Empty follicle syndrome: Successful treatment in a recurrent case and review of the literature

Human Reproduction

Volumn 27, Issue 5, 2012, Pages 1357-1367

  Beck Fruchter, R ^a   Weiss, A ^a   Lavee, M ^a,b   Geslevich, Y ^a   Shalev, E ^a,b  

^a HAEMEK MEDICAL CENTER   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Empty follicle syndrome; Follicle development; GnRH agonist; In vitro fertilization; Oocyte maturation failure

Indexed keywords

CHORIONIC GONADOTROPIN; CLOMIFENE CITRATE; ENOXAPARIN; ESTROFEM; FOLIC ACID; GONADORELIN AGONIST; GONADOTROPIN; PROGESTERONE; RECOMBINANT CHORIONIC GONADOTROPIN; TRIPTORELIN;

ADULT; ARTICLE; ARTIFICIAL INSEMINATION; ASTHENOSPERMIA; CASE REPORT; CELL MATURATION; CONCEPTION; CRYOPRESERVATION; EMPTY FOLLICLE SYNDROME; FEMALE; HUMAN; INCIDENCE; INFERTILITY; INTRACYTOPLASMIC SPERM INJECTION; MALE; OLIGOASTHENOZOOSPERMIA; OOCYTE; OVULATION; PHYSICAL EXAMINATION; PREGNANCY; RECURRENT DISEASE; VARICOCELE;

EID: 84860210324     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/des037     Document Type: Article

References (78)

