Anatomic Abnormalities and Recurrent Implantation Failure

  • Jeffrey M. Goldberg
  • Julian Gingold
  • Natalia Llarena


Intrauterine abnormalities such as myomas, polyps, adhesions, and congenital septa have been shown to adversely affect embryo implantation and pregnancy outcomes. Treating these conditions improves pregnancy rates and outcomes. Hydrosalpinges reduce IVF pregnancy rates by ~50% by impeding embryo implantation. Treating them prior to IVF by salpingectomy, salpingostomy, or tubal ligation restores the success rates back to normal. This chapter reviews the pathophysiology of these abnormalities, therapeutic options, and treatment results.


Fibroids Myomas Myomectomy Endometrial polyps Polypectomy Intrauterine adhesions Uterine anomalies Uterine septoplasty Hydrosalpinx Embryo implantation 


  1. 1.
    Marshall LM, et al. Variation in the incidence of uterine leiomyoma among premenopausal women by age and race. Obstet Gynecol. 1997;90:967–73.PubMedCrossRefGoogle Scholar
  2. 2.
    Munro MG, Critchley HOD, Fraser IS. The FIGO classification of causes of abnormal uterine bleeding in the reproductive years. Fertil Steril. 2011;95:2204–8, 2208.e1–3PubMedCrossRefGoogle Scholar
  3. 3.
    Munro MG. Abnormal uterine bleeding. Cambridge: Cambridge University Press; 2010.Google Scholar
  4. 4.
    Munro MG, Critchley HOD, Broder MS, Fraser IS. FIGO classification system (PALM-COEIN) for causes of abnormal uterine bleeding in nongravid women of reproductive age. Int J Gynaecol Obstet. 2011;113:3–13.PubMedCrossRefGoogle Scholar
  5. 5.
    Mehine M, et al. Characterization of uterine leiomyomas by whole-genome sequencing. N Engl J Med. 2013;369:43–53.PubMedCrossRefGoogle Scholar
  6. 6.
    Mäkinen N, et al. MED12, the mediator complex subunit 12 gene, is mutated at high frequency in uterine leiomyomas. Science. 2011;334:252–5.PubMedCrossRefGoogle Scholar
  7. 7.
    Dou Q, et al. Suppression of transforming growth factor-beta (TGF beta) and TGF beta receptor messenger ribonucleic acid and protein expression in leiomyomata in women receiving gonadotropin-releasing hormone agonist therapy. J Clin Endocrinol Metab. 1996;81:3222–30.PubMedGoogle Scholar
  8. 8.
    Mas A, et al. Stro-1/CD44 as putative human myometrial and fibroid stem cell markers. Fertil Steril. 2015;104:225–34.e3.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Klatsky PC, Tran ND, Caughey AB, Fujimoto VY. Fibroids and reproductive outcomes: a systematic literature review from conception to delivery. Am J Obstet Gynecol. 2008;198:357–66.PubMedCrossRefGoogle Scholar
  10. 10.
    Pritts EA, Parker WH, Olive DL. Fibroids and infertility: an updated systematic review of the evidence. Fertil Steril. 2009;91:1215–23.PubMedCrossRefGoogle Scholar
  11. 11.
    Somigliana E, et al. Fibroids and female reproduction: a critical analysis of the evidence. Hum Reprod Update. 2007;13:465–76.PubMedCrossRefGoogle Scholar
  12. 12.
    Check JH, Choe JK, Lee G, Dietterich C. The effect on IVF outcome of small intramural fibroids not compressing the uterine cavity as determined by a prospective matched control study. Hum Reprod. 2002;17:1244–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Surrey ES, Lietz AK, Schoolcraft WB. Impact of intramural leiomyomata in patients with a normal endometrial cavity on in vitro fertilization-embryo transfer cycle outcome. Fertil Steril. 2001;75:405–10.PubMedCrossRefGoogle Scholar
  14. 14.
    Benecke C, Kruger TF, Siebert TI, Van der Merwe JP, Steyn DW. Effect of fibroids on fertility in patients undergoing assisted reproduction. A structured literature review. Gynecol Obstet Investig. 2005;59:225–30.CrossRefGoogle Scholar
  15. 15.
    Brady PC, Stanic AK, Styer AK. Uterine fibroids and subfertility: an update on the role of myomectomy. Curr Opin Obstet Gynecol. 2013;25:255–9.PubMedCrossRefGoogle Scholar
  16. 16.
