Proximal tubal occlusion and salpingectomy result in similar improvement in in vitro fertilization outcome in patients with hydrosalpinx

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1 Proximal tubal occlusion and salpingectomy result in similar improvement in in vitro fertilization outcome in patients with hydrosalpinx Antonios Kontoravdis, M.D., a Evangelos Makrakis, M.D., a Konstantinos Pantos, M.D., b Dimitrios Botsis, M.D., a Efthimios Deligeoroglou, M.D., a and George Creatsas, M.D. a a Second Department of Obstetrics and Gynecology, University of Athens, Aretaieion Hospital; and b Centre for Human Reproduction, Genesis Clinic, Athens, Greece Objective: To evaluate and compare the clinical impact of proximal tubal occlusion and salpingectomy when performed before IVF in patients with hydrosalpinges. Design: Prospective randomized study. Setting: Assisted reproduction unit in an obstetrics and gynecology department in a university hospital in Greece as well as assisted reproduction unit in an urban clinic in a major city in Greece. Patient(s): One hundred fifteen patients with unilateral or bilateral hydrosalpinges who were candidates for IVF treatment. Intervention(s): Laparoscopic proximal tubal occlusion, laparoscopic salpingectomy, controlled ovarian hyperstimulation, IVF, and embryo transfer. Main Outcome Measure(s): Implantation rate, clinical-pregnancy rate, ongoing-pregnancy rate, abortion rate, and ectopic-pregnancy rate. Result(s): Patients who underwent proximal tubal occlusion before IVF demonstrated significantly increased implantation, clinical-pregnancy, and ongoing-pregnancy rates compared with those with no surgical intervention and demonstrated implantation, clinical-pregnancy, and ongoing-pregnancy rates comparable to those who underwent salpingectomy. Conclusion(s): Proximal tubal occlusion, when performed in women with unilateral or bilateral hydrosalpinges before their IVF treatment, represents a potentially beneficial surgical procedure, increasing significantly the chances for successful implantation and for clinical and ongoing pregnancy. Proximal tubal occlusion may be viewed as a valid alternative when salpingectomy is technically difficult or not feasible. (Fertil Steril 2006;86: by American Society for Reproductive Medicine.) Key Words: Hydrosalpinx, salpingectomy, proximal tubal occlusion, laparoscopy, in vitro fertilization, pregnancy rates The tubal factor accounts for 25% 35% of female infertility (1). Tubal impairment is caused by pelvic inflammatory disease in 50% of cases (2), and distal tubal occlusion may lead to the formation of hydrosalpinges (3). Even though IVF and embryo transfer (ET) initially were performed in patients with tubal impairment, it finally became obvious that the presence of hydrosalpinges was associated with a poorer IVF-ET outcome; many retrospective studies reported significantly lower implantation and pregnancy rates in patients with hydrosalpinges when compared with other types of tubal disease (4 7), as well as increased rates of spontaneous abortions (5, 8) and ectopic pregnancies (9). The theories behind the harmful effect of hydrosalpinges on IVF-ET outcomes include the following: [1] direct toxic effect of the accumulated fluid on the transferred embryos through its leakage in the endometrial cavity (10 14), although studies on human embryos have not revealed such Received December 8, 2005; revised and accepted May 8, Reprint requests: Evangelos Makrakis, M.D., 194, Alexandras Avenue, Athens 11522, Greece (FAX: ; emakrakis@ hotmail.com). a direct embryonic toxicity (15, 16); [2] inhibition of implantation by alterations in endometrial receptivity (17 19) or mechanical washing of the blastocyst (20, 21); and [3] impairment of embryo development as a result of hydrosalpingeal fluid s deficiencies in nutrients and energy stores (22 24). The treatment options for hydrosalpinges include drainage, salpingostomy, proximal tubal occlusion, and salpingectomy. Once the deleterious effect of hydrosalpinges on IVF-ET outcomes has been widely accepted, their so-called prophylactic treatment before the application of assisted reproductive technologies has been proposed. After many retrospective studies, two prospective randomized ones (25, 26) confirmed the beneficial effect of salpingectomy before IVF, whereas a recent meta-analysis concluded that laparoscopic salpingectomy should be considered for all women with hydrosalpinges due to undergo IVF-ET (27). Nevertheless, salpingectomy involves some certain surgical risks, especially in women with previous abdominal surgery and/or extensive pelvic adhesions, whereas the procedure has been associated with an impairment of the ovarian blood flow 1642 Fertility and Sterility Vol. 86, No. 6, December /06/$32.00 Copyright 2006 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert

