Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Review

Changes in sex ratio from fertilization to birth in assisted-reproductive-treatment cycles

Authors: Juan J Tarín, Miguel A García-Pérez, Carlos Hermenegildo, Antonio Cano

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

Login to get access

Abstract

Background

In Western gender-neutral countries, the sex ratio at birth is estimated to be approximately 1.06. This ratio is lower than the estimated sex ratio at fertilization which ranges from 1.07 to 1.70 depending on the figures of sex ratio at birth and differential embryo/fetal mortality rates taken into account to perform these estimations. Likewise, little is known about the sex ratio at implantation in natural and assisted-reproduction-treatment (ART) cycles. In this bioessay, we aim to estimate the sex ratio at fertilization and implantation using data from embryos generated by standard in-vitro fertilization (IVF) or intracytoplasmic sperm injection (ICSI) in preimplantation genetic diagnosis cycles. Thereafter, we compare sex ratios at implantation and birth in cleavage- and blastocyst-stage-transfer cycles to propose molecular mechanisms accounting for differences in post-implantation male and female mortality and thereby variations in sex ratios at birth in ART cycles.

Methods

A literature review based on publications up to December 2013 identified by PubMed database searches.

Results

Sex ratio at both fertilization and implantation is estimated to be between 1.29 and 1.50 in IVF cycles and 1.07 in ICSI cycles. Compared with the estimated sex ratio at implantation, sex ratio at birth is lower in IVF cycles (1.03 after cleavage-stage transfer and 1.25 after blastocyst-stage transfer) but similar and close to unity in ICSI cycles (0.95 after cleavage-stage transfer and 1.04 after blastocyst-stage transfer).

