Subscribe to RSS
DOI: 10.1055/s-0035-1546423
Optimal Human Embryo Culture
Publication History
Publication Date:
03 March 2015 (online)
![](https://www.thieme-connect.de/media/srm/201502/lookinside/thumbnails/10.1055-s-0035-1546423-1.jpg)
Abstract
A large contributor to success during in vitro fertilization (IVF) lies in the processes occurring within the IVF laboratory. These processes make up the “culture system.” This system entails numerous procedures and technical steps that must be optimized to produce a competent embryo. Notably, variations exist between programs that include differences in patient population, clinical stimulation, and other factors. Thus, a single “optimal” culture system to be utilized between all laboratories is likely not feasible. Rather, laboratory procedures should be optimized based on an individual laboratory's performance. That being said, within the scientific literature, there are key components, approaches, and techniques within the culture system that have been shown to be superior to alternatives. These key components important in improving embryo culture are discussed.
-
References
- 1 Hyun CS, Cha JH, Son WY, Yoon SH, Kim KA, Lim JH. Optimal ICSI timing after the first polar body extrusion in in vitro matured human oocytes. Hum Reprod 2007; 22 (7) 1991-1995
- 2 Rienzi L, Ubaldi F, Anniballo R, Cerulo G, Greco E. Preincubation of human oocytes may improve fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod 1998; 13 (4) 1014-1019
- 3 Hassan HA. Cumulus cell contribution to cytoplasmic maturation and oocyte developmental competence in vitro. J Assist Reprod Genet 2001; 18 (10) 539-543
- 4 Ebner T, Moser M, Shebl O, Sommergruber M, Yaman C, Tews G. Blood clots in the cumulus-oocyte complex predict poor oocyte quality and post-fertilization development. Reprod Biomed Online 2008; 16 (6) 801-807
- 5 Daya S, Kohut J, Gunby J, Younglai E. Influence of blood clots in the cumulus complex on oocyte fertilization and cleavage. Hum Reprod 1990; 5 (6) 744-746
- 6 Van de Velde H, De Vos A, Joris H, Nagy ZP, Van Steirteghem AC. Effect of timing of oocyte denudation and micro-injection on survival, fertilization and embryo quality after intracytoplasmic sperm injection. Hum Reprod 1998; 13 (11) 3160-3164
- 7 Rienzi L, Ubaldi F, Martinez F , et al. Relationship between meiotic spindle location with regard to the polar body position and oocyte developmental potential after ICSI. Hum Reprod 2003; 18 (6) 1289-1293
- 8 Taylor TH, Wright G, Jones-Colon S, Mitchell-Leef D, Kort HI, Nagy ZP. Comparison of ICSI and conventional IVF in patients with increased oocyte immaturity. Reprod Biomed Online 2008; 17 (1) 46-52
- 9 Evison M, Pretty C, Taylor E, Franklin C. Human recombinant hyaluronidase (Cumulase) improves intracytoplasmic sperm injection survival and fertilization rates. Reprod Biomed Online 2009; 18 (6) 811-814
- 10 Taylor TH, Elliott T, Colturato LF, Straub RJ, Mitchell-Leef D, Nagy ZP. Comparison of bovine- and recombinant human-derived hyaluronidase with regard to fertilization rates and embryo morphology in a sibling oocyte model: a prospective, blinded, randomized study. Fertil Steril 2006; 85 (5) 1544-1546
- 11 De Vos A, Van Landuyt L, Van Ranst H , et al. Randomized sibling-oocyte study using recombinant human hyaluronidase versus bovine-derived Sigma hyaluronidase in ICSI patients. Hum Reprod 2008; 23 (8) 1815-1819
- 12 Sakkas D. Novel technologies for selecting the best sperm for in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril 2013; 99 (4) 1023-1029
- 13 Said TM, Land JA. Effects of advanced selection methods on sperm quality and ART outcome: a systematic review. Hum Reprod Update 2011; 17 (6) 719-733
- 14 Jayaraman V, Upadhya D, Narayan PK, Adiga SK. Sperm processing by swim-up and density gradient is effective in elimination of sperm with DNA damage. J Assist Reprod Genet 2012; 29 (6) 557-563
- 15 Teixeira DM, Barbosa MA, Ferriani RA , et al. Regular (ICSI) versus ultra-high magnification (IMSI) sperm selection for assisted reproduction. Cochrane Database Syst Rev 2013; 7: CD010167
- 16 Leandri RD, Gachet A, Pfeffer J , et al. Is intracytoplasmic morphologically selected sperm injection (IMSI) beneficial in the first ART cycle? A multicentric randomized controlled trial. Andrology 2013; 1 (5) 692-697
- 17 De Vos A, Van de Velde H, Bocken G , et al. Does intracytoplasmic morphologically selected sperm injection improve embryo development? A randomized sibling-oocyte study. Hum Reprod 2013; 28 (3) 617-626
