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Open Access 01-12-2009 | Review

Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics

Authors: Alberto Revelli, Luisa Delle Piane, Simona Casano, Emanuela Molinari, Marco Massobrio, Paolo Rinaudo

Published in: Reproductive Biology and Endocrinology | Issue 1/2009

Abstract

The assessment of oocyte quality in human in vitro fertilization (IVF) is getting increasing attention from embryologists. Oocyte selection and the identification of the best oocytes, in fact, would help to limit embryo overproduction and to improve the results of oocyte cryostorage programs. Follicular fluid (FF) is easily available during oocyte pick-up and theorically represents an optimal source on non-invasive biochemical predictors of oocyte quality. Unfortunately, however, the studies aiming to find a good molecular predictor of oocyte quality in FF were not able to identify substances that could be used as reliable markers of oocyte competence to fertilization, embryo development and pregnancy. In the last years, a well definite trend toward passing from the research of single molecular markers to more complex techniques that study all metabolites of FF has been observed. The metabolomic approach is a powerful tool to study biochemical predictors of oocyte quality in FF, but its application in this area is still at the beginning. This review provides an overview of the current knowledge about the biochemical predictors of oocyte quality in FF, describing both the results coming from studies on single biochemical markers and those deriving from the most recent studies of metabolomics

Balaban B, Urman B: Effect of oocyte morphology on embryo development and implantation. Reprod Biomed Online. 2006, 12: 608-615.PubMedCrossRef

Patrizio P, Fragouli E, Bianchi V, Borini A, Wells D: Molecular methods for selection of the ideal oocyte. Reprod Biomed Online. 2007, 15: 346-353.PubMedCrossRef

Dawson A, Griesinger G, Diedrich K: Screening oocytes by polar body biopsy. Reprod Biomed Online. 2006, 13: 104-109.PubMedCrossRef

Fortune JE: Ovarian follicular growth and development in mammals. Biol Reprod. 1994, 50: 225-232. 10.1095/biolreprod50.2.225.PubMedCrossRef

Leroy JL, Vanholder T, Delanghe JR, Opsomer G, Van Soom A, Bols PE, Dewulf J, de Kruif A: Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology. 2004, 62: 1131-1143. 10.1016/j.theriogenology.2003.12.017.PubMedCrossRef

Suchanek E, Simunic V, Macas E, Kopjar B, Grizelj V: Prostaglandin F2 alpha, progesterone and estradiol concentrations in human follicular fluid and their relation to success of in vitro fertilization. Eur J Obstet Gynecol Reprod Biol. 1988, 28: 331-339. 10.1016/0028-2243(88)90019-6.PubMedCrossRef

Ellsworth LR, Balmaceda JP, Schenken RS, Silverman AY, Prihoda TJ, Asch RH: Human chorionic gonadotropin and steroid concentrations in human follicular fluid in relation to follicle size and oocyte maturity in stimulated ovarian cycles. Acta Eur Fertil. 1984, 15: 343-346.PubMed

Cha KY, Barnes RB, Marrs RP, Lobo RA: Correlation of the bioactivity of luteinizing hormone in follicular fluid with oocyte maturity in the spontaneous cycle. Fertil Steril. 1986, 45: 338-341.PubMed

Enien WM, Chantler E, Seif MW, Elstein M: Human ovarian granulosa cells and follicular fluid indices: the relationship to oocyte maturity and fertilization in vitro. Hum Reprod. 1998, 13: 1303-1306. 10.1093/humrep/13.5.1303.PubMedCrossRef

10.

Mendoza C, Ruiz-Requena E, Ortega E, Cremades N, Martinez F, Bernabeu R, Greco E, Tesarik J: Follicular fluid markers of oocyte developmental potential. Hum Reprod. 2002, 17: 1017-1022. 10.1093/humrep/17.4.1017.PubMedCrossRef

11.

Lanzone A, Fortini A, Fulghesu AM, Soranna L, Caruso A, Mancuso S: Growth hormone enhances estradiol production follicle-stimulating hormone-induced in the early stage of the follicular maturation. Fertil Steril. 1996, 66: 948-953.PubMed

12.

Jia X, Kalmijn J, Hsueh AJ: Growth hormone enhances follicle-stimulating hormone-induced differentiation of cultured rat granulosa cells. Endocrinology. 1986, 118: 1401-1409.PubMedCrossRef

13.

Izadyar F, Zhao J, Van Tol HT, Colenbrander B, Bevers MM: Messenger RNA expression and protein localization of growth ormone in bovine ovarian tissue and in cumulus oocyte complexes (COCs) during vitro maturation. Mol Reprod Dev. 1999, 53: 398-406. 10.1002/(SICI)1098-2795(199908)53:4<398::AID-MRD5>3.0.CO;2-I.PubMedCrossRef

14.

Tarlatzis BC, Pazaitou K, Bili H, Bontis J, Papadimas J, Lagos S, Spanos E, Mantalenakis S: Growth hormone, oestradiol, progesterone and testosterone concentrations in follicular fluid after ovarian stimulation with various regimes for assisted reproduction. Hum Reprod. 1993, 8: 1612-1616.PubMed

15.

Lindner C, Lichtenberg V, Westhof G, Braendle W, Bettendorf G: Endocrine parameters of human follicular fluid and fertilization capacity of oocytes. Horm Metab Res. 1988, 20: 243-246. 10.1055/s-2007-1010803.PubMedCrossRef

16.

Laufer N, Botero-Ruiz W, DeCherney AH, Haseltine F, Polan ML, Behrman HR: Gonadotropin and prolactin levels in follicular fluid of human ova successfully fertilized in vitro. J Clin Endocrinol Metab. 1984, 58: 430-434.PubMedCrossRef

17.