Conclusions

In-vitro-culture-induced precocious X-chromosome inactivation together with ICSI-induced decrease in number of trophectoderm cells in female blastocysts may account for preferential female mortality at early post-implantation stages and thereby variations in sex ratios at birth in ART cycles.
Literature
2.
go back to reference Pergament E, Toydemir PB, Fiddler M: Sex ratio: a biological perspective of ‘Sex and the City’. Reprod Biomed Online. 2002, 5: 43-46.CrossRefPubMed Pergament E, Toydemir PB, Fiddler M: Sex ratio: a biological perspective of ‘Sex and the City’. Reprod Biomed Online. 2002, 5: 43-46.CrossRefPubMed
3.
go back to reference Griffin DK, Handyside AH, Harper JC, Wilton LJ, Atkinson G, Soussis I, Wells D, Kontogianni E, Tarín J, Geber S, Ao A, Winston RML, Delhanty JDA: Clinical experience with preimplantation diagnosis of sex by dual fluorescent in situ hybridization. J Assist Reprod Genet. 1994, 11: 132-143.CrossRefPubMed Griffin DK, Handyside AH, Harper JC, Wilton LJ, Atkinson G, Soussis I, Wells D, Kontogianni E, Tarín J, Geber S, Ao A, Winston RML, Delhanty JDA: Clinical experience with preimplantation diagnosis of sex by dual fluorescent in situ hybridization. J Assist Reprod Genet. 1994, 11: 132-143.CrossRefPubMed
4.
go back to reference Viloria T, Rubio MC, Rodrigo L, Calderon G, Mercader A, Mateu E, Meseguer M, Remohi J, Pellicer A: Smoking habits of parents and male: female ratio in spermatozoa and preimplantation embryos. Hum Reprod. 2005, 20: 2517-2522.CrossRefPubMed Viloria T, Rubio MC, Rodrigo L, Calderon G, Mercader A, Mateu E, Meseguer M, Remohi J, Pellicer A: Smoking habits of parents and male: female ratio in spermatozoa and preimplantation embryos. Hum Reprod. 2005, 20: 2517-2522.CrossRefPubMed
5.
go back to reference Bowman M, De Boer K, Cullinan R, Catt J, Jansen R: Do alterations in the sex ratio occur at fertilization? a case report using fluorescent in situ hybridization. J Assist Reprod Genet. 1998, 15: 320-322.PubMedCentralCrossRefPubMed Bowman M, De Boer K, Cullinan R, Catt J, Jansen R: Do alterations in the sex ratio occur at fertilization? a case report using fluorescent in situ hybridization. J Assist Reprod Genet. 1998, 15: 320-322.PubMedCentralCrossRefPubMed
6.
go back to reference Graffelman J, Fugger EF, Keyvanfar K, Schulman JD: Human live birth and sperm-sex ratios compared. Hum Reprod. 1999, 14: 2917-2920.CrossRefPubMed Graffelman J, Fugger EF, Keyvanfar K, Schulman JD: Human live birth and sperm-sex ratios compared. Hum Reprod. 1999, 14: 2917-2920.CrossRefPubMed
7.
go back to reference Setti AS, Figueira RC, Braga DP, Iaconelli A, Borges E: Gender incidence of intracytoplasmic morphologically selected sperm injection-derived embryos: a prospective randomized study. Reprod Biomed Online. 2012, 24: 420-423.CrossRefPubMed Setti AS, Figueira RC, Braga DP, Iaconelli A, Borges E: Gender incidence of intracytoplasmic morphologically selected sperm injection-derived embryos: a prospective randomized study. Reprod Biomed Online. 2012, 24: 420-423.CrossRefPubMed
8.
go back to reference Gutiérrez-Adán A, Granados J, Pintado B, De La Fuente J: Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod Fertil Dev. 2001, 13: 361-365.CrossRefPubMed Gutiérrez-Adán A, Granados J, Pintado B, De La Fuente J: Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod Fertil Dev. 2001, 13: 361-365.CrossRefPubMed
9.
go back to reference Kimura K, Spate LD, Green MP, Roberts RM: Effects of D-glucose concentration, D-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts. Mol Reprod Dev. 2005, 72: 201-207.CrossRefPubMed Kimura K, Spate LD, Green MP, Roberts RM: Effects of D-glucose concentration, D-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts. Mol Reprod Dev. 2005, 72: 201-207.CrossRefPubMed
10.
go back to reference Kimura K, Iwata H, Thompson JG: The effect of glucosamine concentration on the development and sex ratio of bovine embryos. Anim Reprod Sci. 2008, 103: 228-238.CrossRefPubMed Kimura K, Iwata H, Thompson JG: The effect of glucosamine concentration on the development and sex ratio of bovine embryos. Anim Reprod Sci. 2008, 103: 228-238.CrossRefPubMed
12.
go back to reference Braude P, Bolton V, Moore S: Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature. 1988, 332: 459-461.CrossRefPubMed Braude P, Bolton V, Moore S: Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature. 1988, 332: 459-461.CrossRefPubMed