    Practice Committee of American Society for Reproductive Medicine in Collaboration with Society of Reproductive Surgeons. Myomas and reproductive function. Fertil Steril. 2008;90:S125–30.Google Scholar
  17. 17.
    Yoshino O, et al. Decreased pregnancy rate is linked to abnormal uterine peristalsis caused by intramural fibroids. Hum Reprod. 2010;25:2475–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Donnez J, Jadoul P. What are the implications of myomas on fertility? A need for a debate? Hum Reprod. 2002;17:1424–30.PubMedCrossRefGoogle Scholar
  19. 19.
    Hunt JE, Wallach EE. Uterine factors in infertility–an overview. Clin Obstet Gynecol. 1974;17:44–64.PubMedCrossRefGoogle Scholar
  20. 20.
    Vollenhoven BJ, Lawrence AS, Healy DL. Uterine fibroids: a clinical review. Br J Obstet Gynaecol. 1990;97:285–98.PubMedCrossRefGoogle Scholar
  21. 21.
    Ingersoll FM. Fertility following myomectomy. Fertil Steril. 1963;14:596–602.PubMedCrossRefGoogle Scholar
  22. 22.
    Yoshino O, et al. Myomectomy decreases abnormal uterine peristalsis and increases pregnancy rate. J Minim Invasive Gynecol. 2012;19:63–7.PubMedCrossRefGoogle Scholar
  23. 23.
    Deligdish L, Loewenthal M. Endometrial changes associated with myomata of the uterus. J Clin Pathol. 1970;23:676–80.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Rackow BW, Taylor HS. Submucosal uterine leiomyomas have a global effect on molecular determinants of endometrial receptivity. Fertil Steril. 2010;93:2027–34.PubMedCrossRefGoogle Scholar
  25. 25.
    Buttram VC, Reiter RC. Uterine leiomyomata: etiology, symptomatology, and management. Fertil Steril. 1981;36:433–45.PubMedCrossRefGoogle Scholar
  26. 26.
    Farrer-Brown G, Beilby JO, Tarbit MH. Venous changes in the endometrium of myomatous uteri. Obstet Gynecol. 1971;38:743–51.PubMedGoogle Scholar
  27. 27.
    Farrer-Brown G, Beilby JO, Tarbit MH. The vascular patterns in myomatous uteri. J Obstet Gynaecol Br Commonw. 1970;77:967–75.PubMedCrossRefGoogle Scholar
  28. 28.
    Donnez J, et al. Ulipristal acetate versus leuprolide acetate for uterine fibroids. N Engl J Med. 2012;366:421–32.PubMedCrossRefGoogle Scholar
  29. 29.
    Stovall TG, Muneyyirci-Delale O, Summitt RL, Scialli AR. GnRH agonist and iron versus placebo and iron in the anemic patient before surgery for leiomyomas: a randomized controlled trial. Leuprolide Acetate Study Group. Obstet Gynecol. 1995;86:65–71.PubMedCrossRefGoogle Scholar
  30. 30.
    Britten JL, et al. Gonadotropin-releasing hormone (GnRH) agonist leuprolide acetate and GnRH antagonist cetrorelix acetate directly inhibit leiomyoma extracellular matrix production. Fertil Steril. 2012;98:1299–307.PubMedCrossRefGoogle Scholar
  31. 31.
    Malik M, et al. Gonadotropin-releasing hormone analogues inhibit leiomyoma extracellular matrix despite presence of gonadal hormones. Fertil Steril. 2016;105:214–24.PubMedCrossRefGoogle Scholar
  32. 32.
    Watanabe Y, et al. Efficacy of a low-dose leuprolide acetate depot in the treatment of uterine leiomyomata in Japanese women. Fertil Steril. 1992;58:66–71.PubMedCrossRefGoogle Scholar
  33. 33.
    Friedman AJ, Hoffman DI, Comite F, Browneller RW, Miller JD. Treatment of leiomyomata uteri with leuprolide acetate depot: a double-blind, placebo-controlled, multicenter study. The Leuprolide Study Group. Obstet Gynecol. 1991;77:720–5.PubMedGoogle Scholar
  34. 34.
    Cirkel U, et al. Experience with leuprorelin acetate depot in the treatment of fibroids: a German multicentre study. Clin Ther. 1992;14(Suppl A):37–50.PubMedGoogle Scholar
  35. 35.
