1
Views
17
CrossRef citations to date
0
Altmetric
Review

Pathophysiology of ovarian hyperstimulation syndrome and strategies for its prevention and treatment

&
Pages 299-311 | Published online: 10 Jan 2014

References

  • Smits G, Olatunbosun O, Delbaere A, Pierson R, Vassart G, Costagliola S. Ovarian hyperstimulation syndrome due to a mutation in the follicle-stimulating hormone receptor. N. Engl. J. Med.349(8), 760–766 (2003).
  • Vasseur C, Rodien P, Beau I et al. A chorionic gonadotropin-sensitive mutation in the follicle-stimulating hormone receptor as a cause of familial gestational spontaneous ovarian hyperstimulation syndrome. N. Engl. J. Med.349(8), 753–759 (2003).
  • Arora R, Merhi ZO, Khulpateea N, Roth D, Minkoff H. Ovarian hyperstimulation syndrome after a molar pregnancy evacuation. Fertil. Steril.90(4), e1195–e1197 (2008).
  • Ludwig M, Gembruch U, Bauer O, Diedrich K. Ovarian hyperstimulation syndrome (OHSS) in a spontaneous pregnancy with fetal and placental triploidy: information about the general pathophysiology of OHSS. Hum. Reprod.13(8), 2082–2087 (1998).
  • Nappi RG, Di Naro E, D’Aries AP, Nappi L. Natural pregnancy in hypothyroid woman complicated by spontaneous ovarian hyperstimulation syndrome. Am. J. Obstet. Gynecol.178(3), 610–611 (1998).
  • Check JH, Choe JK, Nazari A. Hyperreactio luteinalis despite the absence of a corpus luteum and suppressed serum follicle stimulating concentrations in a triplet pregnancy. Hum. Reprod.15(5), 1043–1045 (2000).
  • Suzuki S. Comparison between spontaneous ovarian hyperstimulation syndrome and hyperreactio luteinalis. Arch. Gynecol. Obstet.269(3), 227–229 (2004).
  • Aboulghar MA, Mansour RT. Ovarian hyperstimulation syndrome: classifications and critical analysis of preventive measures. Hum. Reprod. Update9(3), 275–289 (2003).
  • McClure N, Healy DL, Rogers PA et al. Vascular endothelial growth factor as capillary permeability agent in ovarian hyperstimulation syndrome. Lancet344(8917), 235–236 (1994).
  • Goldsman MP, Pedram A, Dominguez CE, Ciuffardi I, Levin E, Asch RH. Increased capillary permeability induced by human follicular fluid: a hypothesis for an ovarian origin of the hyperstimulation syndrome. Fertil. Steril.63(2), 268–272 (1995).
  • Soares SR, Gomez R, Simon C, Garcia-Velasco JA, Pellicer A. Targeting the vascular endothelial growth factor system to prevent ovarian hyperstimulation syndrome. Hum. Reprod. Update14(4), 321–333 (2008).
  • Albert C, Garrido N, Mercader A et al. The role of endothelial cells in the pathogenesis of ovarian hyperstimulation syndrome. Mol. Hum. Reprod.8(5), 409–418 (2002).
  • de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science255(5047), 989–991 (1992).
  • Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem.269(43), 26988–26995 (1994).
  • Pajusola K, Aprelikova O, Korhonen J et al. FLT4 receptor tyrosine kinase contains seven immunoglobulin-like loops and is expressed in multiple human tissues and cell lines. Cancer Res.52(20), 5738–5743 (1992).
  • Tammela T, Enholm B, Alitalo K, Paavonen K. The biology of vascular endothelial growth factors. Cardiovasc. Res.65(3), 550–563 (2005).
  • Gomez R, Simon C, Remohi J, Pellicer A. Administration of moderate and high doses of gonadotropins to female rats increases ovarian vascular endothelial growth factor (VEGF) and VEGF receptor-2 expression that is associated to vascular hyperpermeability. Biol. Reprod.68(6), 2164–2171 (2003).
  • Gomez R, Gonzalez M, Simon C, Remohi J, Pellicer A. Tyroxine hydroxylase (TH) down regulation in hyperstimulated ovaries reveals the dopamine agonist bromocriptine (Br2) as an effective and specific method to block increased vascular permeability (VP) in OHSS. Fertil. Steril.80(Suppl. 3), 43–44 (2003).
  • Hornig C, Barleon B, Ahmad S, Vuorela P, Ahmed A, Weich HA. Release and complex formation of soluble VEGFR-1 from endothelial cells and biological fluids. Lab. Invest.80(4), 443–454 (2000).
  • He Y, Smith SK, Day KA, Clark DE, Licence DR, Charnock-Jones DS. Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol. Endocrinol.13(4), 537–545 (1999).
  • Wang D, Donner DB, Warren RS. Homeostatic modulation of cell surface KDR and Flt1 expression and expression of the vascular endothelial cell growth factor (VEGF) receptor mRNAs by VEGF. J. Biol. Chem.275(21), 15905–15911 (2000).
  • Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res.57(4), 765–772 (1997).
