Fertility and Sterility
Volume 84, Issue 1 , Pages 52-59 , July 2005

Subendometrial and intraendometrial blood flow during the menstrual cycle in patients with endometriosis

  • Pedro Xavier, M.D.

      Affiliations

    • Department of Gynecology and Obstetrics, University of Porto Medical School, Porto, Portugal
    • Corresponding Author InformationReprint requests: Pedro Xavier, M.D., Departamento de Ginecologia e Obstetrícia, Hospital de São João, Alameda Prof. Hernàni Monteiro, 4200 Porto, Portugal (FAX: +351 225096068).
  • ,
  • Jorge Beires, M.D., Ph.D.

      Affiliations

    • Department of Gynecology and Obstetrics, University of Porto Medical School, Porto, Portugal
  • ,
  • Henrique Barros, M.D., Ph.D.

      Affiliations

    • Department of Hygiene and Epidemiology, University of Porto Medical School, Porto, Portugal
  • ,
  • José Martinez-de-Oliveira, M.D., Ph.D.

      Affiliations

    • Department of Gynecology and Obstetrics, University of Porto Medical School, Porto, Portugal

Received 17 August 2004 ,Accepted 8 January 2005.

References 

  1. Halme J , Hammond MG , Hulka JF , Raj SG , Talbert LM . Retrograde menstruation in healthy women and in patients with endometriosis . Obstet Gynecol . 1984;64:151–154
  2. Liu DTY , Hitchcock A . Endometriosis (its association with retrograde menstruation, dysmenorrhoea and tubal pathology) . Br J Obstet Gynaecol . 1986;93:859–862
  3. Donnez J , Smoes P , Gillerot S , Casanas-Roux F , Nisolle M . Vascular endothelial growth factor (VEGF) in endometriosis . Hum Reprod . 1998;13:1686–1690
  4. Healy DL , Rogers PA , Hii L , Wingfield M . Angiogenesis (a new theory for endometriosis) . Hum Reprod Update . 1998;4:736–740
  5. Fasciani A , D’Ambrogio G , Bocci G , Monti M , Genazzani AR , Artini PG . High concentrations of the vascular endothelial growth factor and interleukin-8 in ovarian endometriomata . Mol Hum Reprod . 2000;6:50–54
  6. Fanchin R . Assessing uterine receptivity in 2001 (ultrasonographic glances at the new millennium) . Ann NY Acad Sci . 2001;943:185–202
  7. Tekay A , Martikainen H , Jouppila P . The clinical value of transvaginal colour Doppler ultrasound in assisted reproductive technology procedures . Hum Reprod . 1996;11:1589–1591
  8. Friedler S , Schenker JG , Herman A , Lewin A . The role of ultrasonography in the evaluation of endometrial receptivity following assisted reproductive treatments (a critical review) . Hum Reprod Update . 1996;2:323–335
  9. Chien L , Au H , Chen P , Xiao J , Tzeng C . Assessment of uterine receptivity by the endometrial–subendometrial blood flow distribution pattern in women undergoing in vitro fertilization–embryo transfer . Fertil Steril . 2002;78:245–251
  10. Evans DH , McDicken WN , Skidmore R . The origin of the Doppler power spectrum . In:  Evans DH ,  McDicken WN editor. Doppler ultrasound (physics, instrumentation, and clinical applications) . Chichester, England: Wiley; 1989;p. 115–143
  11. Rubin JM , Bude RO , Carson PL , Bree RL , Adler RS . Power Doppler US (a potentially useful alternative to mean frequency-based color Doppler US) . Radiology . 1994;190:853–856
  12. Sohn C , Weskott HP . The sensitivity of new color systems in blood-flow diagnosis. The maximum entropy method and angio-color-comparative in vitro flow measurements to determine sensitivity . Surg Endosc . 1997;11:1040–1044
  13. Yang JH , Wu MY , Chen CD , Jiang MC , Ho HN , Yang YS . Association of endometrial blood flow as determined by a modified color Doppler technique with subsequent outcome on in-vitro fertilization . Hum Reprod . 1999;14:1606–1610
  14. Schild RL , Holthaus S , D’Alquen J , Fimmers R , Dorn C , van der Ven H , et al.   Quantitative assessment of subendometrial blood flow by three-dimensional ultrasound is an important predictive factor in an in vitro fertilization program . Hum Reprod . 2000;15:89–94