Tarlatzis BC, Laufer N, DeCherney AH, Polan ML, Haseltine FP, Behrman HR: Adenosine 3',5'-monophosphate levels in human follicular fluid: relationship to oocyte maturation and achievement of pregnancy after in vitro fertilization. J Clin Endocrinol Metab. 1985, 60: 1111-1115.PubMedCrossRef

18.

Oda T, Yoshimura Y, Izumi Y, Yoshimura S, Hara T, Takehara Y, Nakamura Y, Ohno T: The effect of the follicular fluid adenosine 3',5'-monophosphate degradation rate on successful fertilization and cleavage of human oocytes. J Clin Endocrinol Metab. 1990, 71: 116-121.PubMedCrossRef

19.

Lee MS, Ben-Rafael Z, Meloni F, Mastroianni L, Flickinger GL: Relationship of human oocyte maturity, fertilization, and cleavage to follicular fluid prolactin and steroids. J In Vitro Fert Embryo Transf. 1987, 4 (3): 168-172. 10.1007/BF01555465.PubMedCrossRef

20.

Messinis IE, Templeton AA: Relationship between intrafollicular levels of prolactin and sex steroids and in-vitro fertilization of human oocytes. Hum Reprod. 1987, 2: 607-609.PubMed

21.

Reinthaller A, Deutinger J, Riss P, Müller-Tyl E, Fischl F, Bieglmayer C, Janisch H: Relationship between the steroid and prolactin concentration in follicular fluid and the maturation and fertilization of human oocytes. J In Vitro Fertil Embryo Transfer. 1987, 4: 228-231. 10.1007/BF01533761.CrossRef

22.

Subramanian MG, Sacco AG, Moghissi KS, Magyar DM, Hayes MF, Lawson DM, Gala RR: Human follicular fluid: prolactin is biologically active and ovum fertilization correlates with estradiol concentration. J In Vitro Fertil Embryo Transfer. 1988, 5: 129-133. 10.1007/BF01131174.CrossRef

23.

Rosenbusch B, Djalali M, Sterzik K: Is there any correlation between follicular fluid hormone concentrations, fertilizability, and cytogenetic analysis of human oocytes recovered for in vitro fertilization?. Fertil Steril. 1992, 57: 1358-1360.PubMed

24.

Tesarik J, Mendoza C: Direct non-genomic effects of follicular steroids on maturing human oocytes: oestrogen versus androgen antagonism. Hum Reprod Update. 1997, 3: 95-100. 10.1093/humupd/3.2.95.PubMedCrossRef

25.

Botero-Ruiz W, Laufer N, DeCherney AH, Polan ML, Haseltine FP, Behrman HR: The relationship between follicular fluid steroid concentration and successful fertilization of human oocytes in vitro. Fertil Steril. 1984, 41: 820-826.PubMed

26.

Kreiner D, Liu HC, Itskovitz J, Veeck L, Rosenwaks Z: Follicular fluid estradiol and progesterone are markers of preovulatory oocyte quality. Fertil Steril. 1987, 48: 991-994.PubMed

27.

Reinthaller A, Deutinger J, Bieglmayer C, Riss P, Müller-Tyl E, Fischl F, Janisch H: Hormonal parameters in follicular fluid and the fertilization rate of in vitro cultured oocytes. Arch Gynecol. 1987, 240: 207-210. 10.1007/BF02134069.PubMedCrossRef

28.

Artini PG, Battaglia C, D'Ambrogio G, Barreca A, Droghini F, Volpe A, Genazzani AR: Relationship between human oocyte maturity, fertilization and follicular fluid growth factors. Hum Reprod. 1994, 9: 902-906.PubMed

29.

Teissier MP, Chable H, Paulhac S, Aubard Y: Comparison of follicle steroidogenesis from normal and polycystic ovaries in women undergoing IVF: relationship between steroid concentrations, follicle size, oocyte quality and fecundability. Hum Reprod. 2000, 15: 2471-2477. 10.1093/humrep/15.12.2471.PubMedCrossRef

30.

Berger MA, Laufer N, Lewin A, Navot D, Rabinowitz R, Eisenberg S, Margalioth EJ, Schenker JG: Cholesterol and steroid levels in human follicular fluids of human menopausal gonadotropin-induced cycles for in vitro fertilization. J In Vitro Fertil Embryo Transfer. 1987, 4: 30-33. 10.1007/BF01555432.CrossRef

31.

Costa LO, Mendes MC, Ferriani RA, Moura MD, Reis RM, Silva de Sá MF: Estradiol and testosterone concentrations in follicular fluid as criteria to discriminate between mature and immature oocytes. Braz J Med Biol Res. 2004, 37: 1747-1755.PubMedCrossRef

32.

Basuray R, Rawlins RG, Radwanska E, Henig I, Sachdeva S, Tummon I, Binor Z, Dmowski WP: High progesterone/estradiol ratio in follicular fluid at oocyte aspiration for in vitro fertilization as a predictor of possible pregnancy. Fertil Steril. 1988, 49: 1007-1011.PubMed

33.

Kobayashi T, Oda T, Yoshimura Y, Takehara Y, Natori M, Nozawa S: Androstenedione and progesterone concentrations in preovulatory follicular fluid correlate with successful fertilization and cleavage of human oocytes in vitro. Fertil Steril. 1991, 56: 301-305.PubMed

34.

Vanluchene E, Hinting A, Dhont M, De Sutter P, Van Maele G, Vandekerckhove D: Follicular fluid steroid levels in relation to oocyte maturity and in vitro fertilization. J Steroid Biochem Mol Biol. 1991, 38: 83-87. 10.1016/0960-0760(91)90405-T.PubMedCrossRef

35.

Enien WM, el Sahwy S, Harris CP, Seif MW, Elstein M: Human chorionic gonadotrophin and steroid concentrations in follicular fluid: the relationship to oocyte maturity and fertilization rates in stimulated and natural in-vitro fertilization c. Hum Reprod. 1995, 10: 2840-2844.PubMed

36.

