Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Evaluation of oocyte quality: morphological, cellular and molecular predictors

Qiang Wang A B and Qing-Yuan Sun A C
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China.

B Graduate School, Chinese Academy of Sciences, Beijing 100080, China.

C Corresponding author. Email: sunqy@ioz.ac.cn

Reproduction, Fertility and Development 19(1) 1-12 https://doi.org/10.1071/RD06103
Published: 12 December 2006

Abstract

Mounting evidence that oocyte quality profoundly affects fertilisation and subsequent embryo development drives the continued search for reliable predictors of oocyte developmental competence. In the present review, we provide an overall summary and analysis of potential criteria that can be used to evaluate oocyte quality. These criteria are specifically classified as morphological and cellular/molecular predictors. Traditional methods for the evaluation of oocyte quality are based on morphological classification of the follicle, cumulus–oocyte complex, polar body and/or meiotic spindle. Although the use of morphological characteristics as predictors of oocyte quality is controversial, such a grading system can provide valuable information for the preselection of oocytes with higher developmental competence and, therefore, may maximise embryo developmental outcome. Several intrinsic markers (such as mitochondrial status and glucose-6-phosphate dehydrogenase l activity) and extrinsic markers (such as apoptosis of follicular cells and levels of the transforming growth factor-β superfamily in follicular fluid or serum) have also been reported as useful indicators of oocyte competence and embryo quality. Compared with the morphological parameters, these cellular and molecular predictors of oocyte quality may prove to be more precise and objective, although further studies and refinement of techniques are needed.


Acknowledgments

Part of the authors’ work reported herein was supported by National Natural Science Foundation of China (No. 30430530, 30225010, 30570944) and the National Basic Research Program of China (2006CB504004). The authors thank Dr Heide Schatten (University of Missouri-Columbia) for her critical reading of the manuscript.


References

Adams, G. P. (1999). Comparative pattern of follicle development and selection in ruminants. J. Reprod. Fertil. Suppl. 54, 17–32.
PubMed | Eppig J. J. (1996). The ovary: oogenesis. In ‘Scientific Essentials of Reproductive Medicine’. (Eds S. G. Hillier, H. C. Kitchener and J. P. Neilson.) pp. 147–159. (W. B. Saunders: London, UK.)

Eppig, J. J. , Wigglesworth, K. , Pendola, F. , and Hirao, Y. (1997). Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol. Reprod. 56, 976–984.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ericsson, S. A. , Boice, M. L. , Funahashi, H. , and Day, B. N. (1993). Assessment of porcine oocytes using brilliant cresyl blue. Theriogenology 39, 214.
Crossref | GoogleScholarGoogle Scholar |

Fan, H. Y. , and Sun, Q. Y. (2004). Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 70, 535–547.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ferrandi, B. , Cremonesti, G. , Geiger, R. , Consiglio, A. L. , Carnevali, A. , and Porcelli, F. (1993). Quantitative cytochemical study of some enzymatic activities in preovulatory bovine oocytes after in vitro maturation. Acta Histochem. 95, 89–96.
PubMed |

Fried, G. , Remaeus, K. , Harlin, J. , Krog, E. , Csemiczky, G. , Aanesen, A. , and Tally, M. (2003). 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. 20, 167–176.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gabrielsen, A. , Lindenberg, S. , and Petersen, K. (2001). The impact of the zona pellucida thickness variation of human embryos on pregnancy outcome in relation to suboptimal embryo development. A prospective randomized controlled study. Hum. Reprod. 16, 2166–2170.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gandolfi, F. , Brevini, T. A. , Cillo, F. , and Antonini, S. (2005). Cellular and molecular mechanisms regulating oocyte quality and the relevance for farm animal reproductive efficiency. Rev. Sci. Tech. 24, 413–423.
PubMed |

