b).

Clinical pregnancy. Direct comparisons between active treatments identified no significant difference in their effects on clinical pregnancy, while direct comparisons between each active treatment method and expectant management revealed a significant difference only for ultrasound‐guided aspiration (OR, 2.60 (95% CI, 1.23–5.50)) (Table 1). NMA estimated a significant beneficial effect of salpingectomy (OR, 2.24 (95% CI, 1.30–3.86)) as well as for LTO (OR, 2.55 (95% CI, 1.20–5.51)) compared with no treatment. Both comparisons were affected by some degree of heterogeneity (Figure 3c). The rankogram classified LTO as the intervention with the highest SUCRA value (0.8; mean rank, 1.6) (Figure 4c).

Main analysis: secondary outcomes

Miscarriage. This outcome was reported by eight randomized clinical trials ¹⁸ , ³⁹ , ⁴⁰ , ⁴¹ , ⁴² , ⁴³ , ⁴⁴ , ⁴⁵ (Appendix S4). No significant differences were identified when comparing the treatments directly or by NMA (Table S3). Ranking of treatment methods determined LTO to be the intervention with the highest SUCRA value (0.8; mean rank, 1.8). The degree of heterogeneity affecting most direct comparisons was not estimable due to the low number of available studies. For all NMA comparisons, heterogeneity was classified as high.

Ectopic pregnancy. Five RCTs reported on ectopic pregnancy, comparing five treatment options^{18,54–56,58} (Appendix S4). No significant differences were detected by direct pairwise comparisons or by NMA estimations (Table S3). Ultrasound‐guided aspiration had the highest SUCRA value (0.7; mean rank, 2.7). Heterogeneity was low or not estimable for all direct comparisons. For NMA estimations, heterogeneity was low.

Gonadotropin dose. Gonadotropin dose was analyzed by seven RCTs ¹⁸ , ³⁸ , ³⁹ , ⁴⁰ , ⁴¹ , ⁴² , ⁴⁵ , which provided five direct comparisons between four management strategies (Appendix S4). The statistical test for overall inconsistency was significant (P < 0.001), such that indirect estimates via NMA were not feasible (Table S3).

Number of retrieved oocytes. Seven RCTs provided five direct comparisons of the effect of four management strategies on the number of oocytes obtained by ovarian stimulation for IVF^{18,53–57,59} (Appendix S4). No significant differences between treatment methods were identified by direct or NMA‐derived comparisons (Table S3). Expectant management was ranked as the option with the highest SUCRA value (0.8; mean rank, 1.6). Heterogeneity was not estimable for most direct comparisons, whereas heterogeneity of NMA comparisons was estimated as low.

Serum AMH variation. The decline in serum AMH levels (before vs after procedure) was significantly greater in patients treated with salpingectomy compared to those treated with LTO (OR, 6.25 (95% CI, 2.38–10.13); I ² = 95%), based on a direct comparison performed by two RCTs ⁴⁴ , ⁴⁵ . NMA was not feasible as only these two studies were available.

Procedural complications. Four types of complication were described by the included RCTs: infection of the abdominal wall or pelvic cavity ⁴⁰ , ⁴¹ , ⁴² , ⁴³ , migration of the ITD ⁴³ , reaccumulation of fluid ²⁴ , ⁴² , ⁵³ and need for repeat intervention or additional surgery (due to failure of the first‐choice procedure) ³⁹ . NMA was considered exclusively for infection and need for repeat intervention or additional surgery, since they were potential complications of all treatments (Table S3 and Appendix S4). However, most comparisons for infection were performed by one study, generating two disconnected subnetworks and rendering NMA unfeasible. No significant differences between treatments were revealed by the two available direct comparisons. Need for repeat intervention or additional surgery was reported by only one RCT ³⁹ , which compared salpingectomy with expectant management and found no significant difference (OR, 2.30 (95% CI, 0.09–57.11)).

Aggregated analysis: primary outcomes

Live birth. Sclerotherapy vs no treatment was the only comparison that showed a significant beneficial effect on live birth rate, according to both direct comparison (OR, 4.60 (95% CI, 1.71–12.43)) and that derived from NMA (OR, 4.60 (95% CI, 1.21–17.46)), using data from both RCTs and cohort studies (Appendix S7 and Table S4). Heterogeneity of NMA comparisons was low, with the exception of that between sclerotherapy and no treatment. Sclerotherapy had the highest SUCRA value (0.9; mean rank, 1.6).