Ben-Rafael Z, Meloni F, Strauss JF, Blasco L, Mastroianni L, Flickinger GL: Relationships between polypronuclear fertilization and follicular fluid hormones in gonadotropin-treated women. Fertil Steril. 1987, 47: 284-288.PubMed

37.

Uehara S, Naganuma T, Tsuiki A, Kyono K, Hoshiai H, Suzuki M: Relationship between follicular fluid steroid concentrations and in vitro fertilization. Obstet Gynecol. 1985, 66: 19-23.PubMed

38.

Andersen CY: Characteristics of human follicular fluid associated with successful conception after in vitro fertilization. J Clin Endocrinol Metab. 1993, 77: 1227-1234. 10.1210/jc.77.5.1227.PubMed

39.

Xia P, Younglai EV: Relationship between steroid concentrations in ovarian follicular fluid and oocyte morphology in patients undergoing intracytoplasmic sperm injection (ICSI) treatment. J Reprod Fertil. 2000, 118: 229-233. 10.1530/reprod/118.2.229.PubMedCrossRef

40.

De Placido G, Alviggi C, Perino A, Strina I, Lisi F, Fasolino A, De Palo R, Ranieri A, Colacurci N, Mollo Al: Recombinant human LH supplementation versus recombinant human FSH (rFSH) step-up protocol during controlled ovarian stimulation in normogonadotrophic women with initial inadequate ovarian response to rFSH. A multicentre, prospective, randomized controlled trial. Hum Reprod. 2005, 20: 390-396. 10.1093/humrep/deh625.PubMedCrossRef

41.

Lisi F, Rinaldi L, Fishel S, Lisi R, Pepe G, Picconeri MG, Campbell A, Rowe P: Use of recombinant LH in a group of unselected IVF patients. Reprod Biomed Online. 2002, 5: 104-108.PubMedCrossRef

42.

Keay SD, Harlow CR, Wood PJ, Jenkins JM, Cahill DJ: Higher cortisol:cortisone ratios in the preovulatory follicle of completely unstimulated IVF cycles indicate oocytes with increased pregnancy potential. Hum Reprod. 2002, 17: 2410-2414. 10.1093/humrep/17.9.2410.PubMedCrossRef

43.

Lewicka S, von Hagens C, Hettinger U, Grunwald K, Vecsei P, Runnebaum B, Rabe T: Chortisol and cortisone in human follicular fluid and serum and the outcome of IVF treatment. Hum Reprod. 2003, 18: 1613-1617. 10.1093/humrep/deg352.PubMedCrossRef

44.

Michael AE, Collins TD, Norgate DP, Gregory L, Wood PJ, Cooke BA: Relationship between ovarian cortisol:cortisone ratios and the clinical outcome of in vitro fertilization and embryo transfer (IVF-ET). Clin Endocrinol. 1999, 51: 535-540. 10.1046/j.1365-2265.1999.00892.x.CrossRef

45.

Revelli A, Dolfin E, Gennarelli G, Lantieri T, Massobrio M, Holte JG, Tur-Kaspa I: Low-dose acetylsalicylic acid plus prednisolone as an adjuvant treatment in IVF: a prospective, randomized study. Fertil Steril. 2008, 5: 1685-1691. 10.1016/j.fertnstert.2007.08.037.CrossRef

46.

Lau CP, Ledger WL, Groome NP, Barlow DH, Muttukrishna S: Dimeric inhibins and activin A in human follicular fluid and oocyte-cumulus culture medium. Hum Reprod. 1999, 14: 2525-2530. 10.1093/humrep/14.10.2525.PubMedCrossRef

47.

Wen X, Tozer AJ, Butler SA, Bell CM, Docherty SM, Iles RK: Follicular fluid levels of inhibin A, inhibin B, and activin A levels reflect changes in follicle size but are not independent markers of the oocyte's ability to fertilize. Fertil Steril. 2006, 85: 1723-1729. 10.1016/j.fertnstert.2005.11.058.PubMedCrossRef

48.

Fujiwara T, Lambert-Messerlian G, Sidis Y, Leykin L, Isaacson K, Toth T, Schneyer A: Analysis of follicular fluid hormone concentrations and granulosa cell mRNA levels for the inhibin-activin-follistatin system: relation to oocyte and embryo characteristics. Fertil Steril. 2000, 74: 348-355. 10.1016/S0015-0282(00)00652-X.PubMedCrossRef

49.

Akande AV, Asselin J, Keay SD, Cahill DJ, Muttukrishna S, Groome NP, Wardle PG: Inhibin A, inhibin B and activin A in follicular fluid of infertile women with tubal damage, unexplained infertility and endometriosis. Am J Reprod Immunol. 2000, 43: 61-69. 10.1111/j.8755-8920.2000.430201.x.PubMedCrossRef

50.

Fried G, Remaeus K, Harlin J, Krog E, Csemiczky G, Aanesen A, Tally M: Inhibin B predicts oocyte number and the ratio IGF-I/IGFBP-1 may indicate oocyte quality during ovarian hyperstimulation for in vitro fertilization. J Assist Reprod Genet. 2003, 20: 167-176. 10.1023/A:1023656225053.PubMedCentralPubMedCrossRef

51.

Chang CL, Wang TH, Horng SG, Wu HM, Wang HS, Soong YK: The concentration of inhibin B in follicular fluid: relation to oocyte maturation and embryo development. Hum Reprod. 2002, 17: 1724-1728. 10.1093/humrep/17.7.1724.PubMedCrossRef

52.