    Lethaby A, Vollenhoven B, Sowter M. Pre-operative GnRH analogue therapy before hysterectomy or myomectomy for uterine fibroids. Cochrane Database Syst Rev. 2001;2:CD000547. Scholar
  36. 36.
    Trefoux Bourdet A, Luton D, Koskas M. Clinical utility of ulipristal acetate for the treatment of uterine fibroids: current evidence. Int J Womens Health. 2015;7:321–30.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Coddington CC, et al. Short term treatment with leuprolide acetate is a successful adjunct to surgical therapy of leiomyomas of the uterus. Surg Gynecol Obstet. 1992;175:57–63.PubMedGoogle Scholar
  38. 38.
    Donnez J, Donnez O, Dolmans M-M. With the advent of selective progesterone receptor modulators, what is the place of myoma surgery in current practice? Fertil Steril. 2014;102:640–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Kalampokas T, Kamath M, Boutas I, Kalampokas E. Ulipristal acetate for uterine fibroids: a systematic review and meta-analysis. Gynecol Endocrinol. 2016;32:91–6.PubMedCrossRefGoogle Scholar
  40. 40.
    Donnez J, et al. Ulipristal acetate versus placebo for fibroid treatment before surgery. N Engl J Med. 2012;366:409–20.PubMedCrossRefGoogle Scholar
  41. 41.
    Chwalisz K, et al. Selective progesterone receptor modulator development and use in the treatment of leiomyomata and endometriosis. Endocr Rev. 2005;26:423–38.PubMedCrossRefGoogle Scholar
  42. 42.
    Maruo T, et al. Effects of progesterone on growth factor expression in human uterine leiomyoma. Steroids. 2003;68:817–24.PubMedCrossRefGoogle Scholar
  43. 43.
    Luyckx M, et al. First series of 18 pregnancies after ulipristal acetate treatment for uterine fibroids. Fertil Steril. 2014;102:1404–9.PubMedCrossRefGoogle Scholar
  44. 44.
    Luyckx M, et al. Long-term nonsurgical control with ulipristal acetate of multiple uterine fibroids, enabling pregnancy. Am J Obstet Gynecol. 2016;214(6):756.e1–2. Scholar
  45. 45.
    Ke L-Q, Yang K, Li J, Li C-M. Danazol for uterine fibroids. Cochrane Database Syst Rev. 2009;3:CD007692. Scholar
  46. 46.
    Unlu C, Celik O, Celik N, Otlu B. Expression of endometrial receptivity genes increase after myomectomy of intramural leiomyomas not distorting the endometrial cavity. Reprod Sci. 2016;23:31–41.PubMedCrossRefGoogle Scholar
  47. 47.
    Casini ML, Rossi F, Agostini R, Unfer V. Effects of the position of fibroids on fertility. Gynecol Endocrinol. 2006;22:106–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Carranza-Mamane B, et al. The management of uterine fibroids in women with otherwise unexplained infertility. J Obstet Gynaecol Can. 2015;37:277–88.PubMedCrossRefGoogle Scholar
  49. 49.
    Dessolle L, et al. Determinants of pregnancy rate and obstetric outcome after laparoscopic myomectomy for infertility. Fertil Steril. 2001;76:370–4.PubMedCrossRefGoogle Scholar
  50. 50.
    Bulletti C, De Ziegler D, Polli V, Flamigni C. The role of leiomyomas in infertility. J Am Assoc Gynecol Laparosc. 1999;6:441–5.PubMedCrossRefGoogle Scholar
  51. 51.
    Metwally M, Cheong YC, Horne AW. Surgical treatment of fibroids for subfertility. Cochrane Database Syst Rev. 2012;11:CD003857.PubMedGoogle Scholar
  52. 52.
    Seracchioli R, et al. Fertility and obstetric outcome after laparoscopic myomectomy of large myomata: a randomized comparison with abdominal myomectomy. Hum Reprod. 2000;15:2663–8.PubMedCrossRefGoogle Scholar
  53. 53.
    Palomba S, et al. A multicenter randomized, controlled study comparing laparoscopic versus minilaparotomic myomectomy: reproductive outcomes. Fertil Steril. 2007;88:933–41.PubMedCrossRefGoogle Scholar
  54. 54.