  • Villasante A, Pacheco A, Ruiz A, Pellicer A, Garcia-Velasco JA. Vascular endothelial cadherin regulates vascular permeability: implications for ovarian hyperstimulation syndrome. J. Clin. Endocrinol. Metab.92(1), 314–321 (2007).
  • Wang TH, Horng SG, Chang CL et al. Human chorionic gonadotropin-induced ovarian hyperstimulation syndrome is associated with up-regulation of vascular endothelial growth factor. J. Clin. Endocrinol. Metab.87(7), 3300–3308 (2002).
  • Pellicer A, Albert C, Mercader A, Bonilla-Musoles F, Remohi J, Simon C. The pathogenesis of ovarian hyperstimulation syndrome: in vivo studies investigating the role of interleukin-1β, interleukin-6, and vascular endothelial growth factor. Fertil. Steril.71(3), 482–489 (1999).
  • Yamamoto S, Konishi I, Tsuruta Y et al. Expression of vascular endothelial growth factor (VEGF) during folliculogenesis and corpus luteum formation in the human ovary. Gynecol. Endocrinol.11(6), 371–381 (1997).
  • Kamat BR, Brown LF, Manseau EJ, Senger DR, Dvorak HF. Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development. Am. J. Pathol.146(1), 157–165 (1995).
  • Gomez R, Simon C, Remohi J, Pellicer A. Vascular endothelial growth factor receptor-2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade. Endocrinology143(11), 4339–4348 (2002).
  • Pau E, Alonso-Muriel I, Gomez R 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.21(6), 1453–1460 (2006).
  • Itskovitz J, Sealey JE. Ovarian prorenin–renin–angiotensin system. Obstet. Gynecol. Surv.42(9), 545–551 (1987).
  • Lightman A, Tarlatzis BC, Rzasa PJ et al. The ovarian renin–angiotensin system: renin-like activity and angiotensin II/III immunoreactivity in gonadotropin-stimulated and unstimulated human follicular fluid. Am. J. Obstet. Gynecol.156(4), 808–816 (1987).
  • Blankestijn PJ, Derkx FH, Van Geelen JA, De Jong FH, Schalekamp MA. Increase in plasma prorenin during the menstrual cycle of a bilaterally nephrectomized woman. Br. J. Obstet. Gynaecol.97(11), 1038–1042 (1990).
  • Glorioso N, Atlas SA, Laragh JH, Jewelewicz R, Sealey JE. Prorenin in high concentrations in human ovarian follicular fluid. Science233(4771), 1422–1424 (1986).
  • Morris RS, Paulson RJ. Ovarian derived prorenin–angiotensin cascade in human reproduction. Fertil. Steril.62(6), 1105–1114 (1994).
  • Huang W, Wu YL, Zhong J, Jiang FX, Tian XL, Yu LF. Angiotensin II type 1 receptor antagonist suppress angiogenesis and growth of gastric cancer xenografts. Dig. Dis. Sci.53(5), 1206–1210 (2008).
  • Shi RZ, Wang JC, Huang SH, Wang XJ, Li QP. Angiotensin II induces vascular endothelial growth factor synthesis in mesenchymal stem cells. Exp. Cell Res.315(1), 10–15 (2009).
  • Anandanadesan R, Gong Q, Chipitsyna G, Witkiewicz A, Yeo CJ, Arafat HA. Angiotensin II induces vascular endothelial growth factor in pancreatic cancer cells through an angiotensin II type 1 receptor and ERK1/2 signaling. J. Gastrointest. Surg.12(1), 57–66 (2008).
  • Sataranatarajan K, Lee MJ, Mariappan MM, Feliers D. PKCd regulates the stimulation of vascular endothelial factor mRNA translation by angiotensin II through hnRNP K. Cell. Signal.20(5), 969–977 (2008).
  • Walter A, Etienne-Selloum N, Sarr M, Kane MO, Beretz A, Schini-Kerth VB. Angiotensin II induces the vascular expression of VEGF and MMP-2 in vivo: preventive effect of red wine polyphenols. J. Vasc. Res.45(5), 386–394 (2008).
  • Herr D, Rodewald M, Fraser HM et al. Regulation of endothelial proliferation by the renin–angiotensin system in human umbilical vein endothelial cells. Reproduction136(1), 125–130 (2008).
  • Ohnuma Y, Toda M, Fujita M et al. Blockade of an angiotensin type I receptor enhances effects of radiation on tumor growth and tumor-associated angiogenesis by reducing vascular endothelial growth factor expression. Biomed. Pharmacother.63(2), 136–145 (2007).
  • Fukumoto M, Takai S, Ishizaki E et al. Involvement of angiotensin II-dependent vascular endothelial growth factor gene expression via NADPH oxidase in the retina in a Type 2 diabetic rat model. Curr. Eye Res.33(10), 885–891 (2008).
  • Delbaere A, Bergmann PJ, Gervy-Decoster C, Camus M, de Maertelaer V, Englert Y. Prorenin and active renin concentrations in plasma and ascites during severe ovarian hyperstimulation syndrome. Hum. Reprod.12(2), 236–240 (1997).
