Fertility and Sterility
Volume 94, Issue 2 , Pages 389-400 , July 2010

Preventing ovarian hyperstimulation syndrome: guidance for the clinician

  • Peter Humaidan, M.D.

      Affiliations

    • The Fertility Clinic, Skive, Denmark
    • Corresponding Author InformationReprint requests: Peter Humaidan, The Fertility Clinic, Skive Regional Hospital, DK7800 Skive, Denmark (FAX: 45-89-27-49-82).
  • ,
  • Jens Quartarolo, M.D.

      Affiliations

    • Schering-Plough, Roseland, New Jersey
  • ,
  • Evangelos G. Papanikolaou, Ph.D.

      Affiliations

    • University Reproduction Unit, Aristotle University of Thessaloniki and Assisted Reproduction Unit “Biogenesis,” Thessaloniki, Greece

Received 23 October 2009 ,Revised 21 December 2009 ,Accepted 9 March 2010.

References 

  1. McArdle C, Seibel M, Hann LE, Weinstein F, Taymor M. The diagnosis of ovarian hyperstimulation (OHS): the impact of ultrasound. Fertil Steril. 1983;39:464–467
  2. Mocanu E, Redmond ML, Hennelly B, Collins C, Harrison R. Odds of ovarian hyperstimulation syndrome (OHSS)—time for reassessment. Hum Fertil (Camb). 2007;10(3):175–181
  3. Lyons CA, Wheeler CA, Frishman GN, Hackett RJ, Seifer DB, Haning RV. Early and late presentation of the ovarian hyperstimulation syndrome: two distinct entities with different risk factors. Hum Reprod. 1994;9:792–799
  4. Mathur RS, Akande VA, Keay SD, Hunt LP, Jenkins JM. Distinction between early and late ovarian hyper-stimulation syndrome. Fertil Steril. 2000;73:901–907
  5. Papanikolaou EG, Pozzobon C, Kolibianakis EM, Camus M, Tournaye H, Fatemi HM, et al. Incidence and prediction of ovarian hyperstimulation syndrome in women undergoing gonadotropin-releasing hormone antagonist in vitro fertilization cycles. Fertil Steril. 2006;85:112–120
  6. Navot D, Bergh PA, Laufer N. Ovarian hyperstimulation syndrome in novel reproductive technologies: prevention and treatment. Fertil Steril. 1992;58:249–261
  7. The Practice Committee of the American Society for Reproductive Medicine (ASRM). Ovarian hyperstimulation syndrome. Fertil Steril. 2008;90(Suppl 5):S188–S193
  8. Lee TH, Liu CH, Huang CC, Wu YL, Shih YT, Ho HN, et al. Serum anti-mullerian hormone and estradiol levels as predictors of ovarian hyperstimulation syndrome in assisted reproduction technology cycles. Hum Reprod. 2008;23:160–167
  9. Esinler I, Bayar U, Bozdag G, Yarali H. Outcome of intracytoplasmic sperm injection in patients with polycystic ovary syndrome or isolated polycystic ovaries. Fertil Steril. 2005;84:932–937
  10. Dor J, Shulman A, Levran D, Ben-Rafael Z, Rudak E, Mashiach S. The treatment of patients with polycycstic ovarian syndrome by in-vitro fertilization and embryo transfer: a comparison of results with those of patients with tubal infertility. Hum Reprod. 1990;5:816–818
  11. MacDougall MJ, Tan SL, Balen A, Jacobs HS. A controlled study comparing patients with and without polycystic ovaries undergoing in-vitro fertilization. Hum Reprod. 1993;8:233–237
  12. Engmann L, Maconochie N, Sladkevicius P, Bekir J, Campbell S, Tan SL. The outcome of in-vitro fertilization treatment in women with sonographic evidence of polycystic ovarian morphology. Hum Reprod. 1999;14:161–171
  13. Ludwig M, Finas DF, Al-Hasani S, Diedrich K, Ortmann O. Oocyte quality and treatment outcome in intracytoplasmic sperm injection cycles of polycystic ovarian syndrome patients. Hum Reprod. 1999;14:354–358