1. Aktas M, Beckers NG, van Inzen WG, Verhoeff A, de Jong D. Oocytes in the empty follicle: a controversial syndrome. Fertil Steril 2005; 84: 1643-1648. (Pubitemid 41785657)
2. Asch RH, Li HP, Yovich JL, Katayama KP, Balmaceda JP, Rojas FJ, Stone SC. Failed oocyte retrieval after lack of human chorionic gonadotropin administration in assisted reproductive technology. Fertil Steril 1992; 58: 361-365.
3. Ashkenazi J, Feldberg D, Shelef M, Dicker D, Goldman JA. Empty follicle syndrome: an entity in the etiology of infertility of unknown origin, or a phenomenon associated with purified follicle-stimulating hormone therapy? Fertil Steril 1987;48: 152-154. (Pubitemid 17093270)
4. Awadalla SG, Friedman CI, Kim MH. Empty follicle syndrome. Fertil Steril 1987;47: 1040-1042.
5. Awonuga A, Govindbhai J, Zierke S, Schnauffer K. Continuing the debate on empty follicle syndrome: can it be associated with normal bioavailability of beta-human chorionic gonadotrophin on the day of oocyte recovery? Hum Reprod 1998;13: 1281-1284. (Pubitemid 28279183)
6. Baum M, Machtinger R, Yerushalmi GM, Maman E, Seidman DS, Dor J, Hourvitz A. Recurrence of empty follicle syndrome with stimulated IVF cycles. Gynecol Endocrinol 2011, Nov 18. [Epub ahead of print].
7. Ben-Shlomo I, Schiff E, Levran D, Ben-Rafael Z, Mashiach S, Dor J. Failure of oocyte retrieval during in vitro fertilization: a sporadic event rather than a syndrome. Fertil Steril 1991;55: 324-327.
8. Bustillo M. Unsuccessful oocyte retrieval: technical artefact or genuine 'empty follicle syndrome'? Reprod Biomed Online 2004;8: 59-67. (Pubitemid 38100690)
9. Byskov AG, Yding Andersen C, Hossaini A, Guoliang X. Cumulus cells of oocyte-cumulus complexes secrete a meiosis-activating substance when stimulated with FSH. Mol Reprod Dev 1997;46: 296-305. (Pubitemid 27098583)
10. Castillo JC, Garcia-Velasco J, Humaidan P. Empty follicle syndrome after GnRHa triggering versus hCG triggering in COS. J Assist Reprod Genet 2012 Jan 12. [Epub ahead of print].
11. Coskun S, Madan S, Bukhari I, Al-Hassan S, Al-Rejjal R, Awartani K. Poor prognosis in cycles following 'genuine' empty follicle syndrome. Eur J Obstet Gynecol Reprod Biol 2010;150: 157-159.
12. Coulam CB, Bustillo M, Schulman JD. Empty follicle syndrome. Fertil Steril 1986;46: 1153-1155. (Pubitemid 17215844)
13. D'Alessandris C, Canipari R, Di Giacomo M, Epifano O, Camaioni A, Siracusa G, Salustri A. Control of mouse cumulus cell-oocyte complex integrity before and after ovulation: plasminogen activator synthesis and matrix degradation. Endocrinology 2001;142: 3033-3040. (Pubitemid 32575541)
14. Dell'Aquila ME, Caillaud M, Maritato F, Martoriati A, Gëard N, Aiudi G, Minoia P, Goudet G. Cumulus expansion, nuclear maturation and connexin 43, cyclooxygenase-2 and FSH receptor mRNA expression in equine cumulus-oocyte complexes cultured in vitro in the presence of FSH and precursors for hyaluronic acid synthesis. Reprod Biol Endocrinol 2004;2: 44.
15. Desai N, Austin C, AbdelHafez F, Goldfarb J, Falcone T. Evidence of 'genuine empty follicles' in follicular aspirate: a case report. Hum Reprod 2009;24: 1171-1175.
16. Driscoll GL, Tyler JP, Knight DC, Cooke S, Kime L, Clark L, Bernstein J. Failure to collect oocytes in assisted reproductive technology: a retrospective. Hum Reprod 1998;13: 84-87. (Pubitemid 28075278)
17. Driscoll GL, Tyler JP, Hangan JT, Fisher PR, Birdsall MA, Knight DC. A prospective, randomized, controlled, double-blind, double-dummy comparison of recombinant and urinary hCG for inducing oocyte maturation and follicular luteinization in ovarian stimulation. Hum Reprod 2000;15: 1305-1310. (Pubitemid 30335955)
18. Duru NK, Cincik M, Dede M, Hasimi A, Baser I. Retrieval of zona-free immature oocytes in a woman with recurrent empty follicle syndrome: a case report. J Reprod Med 2007;52: 858-863.