- 18 Delaroche L, Yazbeck C, Gout C, Kahn V, Oger P, Rougier N. Intracytoplasmic morphologically selected sperm injection (IMSI) after repeated IVF or ICSI failures: a prospective comparative study. Eur J Obstet Gynecol Reprod Biol 2013; 167 (1) 76-80
- 19 Worrilow KC, Eid S, Woodhouse D , et al. Use of hyaluronan in the selection of sperm for intracytoplasmic sperm injection (ICSI): significant improvement in clinical outcomes—multicenter, double-blinded and randomized controlled trial. Hum Reprod 2013; 28 (2) 306-314
- 20 Majumdar G, Majumdar A. A prospective randomized study to evaluate the effect of hyaluronic acid sperm selection on the intracytoplasmic sperm injection outcome of patients with unexplained infertility having normal semen parameters. J Assist Reprod Genet 2013; 30 (11) 1471-1475
- 21 Pool TB, Schoolfield J, Han D. Human embryo culture media comparisons. Methods Mol Biol 2012; 912: 367-386
- 22 Mantikou E, Youssef MA, van Wely M , et al. Embryo culture media and IVF/ICSI success rates: a systematic review. Hum Reprod Update 2013; 19 (3) 210-220
- 23 Mauri AL, Petersen CG, Baruffi RL, Franco Jr JG. A prospective, randomized comparison of two commercial media for ICSI and embryo culture. J Assist Reprod Genet 2001; 18 (7) 378-381
- 24 Ben-Yosef D, Amit A, Azem F , et al. Prospective randomized comparison of two embryo culture systems: P1 medium by Irvine Scientific and the Cook IVF Medium. J Assist Reprod Genet 2004; 21 (8) 291-295
- 25 Van Langendonckt A, Demylle D, Wyns C, Nisolle M, Donnez J. Comparison of G1.2/G2.2 and Sydney IVF cleavage/blastocyst sequential media for the culture of human embryos: a prospective, randomized, comparative study. Fertil Steril 2001; 76 (5) 1023-1031
- 26 Balaban B, Urman B. Comparison of two sequential media for culturing cleavage-stage embryos and blastocysts: embryo characteristics and clinical outcome. Reprod Biomed Online 2005; 10 (4) 485-491
- 27 Zollner KP, Zollner U, Schneider M, Dietl J, Steck T. Comparison of two media for sequential culture after IVF and ICSI shows no differences in pregnancy rates: a randomized trial. Med Sci Monit 2004; 10 (1) CR1-CR7
- 28 Hambiliki F, Sandell P, Yaldir F, Stavreus-Evers A. A prospective randomized sibling-oocyte study of two media systems for culturing cleavage-stage embryos-impact on fertilization rate. J Assist Reprod Genet 2011; 28 (4) 335-341
- 29 Sifer C, Handelsman D, Grange E , et al. An auto-controlled prospective comparison of two embryos culture media (G III series versus ISM) for IVF and ICSI treatments. J Assist Reprod Genet 2009; 26 (11-12) 575-581
- 30 Paternot G, Debrock S, D'Hooghe TM, Spiessens C. Early embryo development in a sequential versus single medium: a randomized study. Reprod Biol Endocrinol 2010; 8: 83
- 31 Sepúlveda S, Garcia J, Arriaga E, Diaz J, Noriega-Portella L, Noriega-Hoces L. In vitro development and pregnancy outcomes for human embryos cultured in either a single medium or in a sequential media system. Fertil Steril 2009; 91 (5) 1765-1770
- 32 Basile N, Morbeck D, García-Velasco J, Bronet F, Meseguer M. Type of culture media does not affect embryo kinetics: a time-lapse analysis of sibling oocytes. Hum Reprod 2013; 28 (3) 634-641
- 33 Ciray HN, Aksoy T, Goktas C, Ozturk B, Bahceci M. Time-lapse evaluation of human embryo development in single versus sequential culture media—a sibling oocyte study. J Assist Reprod Genet 2012; 29 (9) 891-900
- 34 Reed ML, Hamic A, Thompson DJ, Caperton CL. Continuous uninterrupted single medium culture without medium renewal versus sequential media culture: a sibling embryo study. Fertil Steril 2009; 92 (5) 1783-1786
- 35 Wales RG, Whittingham DG. Decomposition of sodium pyruvate in culture media stored at 5 degrees C and its effects on the development of the preimplantation mouse embryo. J Reprod Fertil 1971; 24 (1) 126
- 36 Stewart-Savage J, Bavister BD. Deterioration of stored culture media as monitored by a sperm motility bioassay. J In Vitro Fert Embryo Transf 1988; 5 (2) 76-80
- 37 Edwards LJ, Williams DA, Gardner DK. Intracellular pH of the preimplantation mouse embryo: effects of extracellular pH and weak acids. Mol Reprod Dev 1998; 50 (4) 434-442
- 38 Carrillo AJ, Lane B, Pridman DD , et al. Improved clinical outcomes for in vitro fertilization with delay of embryo transfer from 48 to 72 hours after oocyte retrieval: use of glucose- and phosphate-free media. Fertil Steril 1998; 69 (2) 329-334