    Thomas RL, Winkler N, Carr BR, Doody KM, Doody KJ. Abdominal myomectomy–a safe procedure in an ambulatory setting. Fertil Steril. 2010;94:2277–80.PubMedCrossRefGoogle Scholar
  55. 55.
    Iavazzo C, Mamais I, Gkegkes ID. Robotic assisted vs laparoscopic and/or open myomectomy: systematic review and meta-analysis of the clinical evidence. Arch Gynecol Obstet. 2016;294:5–17.PubMedCrossRefGoogle Scholar
  56. 56.
    van der Kooij SM, Bipat S, Hehenkamp WJK, Ankum WM, Reekers JA. Uterine artery embolization versus surgery in the treatment of symptomatic fibroids: a systematic review and meta-analysis. Am J Obstet Gynecol. 2011;205:317.e1–18.CrossRefGoogle Scholar
  57. 57.
    Moss JG, et al. Randomised comparison of uterine artery embolisation (UAE) with surgical treatment in patients with symptomatic uterine fibroids (REST trial): 5-year results. BJOG. 2011;118:936–44.PubMedCrossRefGoogle Scholar
  58. 58.
    Jun F, et al. Uterine artery embolization versus surgery for symptomatic uterine fibroids: a randomized controlled trial and a meta-analysis of the literature. Arch Gynecol Obstet. 2012;285:1407–13.PubMedCrossRefGoogle Scholar
  59. 59.
    Ananthakrishnan G, et al. Randomized comparison of uterine artery embolization (UAE) with surgical treatment in patients with symptomatic uterine fibroids (REST trial): subanalysis of 5-year MRI findings. Cardiovasc Intervent Radiol. 2013;36:676–81.PubMedCrossRefGoogle Scholar
  60. 60.
    Torre A, et al. Uterine artery embolization for severe symptomatic fibroids: effects on fertility and symptoms. Hum Reprod. 2014;29:490–501.PubMedCrossRefGoogle Scholar
  61. 61.
    Mara M, et al. Midterm clinical and first reproductive results of a randomized controlled trial comparing uterine fibroid embolization and myomectomy. Cardiovasc Intervent Radiol. 2008;31:73–85.PubMedCrossRefGoogle Scholar
  62. 62.
    Goldberg J, et al. Pregnancy outcomes after treatment for fibromyomata: uterine artery embolization versus laparoscopic myomectomy. Am J Obstet Gynecol. 2004;191:18–21.PubMedCrossRefGoogle Scholar
  63. 63.
    Berkane N, Moutafoff-Borie C. Impact of previous uterine artery embolization on fertility. Curr Opin Obstet Gynecol. 2010;22:242–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Hehenkamp WJK, et al. Loss of ovarian reserve after uterine artery embolization: a randomized comparison with hysterectomy. Hum Reprod. 2007;22:1996–2005.PubMedCrossRefGoogle Scholar
  65. 65.
    Clark NA, Mumford SL, Segars JH. Reproductive impact of MRI-guided focused ultrasound surgery for fibroids: a systematic review of the evidence. Curr Opin Obstet Gynecol. 2014;26:151–61.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Rabinovici J, et al. Pregnancy outcome after magnetic resonance-guided focused ultrasound surgery (MRgFUS) for conservative treatment of uterine fibroids. Fertil Steril. 2010;93:199–209.PubMedCrossRefGoogle Scholar
  67. 67.
    Berman JM, et al. Three-year outcome of the Halt trial: a prospective analysis of radiofrequency volumetric thermal ablation of myomas. J Minim Invasive Gynecol. 2014;21:767–74.PubMedCrossRefGoogle Scholar
  68. 68.
    Brucker SY, et al. Laparoscopic radiofrequency volumetric thermal ablation of fibroids versus laparoscopic myomectomy. Int J Gynaecol Obstet. 2014;125:261–5.PubMedCrossRefGoogle Scholar
  69. 69.
    Peterson WF, Novak ER. Endometrial polyps. Obstet Gynecol. 1956;8:40–9.PubMedGoogle Scholar
  70. 70.
    Shokeir TA, Shalan HM, El-Shafei MM. Significance of endometrial polyps detected hysteroscopically in eumenorrheic infertile women. J Obstet Gynaecol Res. 2004;30:84–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Salim S, Won H, Nesbitt-Hawes E, Campbell N, Abbott J. Diagnosis and management of endometrial polyps: a critical review of the literature. J Minim Invasive Gynecol. 2011;18:569–81.PubMedCrossRefGoogle Scholar
  72. 72.
