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DOI: 10.1055/s-0040-1722155
Effects of Hydrosalpinx on Endometrial Implantation Failures: Evaluating Salpingectomy in Women Undergoing in vitro fertilization
Efeitos do Hydrosalpinx no Falho de Implantação Endometrial: Avaliar a salpingectomia nas mulheres em curso de Fertilização in vitro![](https://www.thieme-connect.de/media/10.1055-s-00030576/202104/lookinside/thumbnails/10-1055-s-0040-1722155_200211-1.jpg)
Abstract
Hydrosalpinx is a disease characterized by the obstruction of the salpinx, with progressive accumulation in the shape of a fluid-filled sac at the distal part of the tuba uterina, and closed to the ovary. Women with hydrosalpinges have lower implantation and pregnancy rates due to a combination of mechanical and chemical factors thought to disrupt the endometrial environment. Evidence suggests that the presence of hydrosalpinx reduces the rate of pregnancy with assisted reproductive technology. The main aim of the present is review to make an overview of the possible effects of hydrosalpinx on in vitro fertilization (IVF). We conducted a literature search on the PubMed, Ovid MEDLINE, and Google Scholar data bases regarding hydrosalpinx and IVF outcomes. Hydrosalpinx probably has a direct toxic effect on sperm motility and on the embryos. In addition, the increasing liquid inside the salpinges could alter the mechanisms of endometrial receptivity. The window of endometrial receptivity is essential in the implantation of blastocysts, and it triggers multiple reactions arising from the endometrium as well as the blastocysts. Hydrosalpinx could influence the expression of homeobox A10 (HOXA10) gene, which plays an essential role in directing embryonic development and implantation. Salpingectomy restores the endometrial expression of HOXA10; therefore, it may be one mechanism by which tubal removal could result in improved implantation rates in IVF. In addition, salpingectomy does not affect the ovarian response, nor reduces the antral follicle count. Further studies are needed to establish the therapeutic value of fluid aspiration under ultrasonographic guidance, during or after oocyte retrieval, in terms of pregnancy rate and ongoing pregnancy.
Publication History
Received: 17 June 2020
Accepted: 23 October 2020
Article published online:
18 February 2021
© 2021. Federação Brasileira de Ginecologia e Obstetrícia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
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References
- 1 Schlaff WD. A reconsideration of salpingectomy for hydrosalpinx before in vitro fertilization: why bother?. Fertil Steril 2019; 111 (04) 650-651 DOI: 10.1016/j.fertnstert.2019.02.014.
- 2 Zeyneloglu HB, Arici A, Olive DL. Adverse effects of hydrosalpinx on pregnancy rates after in vitro fertilization-embryo transfer. Fertil Steril 1998; 70 (03) 492-499 DOI: 10.1016/s0015-0282(98)00200-3.
- 3 Camus E, Poncelet C, Goffinet F, Wainer B, Merlet F, Nisand I, Philippe HJ. Pregnancy rates after in-vitro fertilization in cases of tubal infertility with and without hydrosalpinx: a meta-analysis of published comparative studies. Hum Reprod 1999; 14 (05) 1243-1249 DOI: 10.1093/humrep/14.5.1243.
- 4 Savaris RF, Giudice LC. The influence of hydrosalpinx on markers of endometrial receptivity. Semin Reprod Med 2007; 25 (06) 476-482 DOI: 10.1055/s-2007-991045.
- 5 Hill GA, Herbert CM, Fleischer AC, Webster BW, Maxson WS, Wentz AC. Enlargement of hydrosalpinges during ovarian stimulation protocols for in vitro fertilization and embryo replacement. Fertil Steril 1986; 45 (06) 883-885 DOI: 10.1016/s0015-0282(16)49411-2.
- 6 Schiller VL, Tsuchiyama K. Development of hydrosalpinx during ovulation induction. J Ultrasound Med 1995; 14 (11) 799-803 DOI: 10.7863/jum.1995.14.11.799.
- 7 Ng EH, Ajonuma LC, Lau EY, Yeung WS, Ho PC. Adverse effects of hydrosalpinx fluid on sperm motility and survival. Hum Reprod 2000; 15 (04) 772-777 DOI: 10.1093/humrep/15.4.772.