Gibson, T. C. , Kubisch, H. M. , and Brenner, C. A. (2005). Mitochondrial DNA deletions in rhesus macaque oocytes and embryos. Mol. Hum. Reprod. 11, 785–789.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Gioia, L. , Barboni, B. , Turriani, M. , Capacchietti, G. , Pistilli, M. G. , Berardinelli, P. , and Mattioli, M. (2005). The capability of reprogramming the male chromatin after fertilization is dependent on the quality of oocyte maturation. Reproduction 130, 29–39.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hall, J. E. , Welt, C. K. , and Cramer, D. W. (1999). Inhibin A and inhibin B reflect ovarian function in assisted reproduction but are less useful at predicting outcome. Hum. Reprod. 14, 409–415.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hassan-Ali, H. , Hisham-Saleh, A. , El-Gezeiry, D. , Baghdady, I. , Ismaeil, I. , and Mandelbaum, J. (1998). Perivitelline space granularity: a sign of human menopausal gonadotrophin overdose in intracytoplasmic sperm injection. Hum. Reprod. 13, 3425–3430.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Homa, S. T. (1995). Calcium and meiotic maturation of the mammalian oocyte. Mol. Reprod. Dev. 40, 122–134.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Host, E. , Mikkelsen, A. L. , Lindenberg, S. , and Smidt-Jensen, S. (2000). Apoptosis in human cumulus cells in relation to maturation stage and cleavage of the corresponding oocyte. Acta Obstet. Gynecol. Scand. 79, 936–940.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hsieh, R. H. , Tsai, N. M. , Au, H. K. , Chang, S. J. , Wei, Y. H. , and Tzeng, C. R. (2002). Multiple rearrangements of mitochondrial DNA in unfertilized human oocytes. Fertil. Steril. 77, 1012–1017.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hu, C. L. , Cowan, R. G. , Harman, R. M. , Porter, D. A. , and Quirk, S. M. (2001). Apoptosis of bovine granulosa cells after serum withdrawal is mediated by Fas antigen (CD95) and Fas ligand. Biol. Reprod. 64, 518–526.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Hunter, A. G. , and Moor, R. M. (1987). Stage-dependent effects of inhibiting ribonucleic acids and protein synthesis on meiotic maturation of bovine oocytes in vitro. J. Dairy Sci. 70, 1646–1651.
PubMed |

Hunter, M. G. , Brankin, V. , Quinn, R. L. , Ferguson, E. M. , Edwards, S. A. , and Ashworth, C. J. (2005). Oocyte–somatic cell–endocrine interactions in pigs. Domest. Anim. Endocrinol. 29, 371–384.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Iwata, H. , Inoue, J. , Kimura, K. , Kuge, T. , Kuwayama, T. , and Monji, Y. (2006). Comparison between the characteristics of follicular fluid and the developmental competence of bovine oocytes. Anim. Reprod. Sci. 91, 215–223.
Crossref | GoogleScholarGoogle Scholar | PubMed |

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

Kahraman, S. , Yakin, K. , Donmez, E. , Samli, H. , Bahce, M. , Cengiz, G. , Sertyel, S. , Samli, M. , and Imirzalioglu, N. (2000). Relationship between granular cytoplasm of oocytes and pregnancy outcome following intracytoplasmic sperm injection. Hum. Reprod. 15, 2390–2393.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Karlsson, C. , Lindell, K. , Svensson, E. , Bergh, C. , Lind, P. , Billig, H. , Carlsson, L. M. , and Carlsson, B. (1997). Expression of functional leptin receptors in the human ovary. J. Clin. Endocrinol. Metab. 82, 4144–4148.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kastrop, P. M. , Bevers, M. M. , Destree, O. H. , and Kruip, T. A. (1991). Protein synthesis and phosphorylation patterns of bovine oocytes maturing in vivo. Mol. Reprod. Dev. 29, 271–275.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Kawano, Y. , Narahara, H. , Matsui, N. , Nasu, K. , Miyamura, K. , and Miyakawa, I. (1997). Insulin-like growth factor-binding protein-1 in human follicular fluid: a marker for oocyte maturation. Gynecol. Obstet. Invest. 44, 145–148.
PubMed |