19. Edwards RG, Steptoe PC. Induction of follicular growth, ovulation and luteinization in the human ovary. J Reprod Fertil Suppl 1975;22: 121-163.
20. Esposito MA, Patrizio P. Partial follicular aspiration for salvaging an IVF cycle after improper hCG administration. A case report. J Reprod Med 2000;45: 511-514. (Pubitemid 30432267)
21. Evbuomwan IO, Fenwick JD, Shiels R, Herbert M, Murdoch AP. Severe ovarian hyperstimulation syndrome following salvage of empty follicle syndrome. Hum Reprod 1999;14: 1707-1709. (Pubitemid 29358681)
22. Fauser BC, de Jong D, Olivennes F, Wramsby H, Tay C, Itskovitz-Eldor J, van Hooren HG. Endocrine profiles after triggering of final oocyte maturation with GnRH agonist after cotreatment with the GnRH antagonist ganirelix during ovarian hyperstimulation for in vitro fertilization. J Clin Endocrinol Metab 2002;87: 709-715. (Pubitemid 34158241)
23. Fiszbain G, Acosta A, Brugo-Olmedo S, Ruhman C, Papier S, Chillik C. Empty follicle syndrome: etiology and management. J Assist Reprod Genet 1997;14(Suppl): 58s.
24. Godard NM, Pukazhenthi BS, Wildt DE, Comizzoli P. Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro of denuded oocytes in the cat model. Fertil Steril 2009;91(Suppl.5): 2051-2060.
25. Gonen Y, Balakier H, PowellW, Casper RF. Use of gonadotropin-releasing hormone agonist to trigger follicular maturation for in vitro fertilization. J Clin Endocrinol Metab 1990;71: 918-922.
26. Greb R, van Uem JF, Bauer T. Empty follicle syndrome in perimenopausal patients. Fertil Steril 1993;59: 1141-1142. (Pubitemid 23139696)
27. Griesinger G, Diedrich K, Devroey P, Kolibianakis EM. GnRH agonist for triggering final oocyte maturation in the GnRH antagonist ovarian hyperstimulation protocol: a systematic review and meta-analysis. Hum Reprod Update 2006;12: 159-168. (Pubitemid 43239269)
28. Harrison RF, Fawzy M. Empty follicle syndrome (letter). Hum Reprod 1996; 11: 459-460.
29. Hassan HA, Saleh HA, Khalil O, Baghdady I, Ismaiel I. Double oocyte aspiration may be a solution for empty follicle syndrome: case report. Fertil Steril 1998;69: 138-139. (Pubitemid 28073007)
30. Hirshfeld-Cytron J, Kim HH. Empty follicle syndrome in the setting of dramatic weight loss after bariatric surgery: case report and review of available literature. Fertil Steril 2008;90: 1199.e21-3.
31. Hoff JD, Quigley ME, Yen SS. Hormonal dynamics at midcycle: a reevaluation. J Clin Endocrinol Metab 1983;57: 792-796. (Pubitemid 13013538)
32. Honnma H, Hashiba Y, Asada Y, Endo T. Failure of triggering oocyte maturation with a GnRH agonist in polycystic ovary syndrome: two case reports. Eur J Obstet Gynecol Reprod Biol 2011;157: 239-240.
33. Hourvitz A, Maman E, Brengauz M, Machtinger R, Dor J. In vitro maturation for patients with repeated in vitro fertilization failure due to 'oocyte maturation abnormalities'. Fertil Steril 2010;94: 496-501.
34. Humaidan P, Kol S, Papanikolaou E. on behalf of the 'The Copenhagen GnRH Agonist Triggering Workshop Group'. GnRH agonist for triggering of final oocyte maturation: time for a change of practicë Hum Reprod Update 2011;17: 510-524.
35. Inan MS, Al-Hassan S, Ozand P, Coskun S. Transcriptional profiling of granulosa cells from a patient with recurrent empty follicle syndrome. Reprod Biomed Online 2006;13: 481-491. (Pubitemid 44548782)
36. Isk AZ, Vicdan K. Borderline form of empty follicle syndrome: is it really an entity? Eur J Obstet Gynecol Reprod Biol2000 88 213-215. (Pubitemid 30004065)
37. Khalaf Y, Braude P. (letter). Hum Reprod 1997;12: 1601.
38. Khalaf Y, Anderson H, Taylor A, Braude P. Two rare events in one patient undergoing assisted conception: empty follicle syndrome and ovarian hyperstimulation with the sole administration of a gonadotropinreleasing hormone agonist. Fertil Steril 2000;73: 171-172. (Pubitemid 30018044)
