Skip to main content
Journal of Assisted Reproduction and Genetics logoLink to Journal of Assisted Reproduction and Genetics
. 2003 Dec;20(12):506–512. doi: 10.1023/B:JARG.0000013651.37866.0c

Human Oocyte Maturity In Vivo Determines the Outcome of Blastocyst Development In Vitro

Yi-Chi Lin 1, Shiuh-Young Chang 1,2, Kuo-Chung Lan 1, Hsuan-Wei Huang 1, Chih-Yang Chang 1, Meng-Yin Tsai 1, Fu-Tsai Kung 1,2, Fu-Jen Huang 1,2
PMCID: PMC3455306  PMID: 15035550

Abstract

Purpose: To date, the impact of oocyte maturity at aspiration on the blastocyst formation in vitro has not been fully evaluated. This study was undertaken to assess the influence of oocyte maturity in patients undergoing in vitro fertilization and blastocyst transfer program.

Methods: A total of 1278 oocytes derived from 147-IVF cycles were retrospectivly analyzed. Oocyte maturity was graded on a scale from 1 to 5 based on the morphology of the ooplasm, cumulus mass, corona radiata, and membrana granulosa cells.

Results: Mature oocytes yielded the highest fertilization rates. Although the cleavage rates were similar in both groups, the percentage of poor morphology, day-3 embryos from the nonmature-oocyte group was significantly higher than from the mature-oocyte group (54.7% vs. 15.5%, P < 0.001). Although good morphology, day-3 embryos were collected from nonmature oocytes, the incidence of these embryos developing to the blastocyst stage was significantly less than from mature oocytes (33.3% vs. 71.2%, P < 0.001). Although blastocyst stage embryos were collected from nonmature oocytes, the incidence of these embryos developing to the top-scoring blastocysts was significantly less than from mature oocytes (58.3% vs. 89.5%, P < 0.001).

Conclusions: These phenomena suggest that oocyte maturity produced in vivo determine the fertilization potential and subsequent blastocyst quality in vitro.

Keywords: Blastocyst development, corona radiata, oocyte maturity, zona pellucida

Full Text

The Full Text of this article is available as a PDF (70.6 KB).

