Fertility and Sterility
Volume 82, Issue 3 , Pages 586-592 , September 2004

Follicular blood flow is a better predictor of the outcome of in vitro fertilization–embryo transfer than follicular fluid vascular endothelial growth factor and nitric oxide concentrations

Presented in part as a poster (P-346) at the 19th Annual Meeting of the European Society of Human Reproduction and Embryology, Madrid, Spain, June 29–July 2, 2003.

  • Ki Hyung Kim, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, College of Medicine, Pusan National University, Busan, Korea
  • ,
  • Dae Sik Oh, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, College of Medicine, Pochon CHA University, Women CHA Hospital, Daegu, Korea
  • ,
  • Jae Heok Jeong, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, College of Medicine, Pusan National University, Busan, Korea
  • ,
  • Byung Sub Shin, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, College of Medicine, Pusan National University, Busan, Korea
  • ,
  • Bo Sun Joo, Ph.D.

      Affiliations

    • Center for Reproductive Medicine and Infertility, Moonhwa Hospital, Busan, Korea
  • ,
  • Kyu Sup Lee, M.D.

      Affiliations

    • Department of Obstetrics and Gynecology, College of Medicine, Pusan National University, Busan, Korea
    • Corresponding Author InformationReprint requests: Kyu Sup Lee, M.D., Department of Obstetrics and Gynecology, College of Medicine, Pusan National University, 1-10 Amidong, Seoku, Busan 602-739, Korea (FAX: 82-51-248-2384)

Received 23 September 2003 ,Revised 9 February 2004 ,Accepted 9 February 2004.