  14. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, et al. Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology. 2002;143:1076–1084
  15. La Marca A, Giulini S, Tirelli A, Bertucci E, Marsella T, Xella S, et al. Anti-Mullerian hormone measurement on any day of the menstrual cycle strongly predicts ovarian response in assisted reproductive technology. Hum Reprod. 2007;22:766–771
  16. Gnoth C, Schuring AN, Friol K, Tigges J, Mallmann P, Godehardt E. Relevance of anti-Mullerian hormone measurement in a routine IVF program. Hum Reprod. 2008;23:1359–1365
  17. Fanchin R, Taieb J, Mendez Lozano DH, Ducot B. High reproducibility of serum antimullerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod. 2005;20:923–927
  18. La Marca A, Malmusi S, Giulini S, Tamaro LF, Orvieto R, Leveratti P, et al. Anti-mullerian hormone plasma levels in spontaneous menstrual cycle and during treatment with FSH to induce ovulation. Hum Reprod. 2004;19:2738–2741
  19. Hehenkamp WJ, Looman CW, Themmen AP, de Jong FH, Te Velde ER, Broekmans FJ. Anti-Mullerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J Clin Endocrinol Metab. 2006;91:4057–4063
  20. La Marca A, Stabile G, Artenisio AC, Volpe A. Serum anti-Mullerian hormone throughout the human menstrual cycle. Hum Reprod. 2006;21:3103–3107
  21. Seifer DB, MacLaughlin DT. Mullerian inhibiting substance is an ovarian growth factor of emerging clinical significance. Fertil Steril. 2007;88:539–546
  22. Delvigne A, Rozenberg S. Epidemiology and prevention of ovarian hyperstimulation syndrome (OHSS): a review. Hum Reprod Update. 2002;8:559–577
  23. Verhagen TE, Hendriks DJ, Bancsi LF, Mol BW, Broekmans FJ. The accuracy of multivariate models predicting ovarian reserve and pregnancy after in vitro fertilization: a meta-analysis. Hum Reprod Update. 2008;14:95–100
  24. Kwee J, Elting ME, Schats R, McDonnell J, Lambalk CB. Ovarian volume and antral follicle count for the prediction of low and hyper responders with in vitro fertilization. Reprod Biomed Online. 2007;5:9
  25. Asch RH, Li HP, Balmaceda JP, Weckstein LN, Stone SC. Severe ovarian hyperstimulation syndrome in assisted reproductive technology: definition of high risk groups. Hum Reprod. 1991;6:1395–1399
  26. Delvigne A, Dubois M, Battheu B, Bassil S, Meuleman C, De Sutter P, et al. The ovarian hyperstimulation syndrome in in-vitro fertilization: a Belgian multicentric study. II. Multiple discriminant analysis for risk prediction. Hum Reprod. 1993;8:1361–1366
  27. Morris RS, Wong IL, Kirkman E, Gentschein E, Paulson RJ. Inhibition of ovarian-derived prorenin to angiotensin cascade in the treatment of ovarian hyperstimulation syndrome. Hum Reprod. 1995;10:1355–1358
  28. Thomas K, Searle T, Quinn A, Wood S, Lewis-Jones I, Kingsland C. The value of routine estradiol monitoring in assisted conception cycles. Acta Obstet Gynecol Scand. 2002;81:551–554
  29. Homburg R, Howles CM. Low-dose FSH therapy for anovulatory infertility associated with polycystic ovary syndrome: rationale, results, reflections and refinements. Hum Reprod Update. 1999;5:493–499
  30. Hamilton-Fairly D, Kiddy D, Watson H, Sagle M, Franks S. Low dose gonadotrophin therapy for induction of ovulation in 100 women with PCOS. Hum Reprod. 1991;6:1095–1099
  31. Homburg R, Levy T, Ben-Rafael Z. A comparative prospective study of conventional regimen with chronic low-dose administration of follicle-stimulating hormone for anovulation associated with polycystic ovary syndrome. Fertil Steril. 1995;63:729–733