- 8 de Ziegler D, Pirtea P, Galliano D, Cicinelli E, Meldrum D. Optimal uterine anatomy and physiology necessary for normal implantation and placentation. Fertil Steril 2016; 105 (04) 844-854 DOI: 10.1016/j.fertnstert.2016.02.023.
- 9 Li L, Xu BF, Chen QJ, Sun XX. Effects of hydrosalpinx on pinopodes, leukaemia inhibitory factor, integrin beta3 and MUC1 expression in the peri-implantation endometrium. Eur J Obstet Gynecol Reprod Biol 2010; 151 (02) 171-175 DOI: 10.1016/j.ejogrb.2010.04.024.
- 10 Cohen A, Almog B, Tulandi TJM. Hydrosalpinx sclerotherapy before in vitro fertilization: systematic review and meta-analysis. Invasive Gynecol 2018; 25 (04) 600-607 DOI: 10.1016/j.jmig.2017.12.004.
- 11 Harb H, Al-Rshoud F, Karunakaran B, Gallos ID, Coomarasamy A. Hydrosalpinx and pregnancy loss: a systematic review and meta-analysis. Reprod Biomed Online 2019; 38 (03) 427-441 DOI: 10.1016/j.rbmo.2018.12.020.
- 12 Puttemans P, Campo R, Gordts S, Brosens I. Hydrosalpinx and ART: hydrosalpinx--functional surgery or salpingectomy?. Hum Reprod 2000; 15 (07) 1427-1430 DOI: 10.1093/humrep/15.7.1427.
- 13 Puttemans PJ, Brosens IA. Salpingectomy improves in-vitro fertilization outcome in patients with a hydrosalpinx: blind victimization of the fallopian tube?. Hum Reprod 1996; 11 (10) 2079-2081 DOI: 10.1093/oxfordjournals.humrep.a019052.
- 14 Fylstra DL. Ectopic pregnancy after hysterectomy: a review and insight into etiology and prevention. Fertil Steril 2010; 94 (02) 431-435 DOI: 10.1016/j.fertnstert.2009.03.039.
- 15 Cozzolino M, Diaz-Gimeno P, Pellicer A, Garrido N. Evaluation of the endometrial receptivity assay and the preimplantation genetic test for aneuploidy in overcoming recurrent implantation failure. J Assist Reprod Genet 2020; 37 (12) 2989-2997 DOI: 10.1007/s10815-020-01948-7.
- 16 Griffiths AN, Watermeyer SR, Klentzeris LD. Fluid within the endometrial cavity in an IVF cycle--a novel approach to its management. J Assist Reprod Genet 2002; 19 (06) 298-301 DOI: 10.1023/a:1015785431828.
- 17 He RH, Gao HJ, Li YQ, Zhu XM. The associated factors to endometrial cavity fluid and the relevant impact on the IVF-ET outcome. Reprod Biol Endocrinol 2010; 8: 46 DOI: 10.1186/1477-7827-8-46.
- 18 Kassabji M, Sims JA, Butler L, Muasher SJ. Reduced pregnancy outcome in patients with unilateral or bilateral hydrosalpinx after in vitro fertilization. Eur J Obstet Gynecol Reprod Biol 1994; 56 (02) 129-132 DOI: 10.1016/0028-2243(94)90269-0.
- 19 Beyler SA, James KP, Fritz MA, Meyer WR. Hydrosalpingeal fluid inhibits in-vitro embryonic development in a murine model. Hum Reprod 1997; 12 (12) 2724-2728 DOI: 10.1093/humrep/12.12.2724.
- 20 Chan LY, Chiu PY, Cheung LP, Haines CJ, Tung HF, Lau TK. A study of teratogenicity of hydrosalpinx fluid using a whole rat embryo culture model. Hum Reprod 2003; 18 (05) 955-958 DOI: 10.1093/humrep/deg189.