Kim, K. H. , Oh, D. S. , Jeong, J. H. , Shin, B. S. , Joo, B. S. , and Lee, K. S. (2004). Follicular blood flow is a better predictor of the outcome of in vitro fertilization–embryo transfer than follicular fluid vascular endothelial growth factor and nitric oxide concentrations. Fertil. Steril. 82, 586–592.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Klein, N. A. , Illingworth, P. J. , Groome, N. P. , McNeilly, A. S. , Battaglia, D. E. , and Soules, M. R. (1996). Decreased inhibin B secretion is associated with the monotropic FSH rise in older, ovulatory women: a study of serum and follicular fluid levels of dimeric inhibin A and B in spontaneous menstrual cycles. J. Clin. Endocrinol. Metab. 81, 2742–2745.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–E23.
PubMed |

Lau, C. P. , Ledger, W. L. , Groome, N. P. , Barlow, D. H. , and Muttukrishna, S. (1999). Dimeric inhibins and activin A in human follicular fluid and oocyte cumulus culture medium. Hum. Reprod. 14, 2525–2530.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lee, K. S. , Joo, B. S. , Na, Y. J. , Yoon, M. S. , Choi, O. H. , and Kim, W. W. (2000). Relationships between concentrations of tumor necrosis factor-alpha and nitric oxide in follicular fluid and oocyte quality. J. Assist. Reprod. Genet. 17, 222–228.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lee, K. S. , Joo, B. S. , Na, Y. J. , Yoon, M. S. , Choi, O. H. , and Kim, W. W. (2001). Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 18, 490–498.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lee, T. H. , Wu, M. Y. , Chen, M. J. , Chao, K. H. , Ho, H. N. , and Yang, Y. S. (2004). Nitric oxide is associated with poor embryo quality and pregnancy outcome in in vitro fertilization cycles. Fertil. Steril. 82, 126–131.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lindner, C. , Lichtenberg, V. , Westhof, G. , Braendle, W. , and Bettendorf, G. (1988). Endocrine parameters of human follicular fluid and fertilization capacity of oocytes. Horm. Metab. Res. 20, 243–246.
PubMed |

Liu, H. C. , He, Z. Y. , Mele, C. A. , Veeck, L. L. , Davis, O. K. , and Rosenwaks, Z. (1997). Expression of IGFs and their receptors is a potential marker for embryo quality. Am. J. Reprod. Immunol. 38, 237–245.
PubMed |

Lonergan, P. , Monaghan, P. , Rizos, D. , Boland, M. P. , and Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Lonergan, P. , Gutierrez-Adan, A. , Pintado, B. , Fair, T. , Ward, F. , Fuente, J. D. , and Boland, M. (2000). Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor, and two housekeeping genes in bovine two-cell embryos and blastocysts produced in vitro. Mol. Reprod. Dev. 57, 146–152.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Manabe, N. , Imai, Y. , Ohno, H. , Takahagi, Y. , Sugimoto, M. , and Miyamoto, H. (1996). Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in pig ovaries. Experientia 52, 647–651.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Mantzoros, C. S. , Cramer, D. W. , Liberman, R. F. , and Barbieri, R. L. (2000). 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. 15, 539–544.
Crossref | GoogleScholarGoogle Scholar | PubMed |