REFERENCES

  • 1.Edwards RG, Fishel SB, Cohen J, Fehilly CB, Purdy JM, Slater JM, Steptoe PC, Webster JM. Factors influencing the success of in vitro fertilization for alleviating human infertility. J In Vitro Fertil Embryo Transfer. 1984;1:3–23. doi: 10.1007/BF01129615. [DOI] [PubMed] [Google Scholar]
  • 2.Wood C, McMaster R, Rennie G, Trounson A, Leeton J. Factors influencing pregnancy rates following in vitro fertilization and embryo transfer. Fertil Steril. 1985;43:245–250. doi: 10.1016/s0015-0282(16)48380-9. [DOI] [PubMed] [Google Scholar]
  • 3.Jones HW, Jr, Acosta A, Andrews MC, Garcia JE, Jones GS, Mantzavinos T, McDowell J, Sandow B, Veeck L, Whibley T, Wilkes C, Wright G. The importance of the follicular phase to success and failure in in vitro fertilization. Fertil Steril. 1983;40:317–321. doi: 10.1016/s0015-0282(16)47293-6. [DOI] [PubMed] [Google Scholar]
  • 4.Diamond MP, Hill GA, Webster BW, Herbert CM, Rogers BJ, Osteen KG, Maxson WS, Vaughn WK, Wentz AC. Comparison of human menopausal gonadotropin, clomiphene citrate, and combined human menopausal gonadotropin-clomiphene citrate stimulation protocols for in vitro fertilization. Fertil Steril. 1986;46:1108–1112. doi: 10.1016/s0015-0282(16)49889-4. [DOI] [PubMed] [Google Scholar]
  • 5.Neveu S, Hedon B, Bringer J, Chinchole JM, Arnal F, Humeau C, Cristol P, Viala JL. Ovarian stimulation by a combination of a gonadotropin-releasing hormone agonist and gonadotropins for in vitro fertilization. Fertil Steril. 1987;47:639–643. doi: 10.1016/s0015-0282(16)59115-8. [DOI] [PubMed] [Google Scholar]
  • 6.Hwang FR, Chang MY, Soong YK. Gonadotropin stimulation after pituitary desensitization with leuprolide acetate, comparison of FSH/hMG and hMG alone cycles—A study of 166 cases. Chang Gung Med J. 1993;16:223–230. [PubMed] [Google Scholar]
  • 7.Strickler RC, Radwanska E, Williams DB. Controlled ovarian hyperstimulation regimens in assisted reproductive technologies. Am J Obstet Gynecol. 1995;172:733–766. doi: 10.1016/0002-9378(95)90151-5. [DOI] [PubMed] [Google Scholar]
  • 8.Surrey ES, Schoolcraft WB. Evaluating strategies for improving ovarian response of the poor responder undergoing assisted reproductive techniques. Fertil Steril. 2000;73:667–676. doi: 10.1016/s0015-0282(99)00630-5. [DOI] [PubMed] [Google Scholar]
  • 9.Scott RT, Jr, Hofmann GE. Prognostic assessment of ovarian reserve. Fertil Steril. 1995;63:1–11. [PubMed] [Google Scholar]
  • 10.Hansen LM, Batzer FR, Gutmann JN, Corson SL, Kelly MP, Gocial B. Evaluating ovarian reserve: Follicle stimulating hormone and oestradiol variability during cycle days 2–5. Hum Reprod. 1996;11:486–489. doi: 10.1093/humrep/11.3.486. [DOI] [PubMed] [Google Scholar]
  • 11.Licciardi FL, Liu HC, Rosenwaks Z. Day 3 estradiol serum concentrations as prognosticators of ovarian stimulation response and pregnancy outcome in patients undergoing in vitro fertilization. Fertil Steril. 1995;64:991–994. doi: 10.1016/s0015-0282(16)57916-3. [DOI] [PubMed] [Google Scholar]
  • 12.Loumaye E, Billion JM, Mine JM, Psalti I, Pensis M, Thomas K. Prediction of individual response to controlled ovarian hyperstimulation by means of a clomiphene citrate challenge test. Fertil Steril. 1990;53:295–301. doi: 10.1016/s0015-0282(16)53284-1. [DOI] [PubMed] [Google Scholar]
  • 13.Winslow KL, Toner JP, Brzyski RG, Oehninger SC, Acosta AA, Muasher SJ. The gonadotropin-releasing hormone agonist stimulation test—A sensitive predictor of performance in the flare-up in vitro fertilization cycle. Fertil Steril. 1991;56:711–717. doi: 10.1016/s0015-0282(16)54604-4. [DOI] [PubMed] [Google Scholar]
  • 14.Fanchin R, de Ziegler D., Olivennes F, Taieb J, Dzik A, Frydman R. Exogenous follicle stimulating hormone ovarian reserve test (EFORT): A simple and reliable screening test for detecting “poor responders” in in-vitro fertilization. Hum Reprod. 1994;9:1607–1611. doi: 10.1093/oxfordjournals.humrep.a138760. [DOI] [PubMed] [Google Scholar]