- 39 Quinn P, Moinipanah R, Steinberg JM, Weathersbee PS. Successful human in vitro fertilization using a modified human tubal fluid medium lacking glucose and phosphate ions. Fertil Steril 1995; 63 (4) 922-924
- 40 Lane M. Mechanisms for managing cellular and homeostatic stress in vitro. Theriogenology 2001; 55 (1) 225-236
- 41 Gardner DK, Lane M. Alleviation of the ‘2-cell block’ and development to the blastocyst of CF1 mouse embryos: role of amino acids, EDTA and physical parameters. Hum Reprod 1996; 11 (12) 2703-2712
- 42 McKiernan SH, Clayton MK, Bavister BD. Analysis of stimulatory and inhibitory amino acids for development of hamster one-cell embryos in vitro. Mol Reprod Dev 1995; 42 (2) 188-199
- 43 Lane M, Gardner DK. Differential regulation of mouse embryo development and viability by amino acids. J Reprod Fertil 1997; 109 (1) 153-164
- 44 Lane M, Hooper K, Gardner DK. Effect of essential amino acids on mouse embryo viability and ammonium production. J Assist Reprod Genet 2001; 18 (9) 519-525
- 45 Devreker F, Winston RM, Hardy K. Glutamine improves human preimplantation development in vitro. Fertil Steril 1998; 69 (2) 293-299
- 46 Devreker F, Van den Bergh M, Biramane J, Winston RL, Englert Y, Hardy K. Effects of taurine on human embryo development in vitro. Hum Reprod 1999; 14 (9) 2350-2356
- 47 Hammer MA, Kolajova M, Léveillé M, Claman P, Baltz JM. Glycine transport by single human and mouse embryos. Hum Reprod 2000; 15 (2) 419-426
- 48 Biggers JD, McGinnis LK, Lawitts JA. Enhanced effect of glycyl-L-glutamine on mouse preimplantation embryos in vitro. Reprod Biomed Online 2004; 9 (1) 59-69
- 49 Summers MC, McGinnis LK, Lawitts JA, Biggers JD. Mouse embryo development following IVF in media containing either L-glutamine or glycyl-L-glutamine. Hum Reprod 2005; 20 (5) 1364-1371
- 50 Lane M, Gardner DK. Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation, gene expression and subsequently alters fetal development in the mouse. Biol Reprod 2003; 69 (4) 1109-1117
- 51 Virant-Klun I, Tomazevic T, Vrtacnik-Bokal E, Vogler A, Krsnik M, Meden-Vrtovec H. Increased ammonium in culture medium reduces the development of human embryos to the blastocyst stage. Fertil Steril 2006; 85 (2) 526-528
- 52 Kastrop PM, de Graaf-Miltenburg LA, Gutknecht DR, Weima SM. Microbial contamination of embryo cultures in an ART laboratory: sources and management. Hum Reprod 2007; 22 (8) 2243-2248
- 53 Magli MC, Gianaroli L, Fiorentino A, Ferraretti AP, Fortini D, Panzella S. Improved cleavage rate of human embryos cultured in antibiotic-free medium. Hum Reprod 1996; 11 (7) 1520-1524
- 54 Zhou H, McKiernan SH, Ji W, Bavister BD. Effect of antibiotics on development in vitro of hamster pronucleate ova. Theriogenology 2000; 54 (7) 999-1006
- 55 Liu J, Tang S, Xu W, Wang Y, Yin B, Zhang Y. Detrimental effects of antibiotics on mouse embryos in chromatin integrity, apoptosis and expression of zygotically activated genes. Zygote 2011; 19 (2) 137-145
- 56 Zhu J, Li M, Chen L, Liu P, Qiao J. The protein source in embryo culture media influences birthweight: a comparative study between G1 v5 and G1-PLUS v5. Hum Reprod 2014; 29 (7) 1387-1392
- 57 Leonard PH, Charlesworth MC, Benson L, Walker DL, Fredrickson JR, Morbeck DE. Variability in protein quality used for embryo culture: embryotoxicity of the stabilizer octanoic acid. Fertil Steril 2013; 100 (2) 544-549
- 58 Morbeck DE, Paczkowski M, Fredrickson JR , et al. Composition of protein supplements used for human embryo culture. J Assist Reprod Genet 2014; 31 (12) 1703-1711
- 59 Meintjes M. Media composition: macromolecules and embryo growth. Methods Mol Biol 2012; 912: 107-127
- 60 Dyrlund TF, Kirkegaard K, Poulsen ET , et al. Unconditioned commercial embryo culture media contain a large variety of non-declared proteins: a comprehensive proteomics analysis. Hum Reprod 2014; 29 (11) 2421-2430
- 61 Borini A, Bulletti C, Cattoli M , et al. Use of recombinant leukemia inhibitory factor in embryo implantation. Ann N Y Acad Sci 1997; 828: 157-161
- 62 Sjöblom C, Wikland M, Robertson SA. Granulocyte-macrophage colony-stimulating factor promotes human blastocyst development in vitro. Hum Reprod 1999; 14 (12) 3069-3076
- 63 O'Neill C, Ryan JP, Collier M, Saunders DM, Ammit AJ, Pike IL. Supplementation of in-vitro fertilisation culture medium with platelet activating factor. Lancet 1989; 2 (8666) 769-772
- 64 Hegde A, Behr B. Media composition: growth factors. Methods Mol Biol 2012; 912: 177-198
- 65 Weathersbee PS, Pool TB, Ord T. Synthetic serum substitute (SSS): a globulin-enriched protein supplement for human embryo culture. J Assist Reprod Genet 1995; 12 (6) 354-360