- 21 Roberts JE, Clarke HJ, Tulandi T, Tan SL. Effects of hydrosalpingeal fluid on murine embryo development and implantation. J Assist Reprod Genet 1999; 16 (08) 421-424 DOI: 10.1023/A:1020517524857.
- 22 Granot I, Dekel N, Segal I, Fieldust S, Shoham Z, Barash A. Is hydrosalpinx fluid cytotoxic?. Hum Reprod 1998; 13 (06) 1620-1624 DOI: 10.1093/humrep/13.6.1620.
- 23 Strandell A, Sjögren A, Bentin-Ley U, Thorburn J, Hamberger L, Brännström M. Hydrosalpinx fluid does not adversely affect the normal development of human embryos and implantation in vitro. Hum Reprod 1998; 13 (1O): 2921-2925 DOI: 10.1093/humrep/13.10.2921.
- 24 Ajonuma LC, Chan LN, Ng EH, Chow PH, Kung LS, Cheung ANY. et al. Characterization of epithelial cell culture from human hydrosalpinges and effects of its conditioned medium on embryo development and sperm motility. Hum Reprod 2003; 18 (02) 291-298 DOI: 10.1093/humrep/deg078.
- 25 Mansour RT, Aboulghar MA, Serour GI, Riad R. Fluid accumulation of the uterine cavity before embryo transfer: a possible hindrance for implantation. J In Vitro Fert Embryo Transf 1991; 8 (03) 157-159 DOI: 10.1007/BF01131707.
- 26 Andersen AN, Lindhard A, Loft A, Ziebe S, Andersen CY. The infertile patient with hydrosalpinges--IVF with or without salpingectomy?. Hum Reprod 1996; 11 (10) 2081-2084 DOI: 10.1093/oxfordjournals.humrep.a019053.
- 27 Vandromme J, Chasse E, Lejeune B, Van Rysselberge M, Delvigne A, Leroy F. Hydrosalpinges in in-vitro fertilization: an unfavourable prognostic feature. Hum Reprod 1995; 10 (03) 576-579 DOI: 10.1093/oxfordjournals.humrep.a135992.
- 28 Chen Q, Zhang Y, Elad D, Jaffa AJ, Cao Y, Ye X, Duan E. Navigating the site for embryo implantation: biomechanical and molecular regulation of intrauterine embryo distribution. Mol Aspects Med 2013; 34 (05) 1024-1042 DOI: 10.1016/j.mam.2012.07.017.
- 29 Zhang S, Lin H, Kong S, Wang S, Wang H, Wang H, Armant DR. Physiological and molecular determinants of embryo implantation. Mol Aspects Med 2013; 34 (05) 939-980 DOI: 10.1016/j.mam.2012.12.011.
- 30 Salleh N, Baines DL, Naftalin RJ, Milligan SR. The hormonal control of uterine luminal fluid secretion and absorption. J Membr Biol 2005; 206 (01) 17-28 DOI: 10.1007/s00232-005-0770-7.
- 31 Naftalin RJ, Thiagarajah JR, Pedley KC, Pocock VJ, Milligan SR. Progesterone stimulation of fluid absorption by the rat uterine gland. Reproduction 2002; 123 (05) 633-638 DOI: 10.1530/rep.0.1230633.
- 32 Clemetson CA, Mallikarjuneswara VR, Moshfeghi MM, Carr JJ, Wilds JH. The effects of oestrogen and progesterone on the sodium and potassium concentrations of rat uterine fluid. J Endocrinol 1970; 47 (03) 309-319 DOI: 10.1677/joe.0.0470309.
- 33 Ajonuma LC, Ng EH, Chan HC. New insights into the mechanisms underlying hydrosalpinx fluid formation and its adverse effect on IVF outcome. Hum Reprod Update 2002; 8 (03) 255-264 DOI: 10.1093/humupd/8.3.255.
- 34 Ajonuma LC, Chan PK, Ng EH. et al. Involvement of cystic fibrosis transmembrane conductance regulator (CFTR) in the pathogenesis of hydrosalpinx induced by Chlamydia trachomatis infection. J Obstet Gynaecol Res 2008; 34 (06) 923-930 DOI: 10.1111/j.1447-0756.2008.00826.x.
