Download PDF
Semin Reprod Med 2007; 25(6): 476-482
DOI: 10.1055/s-2007-991045
© Thieme Medical Publishers

The Influence of Hydrosalpinx on Markers of Endometrial Receptivity

Ricardo Francalacci Savaris1 , 2 , Linda C. Giudice2
  • 1Departamento de Ginecologia e Obstetricia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
  • 2Department of Obstetrics and Gynecology, University of California, San Francisco, California
Further Information

Publication History

Publication Date:
25 October 2007 (online)

    Permissions and Reprints

ABSTRACT

Hydrosalpinx is a common condition among women of reproductive age. It is related to low pregnancy rates in the settings of in vitro fertilization-embryo transfer programs. Such low rates are not yet well understood, and may be due to poor endometrial receptivity and abnormal expression of key molecules in the endometrium that are important for implantation. The available data on the inflammatory response, endometrial blood flow, integrins, leukemia inhibitory factor, matrix metalloproteinases, and homeobox gene A10 expression in the presence of hydrosalpinx are reviewed. In addition, the evidence for treatment options to improve pregnancy rates is also discussed.

KEYWORDS

Hydrosalpinx - endometrium

REFERENCES

  • 1 Andersen A N, Yue Z, Meng F J, Petersen K. Low implantation rate after in-vitro fertilization in patients with hydrosalpinges diagnosed by ultrasonography.  Hum Reprod. 1994;  9 1935-1938
    PubMedGoogle Scholar
  • 2 Katz E, Akman M A, Damewood M D, Garcia J E. Deleterious effect of the presence of hydrosalpinx on implantation and pregnancy rates with in vitro fertilization.  Fertil Steril. 1996;  66 122-125
    PubMedGoogle Scholar
  • 3 Strandell A, Waldenstrom U, Nilsson L, Hamberger L. Hydrosalpinx reduces in-vitro fertilization/embryo transfer pregnancy rates.  Hum Reprod. 1994;  9 861-863
    PubMedGoogle Scholar
  • 4 Blazar A S, Hogan J W, Seifer D B, Frishman G N, Wheeler C A, Haning R V. The impact of hydrosalpinx on successful pregnancy in tubal factor infertility treated by in vitro fertilization.  Fertil Steril. 1997;  67 517-520
    CrossrefPubMedGoogle Scholar
  • 5 Murray C A, Clarke H J, Tulandi T, Tan S L. Inhibitory effect of human hydrosalpingeal fluid on mouse preimplantation embryonic development is significantly reduced by the addition of lactate.  Hum Reprod. 1997;  12 2504-2507
    CrossrefPubMedGoogle Scholar
  • 6 Lass A. What effect does hydrosalpinx have on assisted reproduction? What is the preferred treatment for hydrosalpines? The ovary's perspective.  Hum Reprod. 1999;  14 1674-1677
    CrossrefPubMedGoogle Scholar
  • 7 Paik C K, Waetjen L E, Xing G, Dai J, Sweet R L. Hospitalizations for pelvic inflammatory disease and tuboovarian abscess.  Obstet Gynecol. 2006;  107 611-616
    PubMedGoogle Scholar
  • 8 Mage G, Pouly J L, de Joliniere J B, Chabrand S, Riouallon A, Bruhat M A. A preoperative classification to predict the intrauterine and ectopic pregnancy rates after distal tubal microsurgery.  Fertil Steril. 1986;  46 807-810
    PubMedGoogle Scholar
  • 9 The American Fertility Society classifications of adnexal adhesions, distal tubal occlusion, tubal occlusion secondary to tubal ligation, tubal pregnancies, mullerian anomalies and intrauterine adhesions.  Fertil Steril. 1988;  49 944-955