Ongoing pregnancy. Compared with untreated patients, the estimated ongoing pregnancy rate was higher in patients treated with salpingectomy (OR, 3.12 (95% CI, 1.95–4.99); I ² = 1% and 3.35 (95% CI, 2.12–5.12) for direct and NMA‐estimated comparisons, respectively) and ultrasound‐guided aspiration (OR, 2.87 (95% CI, 1.10–7.49); I ² = 42% and 2.16 (95% CI, 1.28–3.65) for direct and NMA‐estimated comparisons, respectively) (Appendix S7 and Table S4). The effect of LTO on ongoing pregnancy rate, compared with no treatment, was non‐significant on direct comparison (OR, 7.68 (95% CI, 0.93–63.53)) but significant on NMA (OR, 2.46 (95% CI, 1.11–5.43)). Insertion of an ITD did not improve the ongoing pregnancy rate compared with no treatment on NMA (OR, 1.00 (95% CI, 0.42–2.39)). Salpingectomy and LTO led to greater improvement in ongoing pregnancy rate than ITD insertion, based on both direct and indirect comparisons. NMA did not provide indirect estimations of the effect of sclerotherapy on this outcome. Rankogram analysis assigned the highest SUCRA value to salpingectomy (0.9; mean rank, 1.2).

Clinical pregnancy. Direct comparisons of salpingectomy (OR, 1.99 (95% CI, 1.36–2.93); I ² = 16%), LTO (OR, 8.83 (95% CI, 2.35–33.11); I ² = 23%) and ultrasound‐guided aspiration (OR, 1.97 (95% CI, 1.22–3.19); I ² = 0%) with no treatment‐identified significant effects on clinical pregnancy rate (Table S4). Regarding direct comparisons between active treatment methods, only salpingectomy vs ultrasound‐guided aspiration showed a significant effect on clinical pregnancy rate (OR, 2.18 (95% CI, 1.41–3.34); I ² = 0%). In contrast, NMA found significant effects for pairwise comparisons between each active management strategy and no treatment, with the exception of ITD insertion. The only comparison between active treatment methods that was significant for clinical pregnancy rate on NMA was that of LTO vs ultrasound‐guided aspiration (OR, 2.04 (95% CI, 1.05–3.97)). NMA ranked LTO as the treatment with the highest SUCRA value (0.9; mean rank, 1.5).

Aggregate analysis: secondary outcomes

Miscarriage. Based on indirect comparisons obtained by the NMA, both salpingectomy and LTO significantly reduced the odds of miscarriage compared with no treatment (OR, 0.32 (95% CI, 0.17–0.59) and 0.26 (95% CI, 0.08–0.85), respectively) (Appendix S7 and Table S5). Salpingectomy vs ultrasound‐guided aspiration was the only head‐to‐head comparison of active treatments in which a significant reduction in miscarriage rate was detected (OR, 0.37 (95% CI, 0.17–0.82)). NMA analysis identified LTO as the intervention with the highest SUCRA value (0.8; mean rank, 1.8).

Ectopic pregnancy. Direct and NMA‐derived estimates showed no significant effects on the rate of ectopic pregnancy in the pairwise comparisons of the different active treatment methods vs expectant management, or by means of pairwise comparisons between active treatment methods (Appendix S7 and Table S5).

Gonadotropin use. No significant differences were detected between treatment methods in the dose of gonadotropins consumed either by direct or indirect comparison (Appendix S7 and Table S5). The highest SUCRA value corresponded to sclerotherapy (0.7; mean rank, 2.7).

Number of retrieved oocytes. ITD insertion was associated with fewer retrieved oocytes compared to each of the other treatments (Appendix S7 and Table S5). Sclerotherapy was the treatment method with highest SUCRA value on rankogram analysis (0.8; mean rank, 1.8).

Serum AMH variation. Salpingectomy vs LTO was the only direct comparison available for variation in AMH level; salpingectomy was associated with a significantly greater decrease in serum AMH (OR, 7.58 (95% CI, 4.38–10.79); I ² = 94%) (Appendix S7 and Table S5). Consequently, it was not possible to perform NMA for this outcome.

Procedural complication. Regarding abdominal wall/pelvic infection, aggregate analysis generated one additional direct estimation beyond that obtained from RCTs alone, which was not significant (Table S5). None of the NMA‐derived comparisons for infection was significant. Aggregate analysis of all studies generated two additional direct comparisons plus five indirect comparisons and one mixed comparison for the need for repeat intervention or additional surgery. None of these indicated significant differences between any of the compared treatments.