  32. Christin-Maitre S, Hugues JN on behalf of the Recombinant FSH Study Group. A comparative randomized multicentric study comparing the step-up versus step-down protocol in polycystic ovary syndrome. Hum Reprod. 2003;18:1626–1631
  33. Leader A. Improved monofollicular ovulation in anovulatory or oligo-ovulatory women after a low-dose step-up protocol with weekly increments of 25 international units of follicle-stimulating hormone. Fertil Steril. 2006;85:1766–1773
  34. El-Sheikh MM, Hussein M, Fouad S, El-Sheikh R, Bauer O, Al-Hasani S. Limited ovarian stimulation (LOS), prevents the recurrence of severe forms of ovarian hyperstimulation syndrome in polycystic ovarian disease. Eur J Obstet Gynecol Reprod Biol. 2001;94:245–249
  35. Zhu YM, Gao HJ, He RH, Huang HF. Research on the protocol of limited ovarian stimulation to prevent ovarian hyperstimulation syndrome. Zhonghua Fu Chan Ke Za Zhi. 2006;41:740–744
  36. Kolibianakis EM, Albano C, Camus M, Tournaye H, Van Steirteghem AC, Devroey P. Prolongation of the follicular phase in in vitro fertilization results in a lower ongoing pregnancy rate in cycles stimulated with recombinant follicle-stimulating hormone and gonadotropin-releasing hormone antagonists. Fertil Steril. 2004;82:102–107
  37. Ferraretti AP, Gianaroli L, Magli C, Fortini D, Selman HA, Feliciani E. Elective cryopreservation of all pronucleate embryos in women at risk of ovarian hyperstimulation syndrome: efficiency and safety. Hum Reprod. 1999;14:1457–1460
  38. Claman P, Domingo M, Garner P, Leader A, Spence J. Natural cycle in vitro fertilization–embryo transfer at the University of Ottawa: an inefficient therapy for tubal infertility. Fertil Steril. 1993;60:298–302
  39. Hohmann FP, Macklon NS, Fauser BC. A randomized comparison of two ovarian stimulation protocols with gonadotropin-releasing hormone (GnRH) antagonist cotreatment for in vitro fertilization commencing recombinant follicle-stimulating hormone on cycle day 2 or 5 with the standard long GnRH agonist protocol. J Clin Endocrinol Metab. 2003;88:166–173
  40. Pelinck MJ, Vogel NEA, Hoek A, Arts EGJM, Simons AHM, Heineman MJ. Minimal stimulation IVF with late follicular phase administration of the GnRH antagonist cetrorelix and concomitant substitution with recombinant FSH: a pilot study. Hum Reprod. 2005;20:642–648
  41. Eijkemans MJ, Heijnen EM, de Klerk C, Habbema JD, Fauser BC. Comparison of different treatment strategies in IVF with cumulative live birth over a given period of time as the primary end-point: methodological considerations on a randomized controlled non-inferiority trial. Hum Reprod. 2006;21:344–351
  42. Heijnen EM, Eijkemans MJ, de Klerk C, Polinder S, Beckers NG, Klinkert ER, et al. A mild treatment strategy for in-vitro fertilisation: a randomised non-inferiority trial. Lancet. 2007;369:743–749
  43. MacDougall MJ, Tan SL, Jacobs HS. In-vitro fertilization and the ovarian hyperstimulation syndrome. Hum Reprod. 1992;7:597–600
  44. Forman RG, Frydman R, Egan D, Ross C, Barlow DH. Severe hyperstimulation syndrome using agonists of gonadotropin-releasing hormone for in vitro fertilization: a European series and a proposal for prevention. Fertil Steril. 1990;53:502–509
  45. Jayaprakasan K, Hopkisson JF, Campbell BK, Clewes J, Johnson IR, Raine-Fenning NJ. Quantification of the effect of pituitary down-regulation on 3D ultrasound predictors of ovarian response. Hum Reprod. 2008;23:1538–1544