    PubMedGoogle Scholar
  • 10 Boer-Meisel M E, te Velde E R, Habbema J D, Kardaun J W. Predicting the pregnancy outcome in patients treated for hydrosalpinx: a prospective study.  Fertil Steril. 1986;  45 23-29
    PubMedGoogle Scholar
  • 11 Rock J A, Katayama K P, Martin E J, Woodruff J D, Jones Jr H W. Factors influencing the success of salpingostomy techniques for distal fimbrial obstruction.  Obstet Gynecol. 1978;  52 591-596
    PubMedGoogle Scholar
  • 12 Puttemans P, Brosens I, Delattin P, Vasquez G, Boeckx W. Salpingoscopy versus hysterosalpingography in hydrosalpinges.  Hum Reprod. 1987;  2 535-540
    PubMedGoogle Scholar
  • 13 Donnez J, Casanas-Roux F. Prognostic factors of fimbrial microsurgery.  Fertil Steril. 1986;  46 200-204
    PubMedGoogle Scholar
  • 14 Leese H J, Tay J I, Reischl J, Downing S J. Formation of Fallopian tubal fluid: role of a neglected epithelium.  Reproduction. 2001;  121 339-346
    CrossrefPubMedGoogle Scholar
  • 15 Tay J I, Rutherford A J, Killick S R, Maguiness S D, Partridge R J, Leese H J. Human tubal fluid: production, nutrient composition and response to adrenergic agents.  Hum Reprod. 1997;  12 2451-2456
    CrossrefPubMedGoogle Scholar
  • 16 The influence of hydrosalpinx on IVF and embryo transfer: a review.  Hum Reprod Update. 2000;  6 387-395
    CrossrefPubMedGoogle Scholar
  • 17 Seli E, Kayisli U A, Cakmak H et al.. Removal of hydrosalpinges increases endometrial leukaemia inhibitory factor (LIF) expression at the time of the implantation window.  Hum Reprod. 2005;  20 3012-3017
    CrossrefPubMedGoogle Scholar
  • 18 Gardner D K, Lane M, Calderon I, Leeton J. Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells.  Fertil Steril. 1996;  65 349-353
    PubMedGoogle Scholar
  • 19 Quinton P M. Cystic fibrosis: a disease in electrolyte transport.  FASEB J. 1990;  4 2709-2717
    PubMedGoogle Scholar
  • 20 Quinton P M. Physiological basis of cystic fibrosis: a historical perspective.  Physiol Rev. 1999;  79 S3-S22
    CrossrefPubMedGoogle Scholar
  • 21 Ajonuma L C, Ng E H, Chow P H et al.. Increased cystic fibrosis transmembrane conductance regulator (CFTR) expression in the human hydrosalpinx.  Hum Reprod. 2005;  20 1228-1234
    CrossrefPubMedGoogle Scholar
  • 22 Arredondo J L, Diaz V, Gaitan H et al.. Oral clindamycin and ciprofloxacin versus intramuscular ceftriaxone and oral doxycycline in the treatment of mild-to-moderate pelvic inflammatory disease in outpatients.  Clin Infect Dis. 1997;  24 170-178
    PubMedGoogle Scholar
  • 23 Ajonuma L C, Ng E H, Chan L N et al.. Ultrastructural characterization of whole hydrosalpinx from infertile Chinese women.  Cell Biol Int. 2005;  29 849-856
    CrossrefPubMedGoogle Scholar
  • 24 Ajonuma L C, Ng E H, Chan H C. New insights into the mechanisms underlying hydrosalpinx fluid formation and its adverse effect on IVF outcome.  Hum Reprod Update. 2002;  8 255-264
    CrossrefPubMedGoogle Scholar
  • 25 Gordon J D, Mesiano S, Zaloudek C J, Jaffe R B. Vascular endothelial growth factor localization in human ovary and fallopian tubes: possible role in reproductive function and ovarian cyst formation.  J Clin Endocrinol Metab. 1996;  81 353-359