McKenzie, L. J. , Pangas, S. A. , Carson, S. A. , Kovanci, E. , Cisneros, P. , Buster, J. E. , Amato, P. , and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–2874.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Menezo, Y. , and Barak, Y. (2000). Comparison between day-2 embryos obtained either from ICSI or resulting from short insemination IVF: influence of maternal age. Hum. Reprod. 15, 1776–1780.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Moon, J. H. , Hyun, C. S. , Lee, S. W. , Son, W. Y. , Yoon, S. H. , and Lim, J. H. (2003). Visualization of the metaphase II meiotic spindle in living human oocytes using the Polscope enables the prediction of embryonic developmental competence after ICSI. Hum. Reprod. 18, 817–820.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nagano, M. , Katagiri, S. , and Takahashi, Y. (2006). Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 14, 53–61.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nakahara, K. , Saito, H. , Saito, T. , Ito, M. , Ohta, N. , Takahashi, T. , and Hiroi, M. (1997). The incidence of apoptotic bodies in membrana granulosa can predict prognosis of ova from patients participating in in vitro fertilization programs. Fertil. Steril. 68, 312–317.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nicholas, B. , Alberio, R. , Fouladi-Nashta, A. A. , and Webb, R. (2005). Relationship between low-molecular-weight insulin-like growth factor-binding proteins, caspase-3 activity, and oocyte quality. Biol. Reprod. 72, 796–804.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nogueira, D. , Cortvrindt, R. , Everaerdt, B. , and Smitz, J. (2005). Effects of long-term in vitro exposure to phosphodiesterase type-3 inhibitors on follicle and oocyte development. Reproduction 130, 177–186.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Nogueira, D. , Ron-El, R. , Friedler, S. , Schachter, M. , Raziel, A. , Cortvrindt, R. , and Smitz, J. (2006). Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol. Reprod. 74, 177–184.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oltvai, Z. N. , Milliman, C. L. , and Korsmeyer, S. J. (1993). Bcl-2 heterodimerizes in vitro with a conserved homology, Bax, that accelerates programmed cell death. Cell 74, 609–619.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Oosterhuis, G. J. , Vermes, I. , Lambalk, C. B. , Michgelsen, H. W. , and Schoemaker, J. (1998). Insulin-like growth factor (IGF)-I and IGF binding protein-3 concentrations in fluid from human stimulated follicles. Hum. Reprod. 13, 285–289.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ouellette, Y. , Price, C. A. , and Carriere, P. D. (2005). Follicular fluid concentration of transforming growth factor-β1 is negatively correlated with estradiol and follicle size at the early stage of development of the first-wave cohort of bovine ovarian follicles. Domest. Anim. Endocrinol. 29, 623–633.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pasqualotto, E. B. , Agarwal, A. , Sharma, R. K. , Izzo, V. M. , Pinotti, J. A. , Joshi, N. J. , and Rose, B. I. (2004). Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil. Steril. 81, 973–976.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pavlok, A. , Lucas-Hahn, A. , and Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–67.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pena, J. E. , Chang, P. L. , Chan, L. K. , Zeitoun, K. , Thornton, M. H. , and Sauer, M. V. (2002). Supraphysiological estradiol levels do not affect oocyte and embryo quality in oocyte donation cycles. Hum. Reprod. 17, 83–87.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Piko, L. , and Matsumoto, L. (1976). Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 1–10.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Piquette, G. N. , Tilly, J. L. , Prichard, L. , Simon, C. , and Polan, M. L. (1994). Detection of apoptosis in human and rat ovarian follicles. J. Soc. Gynecol. Invest. 1, 297–301.


Poe-Zeigler, R. , Toner, J. P. , Oehninger, S. , and Muasher, S. J. (1994). Basal FSH affects IVF pregnancy rates primarily by influencing oocyte numbers and not their quality. Fertil. Steril. 63, S8.


Porter, D. A. , Harman, R. M. , Cowan, R. G. , and Quirk, S. M. (2001). Relationship of Fas ligand expression and atresia during bovine follicle development. Reproduction 121, 561–566.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pujol, M. , Lopez-Bejar, M. , and Paramio, M. T. (2004). Developmental competence of heifers oocytes selected using the brilliant cresyl blue (BCB) test. Theriogenology 61, 735–744.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Quinn, P. , and Wales, R. G. (1973). The relationships between the ATP content of preimplantation mouse embryos and their development in vitro during culture. J. Reprod. Fertil. 35, 301–309.
PubMed |