  • 15.Huang FJ, Chang SY, Tsai MY, Kung FT, Wu JF, Chang HW. Determination of the efficiency of controlled ovarian hyperstimulation in the gonadotropin-releasing hormone agonist-suppression cycle using the initial follicle count during gonadotropin stimulation. J Assist Reprod Gen. 2001;18:91–96. doi: 10.1023/A:1026582608645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Marek D, Langley M, Gardner DK, Confer N, Doody KM, Doody KJ. Introduction of blastocyst culture and transfer for all patients in an in vitro fertilization program. Fertil Steril. 1999;72:1035–1040. doi: 10.1016/s0015-0282(99)00409-4. [DOI] [PubMed] [Google Scholar]
  • 17.Langley MT, Marek DM, Gardner DK, Doody KM, Doody KJ. Extended embryo culture in human assisted reproduction treatments. Hum Reprod. 2001;16:902–908. doi: 10.1093/humrep/16.5.902. [DOI] [PubMed] [Google Scholar]
  • 18.Janssenswillen C, Nagy ZP, Van Steirteghem A. Maturation of human cumulus-free germinal vesicle-stage oocytes to metaphase II by coculture with monolayer Vero cells. Hum Reprod. 1995;10:375–378. doi: 10.1093/oxfordjournals.humrep.a135947. [DOI] [PubMed] [Google Scholar]
  • 19.Sirard MA, Florman HM, Leibfried-Rutledge ML, Barnes FL, Sims ML, First NL. Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol Reprod. 1989;40:1257–1263. doi: 10.1095/biolreprod40.6.1257. [DOI] [PubMed] [Google Scholar]
  • 20.WHO Laboratory Manual for Examination of Human Semen and Sperm—Cervical Mucus Interaction, 4th edn. 4th edn. Cambridge, UK: Cambridge University Press; 1999. [Google Scholar]
  • 21.Kruger TF, Menkveld R, Stander FS, Lombard CJ, Van der Merwe J.P., van Zyl J.A., Smith K. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril. 1986;46:1118–1123. doi: 10.1016/s0015-0282(16)49891-2. [DOI] [PubMed] [Google Scholar]
  • 22.Lan KC, Lin YC, Huang FJ, Kung FT, Hsieh CH, Chang SY. Comparison of metaphase II oocytes after stimulation with recombinant follicle-stimulating hormone and urinary follicle-stimulating hormone in a pituitary down-regulation regimen. Fertil Steril. 2002;78:639–641. doi: 10.1016/s0015-0282(02)03299-5. [DOI] [PubMed] [Google Scholar]
  • 23.Veeck LL. An Atlas of Human Gametes and Conceptuses. New York: Parthenon; 1998. pp. 40–45. [Google Scholar]
  • 24.Gardner DK, Lane M, Stevens J, Schlenker T, Schoolcraft WB. Blastocyst score affects implantation and pregnancy outcome: Towards a single blastocyst transfer. Fertil Steril. 2000;73:1155–1158. doi: 10.1016/s0015-0282(00)00518-5. [DOI] [PubMed] [Google Scholar]
  • 25.Kung FT, Lin YC, Tseng YJ, Huang FJ, Tsai MY, Chang SY. Transfer of frozen–thawed blastocysts that underwent quarter laser-assisted hatching at the day 3 cleaving stage before freezing. Fertil Steril. 2003;79(4):893–899. doi: 10.1016/s0015-0282(02)04846-x. [DOI] [PubMed] [Google Scholar]
  • 26.Huang FJ, Chang SY, Tsai MY, Lin YC, Kung FT, Wu JF, Lu YJ. Relationship of the human cumulus-free oocyte maturational profile with in vitro outcome parameters after intracytoplasmic sperm injection. J Assist Reprod Gen. 1999;16:483–487. doi: 10.1023/A:1020551000150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Veeck LL, Wortham JW, Jr, Witmyer J, Sandow BA, Acosta AA, Garcia JE, Jones GS, Jones HW., Jr Maturation and fertilization of morphologically immature human oocytes in a program of in vitro fertilization. Fertil Steril. 1983;39:594–602. doi: 10.1016/s0015-0282(16)47052-4. [DOI] [PubMed] [Google Scholar]
  • 28.Khan I, Staessen C, Van den Abeel E., Camus M, Wisanto A, Smitz J, Devroey P, Van Steirteghem A.C. Time of insemination and its effect on in-vitro fertilizaiton, cleavage and pregnancy rates in GnRH agonist/HMG-stimulated cycles. Hum Reprod. 1989;4:921–926. doi: 10.1093/oxfordjournals.humrep.a137013. [DOI] [PubMed] [Google Scholar]
  • 29.Jacobs M, Stolwijk AM, Wetzels AM. The effect of insemination/injection time on the results of IVF and ICSI. Hum Reprod. 2001;16:1708–1713. doi: 10.1093/humrep/16.8.1708. [DOI] [PubMed] [Google Scholar]
  • 30.Imthum B, Macas E, Rosselli M, Keller PJ. Nuclear maturity and oocyte morphology after stimulation with highly purified follicle stimulating hormone compared to human menopausal gonadotropin. Hum Reprod. 1996;11:2387–2391. doi: 10.1093/oxfordjournals.humrep.a019120. [DOI] [PubMed] [Google Scholar]