13.
go back to reference Munné S, Tang YX, Weier HU, Stein J, Finkelstein M, Grifo J, Cohen J: Sex distribution in arrested precompacted human embryos. Zygote. 1993, 1: 155-162.CrossRefPubMed Munné S, Tang YX, Weier HU, Stein J, Finkelstein M, Grifo J, Cohen J: Sex distribution in arrested precompacted human embryos. Zygote. 1993, 1: 155-162.CrossRefPubMed
14.
go back to reference Ben-Yosef D, Amit A, Malcov M, Frumkin T, Ben-Yehudah A, Eldar I, Mey-Raz N, Azem F, Altarescu G, Renbaum P, Beeri R, Varshaver I, Eldar-Geva T, Epsztejn-Litman S, Levy-Lahad E, Eiges R: Female sex bias in human embryonic stem cell lines. Stem Cells Dev. 2012, 21: 363-372.PubMedCentralCrossRefPubMed Ben-Yosef D, Amit A, Malcov M, Frumkin T, Ben-Yehudah A, Eldar I, Mey-Raz N, Azem F, Altarescu G, Renbaum P, Beeri R, Varshaver I, Eldar-Geva T, Epsztejn-Litman S, Levy-Lahad E, Eiges R: Female sex bias in human embryonic stem cell lines. Stem Cells Dev. 2012, 21: 363-372.PubMedCentralCrossRefPubMed
15.
go back to reference Fiala KL: On estimating the primary sex ratio from incomplete data. Am Nat. 1980, 115: 442-444.CrossRef Fiala KL: On estimating the primary sex ratio from incomplete data. Am Nat. 1980, 115: 442-444.CrossRef
16.
go back to reference Han TL, Flaherty SP, Ford JH, Matthews CD: Detection of X- and Y-bearing human spermatozoa after motile sperm isolation by swim-up. Fertil Steril. 1993, 60: 1046-1051.PubMed Han TL, Flaherty SP, Ford JH, Matthews CD: Detection of X- and Y-bearing human spermatozoa after motile sperm isolation by swim-up. Fertil Steril. 1993, 60: 1046-1051.PubMed
17.
go back to reference De Jonge CJ, Flaherty SP, Barnes AM, Swann NJ, Matthews CD: Failure of multitube sperm swim-up for sex preselection. Fertil Steril. 1997, 67: 1109-1114.CrossRefPubMed De Jonge CJ, Flaherty SP, Barnes AM, Swann NJ, Matthews CD: Failure of multitube sperm swim-up for sex preselection. Fertil Steril. 1997, 67: 1109-1114.CrossRefPubMed
18.
go back to reference Yan J, Feng HL, Chen ZJ, Hu J, Gao X, Qin Y: Influence of swim-up time on the ratio of X- and Y-bearing spermatozoa. Eur J Obstet Gynecol Reprod Biol. 2006, 129: 150-154.CrossRefPubMed Yan J, Feng HL, Chen ZJ, Hu J, Gao X, Qin Y: Influence of swim-up time on the ratio of X- and Y-bearing spermatozoa. Eur J Obstet Gynecol Reprod Biol. 2006, 129: 150-154.CrossRefPubMed
19.
go back to reference Moohan JM, Lindsay KS: Spermatozoa selected by a discontinuous percoll density gradient exhibit better motion characteristics, more hyperactivation, and longer survival than direct swim-up. Fertil Steril. 1995, 64: 160-165.PubMed Moohan JM, Lindsay KS: Spermatozoa selected by a discontinuous percoll density gradient exhibit better motion characteristics, more hyperactivation, and longer survival than direct swim-up. Fertil Steril. 1995, 64: 160-165.PubMed
20.
go back to reference Lin SP, Lee RK, Tsai YJ, Hwu YM, Lin MH: Separating X-bearing human spermatozoa through a discontinuous percoll density gradient proved to be inefficient by double-label fluorescent in situ hybridization. J Assist Reprod Genet. 1998, 15: 565-569.PubMedCentralCrossRefPubMed Lin SP, Lee RK, Tsai YJ, Hwu YM, Lin MH: Separating X-bearing human spermatozoa through a discontinuous percoll density gradient proved to be inefficient by double-label fluorescent in situ hybridization. J Assist Reprod Genet. 1998, 15: 565-569.PubMedCentralCrossRefPubMed
21.
go back to reference Grant VJ, Chamley LW: Can mammalian mothers influence the sex of their offspring peri-conceptually?. Reproduction. 2010, 140: 425-433.CrossRefPubMed Grant VJ, Chamley LW: Can mammalian mothers influence the sex of their offspring peri-conceptually?. Reproduction. 2010, 140: 425-433.CrossRefPubMed
22.
go back to reference Ellis PJ, Yu Y, Zhang S: Transcriptional dynamics of the sex chromosomes and the search for offspring sex-specific antigens in sperm. Reproduction. 2011, 142: 609-619.CrossRefPubMed Ellis PJ, Yu Y, Zhang S: Transcriptional dynamics of the sex chromosomes and the search for offspring sex-specific antigens in sperm. Reproduction. 2011, 142: 609-619.CrossRefPubMed
23.