    CrossrefPubMedGoogle Scholar
  • 26 Lam P M, Briton-Jones C, Cheung C K, Lok I H, Cheung L P, Haines C. In vivo regulation of mRNA expression of vascular endothelial growth factor receptors (KDR and flt-1) in the human oviduct.  Fertil Steril. 2004;  81 416-423
    CrossrefPubMedGoogle Scholar
  • 27 Lam P M, Briton-Jones C, Cheung C K, Po L S, Cheung L P, Haines C. Increased mRNA expression of vascular endothelial growth factor and its receptor (flt-1) in the hydrosalpinx.  Hum Reprod. 2003;  18 2264-2269
    CrossrefPubMedGoogle Scholar
  • 28 Mansour R T, Aboulghar M A, Serour G I, Riad R. Fluid accumulation of the uterine cavity before embryo transfer: a possible hindrance for implantation.  J In Vitro Fert Embryo Transf. 1991;  8 157-159
    PubMedGoogle Scholar
  • 29 Eytan O, Azem F, Gull I, Wolman I, Elad D, Jaffa A J. The mechanism of hydrosalpinx in embryo implantation.  Hum Reprod. 2001;  16 2662-2667
    CrossrefPubMedGoogle Scholar
  • 30 Watermeyer S R, Bhal K. Chronic vaginal discharge secondary to a hydrosalpinx.  J Obstet Gynaecol. 2002;  22 324
    PubMedGoogle Scholar
  • 31 Kiviat N B, Wolner-Hanssen P, Eschenbach D A et al.. Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis.  Am J Surg Pathol. 1990;  14 167-175
    PubMedGoogle Scholar
  • 32 Ness R B, Soper D E, Holley R L et al.. Effectiveness of inpatient and outpatient treatment strategies for women with pelvic inflammatory disease: results from the Pelvic Inflammatory Disease Evaluation and Clinical Health (PEACH) Randomized Trial.  Am J Obstet Gynecol. 2002;  186 929-937
    CrossrefPubMedGoogle Scholar
  • 33 Korn A P, Hessol N A, Padian N S et al.. Risk factors for plasma cell endometritis among women with cervical Neisseria gonorrhoeae, cervical Chlamydia trachomatis, or bacterial vaginosis.  Am J Obstet Gynecol. 1998;  178 987-990
    CrossrefPubMedGoogle Scholar
  • 34 Achilles S L, Amortegui A J, Wiesenfeld H C. Endometrial plasma cells: do they indicate subclinical pelvic inflammatory disease?.  Sex Transm Dis. 2005;  32 185-188
    PubMedGoogle Scholar
  • 35 Copperman A B, Wells V, Luna M, Kalir T, Sandler B, Mukherjee T. Presence of hydrosalpinx correlated to endometrial inflammatory response in vivo.  Fertil Steril. 2006;  86 972-976
    CrossrefPubMedGoogle Scholar
  • 36 Hill J A, Polgar K, Anderson D J. T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion.  JAMA. 1995;  273 1933-1936
    CrossrefPubMedGoogle Scholar
  • 37 Ng S C, Gilman-Sachs A, Thaker P, Beaman K D, Beer A E, Kwak-Kim J. Expression of intracellular Th1 and Th2 cytokines in women with recurrent spontaneous abortion, implantation failures after IVF/ET or normal pregnancy.  Am J Reprod Immunol. 2002;  48 77-86
    CrossrefPubMedGoogle Scholar
  • 38 Ito C, Ito M, Itakura A, Asai M, Narita O, Mizutani S. A prospective evaluation of the effects of salpingectomy on endometrial lymphocyte clusters in patients with hydrosalpinges.  Fertil Steril. 2004;  82 149-153
    PubMedGoogle Scholar
  • 39 Jinno M, Ozaki T, Iwashita M, Nakamura Y, Kudo A, Hirano H. Measurement of endometrial tissue blood flow: a novel way to assess uterine receptivity for implantation.  Fertil Steril. 2001;  76 1168-1174
    CrossrefPubMedGoogle Scholar