Rienzi, L. , Ubaldi, F. , Martinez, F. , Iacobelli, M. , Minasi, M. G. , Ferrero, S. , Tesarik, J. , and Greco, E. (2003). Relationship between meiotic spindle location with regard to the polar body position and oocyte developmental potential after ICSI. Hum. Reprod. 18, 1289–1293.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rubio Pomar, F. J. , Roelen, B. A. , Slot, K. A. , van Tol, H. T. , Colenbrander, B. , and Teerds, K. J. (2004). Role of Fas-mediated apoptosis and follicle-stimulating hormone on the developmental capacity of bovine cumulus oocyte complexes in vitro. Biol. Reprod. 71, 790–796.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Ruiz Anguas, J. , Carballo Mondragon, E. , Anta Jaen, E. , Diaz Calvillo, J. , and Kably Ambe, A. (2005). Usefulness of luteinizing hormone levels to determine the oocyte quality. Ginecol. Obstet. Mex. 73, 28–35.
PubMed |

Saito, H. , Saito, T. , Kaneko, T. , Sasagawa, I. , Kuramoto, T. , and Hiroi, M. (2000). Relatively poor oocyte quality is an indication for intracytoplasmic sperm injection. Fertil. Steril. 73, 465–469.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sanfins, A. , Plancha, C. E. , Overstrom, E. W. , and Albertini, D. F. (2004). Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: insights into the relationship between nuclear and cytoplasmic quality. Hum. Reprod. 19, 2889–2899.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Santos, T. A. , El Shourbagy, S. , and St John, J. C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–591.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Seino, T. , Saito, H. , Kaneko, T. , Takahashi, T. , Kawachiya, S. , and Kurachi, H. (2002). Eight-hydroxy-2′-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization–embryo transfer program. Fertil. Steril. 77, 1184–1190.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Seneda, M. M. , Esper, C. R. , Garcia, J. M. , Oliveira, J. A. , and Vantini, R. (2001). Relationship between follicle size and ultrasound-guided transvaginal oocyte recovery. Anim. Reprod. Sci. 67, 37–43.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Serhal, P. F. , Ranieri, D. M. , Kinis, A. , Marchant, S. , Davies, M. , and Khadum, I. M. (1997). Oocyte morphology predicts outcome of intracytoplasmic sperm injection. Hum. Reprod. 12, 1267–1270.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sharara, F. I. , and McClamrock, H. D. (1999). High estradiol levels and high oocyte yield are not detrimental to in vitro fertilization outcome. Fertil. Steril. 72, 401–405.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Silberstein, T. , MacLaughlin, D. T. , Shai, I. , Trimarchi, J. R. , Lambert-Messerlian, G. , Seifer, D. B. , Keefe, D. L. , and Blazar, A. S. (2006). Müllerian inhibitory substance levels at the time of HCG administration in IVF cycles predict both ovarian reserve and embryo morphology. Hum. Reprod. 21, 159–163.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Silva, C. P. , Kommineni, K. , Oldenbourg, R. , and Keefe, D. L. (1999). The first polar body does not predict accurately the location of the metaphase 2 meiotic spindle in mammalian oocytes. Fertil. Steril. 71, 719–721.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sirard, M. A. , Florman, H. M. , Leibfried-Rutledge, M. L. , Barnes, F. L. , Sims, M. L. , and First, N. L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sirard, M. A. , Richard, F. , Blondin, P. , and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Slotte, H. , Gustafson, O. , Nylund, L. , and Pousette, A. (1990). ATP and ADP in human pre-embryos. Hum. Reprod. 5, 319–322.
PubMed |

Smith, L. C. , Olivera-Angel, M. , Groome, N. P. , Bhatia, B. , and Price, C. A. (1998). Oocyte quality in small antral follicles in the presence or absence of a large follicle in cattle. J. Reprod Fertil. 106, 193–199.