  46. European Orgalutran Study Group. Treatment with the gonadotrophin-releasing hormone antagonist ganirelix in women undergoing ovarian stimulation with recombinant follicle stimulating hormone is effective, safe and convenient: results of a controlled, randomized, multicentre trial. Hum Reprod. 2000;15:1490–1498
  47. European and Middle East Orgalutran Study Group. Comparable clinical outcome using the GnRH antagonist ganirelix or a long protocol of the GnRH agonist triptorelin for the prevention of premature LH surges in women undergoing ovarian stimulation. Hum Reprod. 2001;16:644–651
  48. North American Ganirelix Study Group. Efficacy and safety of ganirelix acetate versus leuprolide acetate in women undergoing controlled ovarian hyperstimulation. Fertil Steril. 2001;75:38–45
  49. Al-Inany HG, Abou-Setta AM, Aboulghar M. Gonadotrophin-releasing hormone antagonists for assisted conception. Cochrane Database Syst Rev. 2006;(3):CD001750
  50. Kolibianakis EM, Collins J, Tarlatzis BC, Devroey P, Diedrich K, Griesinger G. Among patients treated for IVF with gonadotrophins and GnRH analogues, is the probability of live birth dependent on the type of analogue used? A systematic review and meta-analysis. Hum Reprod Update. 2006;12:651–671
  51. Al-Inany HG, Aboulghar M. GnRH antagonist in assisted reproduction: a Cochrane review. Hum Reprod. 2002;17:874–885
  52. Tavaniotou A, Smitz J, Bourgain C, Devroey P. Ovulation induction disrupts luteal phase function. Ann N Y Acad Sci. 2001;943:55–63
  53. Tavaniotou A, Devroey P. Luteal hormonal profile of oocyte donors stimulated with a GnRH antagonist compared with natural cycles. Reprod Biomed Online. 2006;13:326–330
  54. Pritts EA, Atwood AK. Luteal support in infertility treatment: a meta-analysis of the randomized trials. Hum Reprod. 2002;17:2287–2299
  55. Luteal phase support in assisted reproduction cycles. Cochrane Database Syst Rev. 2004;(3):CD004830
  56. Doody KJ, Schnell VL, Foulk RA, Miller CE, Kolb BA, Blake EJ, et al. Endometrin for luteal phase support in a randomized, controlled, open-label, prospective in-vitro fertilization trial using a combination of Menopur and Bravelle for controlled ovarian hyperstimulation. Fertil Steril. 2008;91:1012–1017
  57. Pirard C, Donnez J, Loumaye E. GnRH agonist as novel luteal support: results of a randomized, parallel group, feasibility study using intranasal administration of buserelin. Human Reprod. 2005;20:1798–1804
  58. Suikkari AM. In-vitro maturation: its role in fertility treatment. Curr Opin Obstet Gynecol. 2008;20:242–248
  59. Borini A, Lagalla C, Bonu MA, Bianchi V, Flamigni C, Coticchio G. Cumulative pregnancy rates resulting from the use of fresh and frozen oocytes: 7 years' experience. Reprod Biomed Online. 2006;12:481–486
  60. Adashi EY, Resnick CE, D'Ercole AJ, Svoboda ME, Van Wyk JJ. Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocr Rev. 1985;6:400–420
  61. Barbieri RL, Makris A, Randall RW, Daniels G, Kistner RW, Ryan KJ. Insulin stimulates androgen accumulation in incubations of ovarian stroma obtained from women with hyperandrogenism. J Clin Endocrinol Metab. 1986;62:904–910
  62. Dunaif A, Segal KR, Futterweit W, Dobrjansky A. Profound peripheral insulin resistance, independent of obesity, in polycystic ovary syndrome. Diabetes. 1989;38:1165–1174