  • Delvigne A, Rozenberg S. Preventive attitude of physicians to avoid OHSS in IVF patients. Hum. Reprod.16(12), 2491–2495 (2001).
  • The Practice Committee of the American Society for Reproductive Medicine. Ovarian hyperstimulation syndrome. Fertil. Steril.90(5 Suppl.), S188–S193 (2008).
  • Enskog A, Henriksson M, Unander M, Nilsson L, Brannstrom M. Prospective study of the clinical and laboratory parameters of patients in whom ovarian hyperstimulation syndrome developed during controlled ovarian hyperstimulation for in vitro fertilization. Fertil. Steril.71(5), 808–814 (1999).
  • Delvigne A, Demoulin A, Smitz J et al. The ovarian hyperstimulation syndrome in in vitro fertilization: a Belgian multicentric study. I. Clinical and biological features. Hum. Reprod.8(9), 1353–1360 (1993).
  • Braat D, Bernardus R, Gerris J. Anonymous reports of lethal cases of ovarian hyperstimulation syndrome. In: Ovarian Hyperstimulation Syndrome. Gerris J, Delvigne A, Olivennes F (Eds). Informa Healthcare, Oxon, UK, 59–70 (2006).
  • MacDougall MJ, Tan SL, Balen A, Jacobs HS. A controlled study comparing patients with and without polycystic ovaries undergoing in vitro fertilization. Hum. Reprod.8(2), 233–237 (1993).
  • van Dop P. Epidemiology and primary risk factors for ovarian hyperstimulation syndrome. In: Ovarian Hyperstimulation syndrome. Gerris J, Delvigne A, Olivennes F (Eds). Informa Healthcare, Oxon, UK, 7–11 (2006).
  • Nakhuda GS, Chu MC, Wang JG, Sauer MV, Lobo RA. Elevated serum mullerian-inhibiting substance may be a marker for ovarian hyperstimulation syndrome in normal women undergoing in vitro fertilization. Fertil. Steril.85(5), 1541–1543 (2006).
  • Lee TH, Liu CH, Huang CC et al. Serum anti-Mullerian hormone and estradiol levels as predictors of ovarian hyperstimulation syndrome in assisted reproduction technology cycles. Hum. Reprod.23(1), 160–167 (2008).
  • Lussiana C, Guani B, Mari C, Restagno G, Massobrio M, Revelli A. Mutations and polymorphisms of the FSH receptor (FSHR) gene: clinical implications in female fecundity and molecular biology of FSHR protein and gene. Obstet. Gynecol. Surv.63(12), 785–795 (2008).
  • Meduri G, Bachelot A, Cocca MP et al. Molecular pathology of the FSH receptor: new insights into FSH physiology. Mol. Cell. Endocrinol.282(1–2), 130–142 (2008).
  • Achrekar SK, Modi DN, Desai SK, Mangoli VS, Mangoli RV, Mahale SD. Follicle-stimulating hormone receptor polymorphism (Thr307Ala) is associated with variable ovarian response and ovarian hyperstimulation syndrome in Indian women. Fertil. Steril.91(2), 432–439 (2009).
  • Binder H, Dittrich R, Hager I et al. Association of FSH receptor and CYP19A1 gene variations with sterility and ovarian hyperstimulation syndrome. Reproduction135(1), 107–116 (2008).
  • Daelemans C, Smits G, de Maertelaer V et al. Prediction of severity of symptoms in iatrogenic ovarian hyperstimulation syndrome by follicle-stimulating hormone receptor Ser680Asn polymorphism. J. Clin. Endocrinol. Metab.89(12), 6310–6315 (2004).
  • d’Alva CB, Serafini P, Motta E, Kohek MB, Latronico AC, Mendonca BB. Absence of follicle-stimulating hormone receptor activating mutations in women with iatrogenic ovarian hyperstimulation syndrome. Fertil. Steril.83(6), 1695–1699 (2005).
  • Kerkela E, Skottman H, Friden B, Bjuresten K, Kere J, Hovatta O. Exclusion of coding-region mutations in luteinizing hormone and follicle-stimulating hormone receptor genes as the cause of ovarian hyperstimulation syndrome. Fertil. Steril.87(3), 603–606 (2007).
  • Delvigne A, Rozenberg S. Systematic review of data concerning etiopathology of ovarian hyperstimulation syndrome. Int. J. Fertil. Womens Med.47(5), 211–226 (2002).
  • 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.6(10), 1395–1399 (1991).
  • Morris RS, Paulson RJ, Sauer MV, Lobo RA. Predictive value of serum oestradiol concentrations and oocyte number in severe ovarian hyperstimulation syndrome. Hum. Reprod.10(4), 811–814 (1995).
  • Mathur RS, Akande AV, Keay SD, Hunt LP, Jenkins JM. Distinction between early and late ovarian hyperstimulation syndrome. Fertil. Steril.73(5), 901–907 (2000).