Ocal P, Aydin S, Cepni I, Idil S, Idil M, Uzun H, Benian A: Follicular fluid concentrations of vascular endothelial growth factor, inhibin A and inhibin B in IVF cycles: are they markers for ovarian response and pregnancy outcome?. Eur J Obstet Gynecol Reprod Biol. 2004, 115: 194-199. 10.1016/j.ejogrb.2004.01.034.PubMedCrossRef

53.

Ebner T, Sommergruber M, Moser M, Shebl O, Schreier-Lechner E, Tews G: Basal level of anti-Müllerian hormone is associated with oocyte quality in stimulated cycles. Hum Reprod. 2006, 21: 2022-2026. 10.1093/humrep/del127.PubMedCrossRef

54.

Silberstein T, MacLaughlin DT, Shai I, Trimarchi JR, Lambert-Messerlian G, Seifer DB, Keefe DL, Blazar AS: Müllerian inhibiting substance levels at the time of HCG administration in IVF cycles predict both ovarian reserve and embryo morphology. Hum Reprod. 2006, 21: 159-163. 10.1093/humrep/dei270.PubMedCrossRef

55.

Cupisti S, Dittrich R, Mueller A, Strick R, Stiegler E, Binder H, Beckmann MW, Strissel P: Correlations between anti-müllerian hormone, inhibin B, and activin A in follicular fluid in IVF/ICSI patients for assessing the maturation and developmental potential of oocytes. Eur J Med Res. 2007, 12: 604-608.PubMed

56.

Takahashi C, Fujito A, Kazuka M, Sugiyama R, Ito H, Isaka K: Anti-Müllerian hormone substance from follicular fluid is positively associated with success in oocyte fertilization during in vitro fertilization. Fertil Steril. 2008, 89: 586-591. 10.1016/j.fertnstert.2007.03.080.PubMedCrossRef

57.

Wu YT, Tang L, Cai J, Lu XE, Xu J, Zhu XM, Luo Q, Huang HF: High bone morphogenetic protein-15 level in follicular fluid is associated with high quality oocyte and subsequent embryonic development. Hum Reprod. 2007, 22: 1526-1531. 10.1093/humrep/dem029.PubMedCrossRef

58.

Wang TH, Chang CL, Wu HM, Chiu YM, Chen CK, Wang HS: Insulin-like growth factor-II (IGF-II), IGF-binding protein-3 (IGFBP-3), and IGFBP-4 in follicular fluid are associated with oocyte maturation and embryo development. Fertil Steril. 2006, 86: 1392-1401. 10.1016/j.fertnstert.2006.03.064.PubMedCrossRef

59.

Jimena P, Castilla JA, Peran F, Molina R, Ramirez JP, Acebal M, Vergara F, Herruzo A: Insulin and insulin-like growth factor I in follicular fluid after induction of ovulation in women undergoing in vitro fertilization. J Reprod Fertil. 1992, 96: 641-647.PubMedCrossRef

60.

Oosterhuis GJ, Vermes I, Lambalk CB, Michgelsen HW, Schoemaker J: Insulin-like growth factor (IGF)-I and IGF binding protein-3 concentrations in fluid from human stimulated follicles. Hum Reprod. 1998, 13: 285-289. 10.1093/humrep/13.2.285.PubMedCrossRef

61.

Asimakopoulos B, Abu-Hassan D, Metzen E, Al-Hasani S, Diedrich K, Nikolettos N: The levels of steroid hormones and cytokines in individual follicles are not associated with the fertilization outcome after intracytoplasmic sperm injection. Fertil Steril. 2008, 90: 60-64. 10.1016/j.fertnstert.2007.05.054.PubMedCrossRef

62.

Inoue Y, Miyamoto S, Fukami T, Shirota K, Yotsumoto F, Kawarabayashi T: Amphiregulin is much more abundantly expressed than transforming growth factor-alpha and epidermal growth factor in human follicular fluid obtained from patients undergoing in vitro fertilization-embryo transfer. Fertil Steril. 2008, 91: 1035-1041. 10.1016/j.fertnstert.2008.01.014.PubMedCrossRef

63.

Wang XF, Xing FQ, Chen SL: Interleukin-1beta expression on ovarian granulosa cells and its clinicalimplication in women undergoing in vitro fertilization. Di Yi Jun Yi Da Xue Xue Bao. 2002, 22: 934-936.PubMed

64.

Mendoza C, Cremades N, Ruiz-Requena E, Martinez F, Ortega E, Bernabeu S, Tesarik J: Relationship between fertilization results after intracytoplasmatic sperm injection, and intrafollicular steroid, pituitary hormone and cytokine concentrations. Hum Reprod. 1999, 93: 863-868.

65.

Barak Y, Amit A, Lessing JB, Paz G, Homonnai ZT, Yogev L: Improved fertilization rate in an in vitro fertilization program by egg yolk-treated sperm. Fertil Steril. 1992, 58: 197-198.PubMed

66.

Geva E, Lessing JB, Lerner-Geva L, Azem F, Yovel I, Ben-Yosef D, Barkai U, Amit A: Interleukin-10 in preovulatory follicular fluid of patients undergoing in-vitro fertilization and embryo transfer. Am J Reprod Immunol. 1997, 37: 187-190.PubMedCrossRef

67.

Cerkiene Z, Eidukaite A, Usoniene A: Follicular fluid levels of interleukin-10 and interferon-gamma do not predict outcome of assisted reproductive technologies. Am J Reprod Immunol. 2008, 59: 118-126.PubMedCrossRef

68.

Lédée N, Lombroso R, Lombardelli L, Selva J, Dubanchet S, Chaouat G, Frankenne F, Foidart JM, Maggi E, Romagnani S, Ville Y, Piccinni MP: Cytokines and chemokines in follicular fluids and potential of the corresponding embryo: the role of granulocyte colony-stimulating factor. Hum Reprod. 2008, 23: 2001-2009. 10.1093/humrep/den192.PubMedCrossRef

69.