    Hinckley MD, Milki AA. 1000 office-based hysteroscopies prior to in vitro fertilization: feasibility and findings. JSLS. 2004;8:103–7.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Fatemi HM, et al. Prevalence of unsuspected uterine cavity abnormalities diagnosed by office hysteroscopy prior to in vitro fertilization. Hum Reprod. 2010;25:1959–65.PubMedCrossRefGoogle Scholar
  74. 74.
    Bozkurt M, Şahin L, Ulaş M. Hysteroscopic polypectomy decreases NF-κB1 expression in the mid-secretory endometrium of women with endometrial polyp. Eur J Obstet Gynecol Reprod Biol. 2015;189:96–100.PubMedCrossRefGoogle Scholar
  75. 75.
    Pinheiro A, et al. Expression of hormone receptors, Bcl-2, Cox-2 and Ki67 in benign endometrial polyps and their association with obesity. Mol Med Rep. 2014;9:2335–41.PubMedCrossRefGoogle Scholar
  76. 76.
    Hasegawa E, et al. Expression of leukemia inhibitory factor in the endometrium in abnormal uterine cavities during the implantation window. Fertil Steril. 2012;97:953–8.PubMedCrossRefGoogle Scholar
  77. 77.
    Ben-Nagi J, Miell J, Yazbek J, Holland T, Jurkovic D. The effect of hysteroscopic polypectomy on the concentrations of endometrial implantation factors in uterine flushings. Reprod Biomed Online. 2009;19:737–44.PubMedCrossRefGoogle Scholar
  78. 78.
    Bosteels J, et al. Hysteroscopy for treating subfertility associated with suspected major uterine cavity abnormalities. Cochrane Database Syst Rev. 2015;2:CD009461.Google Scholar
  79. 79.
    Pérez-Medina T, et al. Endometrial polyps and their implication in the pregnancy rates of patients undergoing intrauterine insemination: a prospective, randomized study. Hum Reprod. 2005;20:1632–5.PubMedCrossRefGoogle Scholar
  80. 80.
    Kodaman PH. Hysteroscopic polypectomy for women undergoing IVF treatment: when is it necessary? Curr Opin Obstet Gynecol. 2016;28(3):184–90. Scholar
  81. 81.
    Pundir J, Pundir V, Omanwa K, Khalaf Y, El-Toukhy T. Hysteroscopy prior to the first IVF cycle: a systematic review and meta-analysis. Reprod Biomed Online. 2014;28:151–61.PubMedCrossRefGoogle Scholar
  82. 82.
    Bosteels J, et al. Anti-adhesion therapy following operative hysteroscopy for treatment of female subfertility. Cochrane Database Syst Rev. 2015;11:CD011110.Google Scholar
  83. 83.
    Evans-Hoeker EA, Young SL. Endometrial receptivity and intrauterine adhesive disease. Semin Reprod Med. 2014;32:392–401.PubMedCrossRefGoogle Scholar
  84. 84.
    Schenker JG, Margalioth EJ. Intrauterine adhesions: an updated appraisal. Fertil Steril. 1982;37:593–610.PubMedCrossRefGoogle Scholar
  85. 85.
    Yu D, Wong Y-M, Cheong Y, Xia E, Li T-C. Asherman syndrome–one century later. Fertil Steril. 2008;89:759–79.PubMedCrossRefGoogle Scholar
  86. 86.
    Wang X, Li Z, A YN, Zou S. Hysteroscopy for early abortion after IVF-ET: clinical analysis of 84 cases. Zhonghua Nan Ke Xue. 2011;17:52–4.PubMedGoogle Scholar
  87. 87.
    Thomson AJM, Abbott JA, Deans R, Kingston A, Vancaillie TG. The management of intrauterine synechiae. Curr Opin Obstet Gynecol. 2009;21:335–41.PubMedCrossRefGoogle Scholar
  88. 88.
    Deans R, Abbott J. Review of intrauterine adhesions. J Minim Invasive Gynecol. 2010;17:555–69.PubMedCrossRefGoogle Scholar
  89. 89.
    Leung PL, Tam WH, Yuen PM. Hysteroscopic appearance of the endometrial cavity following thermal balloon endometrial ablation. Fertil Steril. 2003;79:1226–8.PubMedCrossRefGoogle Scholar
  90. 90.