  • Pellicer A, Miro F, Sampaio M, Gomez E, Bonilla-Musoles FM. In vitro fertilization as a diagnostic and therapeutic tool in a patient with partial 17,20-desmolase deficiency. Fertil. Steril.55(5), 970–975 (1991).
  • Schenker JG. Prevention and treatment of ovarian hyperstimulation. Hum. Reprod.8(5), 653–659 (1993).
  • Blankstein J, Shalev J, Saadon T et al. Ovarian hyperstimulation syndrome: prediction by number and size of preovulatory ovarian follicles. Fertil. Steril.47(4), 597–602 (1987).
  • Tal J, Paz B, Samberg I, Lazarov N, Sharf M. Ultrasonographic and clinical correlates of menotropin versus sequential clomiphene citrate: menotropin therapy for induction of ovulation. Fertil. Steril.44(3), 342–349 (1985).
  • 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.21(6), 1387–1399 (2006).
  • Moll E, van der Veen F, van Wely M. The role of metformin in polycystic ovary syndrome: a systematic review. Hum. Reprod. Update13(6), 527–537 (2007).
  • Doronzo G, Russo I, Mattiello L, Anfossi G, Bosia A, Trovati M. Insulin activates vascular endothelial growth factor in vascular smooth muscle cells: influence of nitric oxide and of insulin resistance. Eur. J. Clin. Invest.34(10), 664–673 (2004).
  • Rimington MR, Walker SM, Shaw RW. The use of laparoscopic ovarian electrocautery in preventing cancellation of in vitro fertilization treatment cycles due to risk of ovarian hyperstimulation syndrome in women with polycystic ovaries. Hum. Reprod.12(7), 1443–1447 (1997).
  • Tozer AJ, Al-Shawaf T, Zosmer A et al. Does laparoscopic ovarian diathermy affect the outcome of IVF-embryo transfer in women with polycystic ovarian syndrome? A retrospective comparative study. Hum. Reprod.16(1), 91–95 (2001).
  • Tan SL, Child TJ, Cheung AP et al. A randomized, double-blind, multicenter study comparing a starting dose of 100 IU or 200 IU of recombinant follicle stimulating hormone (Puregon) in women undergoing controlled ovarian hyperstimulation for IVF treatment. J. Assist. Reprod. Genet.22(2), 81–88 (2005).
  • Marci R, Senn A, Dessole S et al. A low-dose stimulation protocol using highly purified follicle-stimulating hormone can lead to high pregnancy rates in in vitro fertilization patients with polycystic ovaries who are at risk of a high ovarian response to gonadotropins. Fertil. Steril.75(6), 1131–1135 (2001).
  • Daya S. Updated meta-analysis of recombinant follicle-stimulating hormone (FSH) versus urinary FSH for ovarian stimulation in assisted reproduction. Fertil. Steril.77(4), 711–714 (2002).
  • Van Wely M, Westergaard LG, Bossuyt PM, Van der Veen F. Human menopausal gonadotropin versus recombinant follicle stimulation hormone for ovarian stimulation in assisted reproductive cycles. Cochrane Database Syst. Rev.1, CD003973 (2003).
  • Coomarasamy A, Afnan M, Cheema D, van der Veen F, Bossuyt PM, van Wely M. Urinary hMG versus recombinant FSH for controlled ovarian hyperstimulation following an agonist long down-regulation protocol in IVF or ICSI treatment: a systematic review and meta-analysis. Hum. Reprod.23(2), 310–315 (2008).
  • Nugent D, Vandekerckhove P, Hughes E, Arnot M, Lilford R. Gonadotrophin therapy for ovulation induction in subfertility associated with polycystic ovary syndrome. Cochrane Database Syst. Rev.4, CD000410 (2000).
  • Bayram N, van Wely M, van Der Veen F. Recombinant FSH versus urinary gonadotrophins or recombinant FSH for ovulation induction in subfertility associated with polycystic ovary syndrome. Cochrane Database Syst. Rev.2, CD002121 (2001).
  • Delvigne A, Rozenberg S. Epidemiology and prevention of ovarian hyperstimulation syndrome (OHSS): a review. Hum. Reprod. Update8(6), 559–577 (2002).
  • Al-Inany HG, Abou-Setta AM, Aboulghar M. Gonadotrophin-releasing hormone antagonists for assisted conception. Cochrane Database Syst. Rev.3, CD001750 (2006).
  • 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. Update12(6), 651–671 (2006).
  • Albano C, Felberbaum RE, Smitz J et al. Ovarian stimulation with HMG: results of a prospective randomized Phase III European study comparing the luteinizing hormone-releasing hormone (LHRH)-antagonist cetrorelix and the LHRH-agonist buserelin. European Cetrorelix Study Group. Hum. Reprod.15(3), 526–531 (2000).
  • Badrawy A, Al-Inany HG, Hussein M, Zaki S, Ramzy AM. Agonist versus antagonist in ICSI cycles: a randomized trial and cost effectiveness analysis. Middle East Fertil. Soc. J.10(1), 49–54 (2005).