  63. Nestler JE, Powers LP, Matt DW, Steingold KA, Plymate SR, Rittmaster RS, et al. A direct effect of hyperinsulinemia on serum sex hormone–binding globulin levels in obese women with the polycystic ovary syndrome. J Clin Endocrinol Metab. 1991;72:83–89
  64. Dunaif A. Drug insight: insulin-sensitizing drugs in the treatment of polycystic ovary syndrome—a reappraisal. Nat Clin Pract Endocrinol Metab. 2008;4:272–283
  65. Costello MF, Chapman M, Conway U. A systematic review and meta-analysis of randomized controlled trials on metformin co-administration during gonadotrophin ovulation induction or IVF in women with polycystic ovary syndrome. Hum Reprod. 2006;21:1387–1399
  66. Rabinovici J, Kushnir O, Shalev J, Goldenberg M, Blankstein J. Rescue of menotrophin cycles prone to develop ovarian hyperstimulation. Br J Obstet Gynaecol. 1987;94:1098–1102
  67. Sher G, Salem R, Feinman M, Dodge S, Zouves C, Knutzen V. Eliminating the risk of life-endangering complications following ovarian overstimulation with menotropin fertility agents: a report on women undergoing in vitro fertilization and embryo transfer. Obstet Gynecol. 1993;81:1009–1011
  68. Delvigne A, Rozenberg S. A qualitative systematic review of coasting, a procedure to avoid ovarian hyperstimulation syndrome in IVF patients. Hum Reprod Update. 2002;8:291–296
  69. D'Angelo A, Amso N. “Coasting” (withholding gonadotrophins) for preventing ovarian hyperstimulation syndrome. Cochrane Database Syst Rev. 2002;(3):CD002811
  70. Delvigne A, Rozenberg S. Preventive attitude of physicians to avoid OHSS in IVF patients. Hum Reprod. 2001;16:2491–2495
  71. Schmidt DW, Maier DB, Nulsen JC, Benadiva CA. Reducing the dose of human chorionic gonadotropin in high responders does not affect the outcomes of in vitro fertilization. Fertil Steril. 2004;82:841–846
  72. Kolibianakis EM, Papanikolaou EG, Tournaye H, Camus M, Van Steirteghem AC, Devroey P. Triggering final oocyte maturation using different doses of human chorionic gonadotropin: a randomized pilot study in patients with polycystic ovary syndrome treated with gonadotropin-releasing hormone antagonists and recombinant follicle-stimulating hormone. Fertil Steril. 2007;88:1382–1388
  73. Chen D, Burmeister L, Goldschlag D, Rosenwaks Z. Ovarian hyperstimulation syndrome: strategies for prevention. Reprod Biomed Online. 2003;7:43–49
  74. Kashyap S, Leveille M, Wells G. Low dose hCG reduces the incidence of early and severe ovarian hyperstimulation syndrome. Fertil Steril. 2006;86(Suppl 2):S182–S183(P-138)
  75. Abdalla HI, Ah-Moye M, Brinsden P, Howe DL, Okonofua F, Craft I. The effect of the dose of human chorionic gonadotropin and the type of gonadotropin stimulation on oocyte recovery rates in an in vitro fertilization program. Fertil Steril. 1987;48:958–963
  76. Aboulghar MA, Mansour RT. Ovarian hyperstimulation syndrome: classifications and critical analysis of preventive measures. Hum Reprod Update. 2003;9:275–289
  77. Wada I, Matson PL, Troup SA, Hughes S, Buck P, Lieberman BA. Outcome of treatment subsequent to the elective cryopreservation of all embryos from women at risk of the ovarian hyperstimulation syndrome. Hum Reprod. 1992;7:962–966
  78. Queenan JT, Veeck LL, Toner JP, Oehninger S, Muasher SJ. Cyropreservation of all prezygotes in patients at risk of severe hyperstimulation does not eliminate the syndrome, but the chances of pregnancy are excellent with subsequent frozen-thaw transfers. Hum Reprod. 1997;12:1573–1576