Bili H, Tarlatzis BC, Daniilidis M, Fleva A, Bontis J, Tourkantonis A, Mantalenakis S: Cytokines in the human ovary: presence in follicular fluid and correlation with leukotriene B4. J Assist Reprod Genet. 1998, 15: 93-98. 10.1007/BF02766833.PubMedCentralPubMedCrossRef

70.

Van Blerkom J: Epigenetic influences on oocyte developmental competence: perifollicular vascularity and intrafollicular oxygen. J Assist Reprod Genet. 1998, 15: 226-234. 10.1023/A:1022523906655.PubMedCentralPubMedCrossRef

71.

Van Blerkom J: Intrafollicular influences on human oocyte developmental competence: perifollicular vascularity, oocyte metabolism and mitochondrial function. Hum Reprod. 2000, 15 (Suppl 2): 173-188.PubMedCrossRef

72.

Van Blerkom J: Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction. 2004, 128: 269-280. 10.1530/rep.1.00240.PubMedCrossRef

73.

Van Blerkom J, Antczak M, Schrader R: The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum Reprod. 1997, 12: 1047-1055. 10.1093/humrep/12.5.1047.PubMedCrossRef

74.

Blondin P, Coenen K, Sirard MA: The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J Androl. 1997, 18: 454-460.PubMed

75.

Attaran M, Pasqualotto E, Falcone T, Goldberg JM, Miller KF, Agarwal A, Sharma RK: The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med. 2000, 45 (5): 314-320.PubMed

76.

Agarwal A, Saleh RA, Bedaiwy MA: Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003, 79: 829-843. 10.1016/S0015-0282(02)04948-8.PubMedCrossRef

77.

Hu Y, Betzendahl I, Cortvrindt R, Smitz J, Eichenlaub-Ritter U: Effects of low O2 and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture. Hum Reprod. 2001, 16: 737-748. 10.1093/humrep/16.4.737.PubMedCrossRef

78.

Sabatini L, Wilson C, Lower A, Al-Shawaf T, Grudzinskas JG: Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization. Fertil Steril. 1999, 72: 1027-1034. 10.1016/S0015-0282(99)00411-2.PubMedCrossRef

79.

Paszkowski T, Traub AI, Robinson SY, McMaster D: Selenium dependent glutathione peroxidase activity in human follicular fluid. Clin Chim Acta. 1995, 236: 173-180. 10.1016/0009-8981(95)98130-9.PubMedCrossRef

80.

Tamura H, Takasaki A, Miwa I, Taniguchi K, Maekawa R, Asada H, Taketani T, Matsuoka A, Yamagata Y, Shimamura K, Morioka H, Ishikawa H, Reiter RJ, Sugino N: Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res. 2008, 44: 280-287. 10.1111/j.1600-079X.2007.00524.x.PubMedCrossRef

81.

Oyawoye O, Abdel Gadir A, Garner A, Constantinovici N, Perrett C, Hardiman P: Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: relationship to outcome. Hum Reprod. 2003, 18: 2270-2274. 10.1093/humrep/deg450.PubMedCrossRef

82.

Pasqualotto EB, Agarwal A, Sharma RK, Izzo VM, Pinotti JA, Joshi NJ, Rose BI: Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril. 2004, 81: 973-976. 10.1016/j.fertnstert.2003.11.021.PubMedCrossRef

83.

Lee KS, Joo BS, Na YJ, Yoon MS, Choi OH, Kim WW: Relationships between concentrations of tumor necrosis factor-alpha and nitric oxide in follicular fluid and oocyte quality. J Assist Reprod Genet. 2000, 17: 222-228. 10.1023/A:1009495913119.PubMedCentralPubMedCrossRef

84.

Barrionuevo MJ, Schwandt RA, Rao PS, Graham LB, Maisel LP, Yeko TR: Nitric oxide (NO) and interleukin-1beta (IL-1beta) in follicular fluid and their correlation with fertilization and embryo cleavage. Am J Reprod Immunol. 2000, 46: 359-364. 10.1111/j.8755-8920.2000.440607.x.CrossRef

85.

Lee TH, Wu MY, Chen MJ, Chao KH, Ho HN, Yang YS: Nitric oxide is associated with poor embryo quality and pregnancy outcome in in vitro fertilization cycles. Fertil Steril. 2004, 82: 126-131. 10.1016/j.fertnstert.2004.02.097.PubMedCrossRef

86.

Manau D, Balasch J, Jiménez W, Fábregues F, Civico S, Casamitjana R, Creus M, Vanrell JA: Follicular fluid concentrations of adrenomedullin, vascular endothelial growth factor and nitric oxide in IVF cycles: relationship to ovarian response. Hum Reprod. 2000, 15: 1295-1299. 10.1093/humrep/15.6.1295.PubMedCrossRef

87.

Monteleone P, Giovanni Artini P, Simi G, Casarosa E, Cela V, Genazzani AR: Follicular fluid VEGF levels directly correlate with perifollicular blood flow in normoresponder patients undergoing IVF. J Assist Reprod Genet. 2008, 25: 183-186. 10.1007/s10815-008-9218-1.PubMedCentralPubMedCrossRef

88.

Malamitsi-Puchner A, Sarandakou A, Baka SG, Tziotis J, Rizos D, Hassiakos D, Creatsas G: Concentrations of angiogenic factors in follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: association with oocyte maturity and fertilization. Fertil Steril. 2001, 76: 98-101. 10.1016/S0015-0282(01)01854-4.PubMedCrossRef

89.

Barroso G, Barrionuevo M, Rao P, Graham L, Danforth D, Huey S, Abuhamad A, Oehninger S: Vascular endothelial growth factor, nitric oxide, and leptin follicular fluid levels correlate negatively with embryo quality in IVF patients. Fertil Steril. 1999, 72: 1024-1026. 10.1016/S0015-0282(99)00442-2.PubMedCrossRef

90.

