Semin Reprod Med 2012; 30(03): 199-213
DOI: 10.1055/s-0032-1311522
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

In Vitro Oocyte Maturation: Current Status

Daniela Nogueira
1   Laboratoire de Biologie de la Reproduction – IFREARES, Clinique Saint Jean Languedoc, Toulouse, France
,
Jean Clair Sadeu
2   Department of Obstetrics and Gynecology-Reproductive Biology, McMaster University, Hamilton, Ontario, Canada
,
Jacques Montagut
1   Laboratoire de Biologie de la Reproduction – IFREARES, Clinique Saint Jean Languedoc, Toulouse, France
› Author Affiliations
Further Information

Publication History

Publication Date:
14 May 2012 (online)

Abstract

Due to its numerous clinical applications, in vitro maturation (IVM) has emerged as a significant topic in the field of assisted reproduction. IVM of germinal vesicle breakdown/metaphase I and germinal vesicle stage oocytes collected from in vitro fertilization (IVF) superovulation cycles are commonly applied with unsatisfactory results. The biological aspect of this so-called rescue in vitro oocyte maturation greatly differs from the actual IVM practice. In the latter, immature oocytes are obtained from small antral follicles of unprimed or minimally stimulated cycles aiming to avoid ovarian hyperstimulation syndrome in high-risk patients or simply as an alternative to conventional IVF in normo-ovulatory patients. Over the past decade, cases reports regarding IVM have been sporadically reported, with ~25 peer-reviewed articles currently available. These studies present variable outcomes and deal with clinical approaches about selecting the most appropriate patient population that could benefit from IVM technology. Although some of the studies are encouraging, the vast majority includes small sample sizes, thus making the data rather inconclusive. As such there is a certain reserve in the IVF community to embark on treatment cycles for IVM in routine use. Laboratory parameters play an important role in the success of IVM, and research for optimal culture conditions is warranted. Existing data from newborns assure us that IVM may be a safe procedure provided in assisted reproductive technology. When optimized, it will serve, not only for infertile patients, but also as a more patient-friendly alternative than standard controlled ovarian stimulation to obtain oocytes for donation or preservation of fecundity.

 
  • References

  • 1 Pincus G, Enzmann EV. Comparative behavior of mammalian eggs in vivo and in vitro. J Exp Med 1935; 62 (5) 665-675
  • 2 Edwards RG. Maturation in vitro of human ovarian oöcytes. Lancet 1965; 2 (7419) 926-929
  • 3 Veeck LL, Wortham Jr JW, Witmyer J , et al. Maturation and fertilization of morphologically immature human oocytes in a program of in vitro fertilization. Fertil Steril 1983; 39 (5) 594-602
  • 4 Cha KY, Koo JJ, Ko JJ, Choi DH, Han SY, Yoon TK. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril 1991; 55 (1) 109-113
  • 5 Trounson A, Wood C, Kausche A. In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients. Fertil Steril 1994; 62 (2) 353-362
  • 6 Chian RC, Lim JH. In vitro maturation of immature oocytes for clinical application: past, today and tomorrow. In: Poncelet C, Sifer C, eds. Physiologie, pathologie et thérapie de la reproduction chez l'humain. Paris, France: Springer-Verlag; 2011: 461-471