- 35 Paavonen J, Eggert-Kruse W. Chlamydia trachomatis: impact on human reproduction. Hum Reprod Update 1999; 5 (05) 433-447 DOI: 10.1093/humupd/5.5.433.
- 36 Jones RB, Mammel JB, Shepard MK, Fisher RR. Recovery of Chlamydia trachomatis from the endometrium of women at risk for chlamydial infection. Am J Obstet Gynecol 1986; 155 (01) 35-39 DOI: 10.1016/0002-9378(86)90073-6.
- 37 Wølner-Hanssen P, Mårdh PA, Møller B, Weström L. Endometrial infection in women with Chlamydial salpingitis. Sex Transm Dis 1982; 9 (02) 84-88 DOI: 10.1097/00007435-198204000-00006.
- 38 Toth M, Jeremias J, Ledger WJ, Witkin SS. In vivo tumor necrosis factor production in women with salpingitis. Surg Gynecol Obstet 1992; 174 (05) 359-362
- 39 Witkin SS, Sultan KM, Neal GS, Jeremias J, Grifo JA, Rosenwaks Z. Unsuspected Chlamydia trachomatis infection and in vitro fertilization outcome. Am J Obstet Gynecol 1994; 171 (05) 1208-1214 DOI: 10.1016/0002-9378(94)90134-1.
- 40 Spandorfer SD, Liu HC, Neuer A, Barmat LI, Davis O, Rosenwaks Z. The embryo toxicity of hydrosalpinx fluid is only apparent at high concentrations: an in vitro model that stimulates in vivo events. Fertil Steril 1999; 71 (04) 619-626 DOI: 10.1016/s0015-0282(98)00541-x.
- 41 Leese HJ. The formation and function of oviduct fluid. J Reprod Fertil 1988; 82 (02) 843-856 DOI: 10.1530/jrf.0.0820843.
- 42 Brunton WJ, Brinster RL. Active chloride transport in the isolated rabbit oviduct. Am J Physiol 1971; 221 (02) 658-661 DOI: 10.1152/ajplegacy.1971.221.2.658.
- 43 Brunton WJ. Beta-adrenergic stimulation of transmembrane potential and short circuit current of isolated rabbit oviduct. Nat New Biol 1972; 236 (61) 12-14 DOI: 10.1038/newbio236012a0.
- 44 Dickens CJ, Comer MT, Southgate J, Leese HJ. Human Fallopian tubal epithelial cells in vitro: establishment of polarity and potential role of intracellular calcium and extracellular ATP in fluid secretion. Hum Reprod 1996; 11 (01) 212-217 DOI: 10.1093/oxfordjournals.humrep.a019021.
- 45 Downing SJ, Maguiness SD, Watson A, Leese HJ. Electrophysiological basis of human fallopian tubal fluid formation. J Reprod Fertil 1997; 111 (01) 29-34 DOI: 10.1530/jrf.0.1110029.
- 46 Sheppard DN, Welsh MJ. Structure and function of the CFTR chloride channel. Physiol Rev 1999; 79 (1, Suppl) S23-S45 DOI: 10.1152/physrev.1999.79.1.S23.
- 47 Pier GB, Grout M, Zaidi T, Meluleni G, Mueschenborn SS, Banting G. et al. Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 1998; 393 (6680): 79-82 DOI: 10.1038/30006.
- 48 Gerçeker AA, Zaidi T, Marks P, Golan DE, Pier GB. Impact of heterogeneity within cultured cells on bacterial invasion: analysis of Pseudomonas aeruginosa and Salmonella enterica serovar typhi entry into MDCK cells by using a green fluorescent protein-labelled cystic fibrosis transmembrane conductance regulator receptor. Infect Immun 2000; 68 (02) 861-870 DOI: 10.1128/iai.68.2.861-870.2000.
- 49 Downing SJ, Tay JI, Maguiness SD, Watson A, Leese HJ. Effect of inflammatory mediators on the physiology of the human Fallopian tube. Hum Fertil (Camb) 2002; 5 (02) 54-60 DOI: 10.1080/1464727022000198932.