39. Kourtis A, Rousso D, Panidis D. The empty follicle syndrome. J Endocrinol Invest 2004;27: 187-191. (Pubitemid 38514814)
40. Krishna D, Rajashekar L, Patil M. Empty follicle syndrome-Still an enigma. J Hum Reprod Sci 2008;1: 86-89.
41. Lamb JD, Shen S, McCulloch C, Jalalian L, Cedars MI, Rosen MP. Follicle-stimulating hormone administered at the time of human chorionic gonadotropin trigger improves oocyte developmental competence in in vitro fertilization cycles: a randomized, double-blind, placebo-controlled trial. Fertil Steril 2011;95: 1655-1660.
42. La Sala GB, Ghirardini G, Cantarelli M, Dotti C, Cavalieri S, Torelli MG. Recurrent empty follicle syndrome. Hum Reprod 1991;6: 651-652.
43. Lok F, Pritchard J, Lashen H. Successful treatment of empty follicle syndrome by triggering endogenous LH surge using GnRH agonist in an antagonist down-regulated IVF cycle. Hum Reprod 2003; 18: 2079-2081. (Pubitemid 37265069)
44. Lorusso F, Depalo R, Tsadilas S, Caradonna F, Di Gilio A, Capotorto MT, Vacca M, Nappi L, Selvaggi L. Is the occurrence of the empty follicle syndrome a predictor that a subsequent stimulated cycle will be an unfavourable onë Reprod Biomed Online 2005;10: 571-574. (Pubitemid 40645533)
45. Meniru GI, Craft IL. Evidence from a salvaged treatment cycle supports an aetiology for the empty follicle syndrome that is related to terminal follicular developmental events. Hum Reprod 1997;12: 2385-2387. (Pubitemid 27522193)
46. Mesen TB, Yu B, Richter KS, Widra E, Decherney AH, Segars JH. The prevalence of genuine empty follicle syndrome. Fertil Steril 2011; 96: 1375-1377.
47. Milki AA, Mooney SB. Failure to recover oocytes during IVF: case reports and suggestions for management. J Assist Reprod Genet 2001; 18: 352-353. (Pubitemid 32673342)
48. Ndukwe G, Thornton S, Fishel S, Dowell K, al-Hassan S, Hunter A. Predicting empty follicle syndrome. Fertil Steril 1996;66: 845-847. (Pubitemid 26357596)
49. Ndukwe G, Thornton S, Fishel S, Dowell K, Aloum M, Green S. 'Curing' empty follicle syndrome. Hum Reprod 1997;12: 21-23.
50. Ng SP, Jamil MA, Nurshaireen A, Zainul MR. The empty follicle syndrome. Med J Malaysia 2006;61: 499-500.
51. Nikolettos N, Asimakopoulos B, Simopoulou M, Al-Hasani S. A borderline form of empty follicle syndrome. Case report. Clin Exp Obstet Gynecol 2004;31: 79-80. (Pubitemid 38200425)
52. Onalan G, Pabuciu R, Onalan R, Ceylaner S, Selam B. Empty follicle syndrome in two sisters with three cycles: case report. Hum Reprod 2003;18: 1864-1867. (Pubitemid 37107559)
53. Papier S, Lipowicz R, De Vincentiis S, Nodar F, Olmedo SB, Acosta A. Pregnancy obtained by the transfer of frozen-thawed embryos originating from a rescued empty follicle syndrome cycle. Fertil Steril 2000;74: 603-604.
54. Peñarrubia J, Balasch J, Faregues F, Creus M, ciico S, Vanrell JA. Recurrent empty follicle syndrome successfully treated with recombinant human chorionic gonadotrophin. Hum Reprod 1999; 14: 1703-1706. (Pubitemid 29358680)
55. Phocas I, Mantzavinos T, Rizos D, Dimitriadou F, Arvaniti K, Zourlas PA. Hormone levels of follicular fluids with and without oocytes in patients who received gonadotropin-releasing hormone analogues and gonadotropins in an in vitro fertilization program. J Assist Reprod Genet 1992;9: 233-237.
56. Qublan H, Tahat Y, Al-Masri A. Primary ovarian pregnancy after the empty follicle syndrome: a case report. J Obstet Gynaecol Res 2008; 34: 422-424. (Pubitemid 351832341)
57. Quintans CJ, Donaldson MJ, Blanco LA, Pasqualini RS. Empty follicle syndrome due to human errors: its occurrence in an in-vitro fertilization programme. Hum Reprod 1998;13: 2703-2705. (Pubitemid 28482713)
58. Reichman DE, Hornstein MD, Jackson KV, Racowsky C. Empty follicle syndrome-does repeat administration of hCG really work? Fertil Steril 2010;94: 375-377.