  15. Amso NN , Watermeyer SR , Pugh N , O’Brien S , D’Angelo A . Quantification of power Doppler energy and its future potential . Fertil Steril . 2001;76:583–587
  16. Kupesic S , Kurjak A . Uterine and ovarian perfusion during the periovulatory period assessed by transvaginal color Doppler . Fertil Steril . 1993;60:439–443
  17. Agrawal R , Conway GS , Sladkevicius P , Payne NN , Bekir J , Campbell S , et al.   Serum vascular endothelial growth factor (VEGF) in the normal menstrual cycle (association with changes in ovarian and uterine Doppler blood flow) . Clin Endocrinol . 1999;50:101–106
  18. Raine-Fenning NJ , Campbell BK , Kendall NR , Clewes JS , Johnson IR . Endometrial and subendometrial perfusion are impaired in women with unexplained subfertility . Hum Reprod . 2004;19:2605–2614
  19. Goodger AM , Rogers PA . Endometrial endothelial cell proliferation during the menstrual cycle . Hum Reprod . 1994;9:399–405
  20. Smith SK . Regulation of angiogenesis in the endometrium . Trends Endocrinol Metab . 2001;12:147–151
  21. Zaidi J , Jurkovic D , Campbell S , Okokon S , Tan SL . Circadian variation in uterine artery blood flow indices during the follicular phase of the menstrual cycle . Ultrasound Obstet Gynecol . 1995;5:406–410
  22. Scoutt LM , Flyn SD , Luthringer DJ , McCauley TR , McCarthy SM . Junctional zone of the uterus (correlation of MR imaging and histologic examination of hysterectomy specimens) . Radiology . 1991;179:403–407
  23. Tetlow RL , Richmond I , Manton DJ , Greenman J , Turnbull LW , Killick SR . Histological analysis of the uterine junctional zone as seen by transvaginal ultrasound . Ultrasound Obstet Gynecol . 1999;14:188–193
  24. Basir GS , Lam TP , O W , Chau MT , Ng EH , Ho PC . Cycle-to-cycle variation in utero-ovarian hemodynamic indices in ovarian stimulation and natural cycles of the same women and its effect on the outcome of assisted reproduction treatment . Fertil Steril . 2002;78:1055–1060
  25. Zondervan KT , Cardon LR , Kennedy SH . What makes a good case-control study? Design issues for complex traits such endometriosis . Hum Reprod . 2002;17:1415–1423
  26. Missmer SA , Cramer DW . The epidemiology of endometriosis . Obstet Gynecol Clin N Am . 2003;30:1–19
  27. Audebert A , Backstrom T , Barlow DH , Benagiano G , Brosens I , Buhler K , et al.   Endometriosis 1991 (a discussion document) . Hum Reprod . 1992;7:432–435
  28. Duleba AJ . Diagnosis of endometriosis . Obstet Gynecol Clin North Am . 1997;24:331–345
  29. Pardanani S , Barbieri RL . The gold standard for the surgical diagnosis of endometriosis (visual findings or biopsy results) . J Gynecol Tech . 1998;4:121–124
  30. Contart P , Baruffi RL , Coelho J , Mauri AL , Peterson C , Franco JG . Power Doppler endometrial evaluation as a method for the prognosis of embryo implantation in an ICSI program . J Assist Reprod Genet . 2000;17:329–334
  31. Kupesic S , Bakavac I , Bjelos D , Kurjak A . Assessment of endometrial receptivity by transvaginal color Doppler and three-dimensional power Doppler ultrasonography in patients undergoing in vitro fertilization procedures . J Ultrasound Med . 2001;15:89–94
  32. Kunz G , Beil D , Huppert P , Leyendecker G . Structural abnormalities of the uterine wall in women with endometriosis and infertility visualized by vaginal sonography and magnetic resonance imaging . Hum Reprod . 2000;15:76–82
  33. Yuval Y , Lipitz S , Dor J , Achiron R . The relationship between endometrial thickness and blood flow and pregnancy rates in in-vitro fertilization . Hum Reprod . 1999;14:1067–1071
  34. Schild RL , Knobloch C , Dorn C , Fimmers R , van der Ven H , Hansmann M . Endometrial receptivity in an in vitro fertilization program as assessed by spiral artery blood flow, endometrial thickness, endometrial volume, and uterine artery blood flow . Fertil Steril . 2001;75:361–366
