Semin Reprod Med 2010; 28(6): 441-447
DOI: 10.1055/s-0030-1265669
© Thieme Medical Publishers

Ovarian Hyperstimulation Syndrome: Definition, Incidence, and Classification

Einat Zivi1 , Alex Simon1 , Neri Laufer1
  • 1Department of Obstetrics and Gynecology, Hadassah University Hospital, Jerusalem, Israel
Further Information

Publication History

Publication Date:
16 November 2010 (online)

ABSTRACT

Ovarian hyperstimulation syndrome (OHSS) is a iatrogenic complication of controlled ovarian stimulation. Although considered uncommon, the severe form is potentially fatal. Different clinical classifications have been developed through the years. No matter whether it is termed “grade C” or “critical” OHSS, life-threatening events may develop. Hence it is prudent to recognize the population at risk. Several risk factors for OHSS have been identified; some are considered major risk factors such as polycystic ovary syndrome; others are less well defined. Preventive measures could be taken before and during the treatment cycle while taking into consideration the patient's characteristics and the various treatment options and approaches that currently exist.

REFERENCES

  • 1 Muller P. In: Beclere C Gonadotrophines en Gynécologie. Paris, France; Masson 1962: 137
  • 2 Schenker J G, Weinstein D. Ovarian hyperstimulation syndrome: a current survey.  Fertil Steril. 1978;  30(3) 255-268
  • 3 Delvigne A, Rozenberg S. Epidemiology and prevention of ovarian hyperstimulation syndrome (OHSS): a review.  Hum Reprod Update. 2002;  8(6) 559-577
  • 4 Daya S. Updated meta-analysis of recombinant follicle-stimulating hormone (FSH) versus urinary FSH for ovarian stimulation in assisted reproduction.  Fertil Steril. 2002;  77(4) 711-714
  • 5 Check J H, Wu C H, Gocial B, Adelson H G. Severe ovarian hyperstimulation syndrome from treatment with urinary follicle-stimulating hormone: two cases.  Fertil Steril. 1985;  43(2) 317-319
  • 6 Hedon B, Out H J, Hugues J N et al. Efficacy and safety of recombinant follicle stimulating hormone (Puregon) in infertile women pituitary-suppressed with triptorelin undergoing in-vitro fertilization: a prospective, randomized, assessor-blind, multicentre trial.  Hum Reprod. 1995;  10(12) 3102-3106
  • 7 European and Israeli Study Group on Highly Purified Menotropin versus Recombinant Follicle-Stimulating Hormone . Efficacy and safety of highly purified menotropin versus recombinant follicle-stimulating hormone in in vitro fertilization/intracytoplasmic sperm injection cycles: a randomized, comparative trial.  Fertil Steril. 2002;  78(3) 520-528
  • 8 Schenker J G, Ezra Y. Complications of assisted reproductive techniques.  Fertil Steril. 1994;  61(3) 411-422
  • 9 Golan A, Ron-el R, Herman A, Soffer Y, Weinraub Z, Caspi E. Ovarian hyperstimulation syndrome: an update review.  Obstet Gynecol Surv. 1989;  44(6) 430-440
  • 10 Brinsden P R, Wada I, Tan S L, Balen A, Jacobs H S. Diagnosis, prevention and management of ovarian hyperstimulation syndrome.  Br J Obstet Gynaecol. 1995;  102(10) 767-772
  • 11 Morris R S, Paulson R J, Sauer M V, Lobo R A. Predictive value of serum oestradiol concentrations and oocyte number in severe ovarian hyperstimulation syndrome.  Hum Reprod. 1995;  10(4) 811-814
  • 12 Abramov Y, Elchalal U, Schenker J G. Severe OHSS: An ‘epidemic’ of severe OHSS: a price we have to pay?.  Hum Reprod. 1999;  14(9) 2181-2183
  • 13 Klemetti R, Sevón T, Gissler M, Hemminki E. Complications of IVF and ovulation induction.  Hum Reprod. 2005;  20(12) 3293-3300
  • 14 Delvigne A. Symposium: update on prediction and management of OHSS. Epidemiology of OHSS.  Reprod Biomed Online. 2009;  19(1) 8-13
  • 15 Enskog A, Henriksson M, Unander M, Nilsson L, Brännström 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. 1999;  71(5) 808-814
  • 16 Delvigne A, Dubois M, Battheu B 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(9) 1361-1366
  • 17 Golan A, Ron-el R, Herman A, Soffer Y, Weinraub Z, Caspi E. Ovarian hyperstimulation syndrome: an update review.  Obstet Gynecol Surv. 1989;  44(6) 430-440
  • 18 Navot D, Relou A, Birkenfeld A, Rabinowitz R, Brzezinski A, Margalioth E J. Risk factors and prognostic variables in the ovarian hyperstimulation syndrome.  Am J Obstet Gynecol. 1988;  159(1) 210-215