  • 40 Ng E H, Chan C C, Tang O S, Ho P C. Comparison of endometrial and subendometrial blood flows among patients with and without hydrosalpinx shown on scanning during in vitro fertilization treatment.  Fertil Steril. 2006;  85 333-338
    CrossrefPubMedGoogle Scholar
  • 41 Hehlgans S, Haase M, Cordes N. Signalling via integrins: implications for cell survival and anticancer strategies.  Biochim Biophys Acta. 2007;  175 163-180
    PubMedGoogle Scholar
  • 42 Achache H, Revel A. Endometrial receptivity markers, the journey to successful embryo implantation.  Hum Reprod Update. 2006;  12 731-746
    CrossrefPubMedGoogle Scholar
  • 43 Lessey B A, Damjanovich L, Coutifaris C, Castelbaum A, Albelda S M, Buck C A. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle.  J Clin Invest. 1992;  90 188-195
    CrossrefPubMedGoogle Scholar
  • 44 Lessey B A, Castelbaum A J, Wolf L et al.. Use of integrins to date the endometrium.  Fertil Steril. 2000;  73 779-787
    CrossrefPubMedGoogle Scholar
  • 45 Meyer W R, Castelbaum A J, Somkuti S et al.. Hydrosalpinges adversely affect markers of endometrial receptivity.  Hum Reprod. 1997;  12 1393-1398
    CrossrefPubMedGoogle Scholar
  • 46 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 2422-2426
    PubMedGoogle Scholar
  • 47 Savaris R F, Pedrini J L, Flores R, Fabris G, Zettler C G. Expression of alpha 1 and beta 3 integrins subunits in the endometrium of patients with tubal phimosis or hydrosalpinx.  Fertil Steril. 2006;  85 188-192
    CrossrefPubMedGoogle Scholar
  • 48 Gearing D P. The leukemia inhibitory factor and its receptor.  Adv Immunol. 1993;  53 31-58
    PubMedGoogle Scholar
  • 49 Hilton D J. LIF: lots of interesting functions.  Trends Biochem Sci. 1992;  17 72-76
    CrossrefPubMedGoogle Scholar
  • 50 Stewart C L, Kaspar P, Brunet L J et al.. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor.  Nature. 1992;  359 76-79
    CrossrefPubMedGoogle Scholar
  • 51 Charnock-Jones D S, Sharkey A M, Fenwick P, Smith S K. Leukaemia inhibitory factor mRNA concentration peaks in human endometrium at the time of implantation and the blastocyst contains mRNA for the receptor at this time.  J Reprod Fertil. 1994;  101 421-426
    CrossrefPubMedGoogle Scholar
  • 52 Talbi S, Hamilton A E, Vo K C et al.. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women.  Endocrinology. 2006;  147 1097-1121
    CrossrefPubMedGoogle Scholar
  • 53 Laird S M, Tuckerman E M, Dalton C F, Dunphy B C, Li T C, Zhang X. The production of leukaemia inhibitory factor by human endometrium: presence in uterine flushings and production by cells in culture.  Hum Reprod. 1997;  12 569-574
    CrossrefPubMedGoogle Scholar
  • 54 Cohen M, Meisser A, Bischof P. Metalloproteinases and human placental invasiveness.  Placenta. 2006;  27 783-793
    CrossrefPubMedGoogle Scholar
  • 55 VanSaun M N, Matrisian L M. Matrix metalloproteinases and cellular motility in development and disease.  Birth Defects Res C Embryo Today. 2006;  78 69-79
    CrossrefPubMedGoogle Scholar
  • 56 Isaka K, Usuda S, Ito H et al.. Expression and activity of matrix metalloproteinase 2 and 9 in human trophoblasts.  Placenta. 2003;  24 53-64
    CrossrefPubMedGoogle Scholar