  • Barmat LI, Chantilis SJ, Hurst BS, Dickey RP. A randomized prospective trial comparing gonadotropin-releasing hormone (GnRH) antagonist/recombinant follicle-stimulating hormone (rFSH) versus GnRH-agonist/rFSH in women pretreated with oral contraceptives before in vitro fertilization. Fertil. Steril.83(2), 321–330 (2005).
  • Causio F, Sarcina E, Leonetti T. GnRH agonist versus GnRH antagonist in an IVF program: luteal phase hormonal characteristics. Hum. Reprod.19(Suppl.), i103 (2004).
  • Cheung LP, Lam PM, Lok IH et al. GnRH antagonist versus long GnRH agonist protocol in poor responders undergoing IVF: a randomized controlled trial. Hum. Reprod.20(3), 616–621 (2005).
  • Franco JJ, Baruffi R, Petersen C, Mauri A, Felipe V, Contart P. Comparison of ovarian stimulation with recombinant FSH after 2nd phase protocols with GnRH analogs (I - estradiol + ganirelix versus II -nafarelin). Comparacao da stimulacao ovariana comFSH recombinante apos protocolo de 2A fase com analogos do GNRH (I - estradiol + ganirelix versus II - nafarelin)]. J. Brasil. Reprod. Assist.7(1), 26–32 (2003).
  • Friedler S, Gilboa S, Schachter M et al. Luteal phase characteristics following GnRH antagonist or agonist treatment: a randomized comparative study. Hum. Reprod.18(Suppl.), xviii 26 (2003).
  • 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.88(1), 166–173 (2003).
  • Kyono K, Nakajo Y, Sasaki S, Kumagai S, Suzuki S. A prospective randomized study of three different controlled ovarian hyperstimulation (COH) protocols. Fertil. Steril.84(Suppl. 1), S299 (2005).
  • Lee TH, Wu MY, Chen HF, Chen MJ, Ho HN, Yang YS. Ovarian response and follicular development for single-dose and multiple-dose protocols for gonadotropin-releasing hormone antagonist administration. Fertil. Steril.83(6), 1700–1707 (2005).
  • Loutradis D, Stefanidis K, Drakakis P, Milingos S, Antsaklis A, Michalas S. A modified gonadotropin-releasing hormone (GnRH) antagonist protocol failed to increase clinical pregnancy rates in comparison with the long GnRH protocol. Fertil. Steril.82(5), 1446–1448 (2004).
  • Marci R, Caserta D, Dolo V, Tatone C, Pavan A, Moscarini M. GnRH antagonist in IVF poor-responder patients: results of a randomized trial. Reprod. Biomed. Online11(2), 189–193 (2005).
  • Olivennes F, Belaisch-Allart J, Emperaire JC et al. Prospective, randomized, controlled study of in vitro fertilization-embryo transfer with a single dose of a luteinizing hormone-releasing hormone (LH-RH) antagonist (cetrorelix) or a depot formula of an LH-RH agonist (triptorelin). Fertil. Steril.73(2), 314–320 (2000).
  • Rombauts L, Healy D, Norman RJ. A comparative randomized trial to assess the impact of oral contraceptive pretreatment on follicular growth and hormone profiles in GnRH antagonist-treated patients. Hum. Reprod.21(1), 95–103 (2006).
  • Zikopoulos K, Kaponis A, Adonakis G et al. A prospective randomized study comparing gonadotropin-releasing hormone agonists or gonadotropin-releasing hormone antagonists in couples with unexplained infertility and/or mild oligozoospermia. Fertil. Steril.83(5), 1354–1362 (2005).
  • Griesinger G, Diedrich K, Tarlatzis BC, Kolibianakis EM. GnRH-antagonists in ovarian stimulation for IVF in patients with poor response to gonadotrophins, polycystic ovary syndrome, and risk of ovarian hyperstimulation: a meta-analysis. Reprod. Biomed. Online13(5), 628–638 (2006).
  • El-Sheikh MM, Hussein M, Sheikh AA, Fouad S, El-Sheikh R, Al-Hasani S. Limited ovarian stimulation results in the recovery of mature oocytes in polycystic ovarian disease patients: a preliminary report. Eur. J. Obstet. Gynecol. Reprod. Biol.83(1), 81–83 (1999).
  • 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.94(2), 245–249 (2001).
  • Lim KS, Yoon SH, Lim JH. IVM as an alternative for over responders. In: In VitroMaturation of Human Oocytes. Basic Science to Clinical Application. Tan SL, Chian RC, Buckett WM (Eds). Informa Healthcare, Oxon, UK, 353–361 (2007).
  • Lipitz S, Ben-Rafael Z, Bider D, Shalev J, Mashiach S. Quintuplet pregnancy and third degree ovarian hyperstimulation despite withholding human chorionic gonadotrophin. Hum. Reprod.6(10), 1478–1479 (1991).
  • The European Recombinant LH Study Group. Human recombinant luteinizing hormone is as effective as, but safer than, urinary human chorionic gonadotropin in inducing final follicular maturation and ovulation in in vitro fertilization procedures: results of a multicenter double-blind study. J. Clin. Endocrinol. Metab.86(6), 2607–2618 (2001).