  79. D'Angelo A, Amso N. Embryo freezing for preventing ovarian hyperstimulation syndrome: a Cochrane review. Hum Reprod. 2002;17:2787–2794
  80. Amso NN, Ahuja KK, Morris N, Shaw RW. The management of predicted ovarian hyperstimulation involving gonadotropin-releasing hormone analog with elective cryopreservation of all pre-embryos. Fertil Steril. 1990;53:1087–1090
  81. Salat-Baroux J, Alvarez S, Antoine JM, Cornet D, Tibi C, Plachot M, et al. Treatment of hyperstimulation during in-vitro fertilization. Hum Reprod. 1990;5:36–39
  82. Wada I, Matson PL, Troup SA, Morroll DR, Hunt L, Lieberman BA. Does elective cryopreservation of all embryos from women at risk of ovarian hyperstimulation syndrome reduce the incidence of the condition?. Br J Obstet Gynaecol. 1993;100:265–269
  83. The CDC 2005 Report—2005 Assisted Reproductive Technology (ART) Report. Available at http://www.cdc.gov/ART/ART2005/section3.htm. Accessed September 2009.
  84. Sills ES, McLoughlin LJ, Genton MG, Walsh DJ, Coull GD, Walsh AP. Results from the advanced reproductive technologies: fresh vs. frozen?. J Ovarian Res. 2008;1(1):7
  85. Schenker JG, Weinstein D. Ovarian hyperstimulation syndrome: a current survey. Fertil Steril. 1978;30:255–268
  86. Damewood MD, Shen W, Zacur HA, Schlaff WD, Rock JA, Wallach EE. Disappearance of exogenously administered human chorionic gonadotropin. Fertil Steril. 1989;52:398–400
  87. Itskovitz J, Boldes R, Levron J, Erlik Y, Kahana L, Brandes JM. Induction of preovulatory luteinizing hormone surge and prevention of ovarian hyperstimulation syndrome by gonadotropin-releasing hormone agonist. Fertil Steril. 1991;56:213–220
  88. Haning RV, Strawn EY, Nolten WE. Pathophysiology of the ovarian hyperstimulation syndrome. Obstet Gynecol. 1985;66:220–224
  89. Al-Inany HG, Aboulghar M, Mansour R, Proctor M. Recombinant versus urinary human chorionic gonadotrophin for ovulation induction in assisted conception. Cochrane Database Syst Rev. 2005;(2):CD003719
  90. Gonen Y, Balakier H, Powell W, Casper RF. Use of gonadotropin-releasing hormone agonist to trigger follicular maturation for in vitro fertilization. J Clin Endocrinol Metab. 1990;71(4):918–922
  91. Babayof R, Margalioth EJ, Huleihel M, Amash A, Zylber-Haran E, Gal M, et al. Serum inhibin A, VEGF and TNFalpha levels after triggering oocyte maturation with GnRH agonist compared with HCG in women with polycystic ovaries undergoing IVF treatment: a prospective randomized trial. Hum Reprod. 2006;21:1260–1265
  92. Engmann L, DiLuigi A, Schmidt D, Nulsen J, Maier D, Benadiva C. The use of gonadotropin-releasing hormone (GnRH) agonist to induce oocyte maturation after cotreatment with GnRH antagonist in high-risk patients undergoing in vitro fertilization prevents the risk of ovarian hyperstimulation syndrome: a prospective randomized controlled study. Fertil Steril. 2008;89:84–91
  93. Humaidan P, Bredkjaer HE, Bungum L, Grondahl ML, Westergaard L, Anderson CY. GnRH agonist (buserelin) or hCG for ovulation induction in GnRH antagonist IVF/ICI cycles: a prospective randomized study. Hum Reprod. 2005;20:1213–1220
  94. Kolibianakis EM, Schultze-Mosgau A, Schroer A, Van Steirteghem AC, Devroey P, Diedrich K, et al. A lower ongoing pregnancy rate can be expected when GnRH agonist is used for triggering final oocyte maturation instead of HCG in patients undergoing IVF with GnRH antagonists. Hum Reprod. 2005;20:2887–2892