  • 7 Jurema MW, Nogueira D. In vitro maturation of human oocytes for assisted reproduction. Fertil Steril 2006; 86 (5) 1277-1291
  • 8 Son WY, Tan SL. Laboratory and embryological aspects of hCG-primed in vitro maturation cycles for patients with polycystic ovaries. Hum Reprod Update 2010; 16 (6) 675-689
  • 9 De Vos A, Van de Velde H, Joris H, Van Steirteghem A. In-vitro matured metaphase-I oocytes have a lower fertilization rate but similar embryo quality as mature metaphase-II oocytes after intracytoplasmic sperm injection. Hum Reprod 1999; 14 (7) 1859-1863
  • 10 Braga DP, Figueira RdeC, Ferreira RC, Pasqualotto FF, Iaconelli Jr A, Borges Jr E. Contribution of in-vitro maturation in ovarian stimulation cycles of poor-responder patients. Reprod Biomed Online 2010; 20 (3) 335-340
  • 11 Coetzee K, Windt ML. Fertilization and pregnancy using metaphase I oocytes in an intracytoplasmic sperm injection program. J Assist Reprod Genet 1996; 13 (10) 768-771
  • 12 Chen SU, Chen HF, Lien YR, Ho HN, Chang HC, Yang YS. Schedule to inject in vitro matured oocytes may increase pregnancy after intracytoplasmic sperm injection. Arch Androl 2000; 44 (3) 197-205
  • 13 Strassburger D, Komarovsky D, Bern O , et al. The outcome of intracytoplasmic sperm injection in immature (MI) oocytes and rescued in vitro matured MII oocytes. Hum Reprod 2004; 19 (7) 1587-1590
  • 14 Balakier H, Sojecki A, Motamedi G, Librach C. Time-dependent capability of human oocytes for activation and pronuclear formation during metaphase II arrest. Hum Reprod 2004; 19 (4) 982-987
  • 15 Vanhoutte L, De Sutter P, Van der Elst J, Dhont M. Clinical benefit of metaphase I oocytes. Reprod Biol Endocrinol 2005; 3: 71
  • 16 Jee BC, Han SH, Moon JH, Suh CS, Kim SH ; Seoul National University College of Medicine Assisted Reproductive Technology (SMART) Study Group. Influence of well defined protein source on in vitro maturation of human oocyte: human follicular fluid versus human serum albumin. Fertil Steril 2008; 89 (2) 348-352
  • 17 Reichman DE, Politch J, Ginsburg ES, Racowsky C. Extended in vitro maturation of immature oocytes from stimulated cycles: an analysis of fertilization potential, embryo development, and reproductive outcomes. J Assist Reprod Genet 2010; 27 (7) 347-356
  • 18 Li M, Li Y, Ma SY , et al. Evaluation of the developmental potential of metaphase I oocytes from stimulated intracytoplasmic sperm injection cycles. Reprod Fertil Dev 2011; 23 (3) 433-437
  • 19 Combelles CM, Cekleniak NA, Racowsky C, Albertini DF. Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod 2002; 17 (4) 1006-1016
  • 20 Cekleniak NA, Combelles CM, Ganz DA, Fung J, Albertini DF, Racowsky C. A novel system for in vitro maturation of human oocytes. Fertil Steril 2001; 75 (6) 1185-1193
  • 21 Sutton ML, Gilchrist RB, Thompson JG. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum Reprod Update 2003; 9 (1) 35-48
  • 22 Curnow EC, Ryan JP, Saunders DM, Hayes ES. Primate model of metaphase I oocyte in vitro maturation and the effects of a novel glutathione donor on maturation, fertilization, and blastocyst development. Fertil Steril 2011; 95 (4) 1235-1240
  • 23 Yan J, Yang Y, Liying Y , et al. In vitro maturation of cumulus-partially enclosed immature human oocytes by priming with gonadotropin. Fertil Steril 2011; 96 (3) 629-634 , e1