  • Manau D, Fabregues F, Arroyo V, Jimenez W, Vanrell JA, Balasch J. Hemodynamic changes induced by urinary human chorionic gonadotropin and recombinant luteinizing hormone used for inducing final follicular maturation and luteinization. Fertil. Steril.78(6), 1261–1267 (2002).
  • Al-Inany H, Aboulghar MA, Mansour RT, Proctor M. Recombinant versus urinary gonadotrophins for triggering ovulation in assisted conception. Hum. Reprod.20(8), 2061–2073 (2005).
  • Delvigne A. Secondary prevention of threatening ovarian hyperstimulation syndrome. In: Ovarian Hyperstimulation Syndrome. Gerris J, Delvigne A, Olivennes F (Eds). Informa Healthcare, Oxon, UK, 217–238 (2006).
  • Acevedo B, Gomez-Palomares JL, Ricciarelli E, Hernandez ER. Triggering ovulation with gonadotropin-releasing hormone agonists does not compromise embryo implantation rates. Fertil. Steril.86(6), 1682–1687 (2006).
  • Kol S. Does ovulation triggering influence the risk for ovarian hyperstimulation syndrome? In: Ovarian Hyperstimulation Syndrome. Gerris J, Delvigne A, Olivennes F (Eds). Informa Healthcare, Oxon, UK, 203–216 (2006).
  • Kol S, Solt I. GnRH agonist for triggering final oocyte maturation in patients at risk of ovarian hyperstimulation syndrome: still a controversy? J. Assist. Reprod. Genet.25(2–3), 63–66 (2008).
  • 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.56(2), 213–220 (1991).
  • 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.89(1), 84–91 (2008).
  • Garcia-Velasco JA, Zuniga A, Pacheco A et al. Coasting acts through downregulation of VEGF gene expression and protein secretion. Hum. Reprod.19(7), 1530–1538 (2004).
  • Mansour R, Aboulghar M, Serour G, Amin Y, Abou-Setta AM. Criteria of a successful coasting protocol for the prevention of severe ovarian hyperstimulation syndrome. Hum. Reprod.20(11), 3167–3172 (2005).
  • Ulug U, Bahceci M, Erden HF, Shalev E, Ben-Shlomo I. The significance of coasting duration during ovarian stimulation for conception in assisted fertilization cycles. Hum. Reprod.17(2), 310–313 (2002).
  • Isaza V, Garcia-Velasco JA, Aragones M, Remohi J, Simon C, Pellicer A. Oocyte and embryo quality after coasting: the experience from oocyte donation. Hum. Reprod.17(7), 1777–1782 (2002).
  • Urman B, Pride SM, Yuen BH. Management of overstimulated gonadotrophin cycles with a controlled drift period. Hum. Reprod.7(2), 213–217 (1992).
  • Sher G, Salem R, Feinman M, Dodge S, Zouves C, Knutzen V. Eliminating the risk of life-endangering complications following overstimulation with menotropin fertility agents: a report on women undergoing in vitro fertilization and embryo transfer. Obstet. Gynecol.81(6), 1009–1011 (1993).
  • Dhont M, Van der Straeten F, De Sutter P. Prevention of severe ovarian hyperstimulation by coasting. Fertil. Steril.70(5), 847–850 (1998).
  • Egbase PE, Sharhan MA, Grudzinskas JG. Early unilateral follicular aspiration compared with coasting for the prevention of severe ovarian hyperstimulation syndrome: a prospective randomized study. Hum. Reprod.14(6), 1421–1425 (1999).
  • Garcia-Velasco JA, Isaza V, Quea G, Pellicer A. Coasting for the prevention of ovarian hyperstimulation syndrome: much ado about nothing? Fertil. Steril.85(3), 547–554 (2006).
  • Mathur R, Kailasam C, Jenkins J. Review of the evidence base of strategies to prevent ovarian hyperstimulation syndrome. Hum. Fertil. (Camb.)10(2), 75–85 (2007).
  • Ho Yuen B, Nguyen TA, Cheung AP, Leung PC. Clinical and endocrine response to the withdrawal of gonadotropin-releasing hormone agonists during prolonged coasting. Fertil. Steril. DOI: 10.1016/j.fertnstert.2008.06.039 (2008) (Epub ahead of print).
  • Giles J, Requena A, Garcia-Velasco JA, Pacheco A, Pellicer J, Pellicer A. GnRH analogue for the prevention of ovarian hyperstimulation syndrome: a pilot study. Fertil. Steril.91(4), 1366–1369(2008).
  • Lainas TG, Sfontouris IA, Zorzovilis IZ, Petsas GK, Lainas GT, Kolibianakis EM. Management of severe early ovarian hyperstimulation syndrome by re-initiation of GnRH antagonist. Reprod. Biomed. Online15(4), 408–412 (2007).
  • Nikolettos N, Asimakopoulos B, Simopoulou M, al-Hasani S. GnRH agonist administration after embryo transfer, in long protocol stimulated cycles, prevents ovarian hyperstimulation syndrome. A report of five cases. In Vivo17(6), 655–658 (2003).