go back to reference Luke B, Brown MB, Grainger DA, Baker VL, Ginsburg E, Stern JE, Society for Assisted Reproductive Technology Writing Group: The sex ratio of singleton offspring in assisted-conception pregnancies. Fertil Steril. 2009, 92: 1579-1585.CrossRefPubMed Luke B, Brown MB, Grainger DA, Baker VL, Ginsburg E, Stern JE, Society for Assisted Reproductive Technology Writing Group: The sex ratio of singleton offspring in assisted-conception pregnancies. Fertil Steril. 2009, 92: 1579-1585.CrossRefPubMed
24.
go back to reference Dean JH, Chapman MG, Sullivan EA: The effect on human sex ratio at birth by assisted reproductive technology (ART) procedures–an assessment of babies born following single embryo transfers, Australia and New Zealand, 2002–2006. BJOG. 2010, 117: 1628-1634.CrossRefPubMed Dean JH, Chapman MG, Sullivan EA: The effect on human sex ratio at birth by assisted reproductive technology (ART) procedures–an assessment of babies born following single embryo transfers, Australia and New Zealand, 2002–2006. BJOG. 2010, 117: 1628-1634.CrossRefPubMed
25.
go back to reference Chang HJ, Lee JR, Jee BC, Suh CS, Kim SH: Impact of blastocyst transfer on offspring sex ratio and the monozygotic twinning rate: a systematic review and meta-analysis. Fertil Steril. 2009, 91: 2381-2390.CrossRefPubMed Chang HJ, Lee JR, Jee BC, Suh CS, Kim SH: Impact of blastocyst transfer on offspring sex ratio and the monozygotic twinning rate: a systematic review and meta-analysis. Fertil Steril. 2009, 91: 2381-2390.CrossRefPubMed
26.
go back to reference Ericson A, Källén B: Congenital malformations in infants born after IVF: a population-based study. Hum Reprod. 2001, 16: 504-509.CrossRefPubMed Ericson A, Källén B: Congenital malformations in infants born after IVF: a population-based study. Hum Reprod. 2001, 16: 504-509.CrossRefPubMed
27.
go back to reference Bonduelle M, Liebaers I, Deketelaere V, Derde MP, Camus M, Devroey P, Van Steirteghem A: Neonatal data on a cohort of 2889 infants born after ICSI (1991–1999) and of 2995 infants born after IVF (1983–1999). Hum Reprod. 2002, 17: 671-694.CrossRefPubMed Bonduelle M, Liebaers I, Deketelaere V, Derde MP, Camus M, Devroey P, Van Steirteghem A: Neonatal data on a cohort of 2889 infants born after ICSI (1991–1999) and of 2995 infants born after IVF (1983–1999). Hum Reprod. 2002, 17: 671-694.CrossRefPubMed
28.
go back to reference Fedder J, Loft A, Parner ET, Rasmussen S, Pinborg A: Neonatal outcome and congenital malformations in children born after ICSI with testicular or epididymal sperm: a controlled national cohort study. Hum Reprod. 2013, 28: 230-240.CrossRefPubMed Fedder J, Loft A, Parner ET, Rasmussen S, Pinborg A: Neonatal outcome and congenital malformations in children born after ICSI with testicular or epididymal sperm: a controlled national cohort study. Hum Reprod. 2013, 28: 230-240.CrossRefPubMed
29.
go back to reference Maalouf WE, Mincheva MN, Campbell BK, Hardy IC: Effects of assisted reproductive technologies on human sex ratio at birth. Fertil Steril. 2014, 101: 1321-1325.CrossRefPubMed Maalouf WE, Mincheva MN, Campbell BK, Hardy IC: Effects of assisted reproductive technologies on human sex ratio at birth. Fertil Steril. 2014, 101: 1321-1325.CrossRefPubMed
30.
go back to reference Alfarawati S, Fragouli E, Colls P, Stevens J, Gutiérrez-Mateo C, Schoolcraft WB, Katz-Jaffe MG, Wells D: The relationship between blastocyst morphology, chromosomal abnormality, and embryo gender. Fertil Steril. 2011, 95: 520-524.CrossRefPubMed Alfarawati S, Fragouli E, Colls P, Stevens J, Gutiérrez-Mateo C, Schoolcraft WB, Katz-Jaffe MG, Wells D: The relationship between blastocyst morphology, chromosomal abnormality, and embryo gender. Fertil Steril. 2011, 95: 520-524.CrossRefPubMed
31.
go back to reference Ray PF, Conaghan J, Winston RM, Handyside AH: Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization. J Reprod Fertil. 1995, 104: 165-171.CrossRefPubMed Ray PF, Conaghan J, Winston RM, Handyside AH: Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization. J Reprod Fertil. 1995, 104: 165-171.CrossRefPubMed
32.
go back to reference Richter KS, Anderson M, Osborn BH: Selection for faster development does not bias sex ratios resulting from blastocyst embryo transfer. Reprod Biomed Online. 2006, 12: 460-465.CrossRefPubMed Richter KS, Anderson M, Osborn BH: Selection for faster development does not bias sex ratios resulting from blastocyst embryo transfer. Reprod Biomed Online. 2006, 12: 460-465.CrossRefPubMed