    Taskin O, et al. Long-term histopathologic and morphologic changes after thermal endometrial ablation. J Am Assoc Gynecol Laparosc. 2002;9:186–90.PubMedCrossRefGoogle Scholar
  91. 91.
    Mukul LV, Linn JG. Pregnancy complicated by uterine synechiae after endometrial ablation. Obstet Gynecol. 2005;105:1179–82.PubMedCrossRefGoogle Scholar
  92. 92.
    Schenker JG. Etiology of and therapeutic approach to synechia uteri. Eur J Obstet Gynecol Reprod Biol. 1996;65:109–13.PubMedCrossRefGoogle Scholar
  93. 93.
    Foix A, et al. The pathology of postcurettage intrauterine adhesions. Am J Obstet Gynecol. 1966;96:1027–33.PubMedCrossRefGoogle Scholar
  94. 94.
    Polishuk WZ, Anteby SO, Weinstein D. Puerperal endometritis and intrauterine adhesions. Int Surg. 1975;60:418–20.PubMedGoogle Scholar
  95. 95.
    Valle RF, Sciarra JJ. Intrauterine adhesions: hysteroscopic diagnosis, classification, treatment, and reproductive outcome. Am J Obstet Gynecol. 1988;158:1459–70.PubMedCrossRefGoogle Scholar
  96. 96.
    Katz Z, Ben-Arie A, Lurie S, Manor M, Insler V. Reproductive outcome following hysteroscopic adhesiolysis in Asherman’s syndrome. Int J Fertil Menopausal Stud. 1996;41:462–5.PubMedGoogle Scholar
  97. 97.
    The American Fertility Society classifications of adnexal adhesions, distal tubal occlusion, tubal occlusion secondary to tubal ligation, tubal pregnancies, müllerian anomalies and intrauterine adhesions. Fertil Steril. 1988;49:944–55.Google Scholar
  98. 98.
    Saravelos SH, Cocksedge KA, Li T-C. Prevalence and diagnosis of congenital uterine anomalies in women with reproductive failure: a critical appraisal. Hum Reprod Update. 2008;14:415–29.PubMedCrossRefGoogle Scholar
  99. 99.
    Patton PE. Anatomic uterine defects. Clin Obstet Gynecol. 1994;37:705–21.PubMedCrossRefGoogle Scholar
  100. 100.
    Grimbizis GF, Camus M, Tarlatzis BC, Bontis JN, Devroey P. Clinical implications of uterine malformations and hysteroscopic treatment results. Hum Reprod Update. 2001;7:161–74.PubMedCrossRefGoogle Scholar
  101. 101.
    Homer HA, Li TC, Cooke ID. The septate uterus: a review of management and reproductive outcome. Fertil Steril. 2000;73:1–14.PubMedCrossRefGoogle Scholar
  102. 102.
    Kupesic S. Clinical implications of sonographic detection of uterine anomalies for reproductive outcome. Ultrasound Obstet Gynecol. 2001;18:387–400.PubMedCrossRefGoogle Scholar
  103. 103.
    Letterie G. Structural abnormalities and reproductive failure: effective techniques for diagnosis and management. New York: Blackwell Science; 1998.Google Scholar
  104. 104.
    Lavergne N, Aristizabal J, Zarka V, Erny R, Hedon B. Uterine anomalies and in vitro fertilization: what are the results? Eur J Obstet Gynecol Reprod Biol. 1996;68:29–34.PubMedCrossRefGoogle Scholar
  105. 105.
    Heinonen PK, Saarikoski S, Pystynen P. Reproductive performance of women with uterine anomalies. An evaluation of 182 cases. Acta Obstet Gynecol Scand. 1982;61:157–62.PubMedCrossRefGoogle Scholar
  106. 106.
    DeCherney AH, Russell JB, Graebe RA, Polan ML. Resectoscopic management of müllerian fusion defects. Fertil Steril. 1986;45:726–8.PubMedCrossRefGoogle Scholar
  107. 107.
    Fayez JA. Comparison between abdominal and hysteroscopic metroplasty. Obstet Gynecol. 1986;68:399–403.PubMedCrossRefGoogle Scholar
  108. 108.
    Devi Wold AS, Pham N, Arici A. Anatomic factors in recurrent pregnancy loss. Semin Reprod Med. 2006;24:25–32.PubMedCrossRefGoogle Scholar
  109. 109.