Høst E, Mikkelsen AL, Lindenberg S, Smidt-Jensen S: Apoptosis in human cumulus cells in relation to maturation stage and cleavage of the of the corresponding oocyte. Acta Obstet Gynecol Scand. 2000, 79: 936-940. 10.1034/j.1600-0412.2000.079011936.x.PubMed

91.

Mercé LT, Bau S, Barco MJ, Troyano J, Gay R, Sotos F, Villa A: Assessment of the ovarian volume, number and volume of follicles and ovarian vascularity by three-dimensional ultrasonography and power Doppler angiography on the HCG day to predict the outcome in IVF/ICSI cycles. Hum Reprod. 2006, 21: 1218-1226. 10.1093/humrep/dei471.PubMedCrossRef

92.

Naz RK, Zhu X, Menge AC: Expression of tumor necrosis factor-alpha and its receptors type I and type II in human oocytes. Mol Reprod Dev. 1997, 47: 127-133. 10.1002/(SICI)1098-2795(199706)47:2<127::AID-MRD1>3.0.CO;2-O.PubMedCrossRef

93.

Watanabe-Fukunaga R, Brannan CI, Itoh N, Yonehara S, Copeland NG, Jenkins NA, Nagata S: The cDNA structure, expression, and chromosomal assigment of the mouse Fas antigen. J Immunol. 1992, 148: 1274-1279.PubMed

94.

Sarandakou A, Malamitsi-Puchner A, Baka S, Rizos D, Hassiakos D, Creatsas G: Apoptosis and proliferation factors in serum and follicular fluid from women undergoing in vitro fertilization. Fertil Steril. 2003, 79: 634-636. 10.1016/S0015-0282(02)04802-1.PubMedCrossRef

95.

Malamitsi-Puchner A, Sarandakou A, Baka S, Vrachnis N, Kouskouni E, Hassiakos D: Soluble Fas concentrations in the follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: association with oocyte maturity, fertilization, and embryo quality. J Soc Gynecol Invest. 2004, 11: 566-569. 10.1016/j.jsgi.2004.05.009.CrossRef

96.

José de los Santos M, Anderson DJ, Racowsky C, Hill JA: Presence of Fas-Fas ligand system and Bcl-2 gene products in cells and fluids from gonadotropin-stimulated human ovaries. Biol Reprod. 2000, 63: 1811-1816. 10.1095/biolreprod63.6.1811.PubMedCrossRef

97.

Onalan G, Selam B, Onalan R, Ceyhan T, Cincik M, Pabuccu R: Serum and follicular fluid levels of soluble Fas and soluble Fas ligand in IVF cycles. Eur J Obstet Gynecol Reprod Biol. 2006, 125: 85-91. 10.1016/j.ejogrb.2005.08.002.PubMedCrossRef

98.

Nandedkar TD, Shahid JK, Mehta R, Moodbidri SB, Hegde UC, Hinduja IN: Localization and detection of ovarian follicular fluid protein in follicles of human ovaries. Indian J Exp Biol. 1992, 30: 271-275.PubMed

99.

Schweigert FJ, Gericke B, Wolfram W, Kaisers U, Dudenhausen JW: Peptide and protein profiles in serum and follicular fluid of women undergoing IVF. Hum Reprod. 2006, 21: 2960-2968. 10.1093/humrep/del257.PubMedCrossRef

100.

Görg A, Weiss W, Dunn MJ: Current two-dimensional electrophoresis technology for proteomics. Proteomics. 2004, 4: 3665-3685. 10.1002/pmic.200401031.PubMedCrossRef

101.

Hanrieder J, Nyakas A, Naessén T, Bergquist J: Proteomic analysis of human follicular fluid using an alternative bottom-up approach. J Proteome Res. 2008, 7: 443-449. 10.1021/pr070277z.PubMedCrossRef

102.

Jimena P, Castilla JA, Ramirez JP, Gil T, Acebal M, Molina R, Herruzo AJ: Follicular fluid alpha-fetoprotein, carcinoembryonic antigen, and CA-125 levels in relation to in vitro fertilization and gonadotropin and steroid hormone concentrations. Fertil Steril. 1993, 59: 1257-1260.PubMed

103.

Sarandakou A, Phocas I, Botsis D, Sikiotis K, Rizos D, Kalambokis D, Trakakis E, Chryssikopoulos A: Tumor associated antigens, CEA, CA-125 and SCC in serum and follicular fluid of stimulated and unstimolated cycles. Eur J Obstet Gynecol Reprod Biol. 1994, 54: 131-136. 10.1016/0028-2243(94)90252-6.PubMedCrossRef

104.

Mordel N, Anteby SO, Zajicek G, Roisman I, Treves A, Barak V: CA-125 is present in significant concentrations in periovulatory follicles of in vitro fertilization patients. Fertil Steril. 1992, 57: 377-380.PubMed

105.

Ohta N, Saito H, Kaneko T, Yoshida M, Takahashi T, Saito T, Nakahara K, Hiroi M: Soluble CD44 in human ovarian follicular fluid. J Assist Reprod Genet. 2001, 18: 21-25. 10.1023/A:1026494528415.PubMedCentralPubMedCrossRef

106.

Imoedemhe D, Shaw RW: Follicular fluid alpha 1-antitrypsin-correlation with fertilizing capacity of oocytes. Br J Obstet Gynaecol. 1986, 93: 863-868.PubMedCrossRef

107.

Nagy B, Pulay T, Szarka G, Csömör S: The serum protein content of human follicular fluid and it's correlation with the maturity of oocytes. Acta Physiol Hung. 1989, 73: 71-75.PubMed

108.