Reporting bias and small‐study effects

The risks of reporting bias and small‐study effects affecting NMA estimates for live birth, ongoing pregnancy and clinical pregnancy were analyzed by visual assessment of funnel plots and were considered to be low (Appendix S8). However, the small number of included studies limits this assessment.

Quality of evidence

Assessment of the certainty of evidence according to GRADE methodology for the primary outcomes of main analysis is presented in Appendix S6.

Appendix S5 contains the per‐comparison risk‐of‐bias assessment regarding primary outcomes. All NMA estimates for live birth were derived from studies affected by a moderate‐to‐high risk of bias. NMA estimates for ongoing and clinical pregnancy were obtained mainly from studies with a moderate risk of bias, although studies with high risk of bias were in the majority for the comparison of salpingectomy vs ultrasound‐guided aspiration.

Most interventions and populations analyzed by the included studies are reflective of daily clinical practice, therefore the risk of indirectness was considered to be low.

Statistical testing did not show significant inconsistency between direct comparisons and the NMA estimates. Additionally, inconsistency was evaluated qualitatively by considering the predefined intervals for a clinically relevant effect. NMA estimates were not affected by high risk of inconsistency in the main analysis of primary outcomes, with the exception of the comparison between salpingectomy and no treatment.

Most of the estimates were affected by a moderate or high degree of imprecision, thus the quality of evidence was downgraded by one level for most outcomes.

Risks of reporting and small‐study effect biases for the three primary outcomes were considered low based on the morphology of the per‐comparison funnel plots. However, the low number of included studies limits this assessment (Appendix S8).

DISCUSSION

This study failed to find a beneficial effect of any hydrosalpinx treatment on live birth rate after IVF when restricted to RCTs. Nevertheless, pairwise comparisons using NMA methodology found a significant increase in ongoing pregnancy rate in patients treated with salpingectomy or ultrasound‐guided aspiration compared to those managed expectantly. Moreover, salpingectomy and LTO were associated with a significant increase in clinical pregnancy rate compared with no treatment on NMA.

In the aggregated analysis, which included RCTs and observational studies, sclerotherapy was associated with a significant increase in live birth rate, according to both direct and NMA estimates. All therapeutic interventions analyzed had a significant beneficial effect on ongoing pregnancy rate and clinical pregnancy rate, with the exception of ITD insertion. Head‐to‐head comparisons between treatment modalities showed a slight additional benefit of LTO over ultrasound‐guided aspiration for clinical pregnancy.

NMA of RCTs found no significant differences between interventions in the rate of miscarriage, rate of ectopic pregnancy, AMH variation, gonadotropin dose, number of oocytes retrieved, risk of infection or need for repeat intervention or additional surgery. Aggregated analysis of RCTs and observational studies showed a reduction in the number of retrieved oocytes associated with ITD insertion, although this estimate may be affected by selection bias.

At least 15 different systematic reviews with meta‐analysis ² , ⁵ , ⁷³ , ⁷⁴ , ⁷⁵ , ⁷⁶ , ⁷⁷ , ⁷⁸ , ⁷⁹ , ⁸⁰ , ⁸¹ , ⁸² , ⁸³ , ⁸⁴ , ⁸⁵ have been published assessing the effectiveness and safety of the techniques compared herein. Among the most recent reviews, Volodarsky‐Perel et al. ⁸⁰ in 2019 failed to find differences in IVF outcome between salpingectomy and LTO. The latest Cochrane review on this topic ⁸⁶ suggested that both salpingectomy and LTO increased clinical pregnancy rate compared with no treatment. In 2021, Capmas et al.² concluded that treatment of hydrosalpinx using any modality increased the pregnancy rate. Recently, Wu et al. ⁸¹ found no difference between LTO and salpingectomy in the effect on ovarian reserve. Most of these reviews included both RCTs and observational studies.

The only previous NMA on the treatment of hydrosalpinx prior to IVF, published by Tsiami et al. ²⁶ in 2016, includes seven clinical trials providing direct comparisons only between salpingectomy, LTO, ultrasound‐guided aspiration and no treatment, with clinical and ongoing pregnancy rates as the sole efficacy outcomes. All treatments were associated with increased clinical pregnancy rate compared to expectant management, but no intertreatment differences in ongoing or clinical pregnancy rate were found, although the precision of the estimates was low. Our study agrees with that of Tsiami et al. ²⁶ in finding a clear benefit of salpingectomy on ongoing pregnancy rate over no treatment. However, our study found no benefit of LTO over no treatment; instead, a significant effect was found when comparing ultrasound‐guided aspiration with no treatment.