- 66 Pool TB, Martin JE. High continuing pregnancy rates after in vitro fertilization-embryo transfer using medium supplemented with a plasma protein fraction containing alpha- and beta-globulins. Fertil Steril 1994; 61 (4) 714-719
- 67 Schneider EG, Hayslip CC. Globulin-enriched protein supplements shorten the pre-compaction mitotic interval and promote hatching of murine embryos. Am J Reprod Immunol 1996; 36 (2) 101-106
- 68 Desai NN, Sheean LA, Martin D , et al. Clinical experience with synthetic serum substitute as a protein supplement in IVF culture media: a retrospective study. J Assist Reprod Genet 1996; 13 (1) 23-31
- 69 Tucker KE, Hurst BS, Guadagnoli S , et al. Evaluation of synthetic serum substitute versus serum as protein supplementation for mouse and human embryo culture. J Assist Reprod Genet 1996; 13 (1) 32-37
- 70 Meintjes M, Chantilis SJ, Ward DC , et al. A randomized controlled study of human serum albumin and serum substitute supplement as protein supplements for IVF culture and the effect on live birth rates. Hum Reprod 2009; 24 (4) 782-789
- 71 Bungum M, Humaidan P, Bungum L. Recombinant human albumin as protein source in culture media used for IVF: a prospective randomized study. Reprod Biomed Online 2002; 4 (3) 233-236
- 72 Ben-Yosef D, Yovel I, Schwartz T, Azem F, Lessing JB, Amit A. Increasing synthetic serum substitute (SSS) concentrations in P1 glucose/phosphate-free medium improves implantation rate: a comparative study. J Assist Reprod Genet 2001; 18 (11) 588-592
- 73 Morbeck DE, Khan Z, Barnidge DR, Walker DL. Washing mineral oil reduces contaminants and embryotoxicity. Fertil Steril 2010; 94 (7) 2747-2752
- 74 Otsuki J, Nagai Y, Chiba K. Damage of embryo development caused by peroxidized mineral oil and its association with albumin in culture. Fertil Steril 2009; 91 (5) 1745-1749
- 75 Otsuki J, Nagai Y, Chiba K. Peroxidation of mineral oil used in droplet culture is detrimental to fertilization and embryo development. Fertil Steril 2007; 88 (3) 741-743
- 76 Hughes PM, Morbeck DE, Hudson SB, Fredrickson JR, Walker DL, Coddington CC. Peroxides in mineral oil used for in vitro fertilization: defining limits of standard quality control assays. J Assist Reprod Genet 2010; 27 (2–3) 87-92
- 77 Lane M, Lyons EA, Bavister BD. Cryopreservation reduces the ability of hamster 2-cell embryos to regulate intracellular pH. Hum Reprod 2000; 15 (2) 389-394
- 78 Zander-Fox DL, Mitchell M, Thompson JG, Lane M. Alterations in mouse embryo intracellular pH by DMO during culture impair implantation and fetal growth. Reprod Biomed Online 2010; 21 (2) 219-229
- 79 Squirrell JM, Lane M, Bavister BD. Altering intracellular pH disrupts development and cellular organization in preimplantation hamster embryos. Biol Reprod 2001; 64 (6) 1845-1854
- 80 Phillips KP, Léveillé MC, Claman P, Baltz JM. Intracellular pH regulation in human preimplantation embryos. Hum Reprod 2000; 15 (4) 896-904
- 81 Phillips KP, Petrunewich MA, Collins JL, Baltz JM. The intracellular pH-regulatory HCO3-/Cl- exchanger in the mouse oocyte is inactivated during first meiotic metaphase and reactivated after egg activation via the MAP kinase pathway. Mol Biol Cell 2002; 13 (11) 3800-3810
- 82 Quinn P. Culture systems: sequential. Methods Mol Biol 2012; 912: 211-230
- 83 Hentemann M, Mousavi K, Bertheussen K. Differential pH in embryo culture. Fertil Steril 2011; 95 (4) 1291-1294
- 84 Swain JE. Is there an optimal pH for culture media used in clinical IVF?. Hum Reprod Update 2012; 18 (3) 333-339
- 85 Moreno-Cuevas JE, Sirbasku DA. Estrogen mitogenic action. III. is phenol red a “red herring”?. In Vitro Cell Dev Biol Anim 2000; 36 (7) 447-464
- 86 Nakayama T, Noda Y, Goto Y, Mori T. Effects of visible light and other environmental factors on the production of oxygen radicals by hamster embryos. Theriogenology 1994; 41 (2) 499-510
- 87 Morgia F, Torti M, Montigiani M , et al. Use of a medium buffered with N-hydroxyethylpiperazine-N-ethanesulfonate (HEPES) in intracytoplasmic sperm injection procedures is detrimental to the outcome of in vitro fertilization. Fertil Steril 2006; 85 (5) 1415-1419
- 88 Swain JE, Pool TB. New pH-buffering system for media utilized during gamete and embryo manipulations for assisted reproduction. Reprod Biomed Online 2009; 18 (6) 799-810
- 89 Will MA, Clark NA, Swain JE. Biological pH buffers in IVF: help or hindrance to success. J Assist Reprod Genet 2011; 28 (8) 711-724