  95. Humaidan P, Bungum L, Bungum M, Yding Anderson C. Rescue of corpus luteum function with peri-ovulatory HCG supplementation in IVF/ICSI GnRH antagonist cycles in which ovulation was triggered with a GnRH agonist: a pilot study. Reprod Biomed Online. 2006;13(2):173–178
  96. Humaidan P, Bredkjaer HE, Westergaard L, Andersen CY. 1500 IU hCG administered at oocyte retrieval rescues the luteal phase when GnRH agonist is used for ovulation induction: a prospective randomized controlled study. Fertil Steril. 2009;93:847–854
  97. Griesinger G, Kolibianakis EM, Papanikolaou EG, Diedrich K, Van Steirteghem AC, Devroey P, et al. Triggering of final oocyte maturation with gonadotropin-releasing hormone agonist or human chorionic gonadotropin. Live birth after frozen-thawed embryo replacement cycles. Fertil Steril. 2007;88:616–621
  98. Andersen CY, Humaidan P, Ejdrup HB, Bungum L, Grøndahl ML, Westergaard LG. Hormonal characteristics of follicular fluid from women receiving either GnRH agonist or hCG for ovulation induction. Hum Reprod. 2006;21:2126–2130
  99. Imoedemhe DA, Sigue AB, Pacpaco EL, Olazo AB. Stimulation of endogenous surge of luteinizing hormone with gonadotropin-releasing hormone analog after ovarian stimulation for in vitro fertilization. Fertil Steril. 1991;55:328–332
  100. Papanikolaou EG, Tournaye H, Verpoest W, Camus M, Vernaeve V, Van Steirteghem A, et al. Early and late ovarian hyperstimulation syndrome: early pregnancy outcome and profile. Hum Reprod. 2005;20:636–641
  101. Orvieto R, Volodarsky M, Hod E, Homburg R, Rabinson J, Zohav E, et al. Controlled ovarian hyperstimulation using multi-dose gonadotropin-releasing hormone (GnRH) antagonist results in less systemic inflammation than the GnRH-agonist long protocol. Gynecol Endocrinol. 2007;22:1–3
  102. Mansour R, Aboulghar M, Serour G, Amin Y, Abou-Setta AM. Criteria for a successful coasting protocol for the prevention of severe ovarian hyperstimulation syndrome. Hum Reprod. 2005;20:3167–3172
  103. Arslan M, Bocca S, Jones E, Mayer J, Stadtmauer L, Oehninger S. Effect of coasting on the implantation potential of embryos transferred after cryopreservation and thawing. Fertil Steril. 2005;84:867–874
  104. Bodri D, Guillén JJ, Galindo A, Mataró D, Pujol A, Coll O. Triggering with human chorionic gonadotropin or a gonadotropin-releasing hormone agonist in gonadotropin-releasing hormone antagonist-treated oocyte donor cycles: findings of a large retrospective cohort study. Fertil Steril. 2009;91:365–371
  105. Emperaire JC, Edwards RG. Time to revolutionize the triggering of ovulation. Reprod Biomed Online. 2004;9:480–483
  106. Shapiro DB, Mitchell-Leef D, Carter M, Nagy ZP. Ganirelix acetate use in normal- and poor-prognosis patients and the impact of estradiol patterns. Fertil Steril. 2005;83:666–670
  107. Asch RH, Ivery G, Goldsman M, Frederick JL, Stone SC, Balmaceda JP. The use of intravenous albumin in patients at high risk for severe ovarian hyperstimulation syndrome. Hum Reprod. 1993;8:1015–1020
  108. Shoham Z, Weissman A, Barash A, Borenstein R, Schachter M, Insler V. Intravenous albumin for the prevention of severe ovarian hyperstimulation syndrome in an in vitro fertilization program: a prospective, randomized, placebo-controlled study. Fertil Steril. 1994;62:137–142
  109. Isik AZ, Gokmen O, Zeyneloglu HB, Kara S, Keles G, Gulekli B. Intravenous albumin prevents moderate-severe ovarian hyperstimulation in in-vitro fertilization patients: a prospective, randomized and controlled study. Eur J Obstet Gynecol Reprod Biol. 1996;70:179–183
