DOI QR코드

DOI QR Code

Relationship between follicular fluid adipocytokines and the quality of the oocyte and corresponding embryo development from a single dominant follicle in in vitro fertilization/intracytoplasmic sperm injection cycles

  • Chang, Hye Jin (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Lee, Ji Hyun (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Lee, Jung Ryeol (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Jee, Byung Chul (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Suh, Chang Suk (Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital) ;
  • Kim, Seok Hyun (Department of Obstetrics and Gynecology, Seoul National University College of Medicine)
  • Received : 2013.11.12
  • Accepted : 2014.02.03
  • Published : 2014.03.31

Abstract

Objective: To investigate the association of individual follicular fluid (FF) leptin and adiponectin levels with the quality of the corresponding oocyte and embryo. Methods: We prospectively enrolled 67 women who underwent controlled ovarian hyperstimulation with 89 FF samples. FF and the corresponding oocyte was obtained from a single dominant preovulatory follicle at the time of oocyte retrieval. Concentrations of leptin and adiponectin were measured by enzyme-linked immunosorbent assay in an individual follicle. The oocyte quality, fertilization rate, and corresponding embryo development were assessed. Results: The FF level of leptin was significantly associated with body mass index (r=0.334, p<0.01). The FF adiponectin level was significantly higher in the normal fertilization group than the abnormal fertilization group (p=0.009) in the non-obese women. A lower FF leptin level was associated with a trend toward mature oocytes, normal fertilization, and good embryo quality, although these relationships were not statistically significant. The leptin:adiponectin ratio of FF did not differ significantly according to oocyte and embryo quality. The quality of the oocyte and embryo was not associated with the FF leptin level tertile. However, the normal fertilization rate was positively associated with FF adiponectin level tertile. There was a trend towards improved oocytes and normal fertilization rates with the lowest tertile of the FF leptin:adiponectin ratio, but this difference was not statistically significant. Conclusion: Our results suggest that a high FF adiponectin concentration could be a predictor of normal fertilization. However, the FF leptin concentration and leptin:adiponectin ratio is not significantly related to oocyte maturity and corresponding embryo development.