- 90 Swain JE. Optimizing the culture environment in the IVF laboratory: impact of pH and buffer capacity on gamete and embryo quality. Reprod Biomed Online 2010; 21 (1) 6-16
- 91 Swain JE. Media composition: pH and buffers. Methods Mol Biol 2012; 912: 161-175
- 92 Hadi T, Hammer MA, Algire C, Richards T, Baltz JM. Similar effects of osmolarity, glucose, and phosphate on cleavage past the 2-cell stage in mouse embryos from outbred and F1 hybrid females. Biol Reprod 2005; 72 (1) 179-187
- 93 Baltz JM, Tartia AP. Cell volume regulation in oocytes and early embryos: connecting physiology to successful culture media. Hum Reprod Update 2010; 16 (2) 166-176
- 94 Dawson KM, Baltz JM. Organic osmolytes and embryos: substrates of the Gly and beta transport systems protect mouse zygotes against the effects of raised osmolarity. Biol Reprod 1997; 56 (6) 1550-1558
- 95 Dawson KM, Collins JL, Baltz JM. Osmolarity-dependent glycine accumulation indicates a role for glycine as an organic osmolyte in early preimplantation mouse embryos. Biol Reprod 1998; 59 (2) 225-232
- 96 Richards T, Wang F, Liu L, Baltz JM. Rescue of postcompaction-stage mouse embryo development from hypertonicity by amino acid transporter substrates that may function as organic osmolytes. Biol Reprod 2010; 82 (4) 769-777
- 97 Swain JE, Cabrera L, Xu X, Smith GD. Microdrop preparation factors influence culture-media osmolality, which can impair mouse embryo preimplantation development. Reprod Biomed Online 2012; 24 (2) 142-147
- 98 Swain JE. Decisions for the IVF laboratory: comparative analysis of embryo culture incubators. Reprod Biomed Online 2014; 28 (5) 535-547
- 99 Hyslop L, Prathalingam N, Nowak L , et al. A novel isolator-based system promotes viability of human embryos during laboratory processing. PLoS ONE 2012; 7 (2) e31010
- 100 Zhang JQ, Li XL, Peng Y, Guo X, Heng BC, Tong GQ. Reduction in exposure of human embryos outside the incubator enhances embryo quality and blastulation rate. Reprod Biomed Online 2010; 20 (4) 510-515
- 101 Kea B, Gebhardt J, Watt J , et al. Effect of reduced oxygen concentrations on the outcome of in vitro fertilization. Fertil Steril 2007; 87 (1) 213-216
- 102 Dumoulin JC, Meijers CJ, Bras M, Coonen E, Geraedts JP, Evers JL. Effect of oxygen concentration on human in-vitro fertilization and embryo culture. Hum Reprod 1999; 14 (2) 465-469
- 103 Catt JW, Henman M. Toxic effects of oxygen on human embryo development. Hum Reprod 2000; 15 (Suppl. 02) 199-206
- 104 Ciray HN, Aksoy T, Yaramanci K, Karayaka I, Bahceci M. In vitro culture under physiologic oxygen concentration improves blastocyst yield and quality: a prospective randomized survey on sibling oocytes. Fertil Steril 2009; 91 (4, Suppl): 1459-1461
- 105 Bahçeci M, Ciray HN, Karagenc L, Uluğ U, Bener F. Effect of oxygen concentration during the incubation of embryos of women undergoing ICSI and embryo transfer: a prospective randomized study. Reprod Biomed Online 2005; 11 (4) 438-443
- 106 Kovacic B, Sajko MC, Vlaisavljević V. A prospective, randomized trial on the effect of atmospheric versus reduced oxygen concentration on the outcome of intracytoplasmic sperm injection cycles. Fertil Steril 2010; 94 (2) 511-519
- 107 Kovacic B, Vlaisavljević V. Influence of atmospheric versus reduced oxygen concentration on development of human blastocysts in vitro: a prospective study on sibling oocytes. Reprod Biomed Online 2008; 17 (2) 229-236
- 108 Nanassy L, Peterson CA, Wilcox AL, Peterson CM, Hammoud A, Carrell DT. Comparison of 5% and ambient oxygen during days 3-5 of in vitro culture of human embryos. Fertil Steril 2010; 93 (2) 579-585
- 109 Waldenström U, Engström AB, Hellberg D, Nilsson S. Low-oxygen compared with high-oxygen atmosphere in blastocyst culture, a prospective randomized study. Fertil Steril 2009; 91 (6) 2461-2465
- 110 Gomes Sobrinho DB, Oliveira JB, Petersen CG , et al. IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis. Reprod Biol Endocrinol 2011; 9: 143
- 111 Petersen A, Mikkelsen AL, Lindenberg S. The impact of oxygen tension on developmental competence of post-thaw human embryos. Acta Obstet Gynecol Scand 2005; 84 (12) 1181-1184
- 112 Bedaiwy MA, Mahfouz RZ, Goldberg JM , et al. Relationship of reactive oxygen species levels in day 3 culture media to the outcome of in vitro fertilization/intracytoplasmic sperm injection cycles. Fertil Steril 2010; 94 (6) 2037-2042