Welt CK, Pagan YL, Smith PC, Rado KB, Hall JE: Control of follicle-stimulating hormone by estradiol and the inhibins: critical role of estradiol at the hypothalamus during the luteal-follicular transition. J Clin Endocrinol Metab. 2003, 88: 1766-1771. 10.1210/jc.2002-021516.PubMedCrossRef

109.

Mantzoros CS, Cramer DW, Liberman RF, Barbieri RL: Predictive value of serum and follicular fluid leptin concentrations during assisted reproductive cycles in normal women and in women with the polycystic ovarian syndrome. Hum Reprod. 2000, 15: 539-544. 10.1093/humrep/15.3.539.PubMedCrossRef

110.

Tsai EM, Yang CH, Chen SC, Liu YH, Chen HS, Hsu SC, Lee JN: Leptin affects pregnancy outcome of in vitro fertilization and steroidogenesis of human granulosa cells. J Assist Reprod Genet. 2002, 19: 169-176. 10.1023/A:1014889928191.PubMedCentralPubMedCrossRef

111.

Wunder DM, Mueller MD, Birkhäuser MH, Bersinger NA: Steroids and protein markers in the follicular fluid as indicators of oocyte quality in patients with and without endometriosis. J Assist Reprod Genet. 2005, 22: 257-264. 10.1007/s10815-005-5149-2.PubMedCentralPubMedCrossRef

112.

De Placido G, Alviggi C, Clarizia R, Mollo A, Alviggi E, Strina I, Fiore E, Wilding M, Pagano T, Matarese G: Intra-follicular leptin concentration as a predictive factor for in vitro oocyte fertilization in assisted reproductive techniques. J Endocrinol Invest. 2006, 29: 719-726.PubMedCrossRef

113.

Sudik R, Chari S, Pascher E, Sturm G: Human follicular fluid levels of endothelins in relation to oocyte maturity status. Exp Clin Endocrinol Diabetes. 1996, 104 (1): 78-84.PubMedCrossRef

114.

Plonowski A, Kaplinski AP, Radzikowska M, Borowiec M, Baranowska B: Correlation between 21 amino acid endothelin, intrafollicular steroids and follicle size in stimulated cycles. Hum Reprod. 1999, 14: 2323-2327. 10.1093/humrep/14.9.2323.PubMedCrossRef

115.

Channing CP, Liu CQ, Jones GS, Jones H: Decline of follicular oocyte maturation inhibitor coincident with maturation and achievement of fertilizability of oocytes recovered at midcycle of gonadotropin-treated women. Proc Nat Acad Sci USA. 1983, 80: 4184-4188. 10.1073/pnas.80.13.4184.PubMedCentralPubMedCrossRef

116.

Szymanski W, Kazdepka-Zieminska A: Effect of homocysteine concentration in follicular fluid on a degree of oocyte maturity. Ginekol Pol. 2003, 74: 1392-1396.PubMed

117.

Boxmeer JC, Steegers-Theunissen RP, Lindemans J, Wildhagen MF, Martini E, Steegers EA, Macklon NS: Homocysteine metabolism in the pre-ovulatory follicle during ovarian stimulation. Hum Reprod. 2008, 23: 2570-2576. 10.1093/humrep/den292.PubMedCrossRef

118.

Facchinetti F, Artini PG, Monaco M, Volpe A, Genazzani AR: Oocyte fertilization in vitro is associated with high follicular immunoreactive beta-endorphin levels. J Endocrinol Invest. 1989, 12: 693-698.PubMedCrossRef

119.

Tam PP, Ng TB, Mao KR: Beta-endorphin levels in the preovulatory follicles and the outcome of in vitro fertilization. J In Vitro Fertil Embryo Transfer. 1988, 5: 91-95. 10.1007/BF01130665.CrossRef

120.

Yanaihara A, Mitsukawa K, Iwasaki S, Otsuki K, Kawamura T, Okai T: High concentrations of lactoferrin in the follicular fluid correlate with embryo quality during in vitro fertilization cycles. Fertil Steril. 2007, 87: 279-282. 10.1016/j.fertnstert.2006.06.025.PubMedCrossRef

121.

Heimler I, Rawlins RG, Binor Z, Aiman J, Raff H, Hutz RJ: Elevated follicular fluid angiotensin II and pregnancy outcome. Fertil Steril. 1995, 63: 528-534.PubMed

122.

Jarry H, Meyer B, Holzapfel G, Hinney B, Kuhn W, Wuttke W: Angiotensin II/III and substance P in human follicular fluid obtained during IVF: relation of the peptide content with follicular size. Acta Endocrinol (Copenh). 1988, 119: 277-282.

123.

Itskovitz J, Rubattu S, Rosenwaks Z, Liu HC, Sealey JE: Relationship of follicular fluid prorenin to oocyte maturation, steroid levels, and outcome of in vitro fertilization. J Clin Endocrinol Metab. 1991, 72: 165-171.PubMedCrossRef

124.

Sinclair KD, Lunn LA, Kwong WY, Wonnacott K, Linforth RS, Craigon J: Amino acid and fatty acid composition of follicular fluid as predictors of in-vitro embryo development. Reprod Biomed Online. 2008, 16: 859-868.PubMedCrossRef

125.

D'Aniello G, Grieco N, Di Filippo MA, Cappiello F, Topo E, D'Aniello E, Ronsini S: Reproductive implication of D-aspartic acid in human pre-ovulatory follicular fluid. Hum Reprod. 2007, 22: 3178-3183. 10.1093/humrep/dem328.PubMedCrossRef

126.

Saito H, Kaneko T, Takahashi T, Kawachiya S, Saito T, Hiroi M: Hyaluronan in follicular fluids and fertilization of oocytes. Fertil Steril. 2000, 74: 1148-1152. 10.1016/S0015-0282(00)01586-7.PubMedCrossRef

127.