Keywords

References

  1. Fedorcsak P, Dale PO, Storeng R, Ertzeid G, Bjercke S, Oldereid N, et al. Impact of overweight and underweight on assisted reproduction treatment. Hum Reprod 2004;19:2523-8. https://doi.org/10.1093/humrep/deh485
  2. Metwally M, Ong KJ, Ledger WL, Li TC. Does high body mass index increase the risk of miscarriage after spontaneous and assisted conception? A meta-analysis of the evidence. Fertil Steril 2008;90:714-26. https://doi.org/10.1016/j.fertnstert.2007.07.1290
  3. Maheshwari A, Stofberg L, Bhattacharya S. Effect of overweight and obesity on assisted reproductive technology: a systematic review. Hum Reprod Update 2007;13:433-44. https://doi.org/10.1093/humupd/dmm017
  4. Lintsen AM, Pasker-de Jong PC, de Boer EJ, Burger CW, Jansen CA, Braat DD, et al. Effects of subfertility cause, smoking and body weight on the success rate of IVF. Hum Reprod 2005;20:1867-75. https://doi.org/10.1093/humrep/deh898
  5. Wang JX, Davies M, Norman RJ. Body mass and probability of pregnancy during assisted reproduction treatment: retrospective study. BMJ 2000;321:1320-1. https://doi.org/10.1136/bmj.321.7272.1320
  6. Fedorcsak P, Storeng R, Dale PO, Tanbo T, Abyholm T. Obesity is a risk factor for early pregnancy loss after IVF or ICSI. Acta Obstet Gynecol Scand 2000;79:43-8. https://doi.org/10.1080/j.1600-0412.2000.079001043.x
  7. ESHRE Task Force on Ethics and Law, including, Dondorp W, de Wert G, Pennings G, Shenfield F, Devroey P, et al. Lifestyle-related factors and access to medically assisted reproduction. Hum Reprod 2010;25:578-83. https://doi.org/10.1093/humrep/dep458
  8. van der Steeg JW, Steures P, Eijkemans MJ, Habbema JD, Hompes PG, Michgelsen HW, et al. Predictive value of pregnancy history in subfertile couples: results from a nationwide cohort study in the Netherlands. Fertil Steril 2008;90:521-7. https://doi.org/10.1016/j.fertnstert.2007.07.1301
  9. Brewer CJ, Balen AH. The adverse effects of obesity on conception and implantation. Reproduction 2010;140:347-64. https://doi.org/10.1530/REP-09-0568
  10. van der Steeg JW, Steures P, Eijkemans MJ, Habbema JD, Hompes PG, Burggraaff JM, et al. Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women. Hum Reprod 2008;23:324-8.
  11. Jensen TK, Scheike T, Keiding N, Schaumburg I, Grandjean P. Fecundability in relation to body mass and menstrual cycle patterns. Epidemiology 1999;10:422-8. https://doi.org/10.1097/00001648-199907000-00014
  12. Robker RL, Akison LK, Bennett BD, Thrupp PN, Chura LR, Russell DL, et al. Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderateweight women. J Clin Endocrinol Metab 2009;94:1533-40. https://doi.org/10.1210/jc.2008-2648
  13. Chudek J, Adamczak M, Nieszporek T, Wiecek A. The adipose tissue as an endocrine organ: a nephrologists' perspective. Contrib Nephrol 2006;151:70-90.
  14. Wozniak SE, Gee LL, Wachtel MS, Frezza EE. Adipose tissue: the new endocrine organ? A review article. Dig Dis Sci 2009;54:1847-56. https://doi.org/10.1007/s10620-008-0585-3
  15. Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol 2010;316:129-39. https://doi.org/10.1016/j.mce.2009.08.018
  16. Li L, Ferin M, Sauer MV, Lobo RA. Ovarian adipocytokines are associated with early in vitro human embryo development independent of the action of ovarian insulin. J Assist Reprod Genet 2012;29:1397-404. https://doi.org/10.1007/s10815-012-9864-1
  17. Rosenbaum M, Nicolson M, Hirsch J, Heymsfield SB, Gallagher D, Chu F, et al. Effects of gender, body composition, and menopause on plasma concentrations of leptin. J Clin Endocrinol Metab 1996;81:3424-7.
  18. Meilleur KG, Doumatey A, Huang H, Charles B, Chen G, Zhou J, et al. Circulating adiponectin is associated with obesity and serum lipids in West Africans. J Clin Endocrinol Metab 2010;95:3517-21. https://doi.org/10.1210/jc.2009-2765
  19. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996;334:292-5. https://doi.org/10.1056/NEJM199602013340503
  20. Anifandis G, Koutselini E, Stefanidis I, Liakopoulos V, Leivaditis C, Mantzavinos T, et al. Serum and follicular fluid leptin levels are correlated with human embryo quality. Reproduction 2005;130:917-21. https://doi.org/10.1530/rep.1.00705
  21. Barroso G, Barrionuevo M, Rao P, Graham L, Danforth D, Huey S, et al. Vascular endothelial growth factor, nitric oxide, and leptin follicular fluid levels correlate negatively with embryo quality in IVF patients. Fertil Steril 1999;72:1024-6. https://doi.org/10.1016/S0015-0282(99)00442-2