2 as a result of the transection of collateral vessels, which might result in a subsequently reduced efficacy of ovarian stimulation (28). As a consequence, the evaluation of alternative to salpingectomy techniques for the management of women with hydrosalpinges before their IVF treatment would be interesting. Such an evaluation of the proximal tubal-occlusion technique has been performed only through retrospective studies (29, 30). The aim of the present study was to evaluate and compare the impact of the salpingectomy and proximal tubal occlusion on IVF-ET outcomes in a prospective randomized trial. MATERIALS AND METHODS Patients Recruitment included patients who presented for IVF treatment to the Second Department of Obstetrics and Gynecology, University of Athens, Aretaieion Hospital (Athens, Greece), as well as to the Centre for Human Reproduction (Athens, Greece), and the study was approved by the Institutional Review Board and Ethics Committee of Aretaieion Hospital. Patient criteria for inclusion in the study were the following: presence of unilateral or bilateral hydrosalpinges confirmed by hysterosalpingography; woman s age of 41 years; suitability for IVF intracytoplasmic sperm injection treatment, with FSH levels on females cycle day 2 3 of 12 miu/ml and available spermatozoa in semen; no contraindication for laparoscopic surgery; no history of IVF attempts before recruitment; and absence of any other obvious pelvic pathology in females. After obtaining an informed consent from patients fulfilling the above criteria, a computergenerated randomization in blocks was performed, and patients were categorized in three groups: group A included 50 patients who underwent laparoscopic unilateral or bilateral proximal tubal occlusion before IVF treatment, group B included 50 patients who underwent laparoscopic unilateral or bilateral salpingectomy before IVF treatment, and group C included 15 patients who proceeded to their IVF treatment with no previous surgical intervention. Surgical Methods All salpingectomies were performed laparoscopically; the mesosalpinx was transected as close as possible to the fallopian tube, and the latter was transected cm from the cornual section. All proximal tubal occlusions were performed laparoscopically; bipolar diathermy was applied on the isthmic segment at two separate sites, and the hydrosalpinx was not drained. In Vitro Fertilization Treatment Group A and B subjects were asked to attend for IVF treatment once two completed menstrual cycles had passed since surgery. All the study subjects who received IVF treatment underwent controlled ovarian hyperstimulation (COH) with a long protocol (down-regulation with SC administration of GnRH analogue, which was initiated in the midluteal phase of the previous cycle, and stimulation with SC administration of recombinant FSH in starting doses of IU daily, which were adapted on the basis of serial ultrasonographic measurements of follicular growth and serum E 2 evaluations), and transvaginal ultrasound-guided oocyte retrieval 35 hours after the administration of 10,000 IU of hcg. In vitro fertilization or intracytoplasmic sperm injection was performed with the respective husband s spermatozoa, and all ETs were performed on day 3 with a Wallace catheter, under ultrasound guidance. The number of transferred embryos depended on women s age and on embryo availability and quality. For assessment of the latter, a two-grade embryo score was used (grade 1 included goodquality embryos with 20% fragmentation). Luteal-phase support included per-vagina administration of P (600 mg daily) and a 6-day-postretrieval course of doxycycline (100 mg, 2 times per day, by mouth) and prednisolone (5 mg, 3 times per day, by mouth). Data Analysis The study was initiated in the year 2000, and a power analysis was undertaken to determine the appropriate sample size. According to the most recent published data by that year (30), to achieve a power of 80% assuming a significance level of 0.05, a sample size of 50 patients per group would be sufficient to detect the reported difference in clinicalpregnancy rate (CPR) between patients undergoing salpingectomy or proximal tubal occlusion (46% vs. 73%, respectively), whereas a sample size of 14 patients per group would be sufficient to detect the reported difference between patients with or without surgical intervention (46% vs. 14%, respectively). Reported parameters for analysis in the study population included the following: woman s age, parity, type of infertility (primary or secondary), presence and treatment of unilateral or bilateral hydrosalpinges in each patient, visibility of the hydrosalpinges on ultrasound scan (USS) before treatment, total units of recombinant FSH administered and required days of COH for each patient, number of retrieved oocytes, type of fertilization (IVF or intracytoplasmic sperm injection), number of fertilized oocytes, number of transferred embryos, number of transfers with impaired embryo quality (grade 2), implanted sacs, clinical pregnancies (gestation sac fetal pole confirmed by USS 4 wk after ET), ongoing pregnancies (pregnancies beyond the first trimester), abortions, and ectopic pregnancies. Implantation rate (IR; implanted sacs per hundred transferred embryos), CPR (clinical pregnancies per hundred ET), and ongoingpregnancy rate (OPR; ongoing pregnancies per hundred ET) were calculated. Only the first IVF attempt for each patient was included in the analysis, and the designed sample size was reached in June Statistical analysis was performed using: Fertility and Sterility 1643