Consistent with the findings of Tsiami et al. ²⁶ , our main analysis found no evidence of a protective effect of any of the treatment methods on miscarriage or ectopic pregnancy. On the contrary, the aggregate analysis of all studies found that salpingectomy and LTO were associated with a significant reduction in miscarriage rate compared to no treatment. This analysis also revealed a significant difference in miscarriage rate between patients undergoing salpingectomy vs ultrasound‐guided aspiration.

A strength of our work is the inclusion of 26 studies, of which nine are RCTs, giving us substantially more observations than that considered by Tsiami et al. ²⁶ . The inconsistency analysis was performed globally and for each comparison loop, resulting in all cases being compatible with the assumption of transitivity. Assessment of imprecision and heterogeneity was based on a predefined clinically relevant effect interval (OR from 0.9 to 1.1), which represents a difference in risk of about 0.5, assuming a 15% live birth rate in untreated patients. In addition, the included studies provided more than 20 direct pairwise comparisons of ultrasound procedures vs no treatment or other interventions.

We acknowledge that performing a secondary aggregated analysis including observational studies may be controversial. Although only observational studies scored as being of fair or good quality according to AHRQ standards were included, the validity of NMA methodology for aggregate analysis of randomized and non‐randomized studies has been questioned ⁸⁷ , ⁸⁸ . Nevertheless, this approach has been suggested to increase precision and statistical power, once a rigorous study selection process has been applied, followed by a sensitivity analysis considering randomized studies separately ⁸⁹ , ⁹⁰ , ⁹¹ .

Our selection of live birth rate as one of the primary outcomes reflects the clinical relevance of this reproductive outcome, but inevitably reduces the number of observations and the accuracy of our estimates because live birth is poorly represented in the included studies. Similarly, the higher number of included studies compared with previous meta‐analysis ¹⁶ was insufficient to offset the low number of direct comparisons between some techniques, especially concerning the less invasive ones. Our study included a conventional analysis of reporting bias and small‐study effects, and found no relevant asymmetries in the funnel plots. Nevertheless, the low number of studies supporting some estimates does not provide certainty on the absence of risk. Our analysis could also have included a temporal perspective, considering the year of publication of the studies as a possible source of bias.

Regarding implications for clinical practice, although the present NMA fails to support the effectiveness of any intervention to treat hydrosalpinx before IVF to improve live birth rate, the beneficial effect of salpingectomy and ultrasound‐guided aspiration on ongoing pregnancy rate and of salpingectomy and LTO on clinical pregnancy rate observed herein reinforces current recommendations ²⁶ . Based on the aggregated analyses, sclerotherapy could be a promising alternative to conventional laparoscopic techniques, combined with a favorable safety profile.

Given the growing interest in less invasive techniques, prospective comparative studies between sclerotherapy and laparoscopic techniques are needed to analyze fertility outcomes (particularly live birth rate) and safety outcomes (AMH variation before vs after the procedure, miscarriage and ectopic pregnancy). The association of these interventions with adverse events, such as pelvic infection following ultrasound‐guided procedures, are particularly difficult to assess due to their low frequency, so NMA methodology could be useful in this context.

In conclusion, the present NMA generated low‐ to very‐low‐quality evidence that fails to support the beneficial effect of any hydrosalpinx treatment compared with no treatment or any other approach on live birth rate after IVF treatment. However, NMA estimated a higher rate of ongoing pregnancy in patients treated with salpingectomy or ultrasound‐guided aspiration compared with no treatment, and a higher clinical pregnancy rate in patients who underwent salpingectomy or LTO compared with no treatment. Although laparoscopic procedures should still be considered as the first‐line approach, the findings of this NMA point to the potential utility of less invasive and presumably safer treatments, such as sclerotherapy.