  • 31.Mercan R, Mayer JF, Walker D, Jones S, Oehninger S, Toner JP, Muasher SJ. Improved oocyte quality is obtained with follicle stimulating hormone alone than with follicle stimulating hormone/human menopausal gonadotropin combination. Hum Reprod. 1997;12:1886–1889. doi: 10.1093/humrep/12.9.1886. [DOI] [PubMed] [Google Scholar]
  • 32.Gianaroli L, Fiorentino A, Magli CM, Ferraretti AP, Montanaro N. Prolonged sperm–oocyte exposure and high sperm concentration affect human embryo viability and pregnancy rate. Hum Reprod. 1996;11:2507–2511. doi: 10.1093/oxfordjournals.humrep.a019149. [DOI] [PubMed] [Google Scholar]
  • 33.Aitken RJ, Irvine DS, Wu FC. Prospective analysis of sperm–oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol. 1991;164:542–551. doi: 10.1016/s0002-9378(11)80017-7. [DOI] [PubMed] [Google Scholar]
  • 34.Jones GM, Trounson AO. Blastocyst stage transfer: Pitfalls and benefits. Hum Reprod. 1999;14:1405–1408. doi: 10.1093/humrep/14.6.1405. [DOI] [PubMed] [Google Scholar]
  • 35.Scott L, Alvero R, Leondires M, Miller B. The morphology of human pronuclear embryos is positively related to blastocyst development and implantation. Hum Reprod. 2000;15:2394–2403. doi: 10.1093/humrep/15.11.2394. [DOI] [PubMed] [Google Scholar]
  • 36.Rijnders PM, Jansen CA. The predictive value of day 3 embryo morphology regarding blastocyst formation, pregnancy and implantation rate after day 5 transfer following in-vitro fertilization or intracytoplasmic sperm injection. Hum Reprod. 1998;13:2869–2973. doi: 10.1093/humrep/13.10.2869. [DOI] [PubMed] [Google Scholar]
  • 37.Racowsky C, Jackson KV, Cekleniak NA, Fox JH, Hornstein MD, Ginsburg ES. The number of eight-cell embryos is a key determinant for selecting day 3 or day 5 transfer. Fertil Steril. 2000;73:558–564. doi: 10.1016/s0015-0282(99)00565-8. [DOI] [PubMed] [Google Scholar]
  • 38.Graham J, Han T, Porter R, Levy M, Stillman R, Tucker MJ. Day 3 morphology is a poor predictor of blastocyst quality in extended culture. Fertil Steril. 2000;74:495–497. doi: 10.1016/s0015-0282(00)00689-0. [DOI] [PubMed] [Google Scholar]
  • 39.Hill GA, Freeman M, Bastias MC, Rogers BJ, Herbert CM, III, Osteen KG, Wentz AC. The influence of oocyte maturity and embryo quality on pregnancy rate in a program for in vitro fertilization–embryo transfer. Fertil Steril. 1989;52:801–806. doi: 10.1016/s0015-0282(16)61034-8. [DOI] [PubMed] [Google Scholar]
  • 40.Ng ST, Chang TH, Wu TC. Prediction of the rates of fertilization, cleavage, and pregnancy success by cumulus–coronal morphology in an in vitro fertilization program. Fertil Steril. 1999;72:412–417. doi: 10.1016/s0015-0282(99)00290-3. [DOI] [PubMed] [Google Scholar]
  • 41.Testart J, Lassalle B, Frydman R, Belaisch JC. A study of factors affecting the success of human fertilization in vitro. II: Influence of semen quality and oocyte maturity on fertilization and cleavage. Biol Reprod. 1983;28:425–431. doi: 10.1095/biolreprod28.2.425. [DOI] [PubMed] [Google Scholar]
  • 42.Huang FJ, Huang HW, Lan KC, Kung FT, Lin YC, Chang HW, Chang SY. The maturity of human cumulus-free oocytes is positively related to blastocyst development and viability. J Assist Reprod Genet. 2002;19:555–560. doi: 10.1023/A:1021259031267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Lan KC, Huang FJ, Lin YC, Kung FT, Hsieh CH, Huang HW, Tan PH, Chang SY. The predictive value of using a combined Z-score for zygote evaluation and socre for day-3 embryo morphology in the assessment of embryo survival on day 5. Hum Reprod. 2003;18:1299–1306. doi: 10.1093/humrep/deg239. [DOI] [PubMed] [Google Scholar]
  • 44.Wassarman PM. The mammalian ovum. In: Knobil E, Neil E, editors. The Physiology of Reproduction. New York: Raven; 1988. pp. 69–103. [Google Scholar]
  • 45.Perreault SD. Chromatin remodeling in mammalian zygotes. Mutat Res. 1992;296:43–55. doi: 10.1016/0165-1110(92)90031-4. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Assisted Reproduction and Genetics are provided here courtesy of Springer Science+Business Media, LLC

RESOURCES