  • 24 Nogueira D, Romero S, Vanhoutte L , et al. Oocyte in-vitro maturation. In: Gardner DK, Weissman A, Howles C, Shoham Z, eds. Assisted Reproductive Techniques: Laboratory and Clinical Perspectives. 3rd ed. London, UK: Martin Dunitz; 2004: 125-161
  • 25 Cha KY, Chian RC. Maturation in vitro of immature human oocytes for clinical use. Hum Reprod Update 1998; 4 (2) 103-120
  • 26 Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 2001; 121 (5) 647-653
  • 27 Zhu XM, Zhu YM, Xu CM, Qian YL, Jin F, Huang HF. Autologous mature follicular fluid: its role in in vitro maturation of human cumulus-removed oocytes. Fertil Steril 2008; 90 (4) 1094-1102
  • 28 Fatehi AN, Zeinstra EC, Kooij RV, Colenbrander B, Bevers MM. Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 2002; 57 (4) 1347-1355
  • 29 Strassburger D, Goldstein A, Friedler S , et al. The cytogenetic constitution of embryos derived from immature (metaphase I) oocytes obtained after ovarian hyperstimulation. Fertil Steril 2010; 94 (3) 971-978
  • 30 Raziel A, Schachter M, Strassburger D, Kasterstein E, Ron-El R, Friedler S. In vivo maturation of oocytes by extending the interval between human chorionic gonadotropin administration and oocyte retrieval. Fertil Steril 2006; 86 (3) 583-587
  • 31 Abdalla HI, Ah-Moye M, Brinsden P, Howe DL, Okonofua F, Craft I. The effect of the dose of human chorionic gonadotropin and the type of gonadotropin stimulation on oocyte recovery rates in an in vitro fertilization program. Fertil Steril 1987; 48 (6) 958-963
  • 32 Gulekli B, Buckett WM, Chian RC, Child TJ, Abdul-Jalil AK, Tan SL. Randomized, controlled trial of priming with 10,000.  IU versus 20,000 IU of human chorionic gonadotropin in women with polycystic ovary syndrome who are undergoing in vitro maturation. Fertil Steril 2004; 82 (5) 1458-1459
  • 33 Combelles CM, Albertini DF, Racowsky C. Distinct microtubule and chromatin characteristics of human oocytes after failed in-vivo and in-vitro meiotic maturation. Hum Reprod 2003; 18 (10) 2124-2130
  • 34 Heindryckx B, Lierman S, Combelles CM, Cuvelier CA, Gerris J, De Sutter P. Aberrant spindle structures responsible for recurrent human metaphase I oocyte arrest with attempts to induce meiosis artificially. Hum Reprod 2011; 26 (4) 791-800
  • 35 Nogueira D, Staessen C, Van de Velde H, Van Steirteghem A. Nuclear status and cytogenetics of embryos derived from in vitro-matured oocytes. Fertil Steril 2000; 74 (2) 295-298
  • 36 DeScisciolo C, Wright DL, Mayer JF, Gibbons W, Muasher SJ, Lanzendorf SE. Human embryos derived from in vitro and in vivo matured oocytes: analysis for chromosomal abnormalities and nuclear morphology. J Assist Reprod Genet 2000; 17 (5) 284-292
  • 37 Lundin K, Ziebe S, Bergh C , et al; Joan-Carles Arce for the CEMAS I Study Group. Effect of rescuing donated immature human oocytes derived after FSH/hCG stimulation following in vitro culture with or without Follicular Fluid Meiosis Activating Sterol (FF-MAS)—an embryo chromosomal and morphological analysis. J Assist Reprod Genet 2007; 24 (2–3) 87-90
  • 38 Smitz J, Picton HM, Platteau P , et al. Principal findings from a multicenter trial investigating the safety of follicular-fluid meiosis-activating sterol for in vitro maturation of human cumulus-enclosed oocytes. Fertil Steril 2007; 87 (4) 949-964
  • 39 Garcia-Cruz R, Casanovas A, Brieño-Enríquez M , et al. Cytogenetic analyses of human oocytes provide new data on non-disjunction mechanisms and the origin of trisomy 16. Hum Reprod 2010; 25 (1) 179-191