  110. Ben-Chetrit A, Eldar-Geva T, Gal M, Huerta M, Mimon T, Algur N, et al. The questionable use of albumin for the prevention of ovarian hyperstimulation syndrome in an IVF programme: a randomized placebo-controlled trial. Hum Reprod. 2001;16:1880–1884
  111. Gokmen O, Ugur M, Ekin M, Keles G, Turan C, Oral H. Intravenous albumin versus hydroxyethyl starch for the prevention of ovarian hyperstimulation in an in-vitro fertilization programme: a prospective randomized placebo controlled study. Eur J Obstet Gynecol Reprod Biol. 2001;96:187–192
  112. Ndukwe G, Thornton S, Fishel S, Dowell K, Aloum M. Severe ovarian hyperstimulation syndrome: is it really preventable by prophylactic intravenous albumin?. Fertil Steril. 1997;68:851–854
  113. McClelland DB. Human albumin solutions. Br Med J. 1990;300:35–57
  114. Erstad BL, Gales BJ, Rappaport WD. The use of albumin in clinical practice. Arch Intern Med. 1991;151:901–911
  115. Papaleo E, Doldi N, De Santis L, Marelli G, Marsiglio E, Rofena S, et al. Cabergoline influences ovarian stimulation in hyperprolactinaemic patients with polycystic ovary syndrome. Hum Reprod. 2001;16:2263–2266
  116. Gille H, Kowalski J, Li B, LeCouter J, Moffat B, Zioncheck TF, et al. Analysis of biological effects and signalling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J Biol Chem. 2001;276:3222–3230
  117. Gómez R, Simón C, Remohí J, Pellicer A. Vascular endothelial growth factor receptor-2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade. Endocrinology. 2002;143:4339–4348
  118. Gómez R, Simón C, Remohí J, Pellicer A. Administration of moderate and high doses of gonadotropins to female rats increases ovarian vascular endothelial growth factor (VEGF) and VEGF receptor expression that is associated to vascular hyperpermeability. Biol Reprod. 2003;68:2164–2171
  119. Garcia-Velasco JA. How to avoid ovarian hyperstimulation syndrome: a new indication for dopamine agonists. Reprod Biomed Online. 2009;18(Suppl 2):71–75
  120. Nauck M, Karakiulakis G, Perruchoud AP, Papkonstantinou E, Roth M. Corticosteroids inhibit the expression of the vascular endothelial growth factor gene in human vascular smooth muscle cells. Eur J Pharmacol. 1998;341:309–315
  121. Perretti M, Ahluwalia A. The microcirculation and inflammation: site of action for glucocorticoids. Microcirculation. 2000;7:147–161
  122. Gonen Y, Powell WA, Casper RF. Effect of follicular aspiration on hormonal parameters in patients undergoing ovarian stimulation. Hum Reprod. 1991;6:356–358
  123. Santen RJ. Inhibition of aromatase: insights from recent studies. Steroids. 2003;68:559–567
  124. Pau E, Alonso-Muriel I, Gómez R, Novella E, Ruiz A, García-Velasco JA, et al. Plasma levels of soluble vascular endothelial growth factor receptor-1 may determine the onset of early and late ovarian hyperstimulation syndrome. Hum Reprod. 2006;21:1453–1460

 Edward E. Wallach, M.D.Associate Editor

 P.H. has nothing to disclose. J.Q. is a former employee of Schering-Plough. E.G.P. has nothing to disclose.

 All authors were involved with the design, writing, and reviewing of this manuscript and have approved the final version for submission.

PII: S0015-0282(10)00465-6

doi: 10.1016/j.fertnstert.2010.03.028

Fertility and Sterility
Volume 94, Issue 2 , Pages 389-400 , July 2010