  22. Welt CK, Schneyer AL, Heist K, Mantzoros CS. Leptin and soluble leptin receptor in follicular fluid. J Assist Reprod Genet 2003;20:495-501. https://doi.org/10.1023/B:JARG.0000013649.38415.2a
  23. Asimakopoulos B, Koster F, Felberbaum R, Tripsiannis G, Caglar GS, Nikolettos N, et al. Intrafollicular and circulating concentrations of leptin do not predict the outcome in IVF-ICSI cycles. Reprod Sci 2009;16:113-9. https://doi.org/10.1177/1933719108324139
  24. Chang HJ, Lee JR, Jee BC, Suh CS, Kim SH. Cessation of gonadotropin- releasing hormone antagonist on triggering day: an alternative method for flexible multiple-dose protocol. J Korean Med Sci 2009;24:262-8. https://doi.org/10.3346/jkms.2009.24.2.262
  25. Brannian JD, Hansen KA. Leptin and ovarian folliculogenesis: implications for ovulation induction and ART outcomes. Semin Reprod Med 2002;20:103-12. https://doi.org/10.1055/s-2002-32501
  26. Adamczak M, Wiecek A. The adipose tissue as an endocrine organ. Semin Nephrol 2013;33:2-13. https://doi.org/10.1016/j.semnephrol.2012.12.008
  27. Ryan NK, Woodhouse CM, Van der Hoek KH, Gilchrist RB, Armstrong DT, Norman RJ. Expression of leptin and its receptor in the murine ovary: possible role in the regulation of oocyte maturation. Biol Reprod 2002;66:1548-54. https://doi.org/10.1095/biolreprod66.5.1548
  28. Craig J, Zhu H, Dyce PW, Petrik J, Li J. Leptin enhances oocyte nuclear and cytoplasmic maturation via the mitogen-activated protein kinase pathway. Endocrinology 2004;145:5355-63. https://doi.org/10.1210/en.2004-0783
  29. Boelhauve M, Sinowatz F, Wolf E, Paula-Lopes FF. Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biol Reprod 2005;73:737-44. https://doi.org/10.1095/biolreprod.105.041103
  30. Ye Y, Kawamura K, Sasaki M, Kawamura N, Groenen P, Sollewijn Gelpke MD, et al. Leptin and ObRa/MEK signalling in mouse oocyte maturation and preimplantation embryo development. Reprod Biomed Online 2009;19:181-90. https://doi.org/10.1016/S1472-6483(10)60070-3
  31. Joo JK, Joo BS, Kim SC, Choi JR, Park SH, Lee KS. Role of leptin in improvement of oocyte quality by regulation of ovarian angiogenesis. Anim Reprod Sci 2010;119:329-34. https://doi.org/10.1016/j.anireprosci.2010.02.002
  32. Tsai EM, Yang CH, Chen SC, Liu YH, Chen HS, Hsu SC, et al. Leptin affects pregnancy outcome of in vitro fertilization and steroidogenesis of human granulosa cells. J Assist Reprod Genet 2002; 19:169-76. https://doi.org/10.1023/A:1014889928191
  33. Asimakopoulos B, Nikolettos N, Papachristou DN, Simopoulou M, Al-Hasani S, Diedrich K. Follicular fluid levels of vascular endothelial growth factor and leptin are associated with pregnancy outcome of normal women participating in intracytoplasmic sperm injection cycles. Physiol Res 2005;54:263-70.
  34. Chabrolle C, Tosca L, Dupont J. Regulation of adiponectin and its receptors in rat ovary by human chorionic gonadotrophin treatment and potential involvement of adiponectin in granulosa cell steroidogenesis. Reproduction 2007;133:719-31. https://doi.org/10.1530/REP-06-0244
  35. Kim ST, Marquard K, Stephens S, Louden E, Allsworth J, Moley KH. Adiponectin and adiponectin receptors in the mouse preimplantation embryo and uterus. Hum Reprod 2011;26:82-95. https://doi.org/10.1093/humrep/deq292
  36. Cikos S, Burkus J, Bukovska A, Fabian D, Rehak P, Koppel J. Expression of adiponectin receptors and effects of adiponectin isoforms in mouse preimplantation embryos. Hum Reprod 2010;25:2247-55. https://doi.org/10.1093/humrep/deq193
  37. Chappaz E, Albornoz MS, Campos D, Che L, Palin MF, Murphy BD, et al. Adiponectin enhances in vitro development of swine embryos. Domest Anim Endocrinol 2008;35:198-207. https://doi.org/10.1016/j.domaniend.2008.05.007
  38. Richards JS, Liu Z, Kawai T, Tabata K, Watanabe H, Suresh D, et al. Adiponectin and its receptors modulate granulosa cell and cumulus cell functions, fertility, and early embryo development in the mouse and human. Fertil Steril 2012;98:471-9.e1. https://doi.org/10.1016/j.fertnstert.2012.04.050
  39. Takemura Y, Osuga Y, Yamauchi T, Kobayashi M, Harada M, Hirata T, et al. Expression of adiponectin receptors and its possible implication in the human endometrium. Endocrinology 2006;147: 3203-10. https://doi.org/10.1210/en.2005-1510

Cited by

  1. Leptin and its potential interest in assisted reproduction cycles vol.22, pp.3, 2016, https://doi.org/10.1093/humupd/dmv057
  2. Adiponectin Deficiency Leads to Female Subfertility and Ovarian Dysfunctions in Mice vol.157, pp.12, 2014, https://doi.org/10.1210/en.2015-2080