  • 40 Clyde JM, Hogg JE, Rutherford AJ, Picton HM. Karyotyping of human metaphase II oocytes by multifluor fluorescence in situ hybridization. Fertil Steril 2003; 80 (4) 1003-1011
  • 41 Magli MC, Ferraretti AP, Crippa A, Lappi M, Feliciani E, Gianaroli L. First meiosis errors in immature oocytes generated by stimulated cycles. Fertil Steril 2006; 86 (3) 629-635
  • 42 Jones GM, Cram DS, Song B , et al. Gene expression profiling of human oocytes following in vivo or in vitro maturation. Hum Reprod 2008; 23 (5) 1138-1144
  • 43 Goud PT, Goud AP, Qian C , et al. In-vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum Reprod 1998; 13 (6) 1638-1644
  • 44 Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 2008; 14 (2) 159-177
  • 45 Ben-Ami I, Komsky A, Bern O, Kasterstein E, Komarovsky D, Ron-El R. In vitro maturation of human germinal vesicle-stage oocytes: role of epidermal growth factor-like growth factors in the culture medium. Hum Reprod 2011; 26 (1) 76-81
  • 46 de Matos DG, Herrera C, Cortvrindt R , et al. Cysteamine supplementation during in vitro maturation and embryo culture: a useful tool for increasing the efficiency of bovine in vitro embryo production. Mol Reprod Dev 2002; 62 (2) 203-209
  • 47 Nogueira D. Oocyte under Arrest: Effect of Phosphodiesterase 3 Inhibitor on Oocyte Meiosis and Development [PhD thesis]. Brussels, Belgium: Vrije Universiteit Brussel; 2005
  • 48 Combelles CM, Fissore RA, Albertini DF, Racowsky C. In vitro maturation of human oocytes and cumulus cells using a co-culture three-dimensional collagen gel system. Hum Reprod 2005; 20 (5) 1349-1358
  • 49 Vanhoutte L, Nogueira D, De Sutter P. Prematuration of human denuded oocytes in a three-dimensional co-culture system: effects on meiosis progression and developmental competence. Hum Reprod 2009; 24 (3) 658-669
  • 50 Nogueira D, Albano C, Adriaenssens T , et al. Human oocytes reversibly arrested in prophase I by phosphodiesterase type 3 inhibitor in vitro. Biol Reprod 2003; 69 (3) 1042-1052
  • 51 Nogueira D, Ron-El R, Friedler S , et al. Meiotic arrest in vitro by phosphodiesterase 3-inhibitor enhances maturation capacity of human oocytes and allows subsequent embryonic development. Biol Reprod 2006; 74 (1) 177-184
  • 52 Vanhoutte L, Nogueira D, Dumortier F, De Sutter P. Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor. Hum Reprod 2009; 24 (8) 1946-1959
  • 53 Qiao J, Feng HL. Extra- and intra-ovarian factors in polycystic ovary syndrome: impact on oocyte maturation and embryo developmental competence. Hum Reprod Update 2011; 17 (1) 17-33
  • 54 Jaroudi KA, Hollanders JM, Sieck UV, Roca GL, El-Nour AM, Coskun S. Pregnancy after transfer of embryos which were generated from in-vitro matured oocytes. Hum Reprod 1997; 12 (4) 857-859
  • 55 Jaroudi KA, Hollanders JM, Elnour AM, Roca GL, Atared AM, Coskun S. Embryo development and pregnancies from in-vitro matured and fertilized human oocytes. Hum Reprod 1999; 14 (7) 1749-1751
  • 56 Chen J, Qian Y, Feng T , et al. Delivery after transfer of frozen-thawed embryos from in vitro-matured oocytes in a woman at risk for ovarian hyperstimulation syndrome. J Reprod Dev 2007; 53 (2) 449-453
  • 57 Lim K, Lee W, Lim J. IVM after interruption of COH for the prevention of OHSS. Fertil Steril 2005; 84: S84-S85
  • 58 Sirard MA. Follicle environment and quality of in vitro matured oocytes. J Assist Reprod Genet 2011; 28 (6) 483-488