  • 19 Aramwit P, Pruksananonda K, Kasettratat N, Jammeechai K. Risk factors for ovarian hyperstimulation syndrome in Thai patients using gonadotropins for in vitro fertilization.  Am J Health Syst Pharm. 2008;  65(12) 1148-1153
  • 20 Lewis C G, Warnes G M, Wang X J, Matthews C D. Failure of body mass index or body weight to influence markedly the response to ovarian hyperstimulation in normal cycling women.  Fertil Steril. 1990;  53(6) 1097-1099
  • 21 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. 1993;  8(9) 1353-1360
  • 22 Rizk B, Smitz J. Ovarian hyperstimulation syndrome after superovulation using GnRH agonists for IVF and related procedures.  Hum Reprod. 1992;  7(3) 320-327
  • 23 Navot D, Bergh P A, Laufer N. Ovarian hyperstimulation syndrome in novel reproductive technologies: prevention and treatment.  Fertil Steril. 1992;  58(2) 249-261
  • 24 Kamat B R, Brown L F, Manseau E J, Senger D R, Dvorak H F. Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development.  Am J Pathol. 1995;  146(1) 157-165
  • 25 Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group . Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome.  Fertil Steril. 2004;  81(1) 19-25
  • 26 Bettendorf G, Lindner C. The ovarian hyperstimulation syndrome.  Horm Metab Res. 1987;  19(11) 519-522
  • 27 Gustafson O, Carlström K, Nylund L. Androstenedione as a predictor of ovarian hyperstimulation syndrome.  Hum Reprod. 1992;  7(7) 918-921
  • 28 Bódis J, Török A, Tinneberg H R. LH/FSH ratio as a predictor of ovarian hyperstimulation syndrome.  Hum Reprod. 1997;  12(4) 869-870
  • 29 Aboulghar M. Prediction of ovarian hyperstimulation syndrome (OHSS). Estradiol level has an important role in the prediction of OHSS.  Hum Reprod. 2003;  18(6) 1140-1141
  • 30 Haning Jr R V, Austin C W, Carlson I H, Kuzma D L, Shapiro S S, Zweibel W J. Plasma estradiol is superior to ultrasound and urinary estriol glucuronide as a predictor of ovarian hyperstimulation during induction of ovulation with menotropins.  Fertil Steril. 1983;  40(1) 31-36
  • 31 Asch R H, Li H P, Balmaceda J P, Weckstein L N, Stone S C. Severe ovarian hyperstimulation syndrome in assisted reproductive technology: definition of high risk groups.  Hum Reprod. 1991;  6(10) 1395-1399
  • 32 Mathur R S, Akande A V, Keay S D, Hunt L P, Jenkins J M. Distinction between early and late ovarian hyperstimulation syndrome.  Fertil Steril. 2000;  73(5) 901-907
  • 33 Levy T, Orvieto R, Homburg R, Peleg D, Dekel A, Ben-Rafael Z. Severe ovarian hyperstimulation syndrome despite low plasma oestrogen concentrations in a hypogonadotrophic, hypogonadal patient.  Hum Reprod. 1996;  11(6) 1177-1179
  • 34 Rizk B, Aboulghar M. Classification, pathophysiology and management of ovarian hyperstimulation syndrome. In: Brinsden P A Textbook of in Vitro Fertilization and Assisted Reproduction. 2nd ed. Lancaster, United Kingdom; Parthenon 1999: 131-155
  • 35 Aboulghar M. Symposium: Update on prediction and management of OHSS. Prevention of OHSS.  Reprod Biomed Online. 2009;  19(1) 33-42
  • 36 Orvieto R, Achiron A, Margalit R, Ben-Rafael Z. The role of intravenous immunoglobulin in the prevention of severe ovarian hyperstimulation syndrome.  J Assist Reprod Genet. 1998;  15(1) 46-49
  • 37 Sher G, Zouves C, Feinman M, Maassarani G. ‘Prolonged coasting’: an effective method for preventing severe ovarian hyperstimulation syndrome in patients undergoing in-vitro fertilization.  Hum Reprod. 1995;  10(12) 3107-3109
  • 38 Benadiva C A, Davis O, Kligman I, Moomjy M, Liu H C, Rosenwaks Z. Withholding gonadotropin administration is an effective alternative for the prevention of ovarian hyperstimulation syndrome.  Fertil Steril. 1997;  67(4) 724-727
  • 39 Haas G G, Seibel M M. Human menopausal gonadotropins for ovulation induction, intrauterine insemination and assisted reproduction. In: Seibel MM, Blackwell RE Ovulation Induction. New York, NY; Raven 1994: 117-133
  • 40 Orvieto R. Prediction of ovarian hyperstimulation syndrome. Challenging the estradiol mythos.  Hum Reprod. 2003;  18(4) 665-667
  • 41 Blankstein J, Shalev J, Saadon T et al. Ovarian hyperstimulation syndrome: prediction by number and size of preovulatory ovarian follicles.  Fertil Steril. 1987;  47(4) 597-602