3 Mann-Whitney U-test for comparison of nondichotomous variables between groups, Fisher s exact test for comparison of dichotomous variables between groups, risk analysis, and Spearman s rank correlation for analysis of correlations between data. P values of.05 were considered to be significant. RESULTS Table 1 shows subjects characteristics on initial recruitment. The number of subjects with primary infertility and history of previous delivery, as well as their age, was comparable among the three groups; in addition, the incidence of bilateral and/or USS-visible hydrosalpinges was not significantly different among the three groups (even though the incidence of bilateral hydrosalpinges was higher in group A subjects). The initially designed procedure (proximal tubal occlusion or salpingectomy) for each subject (on the basis of randomization) was completed in all the cases. In group A, 2 women did not proceed to IVF treatment after the performance of tubal occlusion; of the 48 women receiving IVF treatment, 1 did not respond to COH, and 2 others did not have embryos to transfer. In group B, 1 woman did not proceed to IVF treatment after the performance of salpingectomy; of the 49 women receiving IVF treatment, 1 did not respond to COH, and another 1 did not have embryos to transfer. Finally, in group C, 1 woman did not have embryos to transfer (Fig. 1). Table 2 shows subjects IVF treatment parameters. No significant differences were observed among the three groups regarding required days of COH, total required dose of recombinant FSH, number of collected oocytes at retrieval, number of fertilized oocytes, number of transferred embryos, and number of transfers with grade 2 embryo quality. Table 3 shows the outcomes of IVF treatment in the study groups. Comparing groups A and B, subjects who had undergone proximal tubal occlusion demonstrated IR, CPR, and OPR that were comparable to those of women who had undergone salpingectomy. Comparing groups A and C, subjects who had undergone proximal tubal occlusion demonstrated significantly increased IR, CPR, and OPR compared with those women who had had no surgical intervention. Comparing groups B and C, subjects who had undergone salpingectomy demonstrated significantly increased IR, CPR, and OPR compared with those who had had no surgical intervention. Finally, abortion and ectopic-pregnancy rates per transfer were comparable among subjects in groups A, B, and C. Table 4 demonstrates the outcomes of IVF treatment in the three study groups in relation to the presence of bilateral hydrosalpinges and USS-visible hydrosalpinges on presentation. In group A, the presence of bilateral hydrosalpinges on presentation was not significantly correlated to the IVF outcome after the surgical intervention (for clinical pregnancies, Spearman s r 0.17, P.27; and for ongoing pregnancies, Spearman s r 0.13, P.38). The same applied for the presence of USS-visible hydrosalpinges on presentation (for clinical pregnancies, Spearman s r 0.22, P.14; and for ongoing pregnancies, Spearman s r 0.22, P.13). In group B, the presence of bilateral hydrosalpinges on presentation was not significantly correlated to the IVF outcome after the surgical intervention (for clinical pregnancies, Spearman s r 0.09, P.53; and for ongoing pregnancies, Spearman s r 0.01, P.90). The same applied for the presence of USS-visible hydrosalpinges on presentation (for clinical pregnancies, Spearman s r 0.16; P.29; and for ongoing pregnancies, Spearman s r 0.24, P.10). In group C, the presence of bilateral hydrosalpinges on presentation was not significantly correlated to the IVF outcome (for clinical pregnancies, Spearman s r 0.47, P.08; and for ongoing pregnancies, Spearman s r 0.32, P.26). In the same group, the presence of USS-visible hydrosalpinges on presentation was correlated significantly to the achievement of a clinical pregnancy (Spearman s r 0.54, P.04) but not to that of an ongoing one (Spearman s r 0.37, P.19). In the subgroup of patients with bilateral hydrosalpinges on presentation, CPR after IVF treatment was significantly higher in those who underwent tubal occlusion or salpingec- TABLE 1 Subjects characteristics and statistical analysis on initial recruitment. Groups P values Parameter A B C A vs. B A vs. C B vs. C Age in y, mean ( SD) Primary infertility, n (%) 46 (92) 42 (84) 13 (86.7) Parous, n (%) 2 (4) 3 (6) 1 (6.7) Bilateral hydrosalpinges, n (%) 35 (70) 27 (54) 8 (53.3) USS-visible hydrosalpinges, n (%) 29 (58) 32 (64) 9 (60) Kontoravdis et al. Hydrosalpinx laparoscopic surgery before IVF Vol. 86, No. 6, December 2006