    Propst AM, Hill JA. Anatomic factors associated with recurrent pregnancy loss. Semin Reprod Med. 2000;18:341–50.PubMedCrossRefGoogle Scholar
  110. 110.
    Bailey AP, Jaslow CR, Kutteh WH. Minimally invasive surgical options for congenital and acquired uterine factors associated with recurrent pregnancy loss. Womens Health. 2015;11:161–7.Google Scholar
  111. 111.
    Chan YY, et al. Reproductive outcomes in women with congenital uterine anomalies: a systematic review. Ultrasound Obstet Gynecol. 2011;38:371–82.PubMedCrossRefGoogle Scholar
  112. 112.
    Fedele L, et al. Ultrastructural aspects of endometrium in infertile women with septate uterus. Fertil Steril. 1996;65:750–2.PubMedCrossRefGoogle Scholar
  113. 113.
    Sparac V, Kupesic S, Ilijas M, Zodan T, Kurjak A. Histologic architecture and vascularization of hysteroscopically excised intrauterine septa. J Am Assoc Gynecol Laparosc. 2001;8:111–6.PubMedCrossRefGoogle Scholar
  114. 114.
    Raga F, Casañ EM, Bonilla-Musoles F. Expression of vascular endothelial growth factor receptors in the endometrium of septate uterus. Fertil Steril. 2009;92:1085–90.PubMedCrossRefGoogle Scholar
  115. 115.
    Taylor E, Gomel V. The uterus and fertility. Fertil Steril. 2008;89:1–16.PubMedCrossRefGoogle Scholar
  116. 116.
    Mollo A, et al. Hysteroscopic resection of the septum improves the pregnancy rate of women with unexplained infertility: a prospective controlled trial. Fertil Steril. 2009;91:2628–31.PubMedCrossRefGoogle Scholar
  117. 117.
    Venetis CA, et al. Clinical implications of congenital uterine anomalies: a meta-analysis of comparative studies. Reprod Biomed Online. 2014;29:665–83.PubMedCrossRefGoogle Scholar
  118. 118.
    Kowalik CR, et al. Metroplasty versus expectant management for women with recurrent miscarriage and a septate uterus. Cochrane Database Syst Rev. 2011;6:CD008576. Scholar
  119. 119.
    Raga F, et al. Reproductive impact of congenital Müllerian anomalies. Hum Reprod. 1997;12:2277–81.PubMedCrossRefGoogle Scholar
  120. 120.
    Mucowski SJ, Herndon CN, Rosen MP. The arcuate uterine anomaly: a critical appraisal of its diagnostic and clinical relevance. Obstet Gynecol Surv. 2010;65:449–54.PubMedCrossRefGoogle Scholar
  121. 121.
    Reichman D, Laufer MR, Robinson BK. Pregnancy outcomes in unicornuate uteri: a review. Fertil Steril. 2009;91:1886–94.PubMedCrossRefGoogle Scholar
  122. 122.
    Buttram VC. Müllerian anomalies and their management. Fertil Steril. 1983;40:159–63.PubMedCrossRefGoogle Scholar
  123. 123.
    Heinonen PK. Clinical implications of the didelphic uterus: long-term follow-up of 49 cases. Eur J Obstet Gynecol Reprod Biol. 2000;91:183–90.PubMedCrossRefGoogle Scholar
  124. 124.
    Mashiach S, Ben-Rafael Z, Dor J, Serr DM. Triplet pregnancy in uterus didelphys with delivery interval of 72 days. Obstet Gynecol. 1981;58:519–21.PubMedGoogle Scholar
  125. 125.
    Papp Z, Mezei G, Gávai M, Hupuczi P, Urbancsek J. Reproductive performance after transabdominal metroplasty: a review of 157 consecutive cases. J Reprod Med. 2006;51:544–52.PubMedGoogle Scholar
  126. 126.
    Chu J, et al. Salpingostomy in the treatment of hydrosalpinx: a systematic review and meta-analysis. Hum Reprod. 2015;30:1882–95.PubMedCrossRefGoogle Scholar
  127. 127.
    Bahamondes L, et al. Identification of main risk factors for tubal infertility. Fertil Steril. 1994;61:478–82.PubMedCrossRefGoogle Scholar
  128. 128.