  • Endo T, Honnma H, Hayashi T et al. Continuation of GnRH agonist administration for 1 week, after hCG injection, prevents ovarian hyperstimulation syndrome following elective cryopreservation of all pronucleate embryos. Hum. Reprod.17(10), 2548–2551 (2002).
  • Wada I, Matson PL, Horne G, Buck P, Lieberman BA. Is continuation of a gonadotrophin-releasing hormone agonist (GnRHa) necessary for women at risk of developing the ovarian hyperstimulation syndrome? Hum. Reprod.7(8), 1090–1093 (1992).
  • Farhi J, Ben-Haroush A, Lande Y, Sapir O, Pinkas H, Fisch B. In vitro fertilization cycle outcome after coasting in gonadotropin-releasing hormone (GnRH) agonist versus GnRH antagonist protocols. Fertil. Steril.91(2), 377–382 (2008).
  • Bowling KM, Huang Z, Xu D et al. Direct binding of GTP cyclohydrolase and tyrosine hydroxylase: regulatory interactions between key enzymes in dopamine biosynthesis. J. Biol. Chem.283(46), 31449–31459 (2008).
  • Basu S, Nagy JA, Pal S et al. The neurotransmitter dopamine inhibits angiogenesis induced by vascular permeability factor/vascular endothelial growth factor. Nat. Med.7(5), 569–574 (2001).
  • Sarkar C, Chakroborty D, Mitra RB, Banerjee S, Dasgupta PS, Basu S. Dopamine in vivo inhibits VEGF-induced phosphorylation of VEGFR-2, MAPK, and focal adhesion kinase in endothelial cells. Am. J. Physiol. Heart Circ. Physiol.287(4), H1554–H1560 (2004).
  • Quinn TP, Peters KG, De Vries C, Ferrara N, Williams LT. Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc. Natl Acad. Sci. USA90(16), 7533–7537 (1993).
  • Gomez R, Gonzalez-Izquierdo M, Zimmermann RC et al. Low-dose dopamine agonist administration blocks vascular endothelial growth factor (VEGF)-mediated vascular hyperpermeability without altering VEGF receptor 2-dependent luteal angiogenesis in a rat ovarian hyperstimulation model. Endocrinology147(11), 5400–5411 (2006).
  • Alvarez C, Marti-Bonmati L, Novella-Maestre E et al. Dopamine agonist cabergoline reduces hemoconcentration and ascites in hyperstimulated women undergoing assisted reproduction. J. Clin. Endocrinol. Metab.92(8), 2931–2937 (2007).
  • Alvarez C, Alonso-Muriel I, Garcia G et al. Implantation is apparently unaffected by the dopamine agonist cabergoline when administered to prevent ovarian hyperstimulation syndrome in women undergoing assisted reproduction treatment: a pilot study. Hum. Reprod.22(12), 3210–3214 (2007).
  • Carizza C, Abdelmassih V, Abdelmassih S et al. Cabergoline reduces the early onset of ovarian hyperstimulation syndrome: a prospective randomized study. Reprod. Biomed. Online17(6), 751–755 (2008).
  • Ando H, Furugori K, Shibata D, Harata T, Murata Y, Mizutani S. Dual renin–angiotensin blockade therapy in patients at high risk of early ovarian hyperstimulation syndrome receiving IVF and elective embryo cryopreservation: a case series. Hum. Reprod.18(6), 1219–1222 (2003).
  • Ata B, Yakin K, Alatas C, Urman B. Dual renin–angiotensin blockage and total embryo cryopreservation is not a risk-free strategy in patients at high risk for ovarian hyperstimulation syndrome. Fertil. Steril.90(3), 531–536 (2008).
  • Aboulghar M, Evers JH, Al-Inany H. Intravenous albumin for preventing severe ovarian hyperstimulation syndrome: a Cochrane review. Hum. Reprod.17(12), 3027–3032 (2002).
  • Bellver J, Munoz EA, Ballesteros A et al. Intravenous albumin does not prevent moderate–severe ovarian hyperstimulation syndrome in high-risk IVF patients: a randomized controlled study. Hum. Reprod.18(11), 2283–2288 (2003).
  • Isikoglu M, Berkkanoglu M, Senturk Z, Ozgur K. Human albumin does not prevent ovarian hyperstimulation syndrome in assisted reproductive technology program: a prospective randomized placebo-controlled double blind study. Fertil. Steril.88(4), 982–985 (2007).
  • 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.96(2), 187–192 (2001).
  • Graf MA, Fischer R, Naether OG, Baukloh V, Tafel J, Nuckel M. Reduced incidence of ovarian hyperstimulation syndrome by prophylactic infusion of hydroxyaethyl starch solution in an in-vitro fertilization programme. Hum. Reprod.12(12), 2599–2602 (1997).