4 FIGURE 1 Flow chart of the randomized subjects. tomy compared with those who had no surgical intervention, and it was comparable between proximal tubal occlusion and salpingectomy groups; in the same subgroup of patients, the OPR after IVF treatment in the salpingectomy group was significantly higher compared with the no surgical intervention group and was comparable to that of the proximal tubal-occlusion group, whereas the latter group demonstrated borderline significance regarding the increase in OPR compared with the no surgical intervention group. In the subgroup of patients with USS-visible hydrosalpinges on presentation, CPR after IVF treatment was significantly higher in the proximal tubal occlusion and salpingectomy groups compared with in the no surgical intervention group and was comparable between them; in the same subgroup of patients, the OPR after IVF treatment in the salpingectomy group was significantly higher compared with the no surgical intervention group and was comparable to that in the proximal tubal occlusion group, whereas the latter group demonstrated a suggestive increase in OPR compared with the no surgical intervention group. DISCUSSION The presence of hydrosalpinges in women undergoing IVF-ET widely has been suggested as an adverse prognostic factor for the assisted reproductive technologies outcome, reducing the implantation and pregnancy rates. The majority of the published retrospective studies reported such a statistically significant (4 7, 31 34) or suggestive (35, 36) negative impact, and meta-analyses confirmed a significant decrease in the probability of pregnancy, along with a significant increase in the probability of spontaneous abortion in the presence of hydrosalpinx (37, 38). More specifically, in a meta-analysis of nine retrospective controlled studies and five published abstracts that was performed by Fertility and Sterility 1645

5 TABLE 2 Subjects IVF treatment parameters and statistical analysis. Parameter Groups A B C A vs. B P values A vs. C B vs. C Days of COH (mean SD) Units of FSH (mean SD) 2, , , , Collected oocytes (mean SD) ICSI procedures, n (%) 7 (14.9) 6 (12.5) 3 (20) Fertilized oocytes (mean SD) No. of transferred embryos Embryos per ET (mean SD) No. of transfers with all embryos grade Camus et al. (37), including 1,004 patients with hydrosalpinges and 4,588 patients with tubal-factor infertility without hydrosalpinges, significant decreases in IRs and in pregnancy and delivery rates were confirmed in the hydrosalpinx patients (odds ratios: 0.63, 0.64, and 0.58, respectively). The present study included a control group of patients with hydrosalpinges who underwent IVF-ET without prior intervention to allow for a comparison of the outcomes with those of patients who underwent proximal tubal occlusion (because such a comparison has not been prospectively investigated in the literature); the results of our control group were disappointing but were in general agreement with those of many of the above-mentioned studies. The beneficial effect of so-called prophylactic salpingectomy in infertile patients before IVF-ET cycles on IRs and pregnancy rates initially was documented in retrospective studies (6, 8, 18, 39) and finally was evaluated in two prospective randomized ones. In a relatively small prospective trial by Dechaud et al. (25), a trend toward increased IRs and pregnancy rates that did not reach significance was reported in patients after salpingectomy; the small size of the study, with a power of 11% to detect any true differences between groups, did not allow any definite conclusion, and the investigators proposed further larger studies to be conducted. Therefore, in 1999, Strandell et al. (26) published a large, multicenter, prospective study, in which 204 patients with hydrosalpinges were randomized to either salpingectomy or to no intervention before IVF-ET. They reported a trend toward increased CPR per patient in the salpingectomy group (36.6% vs. 23.9%) and a significantly increased delivery rate per patient in the same group (28.6% vs. 16.3%). Interestingly, a subgroup analysis revealed significant differ- TABLE 3 Subjects IVF treatment outcomes and statistical analysis. Groups A vs. B A vs. C B vs. C Parameter A B C P OR 95% CI P OR 95% CI P OR 95% CI No. of transfers Implantation rate (%) Clinical-pregnancy rate (%) Ongoing-pregnancy rate (%) Abortion rate (%) Ectopic-pregnancy rate (%) Note: OR odds ratio; CI confidence interval Kontoravdis et al. Hydrosalpinx laparoscopic surgery before IVF Vol. 86, No. 6, December 2006