- 50 Meyer WR, Castelbaum AJ, Somkuti S. et al. Hydrosalpinges adversely affect markers of endometrial receptivity. Hum Reprod 1997; 12 (07) 1393-1398 DOI: 10.1093/humrep/12.7.1393.
- 51 Yoshinaga K. Research on Blastocyst Implantation Essential Factors (BIEFs). Am J Reprod Immunol 2010; 63 (06) 413-424 DOI: 10.1111/j.1600-0897.2010.00853.x.
- 52 Paulson RJ. Introduction: Endometrial receptivity: evaluation, induction and inhibition. Fertil Steril 2019; 111 (04) 609-610 DOI: 10.1016/j.fertnstert.2019.02.029.
- 53 Aghajanova L, Hamilton AE, Giudice LC. Uterine receptivity to human embryonic implantation: histology, biomarkers, and transcriptomics. Semin Cell Dev Biol 2008; 19 (02) 204-211 DOI: 10.1016/j.semcdb.2007.10.008.
- 54 Block K, Kardana A, Igarashi P, Taylor HS. In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing müllerian system. FASEB J 2000; 14 (09) 1101-1108 DOI: 10.1096/fasebj.14.9.1101.
- 55 Taylor HS, Daftary GS, Selam B. Endometrial HOXA10 expression after controlled ovarian hyperstimulation with recombinant follicle-stimulating hormone. Fertil Steril 2003; 80 (Suppl. 02) 839-843 DOI: 10.1016/s0015-0282(03)00985-3.
- 56 Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest 1998; 101 (07) 1379-1384 DOI: 10.1172/JCI1057.
- 57 Daftary GS, Taylor HS. Endocrine regulation of HOX genes. Endocr Rev 2006; 27 (04) 331-355 DOI: 10.1210/er.2005-0018.
- 58 Satokata I, Benson G, Maas R. Sexually dimorphic sterility phenotypes in Hoxa10-deficient mice. Nature 1995; 374 (6521): 460-463 DOI: 10.1038/374460a0.
- 59 Eun Kwon H, Taylor HS. The role of HOX genes in human implantation. Ann N Y Acad Sci 2004; 1034: 1-18 DOI: 10.1196/annals.1335.001.
- 60 Sarno JL, Kliman HJ, Taylor HS. HOXA10, Pbx2, and Meis1 protein expression in the human endometrium: formation of multimeric complexes on HOXA10 target genes. J Clin Endocrinol Metab 2005; 90 (01) 522-528 DOI: 10.1210/jc.2004-0817.
- 61 Gui Y, Zhang J, Yuan L, Lessey BA. Regulation of HOXA-10 and its expression in normal and abnormal endometrium. Mol Hum Reprod 1999; 5 (09) 866-873 DOI: 10.1093/molehr/5.9.866.
- 62 Daftary GS, Taylor HS. Pleiotropic effects of Hoxa10 on the functional development of peri-implantation endometrium. Mol Reprod Dev 2004; 67 (01) 8-14 DOI: 10.1002/mrd.20013.
- 63 Bagot CN, Troy PJ, Taylor HS. Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation. Gene Ther 2000; 7 (16) 1378-1384 DOI: 10.1038/sj.gt.3301245.
- 64 Bagot CN, Kliman HJ, Taylor HS. Maternal Hoxa10 is required for pinopod formation in the development of mouse uterine receptivity to embryo implantation. Dev Dyn 2001; 222 (03) 538-544 DOI: 10.1002/dvdy.1209.
- 65 Lim H, Ma L, Ma WG, Maas RL, Dey SK. Hoxa-10 regulates uterine stromal cell responsiveness to progesterone during implantation and decidualization in the mouse. Mol Endocrinol 1999; 13 (06) 1005-1017 DOI: 10.1210/mend.13.6.0284.
- 66 Daftary GS, Kayisli U, Seli E, Bukulmez O, Arici A, Taylor HS. Salpingectomy increases peri-implantation endometrial HOXA10 expression in women with hydrosalpinx. Fertil Steril 2007; 87 (02) 367-372 DOI: 10.1016/j.fertnstert.2006.06.041.