Supporting information

Appendix S1 Search strategy

UOG-65-414-s012.docx^{(20.6KB, docx)}

Appendix S2 Risk of bias assessment

UOG-65-414-s001.docx^{(148.5KB, docx)}

Appendix S3 Results of individual studies

UOG-65-414-s005.docx^{(28.6KB, docx)}

Appendix S4 Network meta‐analysis results for secondary outcomes

UOG-65-414-s004.docx^{(333.2KB, docx)}

Appendix S5 Risk of bias within studies: primary outcomes

UOG-65-414-s011.docx^{(89KB, docx)}

Appendix S6 Summary of findings and certainty of evidence for primary outcomes according to GRADE methodology

UOG-65-414-s010.docx^{(30.2KB, docx)}

Appendix S7 Aggregated analysis of randomized and observational studies

UOG-65-414-s007.docx^{(894.2KB, docx)}

Appendix S8 Funnel plots evaluating reporting bias and small‐study effects

UOG-65-414-s008.docx^{(424KB, docx)}

Table S1 Characteristics of included studies

UOG-65-414-s013.docx^{(35.2KB, docx)}

Table S2 Excluded studies and reasons for exclusion

UOG-65-414-s006.docx^{(22.9KB, docx)}

Table S3 Direct and network meta‐analysis‐derived comparisons of treatment effects in main analysis: secondary outcomes

UOG-65-414-s002.docx^{(42.8KB, docx)}

Table S4 Direct and network meta‐analysis‐derived comparisons of treatment effects in aggregated analysis: primary outcomes

UOG-65-414-s003.docx^{(35.3KB, docx)}

Table S5 Direct and network meta‐analysis‐derived comparisons of treatment effects aggregated analysis: secondary outcomes

UOG-65-414-s009.docx^{(39.4KB, docx)}

DATA AVAILABILITY STATEMENT

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Appendix S1 Search strategy

UOG-65-414-s012.docx^{(20.6KB, docx)}

Appendix S2 Risk of bias assessment

UOG-65-414-s001.docx^{(148.5KB, docx)}

Appendix S3 Results of individual studies

UOG-65-414-s005.docx^{(28.6KB, docx)}

Appendix S4 Network meta‐analysis results for secondary outcomes

UOG-65-414-s004.docx^{(333.2KB, docx)}

Appendix S5 Risk of bias within studies: primary outcomes

UOG-65-414-s011.docx^{(89KB, docx)}

Appendix S6 Summary of findings and certainty of evidence for primary outcomes according to GRADE methodology

UOG-65-414-s010.docx^{(30.2KB, docx)}

Appendix S7 Aggregated analysis of randomized and observational studies

UOG-65-414-s007.docx^{(894.2KB, docx)}

Appendix S8 Funnel plots evaluating reporting bias and small‐study effects

UOG-65-414-s008.docx^{(424KB, docx)}

Table S1 Characteristics of included studies

UOG-65-414-s013.docx^{(35.2KB, docx)}

Table S2 Excluded studies and reasons for exclusion

UOG-65-414-s006.docx^{(22.9KB, docx)}

Table S3 Direct and network meta‐analysis‐derived comparisons of treatment effects in main analysis: secondary outcomes

UOG-65-414-s002.docx^{(42.8KB, docx)}

Table S4 Direct and network meta‐analysis‐derived comparisons of treatment effects in aggregated analysis: primary outcomes

UOG-65-414-s003.docx^{(35.3KB, docx)}

Table S5 Direct and network meta‐analysis‐derived comparisons of treatment effects aggregated analysis: secondary outcomes

UOG-65-414-s009.docx^{(39.4KB, docx)}

Data Availability Statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

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PERMALINK

Hydrosalpinx treatment before in‐vitro fertilization: systematic review and network meta‐analysis

F Pérez‐Milán

M Caballero‐Campo

M Carrera‐Roig

E Moratalla‐Bartolomé

J A Domínguez‐Arroyo

J L Alcázar‐Zambrano

L Alonso‐Pacheco

J A Carugno

ABSTRACT

Objective

Methods

Results

Conclusions

INTRODUCTION

METHODS

Eligibility criteria

Literature search and selection of studies

Data collection

Network geometry

Assessment of transitivity

Statistical analysis

RESULTS

Study selection

Figure 1.

Network geometry

Figure 2.

Assessment of transitivity

Risk of bias within studies

Assessment of inconsistency

Table 1.

Synthesis of results

Main analysis: primary outcomes

Figure 3.

Figure 4.

Main analysis: secondary outcomes

Aggregated analysis: primary outcomes

Aggregate analysis: secondary outcomes

Reporting bias and small‐study effects

Quality of evidence

DISCUSSION

Supporting information

DATA AVAILABILITY STATEMENT

REFERENCES

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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