  • 59 Chian RC, Buckett WM, Tulandi T, Tan SL. Prospective randomized study of human chorionic gonadotrophin priming before immature oocyte retrieval from unstimulated women with polycystic ovarian syndrome. Hum Reprod 2000; 15 (1) 165-170
  • 60 Son WY, Tan SL. Laboratory and embryological aspects of hCG-primed in vitro maturation cycles for patients with polycystic ovaries. Hum Reprod Update 2010; 16 (6) 675-689
  • 61 Le Du A, Kadoch IJ, Bourcigaux N , et al. In vitro oocyte maturation for the treatment of infertility associated with polycystic ovarian syndrome: the French experience. Hum Reprod 2005; 20 (2) 420-424
  • 62 Söderström-Anttila V, Mäkinen S, Tuuri T, Suikkari AM. Favourable pregnancy results with insemination of in vitro matured oocytes from unstimulated patients. Hum Reprod 2005; 20 (6) 1534-1540
  • 63 Ge HS, Huang XF, Zhang W, Zhao JZ, Lin JJ, Zhou W. Exposure to human chorionic gonadotropin during in vitro maturation does not improve the maturation rate and developmental potential of immature oocytes from patients with polycystic ovary syndrome. Fertil Steril 2008; 89 (1) 98-103
  • 64 Dal Canto MB, Mignini Renzini M, Brambillasca F , et al. IVM—the first choice for IVF in Italy. Reprod Biomed Online 2006; 13 (2) 159-165
  • 65 Cha KY, Han SY, Chung HM , et al. Pregnancies and deliveries after in vitro maturation culture followed by in vitro fertilization and embryo transfer without stimulation in women with polycystic ovary syndrome. Fertil Steril 2000; 73 (5) 978-983
  • 66 Cha KY, Chung HM, Lee DR , et al. Obstetric outcome of patients with polycystic ovary syndrome treated by in vitro maturation and in vitro fertilization-embryo transfer. Fertil Steril 2005; 83 (5) 1461-1465
  • 67 Child TJ, Abdul-Jalil AK, Gulekli B, Tan SL. In vitro maturation and fertilization of oocytes from unstimulated normal ovaries, polycystic ovaries, and women with polycystic ovary syndrome. Fertil Steril 2001; 76 (5) 936-942
  • 68 Child TJ, Phillips SJ, Abdul-Jalil AK, Gulekli B, Tan SL. A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovaries. Obstet Gynecol 2002; 100 (4) 665-670
  • 69 Son WY, Lee SY, Yoon SH, Lim JH. Pregnancies and deliveries after transfer of human blastocysts derived from in vitro matured oocytes in in vitro maturation cycles. Fertil Steril 2007; 87 (6) 1491-1493
  • 70 Lin YH, Hwang JL, Huang LW , et al. Combination of FSH priming and hCG priming for in-vitro maturation of human oocytes. Hum Reprod 2003; 18 (8) 1632-1636
  • 71 Son WY, Chung JT, Herrero B , et al. Selection of the optimal day for oocyte retrieval based on the diameter of the dominant follicle in hCG-primed in vitro maturation cycles. Hum Reprod 2008; a; 23 (12) 2680-2685
  • 72 Benkhalifa M, Demirol A, Ménézo Y , et al. Natural cycle IVF and oocyte in-vitro maturation in polycystic ovary syndrome: a collaborative prospective study. Reprod Biomed Online 2009; 18 (1) 29-36
  • 73 Mikkelsen AL, Lindenberg S. Benefit of FSH priming of women with PCOS to the in vitro maturation procedure and the outcome: a randomized prospective study. Reproduction 2001; 122 (4) 587-592
  • 74 Son WY, Yoon SH, Lim JH. Effect of gonadotrophin priming on in-vitro maturation of oocytes collected from women at risk of OHSS. Reprod Biomed Online 2006; 13 (3) 340-348