References 

  1. Gordon JD , Shifren JL , Foulk RA , Taylor RN , Jaffe RB . Angiogenesis in the human female reproductive tract . Obstet Gynecol Surv . 1995;50:688–697
  2. Geva E , Jaffe RB . Role of vascular endothelial growth factor in ovarian physiology and pathology . Fertil Steril . 2000;74:429–438
  3. Adams J , Franks S , Polson DW , Mason HD , Abdulwahid N , Tucker M , et al.  Multifollicular ovaries: clinical and endocrine features and response to pulsatile gonadotropin releasing hormone . Lancet . 1985;2:1375–1379
  4. Agarwal R , Sladkevicius P , Engmann L , Conway GS , Payne NN , Bekir J , et al.  Serum vascular endothelial growth factor concentrations and ovarian stromal blood flow are increased in women with polycystic ovaries . Hum Reprod . 1998;13:651–655
  5. Shifren JL , Doldi N , Ferrara N , Mesiano S , Jaffe RB . In the human fetus, vascular endothelial growth factor is expressed in epithelial cells and myocytes, but not vascular endothelium: implications for mode of action . J Clin Endocrinol Metab . 1994;79:316–322
  6. Ferrara N , Carver-Moore K , Chen H , Dowd M , Lu L , O'Shea KS , et al.  Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene . Nature . 1996;380:439–442
  7. Brisden PR , Wada I , Tan SL , Balen A , Jacobs HS . Diagnosis, prevention and management of ovarian hyperstimulation syndrome . Br J Obstet Gynecol . 1995;102:767–772
  8. Levin ER , Rosen GF , Cassidenti DL , Yee B , Meldrum D , Wisot A , et al.  Role of vascular endothelial cell growth factor in ovarian hyperstimulation syndrome . J Clin Invest . 1998;102:1978–1985
  9. Collins W , Jurkovic D , Bourne T , Kurjak A , Campbell S . Ovarian morphology, endocrine function and follicular blood flow during the peri-ovulatory period . Hum Reprod . 1991;6:319–324
  10. Campbell S , Bourne TH , Waterstone J , Reynolds KM , Crayford TJ , Jurkovic D , et al.  Transvaginal color flow imaging of the periovulatory follicle . Fertil Steril . 1993;60:433–438
  11. Sladkevicius P , Valentin L , Marsal K . Blood flow velocity in the uterine and ovarian arteries during the normal menstrual cycle . Ultrasound Obstet Gynecol . 1993;3:199–208
  12. Engmann L , Sladkevicius P , Agrawal R , Bekir JS , Campbell S , Tan SL . Value of ovarian stromal blood flow velocity measurement after pituitary suppression in the prediction of ovarian responsiveness and outcome of in vitro fertilization treatment . Fertil Steril . 1999;71:22–29
  13. Tan SL , Zaidi J , Campbell S , Doyle P , Collins W . Blood flow changes in the ovarian and uterine arteries during the normal menstrual cycle . Am J Obstet Gynecol . 1996;175:625–631
  14. Van Blerkom J , Antczak M , Schrader R . The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics . Hum Reprod . 1997;12:1047–1055
  15. Van Blerkom J . Epigenetic influences on oocyte developmental competence: perifollicular vascularity and intrafollicular oxygen . J Assist Reprod Genet . 1998;15:226–234
  16. Chui DK , Pugh ND , Walker SM , Gregory L , Shaw RW . Follicular vascularity—the predictive value of transvaginal power Doppler ultrasonography in an in-vitro fertilization programme: a preliminary study . Hum Reprod . 1997;12:191–196
  17. Koos RD . Increased expression of vascular endothelial growth/permeability factor in the rat ovary following an ovulatory gonadotropin stimulus: potential roles in follicle rupture . Biol Reprod . 1995;52:1426–1435
  18. Powers RW , Chen L , Russell PT , Larsen WJ . Gonadotropin-stimulated regulation of blood-follicle barrier is mediated by nitric oxide . Am J Physiol . 1995;269:E290–8
  19. Friedman CI , Seifer DB , Kennard EA , Arbogast L , Alak B , Danforth DR . Elevated level of follicular fluid vascular endothelial growth factor is a marker of diminished pregnancy potential . Fertil Steril . 1998;70:836–839
  20. Barroso G , Barrionuevo M , Rao P , Graham L , Danforth D , Huey S , et al.  Vascular endothelial growth factor, nitric oxide, and leptin follicular fluid levels correlate negatively with embryo quality in IVF patients . Fertil Steril . 1999;72:1024–1026
  21. Manau D , Balasch J , Wladimiro J , Fabregues F , Civico S , Casamitjana R , et al.  Follicular fluid concentrations of adrenomedullin, vascular endothelial growth factor and nitric oxide in IVF cycles: relationship to ovarian response . Hum Reprod . 2000;15:1295–1299
  22. Benifla JL , Bringuier AF , Sifer C , Porcher R , Madelenat P , Feldmann G . Vascular endothelial growth factor, platelet endothelial cell adhesion molecule-1 and vascular cell adhesion molecule-1 in the follicular fluid of patients undergoing IVF . Hum Reprod . 2001;16:1376–1381
  23. Lee KS , Joo BS , Na YJ , Yoon MS , Choi OH , Kim WH . Relationship between concentrations of tumor necrosis factor-α and nitric oxide in follicular fluid and oocyte quality . J Assist Reprod Genet . 2000;17:222–228
  24. Murohara T , Horoxitz JR , Silver M , Tsurumi Y , Chen D , Sullivan A , et al.  Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin . Circulation . 1998;97:99–9107
  25. Rosselli M , Keller PJ , Dubey RK . Role of nitric oxide in the biology, physiology, and pathophysiology of reproduction . Hum Reprod Update . 1998;4:3–24
  26. Lee A , Burry KA , Christenson LK , Patton PE , Stouffer RL . Vascular endothelial growth factor levels in serum and follicular fluid of patients undergoing in vitro fertilization . Fertil Steril . 1997;68:305–311
  27. Friedman CI , Arbogast L , Danforth DR , Alak BM , Herbosa-Encarnacion C , Seifer DB . Follicular fluid vascular endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction . Fertil Steril . 1997;68:607–612
  28. Van der Zee R , Murohara T , Luo Z , Zollmann F , Passeri J , Lekutat C , et al.  Vascular endothelial growth factor (VEGF)/vascular permeability factor (VPF) augments nitric oxide release from quiescent rabbit and human vascular endothelium . Circulation . 1997;95:1030–1037
  29. Nargund G , Bourne T , Doyle P , Parsons J , Cheng W , Campbell S , et al.  Associations between ultrasound indices of follicular blood flow, oocyte recovery and preimplantation embryo quality . Hum Reprod . 1996;11:109–113

PII: S0015-0282(04)01076-3

doi: 10.1016/j.fertnstert.2004.02.120

Fertility and Sterility
Volume 82, Issue 3 , Pages 586-592 , September 2004