  35. Yalti S , Gurbuz B , Ficicioglu C , Canova H . Doppler evaluation of the uterine, intraovarian, stromal and spiral arteries on the day of human chorionic gonadotrophin administration in controlled ovarian hyperstimulation . J Obstet Gynaecol . 2003;23:402–406
  36. Schindl M , Birner P , Obermair A , Kiesel L , Wenzl R . Increased microvessel density in adenomyosis uteri . Fertil Steril . 2001;75:131–135
  37. Goswamy RK , Steptoe PC . Doppler ultrasound studies of the uterine artery in spontaneous ovarian cycles . Hum Reprod . 1988;3:721–726
  38. Kurjak A , Kupesic-Urek S , Schulman H , Zalud I . Transvaginal color Doppler in the assessment of ovarian and uterine blood flow in infertile women . Fertil Steril . 1991;56:870–873
  39. Schurz B , Schon HJ , Wenzl R , Eppel W , Huber J , Reinold E . Endovaginal Doppler flow measurements of the ovarian artery in patients with a normal menstrual cycle and with polycystic ovary syndrome during in vitro fertilization . J Clin Ultrasound . 1993;21:19–24
  40. Steer CV , Tan SL , Dillon D , Mason BA , Campbell S . Vaginal color Doppler assessment of uterine artery impedance correlates with immunohistochemical markers of endometrial receptivity required for the implantation of an embryo . Fertil Steril . 1995;63:101–108
  41. Bourne TH , Hagström HG , Granberg S , Josefsson B , Hahlin M , Hellberg P , et al.   Ultrasound studies of vascular and morphological changes in the human uterus after a positive self-test for the urinary luteinizing hormone surge . Hum Reprod . 1996;11:369–375
  42. Ferrara N , Davis-Smyth T . The biology of vascular endothelial growth factor . Endocrinol Rev . 1997;18:4–25
  43. 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
  44. Folkman J , Klagsbrun M . Angiogenic factors . Science . 1987;23:442–447
  45. Folkman J , Shing Y . Angiogenesis . J Biol Chem . 1992;5:10931–10934
  46. Gordon JD , Shifren JL , Foulk RA , Taylor RN , Jaffe RB . Angiogenesis in the human female reproductive tract . Obstet Gynecol Surv . 1995;50:688–697
  47. Smith SK . Angiogenesis, vascular endothelial growth factor and the endometrium . Hum Reprod Update . 1998;4:509–519
  48. Kooy J , Taylor NH , Healy DL , Rogers PA . Endothelial cell proliferation in the endometrium of women with menorrhagia and in women following endometrial ablation . Hum Reprod . 1996;11:1067–1072
  49. Rogers PA , Plunkett D , Affandi B . Perivascular smooth muscle alpha-actin is reduced in the endometrium of women with progestin-only contraceptive breakthrough bleeding . Hum Reprod . 2000;15(Suppl 3):78–84
  50. Prentice A , Randall BJ , Weddell A , McGill A , Henry L , Horne CH , et al.   Ovarian steroid receptor expression in endometriosis and in two potential parent epithelia (endometrium and peritoneal mesothelium) . Hum Reprod . 1992;7:1318–1325
  51. Bergqvist A , Ferno M . Oestrogen and progesterone receptors in endometriotic tissue and endometrium (comparison of different cycle phases and ages) . Hum Reprod . 1993;8:2211–2217
  52. Attia GR , Zeitoun K , Edwards D , Johns A , Carr BR , Bulun SE . Progesterone receptor isoform A but not B is expressed in endometriosis . J Clin Endocrinol Metab . 2000;85:2897–2902
  53. Tora L , Gronemeyer H , Turcotte B , Gaub MP , Chambon P . The N-terminal region of the chicken progesterone receptor specifies target gene activation . Nature . 1988;333:185–188
  54. Kastner P , Krust A , Turcotte B , Stropp U , Tora L , Gronemeyer H , et al.   Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B . EMBO J . 1990;9:1603–1614

 Supported by the Fundaçâo para a Ciência e a Tecnologia, project: POCTI/CBO/46776/2002.

PII: S0015-0282(05)00594-7

doi: 10.1016/j.fertnstert.2005.01.114

Fertility and Sterility
Volume 84, Issue 1 , Pages 52-59 , July 2005