Stojkovic, M. , Machado, S. A. , Stojkovic, P. , Zakhartchenko, V. , Hutzler, P. , Goncalves, P. B. , and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sun, Q. Y. , and Nagai, T. (2003). Molecular mechanisms underlying pig oocyte maturation and fertilization. J. Reprod. Dev. 49, 347–359.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sun, Q. Y. , Wu, G. M. , Lai, L. , Park, K. W. , Cabot, R. , Cheong, H. T. , Day, B. N. , Prather, R. S. , and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–163.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Swann, K. , and Parrington, J. (1999). Mechanism of Ca2+ release at fertilization in mammals. J. Exp. Zool. 285, 267–275.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Szoltys, M. , Tabarowski, Z. , and Pawlik, A. (2000). Apoptosis of postovulatory cumulus granulosa cells of the rat. Anat. Embryol. 202, 523–529.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Talevi, R. , Gualtieri, R. , Tartaglione, G. , and Fortunato, A. (1997). Heterogeneity of the zona pellucida carbohydrate distribution in human oocytes failing to fertilize in vitro. Hum. Reprod. 12, 2773–2780.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tamassia, M. , Nuttinck, F. , May-Panloup, P. , Reynier, P. , Heyman, Y. , Charpigny, G. , Stojkovic, M. , Hiendleder, S. , Renard, J. P. , and Chastant-Maillard, S. (2004). In vitro embryo production efficiency in cattle and its association with oocyte adenosine triphosphate content, quantity of mitochondrial DNA, and mitochondrial DNA haplogroup. Biol. Reprod. 71, 697–704.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Toner, J. P. (2003). Age = egg quality, FSH level = egg quantity. Fertil. Steril. 79, 491.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Trimarchi, J. R. , and Keefe, D. L. (2006). Assessing the quality of oocytes derived from in vitro maturation: are we looking under the lamppost? Fertil. Steril. 85, 839–840.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tsai, E. M. , Yang, C. H. , Chen, S. C. , Liu, Y. H. , Chen, H. S. , Hsu, S. C. , and Lee, J. N. (2002). Leptin affects pregnancy outcome of in vitro fertilisation and steroidogenesis of human granulosa cells. J. Assist. Reprod. Genet. 19, 169–176.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Tsuchiya, K. , Seki, M. , and Itoh, M. (1989). Correlation of serum inhibin concentrations with results in an ovarian hyperstimulation program. Fertil. Steril. 52, 88–94.
PubMed |

Tsutsumi, O. , Satoh, K. , Taketani, Y. , and Kato, T. (1992). Determination of enzyme activity of energy metabolism in the maturing rat oocyte. Mol. Reprod. Dev. 33, 333–337.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Van Blerkom, J. , and Henry, G. (1992). Oocyte dysmorphism and aneuploidy in meiotically mature human oocytes after ovarian stimulation. Hum. Reprod. 7, 379–390.
PubMed |

Van Blerkom, J. , and Runner, M. N. (1984). Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am. J. Anat. 171, 335–355.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Van Blerkom, J. , Davis, P. , and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 10, 415–424.
PubMed |

Varisanga, M. D. , Sumantri, C. , Murakami, M. , Fahrudin, M. , and Suzuki, T. (1998). Morphological classification of the ovaries in relation to the subsequent oocyte quality for IVF-produced bovine embryos. Theriogenology 50, 1015–1023.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vassena, R. , Mapletoft, R. J. , Allodi, S. , Singh, J. , and Adams, G. P. (2003). Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology 60, 923–932.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Vickers, S. L. , Cowan, R. G. , Harman, R. M. , Porter, D. A. , and Quirk, S. M. (2000). Expression and activity of the Fas antigen in bovine ovarian follicle cells. Biol. Reprod. 62, 54–61.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wang, W. H. , and Day, B. N. (2002). Development of porcine embryos produced by IVM/IVF in a medium with or without protein supplementation: effects of extracellular glutathione. Zygote 10, 109–115.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wang, W. H. , Meng, L. , Hackett, R. J. , and Keefe, D. L. (2001a). Developmental ability of human oocytes with or without birefringent spindles imaged by Polscope before insemination. Hum. Reprod. 16, 1464–1468.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wang, W. H. , Meng, L. , Hackett, R. J. , Odenbourg, R. , and Keefe, D. L. (2001b). The spindle observation and its relationship with fertilization after intracytoplasmic sperm injection in living human oocytes. Fertil. Steril. 75, 348–353.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wang, Q. , Yin, S. , Ai, J. S. , Liang, C. G. , Hou, Y. , Chen, D. Y. , Schatten, H. , and Sun, Q. Y. (2006). Histone deacetylation is required for orderly meiosis. Cell Cycle 5, 766–774.
PubMed |