- 67 Strandell A, Lindhard A, Waldenström U, Thorburn J. Hydrosalpinx and IVF outcome: cumulative results after salpingectomy in a randomized controlled trial. Hum Reprod 2001; 16 (11) 2403-2410 DOI: 10.1093/humrep/16.11.2403.
- 68 Johnson N, van Voorst S, Sowter MC, Strandell A, Mol BW. Surgical treatment for tubal disease in women due to undergo in vitro fertilisation. Cochrane Database Syst Rev 2010; (01) CD002125 DOI: 10.1002/14651858.CD002125.pub3.
- 69 Practice Committee of American Society for Reproductive Medicine in collaboration with Society of Reproductive Surgeons. Salpingectomy for hydrosalpinx prior to in vitro fertilization. Fertil Steril 2008; 90 (5, Suppl) S66-S68 DOI: 10.1016/j.fertnstert.2008.08.089.
- 70 Sowter MC, Akande VA, Williams JA, Hull MG. Is the outcome of in-vitro fertilization and embryo transfer treatment improved by spontaneous or surgical drainage of a hydrosalpinx?. Hum Reprod 1997; 12 (10) 2147-2150 DOI: 10.1093/humrep/12.10.2147.
- 71 Van Voorhis BJ, Sparks AE, Syrop CH, Stovall DW. Ultrasound-guided aspiration of hydrosalpinges is associated with improved pregnancy and implantation rates after in-vitro fertilization cycles. Hum Reprod 1998; 13 (03) 736-739 DOI: 10.1093/humrep/13.3.736.
- 72 Lorente González J, Ríos Castillo JE, Pomares Toro E, Romero Nieto MI, Castelo-Branco C, Arjona Berral JE. Essure a novel option for the treatment of hydrosalpinx: a case series and literature review. Gynecol Endocrinol 2016; 32 (02) 166-170 DOI: 10.3109/09513590.2015.1103221.
- 73 Barbosa MW, Sotiriadis A, Papatheodorou SI, Mijatovic V, Nastri CO, Martins WP. High miscarriage rate in women treated with Essure® for hydrosalpinx before embryo transfer: a systematic review and meta-analysis. Ultrasound Obstet Gynecol 2016; 48 (05) 556-565 DOI: 10.1002/uog.15960.
- 74 Sills ES, Walsh DJ, Jones CA, Wood SH. Endometrial fluid associated with Essure implants placed before in vitro fertilization: Considerations for patient counseling and surgical management. Clin Exp Reprod Med 2015; 42 (03) 126-129 DOI: 10.5653/cerm.2015.42.3.126.
- 75 Xu B, Zhang Q, Zhao J, Wang Y, Xu D, Li Y. Pregnancy outcome of in vitro fertilization after Essure and laparoscopic management of hydrosalpinx: a systematic review and meta-analysis. Fertil Steril 2017; 108 (01) 84-95.e5 DOI: 10.1016/j.fertnstert.2017.05.005.
- 76 Hamilton CJ, Evers JL, Hoogland HJ. Ovulatory disorders and inflammatory adnexal damage: a neglected cause of the failure of fertility microsurgery. Br J Obstet Gynaecol 1986; 93 (03) 282-284 DOI: 10.1111/j.1471-0528.1986.tb07909.x.
- 77 Gomel V, Wang I. Laparoscopic surgery for infertility therapy. Curr Opin Obstet Gynecol 1994; 6 (02) 141-148
- 78 Demir B, Bozdag G, Sengul O, Kahyaoglu I, Mumusoglu S, Zengin D. The impact of unilateral salpingectomy on antral follicle count and ovarian response in ICSI cycles: comparison of contralateral side. Gynecol Endocrinol 2016; 32 (09) 741-744 DOI: 10.3109/09513590.2016.1161741.
- 79 Yoon SH, Lee JY, Kim SN, Chung HW, Park SY, Lee C. Does salpingectomy have a deleterious impact on ovarian response in in vitro fertilization cycles?. Fertil Steril 2016; 106 (05) 1083-1092.e5 DOI: 10.1016/j.fertnstert.2016.05.030.