59. Rudak E, Dor J, Kimchi M, Goldman B, Levran D, Mashiach S. Anomalies of human oocytes from infertile women undergoing treatment by in vitro fertilization. Fertil Steril 1990;54: 292-296. (Pubitemid 20256239)
60. Seibel MM, Smith DM, Levesque L, Borten M, Taymor ML. The temporal relationship between the luteinizing hormone surge and human oocyte maturation. Am J Obstet Gynecol 1982;142: 568-572. (Pubitemid 12192143)
61. Shalev E, Geslevich Y, Ben-Ami M. Induction of pre-ovulatory luteinizing hormone surge by gonadotrophin-releasing hormone agonist for women at risk for developing the ovarian hyperstimulation syndrome. Hum Reprod 1994;9: 417-419. (Pubitemid 24096392)
62. Snaifer E, Hugues JN, Poncelet C, Sifer C, Pasquier M, Cedrin-Durnerin I. 'Empty follicle syndrome' after human error: pregnancy obtained after repeated oocyte retrieval in a gonadotropin-releasing hormone antagonist cycle. Fertil Steril 2008;90: 850.e13-5.
63. Stefunidis K, Grammatis M, Pappas K, Haidopoulos D, Chronopoulos K, Pantos K, Diakomanolis E. Empty follicle syndrome associated with ovarian torsion in an in vitro fertilization program. J Soc Laparoendoscopic Surg 2002;6: 215-216.
64. Stevenson TL, Lashen H.Empty follicle syndrome: the reality of a controversial syndrome, a systematic review. Fertil Steril 2008;90: 691-698.
65. Strickland S, Beers WH. Studies on the role of plasminogen activator in ovulation. In vitro response of granulosa cells to gonadotropins, cyclic nucleotides, and prostaglandins. J Biol Chem 1976;251: 5694-5702.
66. Sun QY, Miao YL, Schatten H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 2009; 8: 2741-2747.
67. Traina V, Boyer P, Piccinni O, Costantino G, D'Amato G, D'Addario V, Cho YS. Failed oocyte retrieval in in-vitro fertilization with documented positive serum beta-human chorionic gonadotrophin (HCG) concentration on day HCG+1. Hum Reprod 1993;8: 1854-1855. (Pubitemid 23337146)
68. Tsuiki A, Rose BI, Hung TT. Steroid profiles of follicular fluids from a patient with the empty follicle syndrome. Fertil Steril 1988;49: 104-107. (Pubitemid 18033900)
69. Ubaldi F, Nagy Z, Janssenwillen C, Smitz J, Van Steirteghem A, Devroey P. Ovulation by repeated human chorionic gonadotrophin in 'empty follicle syndrome' yields a twin clinical pregnancy. Hum Reprod 1997; 12: 454-456. (Pubitemid 27156435)
70. Uygur D, Alkan RN, Batuoglu S. Recurrent empty follicle syndrome. J Assist Reprod Genet 2003;20: 390-392. (Pubitemid 37158961)
71. van Heusden AM, van Santbrink EJ, Schipper I, de Jong D. The empty follicle syndrome is dead! Fertil Steril 2008;89: 746.
72. Vujisic S, Stipoljev F, Bauman R, Dmitrovic R, Jezek D. Pericentric inversion of chromosome 2 in a patient with the empty follicle syndrome: case report. Hum Reprod 2005;20: 2552-2555. (Pubitemid 41222507)
73. Vutyavanich T, Piromlertamorn W, Ellis J. Immature oocytes in 'apparent empty follicle syndrome': a case report. Case Report Med 2010; 2010: 367505.
74. Yariz KO, Walsh T, Uzak A, Spiliopoulos M, Duman D, Onalan G, King MC, Tekin M. Inherited mutation of the luteinizing hormone/choriogonadotropin receptor (LHCGR) in empty follicle syndrome. Fertil Steril 2011;96: e125-e130.
75. Yu B, Ruman J, Christman G. The role of peripheral gonadotropinreleasing hormone receptors in female reproduction. Fertil Steril 2011; 95: 465-473.
76. Zegers-Hochschild F, Fernadez E, Mackenna A, Fabres C, Altieri E, Lopez T. The empty follicle syndrome: a pharmaceutical industry syndrome. Hum Reprod 1995;10: 2262-2265.
77. Zelinski-Wooten MB, Hutchison JS, Chandrasekher YA, Wolf DP, Stouffer RL. Administration of human luteinizing hormone (hLH) to macaques after follicular development: further titration of LH surge requirements for ovulatory changes in primate follicles. J Clin Endocrinol Metab 1992;75: 502-507.
78. Zreik TG, Garcia-Velasco JA, Vergara TM, Arici A, Olive D, Jones EF. Empty follicle syndrome: evidence for recurrence. Hum Reprod 2000; 15: 999-1000.