- 113 Meintjes M, Chantilis SJ, Douglas JD , et al. A controlled randomized trial evaluating the effect of lowered incubator oxygen tension on live births in a predominantly blastocyst transfer program. Hum Reprod 2009; 24 (2) 300-307
- 114 Kasterstein E, Strassburger D, Komarovsky D , et al. The effect of two distinct levels of oxygen concentration on embryo development in a sibling oocyte study. J Assist Reprod Genet 2013; 30 (8) 1073-1079
- 115 Thomas T. Culture systems: air quality. Methods Mol Biol 2012; 912: 313-324
- 116 Hall J, Gilligan A, Schimmel T, Cecchi M, Cohen J. The origin, effects and control of air pollution in laboratories used for human embryo culture. Hum Reprod 1998; 13 (Suppl. 04) 146-155
- 117 Cohen J, Gilligan A, Willadsen S. Culture and quality control of embryos. Hum Reprod 1998; 13 (Suppl. 03) 137-144 , discussion 145–147
- 118 Cohen J, Gilligan A, Esposito W, Schimmel T, Dale B. Ambient air and its potential effects on conception in vitro. Hum Reprod 1997; 12 (8) 1742-1749
- 119 Boone WR, Johnson JE, Locke AJ, Crane IV MM, Price TM. Control of air quality in an assisted reproductive technology laboratory. Fertil Steril 1999; 71 (1) 150-154
- 120 Khoudja RY, Xu Y, Li T, Zhou C. Better IVF outcomes following improvements in laboratory air quality. J Assist Reprod Genet 2013; 30 (1) 69-76
- 121 Merton JS, Vermeulen ZL, Otter T, Mullaart E, de Ruigh L, Hasler JF. Carbon-activated gas filtration during in vitro culture increased pregnancy rate following transfer of in vitro-produced bovine embryos. Theriogenology 2007; 67 (7) 1233-1238
- 122 Higdon III HL, Blackhurst DW, Boone WR. Incubator management in an assisted reproductive technology laboratory. Fertil Steril 2008; 89 (3) 703-710
- 123 Schimmel T, Gilligan A, Garrisi G , et al. Removal of volatile organic compounds from incubators used for gamete and embryo culture. Fertil Steril 1997; 68 (Suppl. 01) s165
- 124 Mayer J, Nechchiri F, Weedon V , et al. Prospective randomized crossover analysis of the impact of an IVF incubator air filtration system (coda, GenX) on clinical pregnancy rates. Fertil Steril Suppl 1999; 72 (Suppl. 01) S42
- 125 McLellan S, Panagoulopoulos C, Dickinson K , et al. Effect of incubator air filtration system on IVF outcomes. Fertil Steril 2001; 76 (Suppl. 01) s103
- 126 Battaglia D, Khabani A, Rainer C , et al. Prospective randomized trial of incubator CODA filtration unites revealed no effect on outcome. Fertil Steril 2001; 75 (Suppl. 01) s6
- 127 Sun XF, Wang WH, Keefe DL. Overheating is detrimental to meiotic spindles within in vitro matured human oocytes. Zygote 2004; 12 (1) 65-70
- 128 Wang WH, Meng L, Hackett RJ, Oldenbourg R, Keefe DL. Rigorous thermal control during intracytoplasmic sperm injection stabilizes the meiotic spindle and improves fertilization and pregnancy rates. Fertil Steril 2002; 77 (6) 1274-1277
- 129 Wang WH, Meng L, Hackett RJ, Odenbourg R, Keefe DL. Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum Reprod 2001; 16 (11) 2374-2378
- 130 Leese HJ, Baumann CG, Brison DR, McEvoy TG, Sturmey RG. Metabolism of the viable mammalian embryo: quietness revisited. Mol Hum Reprod 2008; 14 (12) 667-672
- 131 Pollard JW, Martino A, Rumph ND, Songsasen N, Plante C, Leibo SP. Effect of ambient temperatures during oocyte recovery on in vitro production of bovine embryos. Theriogenology 1996; 46 (5) 849-858
- 132 Lane M, Mitchell M, Cashman KS, Feil D, Wakefield S, Zander-Fox DL. To QC or not to QC: the key to a consistent laboratory?. Reprod Fertil Dev 2008; 20 (1) 23-32
- 133 Grinsted J, Kjer JJ, Blendstrup K, Pedersen JF. Is low temperature of the follicular fluid prior to ovulation necessary for normal oocyte development?. Fertil Steril 1985; 43 (1) 34-39
- 134 David A, Vilensky A, Nathan H. Temperature changes in different parts of the rabbit oviduct. Preliminary report [in Hebrew]. Harefuah 1971; 80 (4) 180-182
- 135 Hunter RH, Bogh IB, Einer-Jensen N, Müller S, Greve T. Pre-ovulatory graafian follicles are cooler than neighbouring stroma in pig ovaries. Hum Reprod 2000; 15 (2) 273-283
- 136 Hunter RH, Grøndahl C, Greve T, Schmidt M. Graafian follicles are cooler than neighbouring ovarian tissues and deep rectal temperatures. Hum Reprod 1997; 12 (1) 95-100
- 137 Hunter RH, Nichol R. A preovulatory temperature gradient between the isthmus and ampulla of pig oviducts during the phase of sperm storage. J Reprod Fertil 1986; 77 (2) 599-606
- 138 Hunter RH. Temperature gradients in female reproductive tissues. Reprod Biomed Online 2012; 24 (4) 377-380