Suchanek E, Simunic V, Juretic D, Grizelj V: Follicular fluid contents of hyaluronic acid, follicle-stimulating hormone and steroids relative to the success of in vitro fertilization of human oocytes. Fertil Steril. 1994, 62: 347-352.PubMed

128.

Chiu TT, Rogers MS, Law EL, Briton-Jones CM, Cheung LP, Haines CJ: Follicular fluid and serum concentrations of myo-inositol in patients undergoing IVF: relationship with oocyte quality. Hum Reprod. 2002, 17: 1591-1596. 10.1093/humrep/17.6.1591.PubMedCrossRef

129.

Jeremy JY, Okonofua FE, Thomas M, Wojdyla J, Smith W, Craft IL, Dandona P: Oocyte maturity and human follicular fluid prostanoids, gonadotropins, and prolactin after administration of clomiphene and pergonal. J Clin Endocrinol Metab. 1987, 65: 402-406.PubMedCrossRef

130.

Webster BW, Diamond MP: Endocrine profile of follicles containing oocytes with subsequent polyploid fertilization. Fertil Steril. 1988, 50: 727-731.PubMed

131.

Bayer SR, Armant DR, Dlugi AM, Seibel MM: Spectrophometric absorbance of follicular fluid: a predictor of oocyte fertilizing capability. Fertil Steril. 1988, 49: 442-446.PubMed

132.

Fisch B, Goldberg I, Ovadia J, Tadir Y: Physicochemical properties of follicular fluid and their relation to in vitro fertilization (IVF) outcome. J In Vitro Fertil Embryo Transfer. 1990, 7: 67-73. 10.1007/BF01135577.CrossRef

133.

Botros L, Sakkas D, Seli E: Metabolomics and its application for non-invasive embryo assessment in IVF. Mol Hum Reprod. 2008, 14: 679-690. 10.1093/molehr/gan066.PubMedCentralPubMedCrossRef

134.

Nagy ZP, Sakkas D, Behr B: Non-invasive assessment of embryo viability by metabolomic profiling of culture media ("metabolomics"). Reprod Biomed Online. 2008, 17: 502-507.PubMedCrossRef

135.

Seli E, Botros L, Sakkas D, Burns DH: Noninvasive metabolomic profiling of embryo culture media using proton nuclear magnetic resonance correlates with reproductive potential of embryos in women undergoing in vitro fertilization. Fertil Steril. 2008, 90: 2183-2189. 10.1016/j.fertnstert.2008.07.1739.PubMedCrossRef

136.

Singh R, Sinclair KD: Metabolomics: approaches to assessing oocyte and embryo quality. Theriogenology. 2007, 68 (Suppl 1): S56-S62. 10.1016/j.theriogenology.2007.04.007.PubMedCrossRef

137.

Aharoni A, Ric de Vos CH, Verhoeven HA, Maliepaard CA, Kruppa G, Bino R, Goodenowe DB: Nontargeted metabolome analysis by use of Fourier Transform Ion Cyclotron Mass Spectrometry. OMICS. 2002, 6: 217-234. 10.1089/15362310260256882.PubMedCrossRef

138.

Dunn WB, Bailey NJ, Johnson HE: Measuring the metabolome: current analytical technologies. Analyst. 2005, 130: 606-625. 10.1039/b418288j.PubMedCrossRef

139.

Goodacre R, Vaidyanathan S, Dunn WB, Harrigan GG, Kell DB: Metabolomics by numbers: acquiring and understanding global metabolite data. Trends Biotechnol. 2004, 22: 245-252. 10.1016/j.tibtech.2004.03.007.PubMedCrossRef

140.

Wells D, Patrizio P: Gene expression profiling of human oocytes at different maturational stages and after in vitro maturation. Am J Obstet Gynecol. 2008, 198: 455e1-455e11. 10.1016/j.ajog.2007.12.030.CrossRef

141.

Kocabas AM, Crosby J, Ross PJ, Otu HH, Beyhan Z, Can H, Tam WL, Rosa GJ, Halgren RG, Lim B, Fernandez E, Cibelli JB: The transcriptome of human oocytes. Proc Nat Acad Sci USA. 2006, 103: 14027-14032. 10.1073/pnas.0603227103.PubMedCentralPubMedCrossRef

142.

Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A: Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction. 2001, 121: 447-454. 10.1530/rep.0.1210447.PubMedCrossRef

143.

Booth PJ, Humpherson PG, Watson TJ, Leese HJ: Amino acid depletion and appearance during porcine preimplantation embryo development in vitro. Reproduction. 2005, 130: 655-668. 10.1530/rep.1.00727.PubMedCrossRef

144.

Preis KA, Seidel G, Gardner DK: Metabolic markers of developmental competence for in vitro-matured mouse oocytes. Reproduction. 2005, 130: 475-483. 10.1530/rep.1.00831.PubMedCrossRef

145.

Thomas N, Goodacre R, Timmins EM, Gaudoin M, Fleming R: Fourier transform infrared spectroscopy of follicular fluids from large and small antral follicles. Hum Reprod. 2000, 15: 1667-1671. 10.1093/humrep/15.8.1667.PubMedCrossRef

146.

Roberts R, Stark J, Iatropoulou A, Becker DL, Franks S, Hardy K: Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol Reprod. 2004, 71: 199-209. 10.1095/biolreprod.103.023549.PubMedCrossRef

147.

Scott L, Berntsen J, Davies D, Gundersen J, Hill J, Ramsing N: Human oocyte respiration rate measurement – potential to improve oocyte and embryo selection?. Reprod Biomed Online. 2008, 17: 461-469.PubMedCrossRef

Title: Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics
Authors: Alberto Revelli
Luisa Delle Piane
Simona Casano
Emanuela Molinari
Marco Massobrio
Paolo Rinaudo
Publication date: 01-12-2009
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2009
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-7-40

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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