  • 57 Xu P, Wang Y L, Zhu S J, Luo S Y, Piao Y S, Zhuang L Z. Expression of matrix metalloproteinase-2, -9, and -14, tissue inhibitors of metalloproteinase-1, and matrix proteins in human placenta during the first trimester.  Biol Reprod. 2000;  62 988-994
    CrossrefPubMedGoogle Scholar
  • 58 Dong J C, Dong H, Campana A, Bischof P. Matrix metalloproteinases and their specific tissue inhibitors in menstruation.  Reproduction. 2002;  123 621-631
    CrossrefPubMedGoogle Scholar
  • 59 Salamonsen L A, Woolley D E. Matrix metalloproteinases in normal menstruation.  Hum Reprod. 1996;  11(suppl 2) 124-133
    PubMedGoogle Scholar
  • 60 Jastrow N, Chardonnens D, Araman M, Meisser A, Campana A, Bischof P. Effect of hydrosalpinx fluid on secretion of trophoblastic matrix metalloproteinases.  Fertil Steril. 2002;  77 588-594
    CrossrefPubMedGoogle Scholar
  • 61 Daftary G S, Taylor H S. Endocrine regulation of HOX genes.  Endocr Rev. 2006;  27 331-355
    CrossrefPubMedGoogle Scholar
  • 62 Daftary G S, Taylor H S. Hydrosalpinx fluid diminishes endometrial cell HOXA10 expression.  Fertil Steril. 2002;  78 577-580
    CrossrefPubMedGoogle Scholar
  • 63 Daftary G S, Kayisli U, Seli E, Bukulmez O, Arici A, Taylor H S. Salpingectomy increases peri-implantation endometrial HOXA10 expression in women with hydrosalpinx.  Fertil Steril. 2007;  87 367-372
    Google Scholar
  • 64 Kelekci S, Yilmaz B, Yakut Y, Yasar L, Savan K, Sonmez S. Hormonal and ovarian stromal blood supply changes after laparoscopic tubal sterilization: a prospective controlled study.  Contraception. 2006;  73 279-283
    CrossrefPubMedGoogle Scholar
  • 65 Baloglu A, Uysal D, Karci L, Guven C M, Yavuz E. Effects of laparoscopic tubal ligation on ovarian blood flow and steroidogenesis.  Clin Exp Obstet Gynecol. 2005;  32 230-232
    PubMedGoogle Scholar
  • 66 Dede F S, Akyuz O, Dilbaz B, Caliskan E, Haberal A. Color Doppler flow analysis of uterine and ovarian arteries before and after tubal sterilization: electrocautery versus Pomeroy.  Gynecol Obstet Invest. 2006;  61 45-48
    CrossrefPubMedGoogle Scholar
  • 67 Kutlar I, Ozkur A, Balat O, Ugur M G, Genco Y, Aksoy F. Effects of three different sterilization methods on utero-ovarian Doppler blood flow and serum levels of ovarian hormones.  Eur J Obstet Gynecol Reprod Biol. 2005;  122 112-117
    CrossrefPubMedGoogle Scholar
  • 68 Kelekci S, Yilmaz B, Yasar L, Savan K, Sonmez S, Kart C. Ovarian reserve and ovarian stromal blood supply after tubal ligation by the Pomeroy technique: comparison with controls.  Gynecol Endocrinol. 2005;  20 279-283
    CrossrefPubMedGoogle Scholar
  • 69 Johnson N P, Mak W, Sowter M C. Surgical treatment for tubal disease in women due to undergo in vitro fertilisation.  Cochrane Database Syst Rev. 2004;  CD002125
    PubMedGoogle Scholar
  • 70 Kontoravdis A, Makrakis E, Pantos K, Botsis D, Deligeoroglou E, Creatsas G. Proximal tubal occlusion and salpingectomy result in similar improvement in in vitro fertilization outcome in patients with hydrosalpinx.  Fertil Steril. 2006;  86 1642-1649
    CrossrefPubMedGoogle Scholar

Ricardo Francalacci SavarisM.D. 

Department of Obstetrics and Gynecology, University of San Francisco

505 Parnassus Ave., M1496, Box 0.132, San Francisco, CA 94143-013

Email: rsavaris@hcpa.ufrgs.br