  • Konig E, Bussen S, Sutterlin M, Steck T. Prophylactic intravenous hydroxyethyle starch solution prevents moderate–severe ovarian hyperstimulation in in-vitro fertilization patients: a prospective, randomized, double-blind and placebo-controlled study. Hum. Reprod.13(9), 2421–2424 (1998).
  • Enskog A, Brannstrom M. Immunological aspects of ovarian hyperstimulation syndrome. In: Ovarian Hyperstimulation Syndrome. Gerris J, Delvigne A, Olivennes F (Eds). Informa Healthcare, Oxon, UK, 107–120 (2006).
  • Tan SL, Balen A, el Hussein E, Campbell S, Jacobs HS. The administration of glucocorticoids for the prevention of ovarian hyperstimulation syndrome in in vitro fertilization: a prospective randomized study. Fertil. Steril.58(2), 378–383 (1992).
  • Lyons CA, Wheeler CA, Frishman GN, Hackett RJ, Seifer DB, Haning RV Jr. Early and late presentation of the ovarian hyperstimulation syndrome: two distinct entities with different risk factors. Hum. Reprod.9(5), 792–799 (1994).
  • Papanikolaou EG, Tournaye H, Verpoest W et al. Early and late ovarian hyperstimulation syndrome: early pregnancy outcome and profile. Hum. Reprod.20(3), 636–641 (2005).
  • De Neubourg D, Mangelschots K, Van Royen E, Vercruyssen M, Gerris J. Singleton pregnancies are as affected by ovarian hyperstimulation syndrome as twin pregnancies. Fertil. Steril.82(6), 1691–1693 (2004).
  • D’Angelo A, Amso N. Embryo freezing for preventing ovarian hyperstimulation syndrome. Cochrane Database Syst. Rev.3, CD002806 (2007).
  • Daya S, Gunby JL. Luteal phase support in assisted reproduction cycles. Cochrane Database Syst. Rev.3, CD004830 (2008).
  • Abramov Y, Elchalal U, Schenker JG. Pulmonary manifestations of severe ovarian hyperstimulation syndrome: a multicenter study. Fertil. Steril.71(4), 645–651 (1999).
  • Rackow EC, Falk JL, Fein IA et al. Fluid resuscitation in circulatory shock: a comparison of the cardiorespiratory effects of albumin, hetastarch, and saline solutions in patients with hypovolemic and septic shock. Crit. Care Med.11(11), 839–850 (1983).
  • Abramov Y, Fatum M, Abrahamov D, Schenker JG. Hydroxyethylstarch versus human albumin for the treatment of severe ovarian hyperstimulation syndrome: a preliminary report. Fertil. Steril.75(6), 1228–1230 (2001).
  • Gamzu R, Almog B, Levin Y, Avni A, Lessing JB, Baram A. Efficacy of hydroxyethyl starch and haemaccel for the treatment of severe ovarian hyperstimulation syndrome. Fertil. Steril.77(6), 1302–1303 (2002).
  • Endo T, Kitajima Y, Hayashi T, Fujii M, Hata H, Azumaguchi A. Low-molecular-weight dextran infusion is more effective for the treatment of hemoconcentration due to severe ovarian hyperstimulation syndrome than human albumin infusion. Fertil. Steril.82(5), 1449–1451 (2004).
  • Levin I, Almog B, Avni A, Baram A, Lessing JB, Gamzu R. Effect of paracentesis of ascitic fluids on urinary output and blood indices in patients with severe ovarian hyperstimulation syndrome. Fertil. Steril.77(5), 986–988 (2002).
  • Chen CD, Yang JH, Chao KH, Chen SU, Ho HN, Yang YS. Effects of repeated abdominal paracentesis on uterine and intraovarian haemodynamics and pregnancy outcome in severe ovarian hyperstimulation syndrome. Hum. Reprod.13(8), 2077–2081 (1998).
  • Ron-El R, Friedler S, Schachter M, Raziel R. Clinical management, ascites management and obstetrical outcome in patients with ovarian hyperstimulation syndrome. In: Ovarian Hyperstimulation Syndrome. Gerris J, Delvigne A, Olivennes F (Eds). Informa Healthcare, Oxon, UK, 149–158 (2006).
  • Ozgun MT, Batukan C, Oner G, Uludag S, Aygen EM, Sahin Y. Removal of ascites up to 7.5 liters on one occasion and 45 liters in total may be safe in patients with severe ovarian hyperstimulation syndrome. Gynecol. Endocrinol.24(11), 656–658 (2008).
  • Smith LP, Hacker MR, Alper MM. Patients with severe ovarian hyperstimulation syndrome can be managed safely with aggressive outpatient transvaginal paracentesis. Fertil. Steril. DOI: 10.1016/j.fertnstert.2008.09.011 (2008) (Epub ahead of print).
  • Csokmay JM, Yauger BJ, Henne MB, Armstrong AY, Queenan JT, Segars JH. Cost analysis model of outpatient management of ovarian hyperstimulation syndrome with paracentesis: ‘tap early and often’ versus hospitalization. Fertil. Steril. DOI: 10.1016/j.fertnstert.2008.09.054 (2008) (Epub ahead of print).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.