  • 75 Wei Z, Cao Y, Cong L, Zhou P, Zhang Z, Li J. Effect of metformin pretreatment on pregnancy outcome of in vitro matured oocytes retrieved from women with polycystic ovary syndrome. Fertil Steril 2008; 90 (4) 1149-1154
  • 76 Fadini R, Colpi E, Mignini Renzini M , et al. Outcome of cycles of oocyte in vitro maturation requiring testicular sperm extraction for nonobstructive azoospermia. Fertil Steril 2011; 96 (2) 321-323
  • 77 Fridén B, Hreinsson J, Hovatta O. Birth of a healthy infant after in vitro oocyte maturation and ICSI in a woman with diminished ovarian response: case report. Hum Reprod 2005; 20 (9) 2556-2558
  • 78 Holzer H, Scharf E, Chian RC, Demirtas E, Buckett W, Tan SL. In vitro maturation of oocytes collected from unstimulated ovaries for oocyte donation. Fertil Steril 2007; 88 (1) 62-67
  • 79 Mikkelsen AL, Smith S, Lindenberg S. Impact of oestradiol and inhibin A concentrations on pregnancy rate in in-vitro oocyte maturation. Hum Reprod 2000; 15 (8) 1685-1690
  • 80 Mikkelsen AL, Andersson AM, Skakkebaek NE, Lindenberg S. Basal concentrations of oestradiol may predict the outcome of in-vitro maturation in regularly menstruating women. Hum Reprod 2001; b; 16 (5) 862-867
  • 81 Yoon HG, Yoon SH, Son WY , et al. Pregnancies resulting from in vitro matured oocytes collected from women with regular menstrual cycle. J Assist Reprod Genet 2001; 18 (6) 325-329
  • 82 Fadini R, Dal Canto MB, Renzini MM , et al. Predictive factors in in-vitro maturation in unstimulated women with normal ovaries. Reprod Biomed Online 2009; 18 (2) 251-261
  • 83 Fadini R, Dal Canto MB, Mignini Renzini M , et al. Effect of different gonadotrophin priming on IVM of oocytes from women with normal ovaries: a prospective randomized study. Reprod Biomed Online 2009; 19 (3) 343-351
  • 84 Mikkelsen AL, Smith SD, Lindenberg S. In-vitro maturation of human oocytes from regularly menstruating women may be successful without follicle stimulating hormone priming. Hum Reprod 1999; 14 (7) 1847-1851
  • 85 Lim JH, Yang SH, Xu Y, Yoon SH, Chian RC. Selection of patients for natural cycle in vitro fertilization combined with in vitro maturation of immature oocytes. Fertil Steril 2009; 91 (4) 1050-1055
  • 86 Yang SH, Son WY, Yoon SH, Ko Y, Lim JH. Correlation between in vitro maturation and expression of LH receptor in cumulus cells of the oocytes collected from PCOS patients in HCG-primed IVM cycles. Hum Reprod 2005; 20 (8) 2097-2103
  • 87 Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 2004; 303 (5658) 682-684
  • 88 Ashkenazi H, Cao X, Motola S, Popliker M, Conti M, Tsafriri A. EGF-like growth factors: endogenous mediators of the ovulatory response. Endocrinology 2005; 146: 77-84
  • 89 Son WY, Lee SY, Lim JH. Fertilization, cleavage and blastocyst development according to the maturation timing of oocytes in in vitro maturation cycles. Hum Reprod 2005; 20 (11) 3204-3207
  • 90 Nogueira D, Prat L, Degoy J, Bonald F, Montagut J. Rates of maturation in PCO and non-PCO patients when a mild gonadotropin-stimulation protocol is applied in IVM cycles. Paper presented at: Annual Meeting of European Society of Human Reproduction and Embryology; June 27, 2010; Rome, Italy
  • 91 Wynn P, Picton HM, Krapez JA, Rutherford AJ, Balen AH, Gosden RG. Pretreatment with follicle stimulating hormone promotes the numbers of human oocytes reaching metaphase II by in-vitro maturation. Hum Reprod 1998; 13 (11) 3132-3138