- 139 Edwards JL, Hansen PJ. Elevated temperature increases heat shock protein 70 synthesis in bovine two-cell embryos and compromises function of maturing oocytes. Biol Reprod 1996; 55 (2) 341-346
- 140 Edwards JL, Hansen PJ. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev 1997; 46 (2) 138-145
- 141 Chandolia RK, Peltier MR, Tian W, Hansen PJ. Transcriptional control of development, protein synthesis, and heat-induced heat shock protein 70 synthesis in 2-cell bovine embryos. Biol Reprod 1999; 61 (6) 1644-1648
- 142 Aréchiga CF, Hansen PJ. Response of preimplantation murine embryos to heat shock as modified by developmental stage and glutathione status. In Vitro Cell Dev Biol Anim 1998; 34 (8) 655-659
- 143 Hong K, Forman E, Lee H , et al. Optimizing the temperature for embryo culture in IVF: a randomized controlled trial (RCT) comparing standard culture temperature of 37C to the reduced more physiologic temperature of 36C. Fertil Steril 2012; 98 (3) s167
- 144 Cortezzi SS, Garcia JS, Ferreira CR , et al. Secretome of the preimplantation human embryo by bottom-up label-free proteomics. Anal Bioanal Chem 2011; 401 (4) 1331-1339
- 145 Beardsley AJ, Li Y, O'Neill C. Characterization of a diverse secretome generated by the mouse preimplantation embryo in vitro. Reprod Biol Endocrinol 2010; 8: 71
- 146 Brison DR, Hollywood K, Arnesen R, Goodacre R. Predicting human embryo viability: the road to non-invasive analysis of the secretome using metabolic footprinting. Reprod Biomed Online 2007; 15 (3) 296-302
- 147 Katz-Jaffe MG, Schoolcraft WB, Gardner DK. Analysis of protein expression (secretome) by human and mouse preimplantation embryos. Fertil Steril 2006; 86 (3) 678-685
- 148 Bormann C, Swain J, Ni Q , et al. Preimplantation embryo secretome identification. Fertil Steril 2006; 86 (Suppl. 02) s116
- 149 Trimarchi JR, Liu L, Smith PJ, Keefe DL. Noninvasive measurement of potassium efflux as an early indicator of cell death in mouse embryos. Biol Reprod 2000; 63 (3) 851-857
- 150 Trimarchi JR, Liu L, Porterfield DM, Smith PJ, Keefe DL. A non-invasive method for measuring preimplantation embryo physiology. Zygote 2000; 8 (1) 15-24
- 151 Trimarchi JR, Liu L, Porterfield DM, Smith PJ, Keefe DL. Oxidative phosphorylation-dependent and -independent oxygen consumption by individual preimplantation mouse embryos. Biol Reprod 2000; 62 (6) 1866-1874
- 152 Canseco RS, Sparks AE, Pearson RE, Gwazdauskas FC. Embryo density and medium volume effects on early murine embryo development. J Assist Reprod Genet 1992; 9 (5) 454-457
- 153 Lane M, Gardner DK. Effect of incubation volume and embryo density on the development and viability of mouse embryos in vitro. Hum Reprod 1992; 7 (4) 558-562
- 154 Kato Y, Tsunoda Y. Effects of the culture density of mouse zygotes on the development in vitro and in vivo. Theriogenology 1994; 41 (6) 1315-1322
- 155 Salahuddin S, Ookutsu S, Goto K, Nakanishi Y, Nagata Y. Effects of embryo density and co-culture of unfertilized oocytes on embryonic development of in-vitro fertilized mouse embryos. Hum Reprod 1995; 10 (9) 2382-2385
- 156 Teruel M, Smith R. Effect of embryo density and growth factors on in vitro preimplantation development of mouse embryos. Acta Physiol Pharmacol Ther Latinoam 1997; 47 (2) 87-96
- 157 Gardner DK, Lane M, Spitzer A, Batt PA. Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins, and culturing embryos in groups stimulate development. Biol Reprod 1994; 50 (2) 390-400
- 158 Donnay I, Van Langendonckt A, Auquier P , et al. Effects of co-culture and embryo number on the in vitro development of bovine embryos. Theriogenology 1997; 47 (8) 1549-1561
- 159 O'Doherty EM, Wade MG, Hill JL, Boland MP. Effects of culturing bovine oocytes either singly or in groups on development to blastocysts. Theriogenology 1997; 48 (1) 161-169
- 160 Fujita T, Umeki H, Shimura H, Kugumiya K, Shiga K. Effect of group culture and embryo-culture conditioned medium on development of bovine embryos. J Reprod Dev 2006; 52 (1) 137-142
- 161 Keefer CL, Stice SL, Paprocki AM, Golueke P. In vitro culture of bovine IVM-IVF embryos: Cooperative interaction among embryos and the role of growth factors. Theriogenology 1994; 41 (6) 1323-1331
- 162 Khurana NK, Niemann H. Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos. Theriogenology 2000; 54 (5) 741-756
- 163 Nagao Y, Iijima R, Saeki K. Interaction between embryos and culture conditions during in vitro development of bovine early embryos. Zygote 2008; 16 (2) 127-133
- 164 Larson MA, Kubisch HM. The effects of group size on development and interferon-tau secretion by in-vitro fertilized and cultured bovine blastocysts. Hum Reprod 1999; 14 (8) 2075-2079