  • 42 Jayaprakasan K, Herbert M, Moody E, Stewart J A, Murdoch A P. Estimating the risks of ovarian hyperstimulation syndrome (OHSS): implications for egg donation for research.  Hum Fertil (Camb). 2007;  10(3) 183-187
  • 43 Verwoerd G R, Mathews T, Brinsden P R. Optimal follicle and oocyte numbers for cryopreservation of all embryos in IVF cycles at risk of OHSS.  Reprod Biomed Online. 2008;  17(3) 312-317
  • 44 Papanikolaou E G, Pozzobon C, Kolibianakis E M et al. Incidence and prediction of ovarian hyperstimulation syndrome in women undergoing gonadotropin-releasing hormone antagonist in vitro fertilization cycles.  Fertil Steril. 2006;  85(1) 112-120
  • 45 Forman R G, Frydman R, Egan D, Ross C, Barlow D H. Severe ovarian hyperstimulation syndrome using agonists of gonadotropin-releasing hormone for in vitro fertilization: a European series and a proposal for prevention.  Fertil Steril. 1990;  53(3) 502-509
  • 46 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. 1985;  44(3) 342-349
  • 47 Ragni G, Vegetti W, Riccaboni A, Engl B, Brigante C, Crosignani P G. Comparison of GnRH agonists and antagonists in assisted reproduction cycles of patients at high risk of ovarian hyperstimulation syndrome.  Hum Reprod. 2005;  20(9) 2421-2425
  • 48 Whelan III J G, Vlahos N F. The ovarian hyperstimulation syndrome.  Fertil Steril. 2000;  73(5) 883-896
  • 49 Laufer N, Simon A, Hurwitz A, Glaststein I Z. In vitro fertilization. In: Seibel MM Infertility: A Comprehensive Text. 2nd ed. Norwalk, CT; Appleton & Lange 1997: 703-736
  • 50 MacDougall M J, Tan S L, Jacobs H S. In-vitro fertilization and the ovarian hyperstimulation syndrome.  Hum Reprod. 1992;  7(5) 597-600
  • 51 Kol S, Dor J. Symposium: Update on prediction and management of OHSS. Prevention of OHSS: GnRH agonist versus HCG to trigger ovulation.  Reprod Biomed Online. 2009;  19(1) 59-60
  • 52 Al-Inany H G, Aboulghar M, Aboulghar M. Gonadotrophin-releasing hormone antagonists for assisted conception.  Cochrane Database Syst Rev. 2001;  (4) CD001750
  • 53 Smitz J, Camus M, Devroey P, Erard P, Wisanto A, Van Steirteghem A C. Incidence of severe ovarian hyperstimulation syndrome after GnRH agonist/HMG superovulation for in-vitro fertilization.  Hum Reprod. 1990;  5(8) 933-937
  • 54 Rabau E, David A, Serr D M, Mashiach S, Lunenfeld B. Human menopausal gonadotropins for anovulation and sterility. Results of 7 years of treatment.  Am J Obstet Gynecol. 1967;  98(1) 92-98
  • 55 Report of a WHO scientific group . Agents stimulating gonadal function in the human. Report of a WHO scientific group.  World Health Organ Tech Rep Ser. 1973;  514 1-30
  • 56 Golan A, Weissman A. Symposium: Update on prediction and management of OHSS. A modern classification of OHSS.  Reprod Biomed Online. 2009;  19(1) 28-32
  • 57 Lyons C A, Wheeler C A, Frishman G N, Hackett R J, Seifer D B, Haning Jr R V. Early and late presentation of the ovarian hyperstimulation syndrome: two distinct entities with different risk factors.  Hum Reprod. 1994;  9(5) 792-799
  • 58 Papanikolaou E G, Tournaye H, Verpoest W et al. Early and late ovarian hyperstimulation syndrome: early pregnancy outcome and profile.  Hum Reprod. 2005;  20(3) 636-641
  • 59 Lee K H, Kim S H, Jee B C et al. Comparison of clinical characteristics between early and late patterns in hospitalized patients with ovarian hyperstimulation syndrome.  Fertil Steril. 2010;  93(7) 2274-2280
  • 60 Check J H, Choe J K, Nazari A. Hyperreactio luteinalis despite the absence of a corpus luteum and suppressed serum follicle stimulating concentrations in a triplet pregnancy.  Hum Reprod. 2000;  15(5) 1043-1045
  • 61 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. 1998;  13(8) 2082-2087
  • 62 Rizk B. Symposium: Update on prediction and management of OHSS. Genetics of ovarian hyperstimulation syndrome.  Reprod Biomed Online. 2009;  19(1) 14-27
  • 63 Delbaere A, Smits G, Olatunbosun O, Pierson R, Vassart G, Costagliola S. New insights into the pathophysiology of ovarian hyperstimulation syndrome. What makes the difference between spontaneous and iatrogenic syndrome?.  Hum Reprod. 2004;  19(3) 486-489

Einat ZiviM.D. 

Department of Obstetrics and Gynecology, Hadassah University Hospital

Jerusalem, Israel

Email: zivi_e@hotmail.com

    >