6 TABLE 4 Subgroup IVF treatment outcomes. Groups A vs. B A vs. C B vs. C Parameter A B C P OR 95% CI P OR 95% CI P OR 95% CI Transfers (n) With bilateral HS With USS-visible HS Clinical-pregnancy rate (%) With bilateral HS With USS-visible HS Ongoing-pregnancy rate (%) With bilateral HS With USS-visible HS Note: HS hydrosalpinges; OR odds ratio; CI confidence interval. ences in favor of the salpingectomy group, in IRs in patients with bilateral hydrosalpinges (25.6% vs. 12.3%), as well as in CPRs and delivery rates in patients with USS-visible hydrosalpinges (45.7% vs. 22.5% and 40% vs. 17.5%, respectively). The results of the present prospective randomized study support the beneficial effect of prophylactic salpingectomy before IVF treatment; CPRs and OPRs were found significantly to be increased in the study subjects who had undergone salpingectomy when compared with those with no surgical intervention, whereas in the subgroup of patients with bilateral or USS-visible hydrosalpinges, the performance of salpingectomy had a significantly positive effect on rates of clinical and ongoing pregnancies after IVF-ET when compared with case of the no surgical intervention group. Since the above-mentioned studies, most investigators and clinicians have supported and adopted the prophylactic salpingectomy. Additional benefits of the procedure include the ultimate removal of a chronically infected tissue that is prone to abscess formation or torsion, as well as the optimization of oocyte-retrieval conditions by increasing the access to the ovary and reducing the risk of infection. However, the procedure carries some intrinsic disadvantages. Salpingectomy is more or less an invasive procedure that may be more difficult or risky in cases with extensive pelvic adhesions or previous abdominal surgery. The transection of the oviduct at a site too close to the cornua has been associated with an increased risk of interstitial pregnancy, with overwhelming consequences (40, 41). A theoretical decrease in ovarian blood perfusion may result after the salpingectomy, once some of the blood supply to the ovary is received through branches of the uterine artery and the mesosalpingeal vascular arcade. In the rat model, a reduction in ovarian blood supply may have a direct effect on ovulatory function (42), whereas in the rabbit model, fimbriectomy results in a reduced number of corpora lutea (43). Patients who underwent salpingectomy showed no impairment of ovulation stimulation variables in retrospective (6, 8, 23, 29, 39, 44), as well as in prospective studies (26); nevertheless, when adnexal sides were examined separately in a study by Lass et al. (45), a significant reduction in the number of developed follicles and retrieved oocytes was noted from the ovary ipsilateral to which a unilateral salpingectomy had been performed, whereas in a retrospective study by Freeman et al. (46), the surgical correction of hydrosalpinges did not improve the low implantation and blastulation rates, as well as the high rates of in vitro embryo arrest and degeneration. The results of the present study are in agreement with the assumption that the performance of a salpingectomy (as well as that of proximal tubal occlusion) has no significant adverse effects on ovarian hyperstimulation parameters, as is reflected in the comparable number of collected and fertilized oocytes among the three study groups; nevertheless, it has to be noted that an analysis per adnexal side was not available. In any case, when performing a salpingectomy, great effort should be taken to transect the mesosalpinx as closely as possible to the fallopian tube to minimize the injury to the ovarian blood supply. Proximal tubal occlusion represents an interesting alternative to salpingectomy. It is a less invasive, easier to perform, and quicker technique that addresses the main demand for elimination of the hydrosalpingeal fluid s retrograde flow in the uterine cavity. The technique was evaluated in retrospective-only studies: Murray et al. (23), who reported comparable IRs and OPRs in women who had undergone proximal tubal occlusion, salpingectomy, and neosalpingostomy; Stadtmauer et al. (30), who reported significantly improved outcomes in patients after tubal occlusion when compared with patients with no Fertility and Sterility 1647