    Zeyneloglu HB, Arici A, Olive DL. Adverse effects of hydrosalpinx on pregnancy rates after in vitro fertilization-embryo transfer. Fertil Steril. 1998;70:492–9.PubMedCrossRefGoogle Scholar
  129. 129.
    Camus E, et al. 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;14:1243–9.PubMedCrossRefGoogle Scholar
  130. 130.
    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;8:157–9.PubMedCrossRefGoogle Scholar
  131. 131.
    Andersen AN, Lindhard A, Loft A, Ziebe S, Andersen CY. The infertile patient with hydrosalpinges–IVF with or without salpingectomy? Hum Reprod. 1996;11:2081–4.PubMedCrossRefGoogle Scholar
  132. 132.
    Vandromme J, et al. Hydrosalpinges in in-vitro fertilization: an unfavourable prognostic feature. Hum Reprod. 1995;10:576–9.PubMedCrossRefGoogle Scholar
  133. 133.
    Strandell A, Lindhard A. Why does hydrosalpinx reduce fertility? The importance of hydrosalpinx fluid. Hum Reprod. 2002;17(5):1141.PubMedCrossRefGoogle Scholar
  134. 134.
    Jiang H, Pei H, Zhang W, Wang X. A prospective clinical study of interventional ultrasound sclerotherapy on women with hydrosalpinx before in vitro fertilization and embryo transfer. Fertil Steril. 2010;94:2854–6.PubMedCrossRefGoogle Scholar
  135. 135.
    Li L, et al. 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;151:171–5.PubMedCrossRefGoogle Scholar
  136. 136.
    Song Y, et al. NF κB expression increases and CFTR and MUC1 expression decreases in the endometrium of infertile patients with hydrosalpinx: a comparative study. Reprod Biol Endocrinol. 2012;10:86.PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Daftary GS, et al. Salpingectomy increases peri-implantation endometrial HOXA10 expression in women with hydrosalpinx. Fertil Steril. 2007;87:367–72.PubMedCrossRefGoogle Scholar
  138. 138.
    Seli E, et al. Removal of hydrosalpinges increases endometrial leukaemia inhibitory factor (LIF) expression at the time of the implantation window. Hum Reprod. 2005;20:3012–7.PubMedCrossRefGoogle Scholar
  139. 139.
    Bildirici I, Bukulmez O, Ensari A, Yarali H, Gurgan T. A prospective evaluation of the effect of salpingectomy on endometrial receptivity in cases of women with communicating hydrosalpinges. Hum Reprod. 2001;16:2422–6.PubMedCrossRefGoogle Scholar
  140. 140.
    Bedaiwy MA, et al. Relationship between oxidative stress and embryotoxicity of hydrosalpingeal fluid. Hum Reprod. 2002;17:601–4.PubMedCrossRefGoogle Scholar
  141. 141.
    Bedaiwy MA, et al. Relationship between cytokines and the embryotoxicity of hydrosalpingeal fluid. J Assist Reprod Genet. 2005;22:161–5.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Johnson N, van Voorst S, Sowter MC, Strandell A, Mol BWJ. Surgical treatment for tubal disease in women due to undergo in vitro fertilisation. Cochrane Database Syst Rev. 2010;1:CD002125. Scholar
  143. 143.
    Kontoravdis A, et al. Proximal tubal occlusion and salpingectomy result in similar improvement in in vitro fertilization outcome in patients with hydrosalpinx. Fertil Steril. 2006;86:1642–9.PubMedCrossRefGoogle Scholar
  144. 144.
    Chanelles O, et al. Hydrosalpinx and infertility: what about conservative surgical management? Eur J Obstet Gynecol Reprod Biol. 2011;159:122–6.PubMedCrossRefGoogle Scholar
  145. 145.
    Dreyer K, et al. Hysteroscopic proximal tubal occlusion versus laparoscopic salpingectomy as a treatment for hydrosalpinges prior to IVF or ICSI: an RCT. Hum Reprod. 2016.
  146. 146.
    Hammadieh N, et al. Ultrasound-guided hydrosalpinx aspiration during oocyte collection improves pregnancy outcome in IVF: a randomized controlled trial. Hum Reprod. 2008;23:1113–7.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Jeffrey M. Goldberg
    • 1
  • Julian Gingold
    • 1
  • Natalia Llarena
    • 1
  1. 1.Department of Gynecology and ObstetricsCleveland ClinicClevelandUSA

Personalised recommendations