  • 92 Son WY, Chung JT, Chian RC , et al. A 38 h interval between hCG priming and oocyte retrieval increases in vivo and in vitro oocyte maturation rate in programmed IVM cycles. Hum Reprod 2008; 23 (9) 2010-2016
  • 93 Hreinsson J, Rosenlund B, Fridén B , et al. Recombinant LH is equally effective as recombinant hCG in promoting oocyte maturation in a clinical in-vitro maturation programme: a randomized study. Hum Reprod 2003; 18 (10) 2131-2136
  • 94 Anderiesz C, Fong CY, Bongso A, Trounson AO. Regulation of human and mouse oocyte maturation in vitro with 6-dimethylaminopurine. Hum Reprod 2000; 15 (2) 379-388
  • 95 Roberts R, Iatropoulou A, Ciantar D , et al. Follicle-stimulating hormone affects metaphase I chromosome alignment and increases aneuploidy in mouse oocytes matured in vitro. Biol Reprod 2005; 72 (1) 107-118
  • 96 de Araujo CH, Nogueira D, de Araujo MC, Martins Wde P, Ferriani RA, dos Reis RM. Supplemented tissue culture medium 199 is a better medium for in vitro maturation of oocytes from women with polycystic ovary syndrome women than human tubal fluid. Fertil Steril 2009; 91 (2) 509-513
  • 97 Mikkelsen AL, Høst E, Blaabjerg J, Lindenberg S. Maternal serum supplementation in culture medium benefits maturation of immature human oocytes. Reprod Biomed Online 2001; 3 (2) 112-116
  • 98 Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 2008; 14 (2) 159-177
  • 99 Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod 2010; 25 (12) 2999-3011
  • 100 Smitz JE, Thompson JG, Gilchrist RB. The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med 2011; 29 (1) 24-37
  • 101 Combelles CM, Gupta S, Agarwal A. Could oxidative stress influence the in-vitro maturation of oocytes?. [review] Reprod Biomed Online 2009; 18 (6) 864-880
  • 102 Shalgi R, Kraicer PF, Soferman N. Gases and electrolytes of human follicular fluid. J Reprod Fertil 1972; 28 (3) 335-340
  • 103 Fraser IS, Baird DT, Cockburn F. Ovarian venous blood PO 2, PCO 2 and pH in women. J Reprod Fertil 1973; 33 (1) 11-17
  • 104 Fischer B, Künzel W, Kleinstein J, Gips H. Oxygen tension in follicular fluid falls with follicle maturation. Eur J Obstet Gynecol Reprod Biol 1992; 43 (1) 39-43
  • 105 Van Blerkom J. Epigenetic influences on oocyte developmental competence: perifollicular vascularity and intrafollicular oxygen. J Assist Reprod Genet 1998; 15 (5) 226-234
  • 106 Huey S, Abuhamad A, Barroso G , et al. Perifollicular blood flow Doppler indices, but not follicular pO2, pCO2, or pH, predict oocyte developmental competence in in vitro fertilization. Fertil Steril 1999; 72 (4) 707-712
  • 107 Iwamoto M, Onishi A, Fuchimoto D , et al. Low oxygen tension during in vitro maturation of porcine follicular oocytes improves parthenogenetic activation and subsequent development to the blastocyst stage. Theriogenology 2005; 63 (5) 1277-1289
  • 108 Park JI, Hong JY, Yong HY, Hwang WS, Lim JM, Lee ES. High oxygen tension during in vitro oocyte maturation improves in vitro development of porcine oocytes after fertilization. Anim Reprod Sci 2005; 87 (1–2) 133-141
  • 109 Preis KA, Seidel Jr GE, Gardner DK. Reduced oxygen concentration improves the developmental competence of mouse oocytes following in vitro maturation. Mol Reprod Dev 2007; 74 (7) 893-903
  • 110 Banwell KM, Lane M, Russell DL, Kind KL, Thompson JG. Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum Reprod 2007; 22 (10) 2768-2775