- 165 Reed M, Woodward B, Swain J. Single versus group culture of mammalian embryos: the verdict of the literature. J Reprod Stem Cel Biol 2011; 2 (2) 77-87
- 166 Moessner J, Dodson WC. The quality of human embryo growth is improved when embryos are cultured in groups rather than separately. Fertil Steril 1995; 64 (5) 1034-1035
- 167 Almagor M, Bejar C, Kafka I, Yaffe H. Pregnancy rates after communal growth of preimplantation human embryos in vitro. Fertil Steril 1996; 66 (3) 394-397
- 168 Rebollar-Lazaro I, Matson P. The culture of human cleavage stage embryos alone or in groups: effect upon blastocyst utilization rates and implantation. Reprod Biol 2010; 10 (3) 227-234
- 169 Spyropoulou I, Karamalegos C, Bolton VN. A prospective randomized study comparing the outcome of in-vitro fertilization and embryo transfer following culture of human embryos individually or in groups before embryo transfer on day 2. Hum Reprod 1999; 14 (1) 76-79
- 170 Ebner T, Shebl O, Moser M, Mayer RB, Arzt W, Tews G. Group culture of human zygotes is superior to individual culture in terms of blastulation, implantation and life birth. Reprod Biomed Online 2010; 21 (6) 762-768
- 171 Smith GD, Takayama S, Swain JE. Rethinking in vitro embryo culture: new developments in culture platforms and potential to improve assisted reproductive technologies. Biol Reprod 2012; 86 (3) 62
- 172 Swain JE, Lai D, Takayama S, Smith GD. Thinking big by thinking small: application of microfluidic technology to improve ART. Lab Chip 2013; 13 (7) 1213-1224
- 173 Swain JE, Smith GD. Advances in embryo culture platforms: novel approaches to improve preimplantation embryo development through modifications of the microenvironment. Hum Reprod Update 2011; 17 (4) 541-557
- 174 Vajta G, Korösi T, Du Y , et al. The well-of-the-well system: an efficient approach to improve embryo development. Reprod Biomed Online 2008; 17 (1) 73-81
- 175 Morbeck DE. Importance of supply integrity for in vitro fertilization and embryo culture. Semin Reprod Med 2012; 30 (3) 182-190
- 176 Lee BE, Boone WR, Brackelsberg PO, Carmichael RA. Development of screening systems for evaluation of materials used in mammalian embryo transfer. Theriogenology 1988; 30 (3) 605-612
- 177 Scott LF, Sundaram SG, Smith S. The relevance and use of mouse embryo bioassays for quality control in an assisted reproductive technology program. Fertil Steril 1993; 60 (3) 559-568
- 178 Esterhuizen AD, Bosman E, Botes AD , et al. A comparative study on the diagnostic sensitivity of rodent sperm and embryos in the detection of endotoxin in Earle's balanced salt solution. J Assist Reprod Genet 1994; 11 (1) 38-42
- 179 Rinehart JS, Bavister BD, Gerrity M. Quality control in the in vitro fertilization laboratory: comparison of bioassay systems for water quality. J In Vitro Fert Embryo Transf 1988; 5 (6) 335-342
- 180 van den Bergh M, Baszó I, Biramane J, Bertrand E, Devreker F, Englert Y. Quality control in IVF with mouse bioassays: a four years' experience. J Assist Reprod Genet 1996; 13 (9) 733-738
- 181 Gardner DK, Reed L, Linck D, Sheehan C, Lane M. Quality control in human in vitro fertilization. Semin Reprod Med 2005; 23 (4) 319-324
- 182 Punt-van der Zalm JP, Hendriks JC, Westphal JR, Kremer JA, Teerenstra S, Wetzels AM. Toxicity testing of human assisted reproduction devices using the mouse embryo assay. Reprod Biomed Online 2009; 18 (4) 529-535
- 183 Morimoto Y, Hayashi E, Ohno T, Kawata A, Horikoshi Y, Kanzaki H. Quality control of human IVF/ICSI program using endotoxin measurement and sperm survival test. Hum Cell 1997; 10 (4) 271-276
- 184 Fleetham JA, Pattinson HA, Mortimer D. The mouse embryo culture system: improving the sensitivity for use as a quality control assay for human in vitro fertilization. Fertil Steril 1993; 59 (1) 192-196
- 185 Davidson A, Vermesh M, Lobo RA, Paulson RJ. Mouse embryo culture as quality control for human in vitro fertilization: the one-cell versus the two-cell model. Fertil Steril 1988; 49 (3) 516-521
- 186 Khan Z, Wolff HS, Fredrickson JR, Walker DL, Daftary GS, Morbeck DE. Mouse strain and quality control testing: improved sensitivity of the mouse embryo assay with embryos from outbred mice. Fertil Steril 2013; 99 (3) 847-854.e2
- 187 Wolff HS, Fredrickson JR, Walker DL, Morbeck DE. Advances in quality control: mouse embryo morphokinetics are sensitive markers of in vitro stress. Hum Reprod 2013; 28 (7) 1776-1782