Warriach, H. M. , and Chohan, K. R. (2004). Thickness of cumulus cell layer is a significant factor in meiotic competence of buffalo oocytes. J. Vet. Sci. 5, 247–251.
PubMed |

Waterman-Storer, C. M. (1998). Microtubules and microscopes: how the development of light microscopic imaging technologies has contributed to discoveries about microtubule dynamics in living cells. Mol. Biol. Cell 9, 3263–3271.
PubMed |

Welt, C. K. , Schneyer, A. L. , Heist, K. , and Mantzoros, C. S. (2003). Leptin and soluble leptin receptor in follicular fluid. J. Assist. Reprod. Genet. 20, 495–501.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wen, X. , Tozer, A. J. , Butler, S. A. , Bell, C. M. , Docherty, S. M. , and Iles, R. K. (2006). 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. 85, 1723–1729.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wise, T. , Suss, U. , and Maurer, R. R. (1987). The relationships of oocyte quality and follicular fluid prolactin and progesterone in superovulated beef heifers with and without norgestomet implants. Adv. Exp. Med. Biol. 219, 697–701.
PubMed |

Wiswedel, K. (1987). Granulosa cell metabolism and the assessment of oocyte quality in IVF. Hum. Reprod. 2, 589–591.
PubMed |

Wunder, D. M. , Kretschmer, R. , and Bersinger, N. A. (2005a). Concentrations of leptin and C-reactive protein in serum and follicular fluid during assisted reproductive cycles. Hum. Reprod. 20, 1266–1271.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wunder, D. M. , Mueller, M. D. , Birkhauser, M. H. , and Bersinger, N. A. (2005b). Steroids and protein markers in the follicular fluid as indicators of oocyte quality in patients with and without endometriosis. J. Assist. Reprod. Genet. 22, 257–264.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Xia, P. (1997). Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum. Reprod. 12, 1750–1755.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Xia, P. , and Younglai, E. V. (2000). Relationship between steroid concentrations in ovarian follicular fluid and oocyte morphology in patients undergoing intracytoplasmic sperm injection (ICSI) treatment. J. Reprod. Fertil. 118, 229–233.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yang, M. Y. , and Rajamahendran, R. (2002). Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro. Anim. Reprod. Sci. 70, 159–169.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yang, J. , Liu, X. , and Bhalla, K. (1997). Prevention of apoptosis by bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129–1136.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yu Ng, E. H. , Yeung, W. S. , Yee Lan Lau, E. , So, W. W. , and Ho, P. C. (2000). High serum oestradiol concentrations in fresh IVF cycles do not impair implantation and pregnancy rates in subsequent frozen–thawed embryo transfer cycles. Hum. Reprod. 15, 250–255.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Yuan, Y. Q. , Van Soom, A. , Leroy, J. L. , Dewulf, J. , Van Zeveren, A. , de Kruif, A. , and Peelman, L. J. (2005). Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 63, 2147–2163.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zeuner, A. , Muller, K. , Reguszynski, K. , and Jewgenow, K. (2003). Apoptosis within bovine follicular cells and its effect on oocyte development during in vitro maturation. Theriogenology 59, 1421–1433.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Zhang, X. , Jafari, N. , Barnes, R. B. , Confino, E. , Milad, M. , and Kazer, R. R. (2005). Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil. Steril. 83(Suppl. 1), 1169–1179.
Crossref | GoogleScholarGoogle Scholar | PubMed |