7 surgical intervention and reported a trend toward higher IRs and pregnancy rates when compared with patients treated with salpingectomy; and Surrey and Schoolcraft (29), who reported similar IRs and CPRs in patients treated with proximal tubal occlusion or salpingectomy (19.4% 6.1% and 46.7% vs. 29.2% 5.9% and 57.1%, respectively). The results of the present prospective randomized study revealed that the prophylactic performance of proximal tubal occlusion before IVF treatment may have benefits that were found to be statistically comparable to those of salpingectomy, at least in our sample size. All of the IVF positiveoutcome parameters (such as IRs, CPRs, and OPRs) were found to be significantly improved in subjects who had undergone this kind of surgical intervention before their IVF treatment, whereas rates of abortions and ectopic pregnancies were not increased. In addition, the above parameters were found to be increased in the salpingectomy group compared with the tubal-occlusion group, but the difference did not reach significance. Therefore, proximal tubal occlusion could be considered not only as a beneficial intervention for women with hydrosalpinges before their IVF treatment but as a valid alternative to the technique of salpingectomy. The favorable effects of proximal tubal occlusion may gain more importance if we consider the intrinsic advantages of this approach, such as less invasiveness, shorter operative learning curve, and easier technique, especially in cases in which the pelvic anatomy is distorted; as well as the theoretical advantages, such as the preservation of the ovarian blood supply. Other approaches intending to limit the adverse effects of hydrosalpinges include the transvaginal drainage of hydrosalpinx fluid and the administration of antibiotics before an IVF-ET cycle. The former was found to improve pregnancy rates and IRs in some small retrospective studies (47, 48) but not in others (49); a major disadvantage of this technique is that it cannot eradicate the source of fluid, which rapidly reaccumulates (50, 51). The latter approach was evaluated in a noncontrolled study that reported a nonsignificant trend toward improving implantation and pregnancy rates (35), but it has to be mentioned that the administration of antibiotics could not eliminate the possible noninfectious effects of hydrosalpinx fluid on embryo implantation and development. Regarding more specific parameters that could affect the IVF-ET outcome in patients with hydrosalpinges, the visibility of hydrosalpinx on USS has been shown to serve as an adverse factor. Many studies have shown larger differences in pregnancy rates between women with visible and notvisible hydrosalpinges and controls (5, 32, 48), as well as compared with the case of other tubal factors (52). In addition, Strandell et al. (26), in their randomized trial, reported a significantly improved outcome after salpingectomy in the USS-visible hydrosalpinges group. Finally, in the latter study, the effect of bilateral hydrosalpinges was addressed, and the investigators suggested a nonsignificant increased degree of poor-quality embryos compared with patients with unilateral disease but significantly increased IRs and pregnancy rates after salpingectomy in this subgroup. The results of the present study are in agreement with the above-mentioned ones, because CPRs and OPRs were significantly improved after prophylactic salpingectomy, not only in the USS-visible hydrosalpinges subgroup but in the bilateral-hydrosalpinges one as well. Regarding the effect of proximal tubal occlusion in these subgroups, the latter technique, when compared with the nonsurgical intervention, resulted in significantly increased clinical pregnancies and in an increased number of ongoing pregnancies (P values of.05 and.06). Finally, both surgical interventions (proximal tubal occlusion and salpingectomy) yielded similar results in these subgroups. In conclusion, proximal tubal occlusion and salpingectomy, when performed in women with unilateral or bilateral hydrosalpinges before their IVF treatment, could significantly increase the chances for successful implantation and for clinical and ongoing pregnancy. In the present study, these outcomes were found to be better in the salpingectomy group compared with the tubal-occlusion one, even though differences were not significant. Until studies in a larger population will strengthen our results, proximal tubal occlusion can be viewed as a valid alternative when salpingectomy is technically difficult or not feasible. REFERENCES 1. Serafini P, Batzofin J. Diagnosis of female infertility. A comprehensive approach. J Reprod Med 1989;34: Honore GM, Holden AE, Schenken RS. Pathophysiology and management of proximal tubal blockage. Fertil Steril 1999;71: Rock JA, Katayama KP, Martin EJ, Woodruff JD, Jones HW Jr. Factors influencing the success of salpingostomy techniques for distal fimbrial obstruction. Obstet Gynecol 1978;52: Strandell A, Waldenstrom U, Nilsson L, Hamberger L. Hydrosalpinx reduces in-vitro fertilization/embryo transfer pregnancy rates. Hum Reprod 1994;9: Andersen AN, Yue Z, Meng FJ, Petersen K. Low implantation rate after in-vitro fertilization in patients with hydrosalpinges diagnosed by ultrasonography. Hum Reprod 1994;9: Vandromme J, Chasse E, Lejeune B, Van Rysselberge M, Delvigne A, Leroy F. 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