33.
go back to reference Csokmay JM, Hill MJ, Cioppettini FV, Miller KA, Scott RT, Frattarelli JL: Live birth sex ratios are not influenced by blastocyst-stage embryo transfer. Fertil Steril. 2009, 92: 913-917.CrossRefPubMed Csokmay JM, Hill MJ, Cioppettini FV, Miller KA, Scott RT, Frattarelli JL: Live birth sex ratios are not influenced by blastocyst-stage embryo transfer. Fertil Steril. 2009, 92: 913-917.CrossRefPubMed
34.
go back to reference Weston G, Osianlis T, Catt J, Vollenhoven B: Blastocyst transfer does not cause a sex-ratio imbalance. Fertil Steril. 2009, 92: 1302-1305.CrossRefPubMed Weston G, Osianlis T, Catt J, Vollenhoven B: Blastocyst transfer does not cause a sex-ratio imbalance. Fertil Steril. 2009, 92: 1302-1305.CrossRefPubMed
35.
go back to reference Krackow S: The developmental asynchrony hypothesis for sex ratio manipulation. J Theor Biol. 1995, 176: 273-280.CrossRefPubMed Krackow S: The developmental asynchrony hypothesis for sex ratio manipulation. J Theor Biol. 1995, 176: 273-280.CrossRefPubMed
36.
go back to reference Tarín JJ, Bernabeu R, Baviera A, Bonada M, Cano A: Sex selection may be inadvertently performed in in-vitro fertilization-embryo transfer programmes. Hum Reprod. 1995, 10: 2992-2998.PubMed Tarín JJ, Bernabeu R, Baviera A, Bonada M, Cano A: Sex selection may be inadvertently performed in in-vitro fertilization-embryo transfer programmes. Hum Reprod. 1995, 10: 2992-2998.PubMed
37.
go back to reference Krackow S, Burgoyne PS: Timing of mating, developmental asynchrony and the sex ratio in mice. Physiol Behav. 1998, 63: 81-84.CrossRef Krackow S, Burgoyne PS: Timing of mating, developmental asynchrony and the sex ratio in mice. Physiol Behav. 1998, 63: 81-84.CrossRef
38.
go back to reference Jiménez A, Fernández R, Madrid-Bury N, Moreira PN, Borque C, Pintado B, Gutiérrez-Adán A: Experimental demonstration that pre- and post-conceptional mechanisms influence sex ratio in mouse embryos. Mol Reprod Dev. 2003, 66: 162-165.CrossRefPubMed Jiménez A, Fernández R, Madrid-Bury N, Moreira PN, Borque C, Pintado B, Gutiérrez-Adán A: Experimental demonstration that pre- and post-conceptional mechanisms influence sex ratio in mouse embryos. Mol Reprod Dev. 2003, 66: 162-165.CrossRefPubMed
39.
go back to reference Lee JT, Bartolomei MS: X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013, 152: 1308-1323.CrossRefPubMed Lee JT, Bartolomei MS: X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013, 152: 1308-1323.CrossRefPubMed
40.
go back to reference Lessing D, Lee JT: X chromosome inactivation and epigenetic responses to cellular reprogramming. Annu Rev Genomics Hum Genet. 2013, 14: 85-110.CrossRefPubMed Lessing D, Lee JT: X chromosome inactivation and epigenetic responses to cellular reprogramming. Annu Rev Genomics Hum Genet. 2013, 14: 85-110.CrossRefPubMed
41.
go back to reference Hemberger M: Epigenetic landscape required for placental development. Cell Mol Life Sci. 2007, 64: 2422-2436.CrossRefPubMed Hemberger M: Epigenetic landscape required for placental development. Cell Mol Life Sci. 2007, 64: 2422-2436.CrossRefPubMed
42.
go back to reference Gasperowicz M, Natale DR: Establishing three blastocyst lineages–then what?. Biol Reprod. 2011, 84: 621-630.CrossRefPubMed Gasperowicz M, Natale DR: Establishing three blastocyst lineages–then what?. Biol Reprod. 2011, 84: 621-630.CrossRefPubMed
43.
go back to reference van den Berg IM, Laven JS, Stevens M, Jonkers I, Galjaard RJ, Gribnau J, van Doorninck JH: X chromosome inactivation is initiated in human preimplantation embryos. Am J Hum Genet. 2009, 84: 771-779.PubMedCentralCrossRefPubMed van den Berg IM, Laven JS, Stevens M, Jonkers I, Galjaard RJ, Gribnau J, van Doorninck JH: X chromosome inactivation is initiated in human preimplantation embryos. Am J Hum Genet. 2009, 84: 771-779.PubMedCentralCrossRefPubMed
44.
go back to reference Okamoto I, Patrat C, Thépot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V, Heard E: Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature. 2011, 472: 370-374.CrossRefPubMed Okamoto I, Patrat C, Thépot D, Peynot N, Fauque P, Daniel N, Diabangouaya P, Wolf JP, Renard JP, Duranthon V, Heard E: Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature. 2011, 472: 370-374.CrossRefPubMed
45.
go back to reference Teklenburg G, Weimar CH, Fauser BC, Macklon N, Geijsen N, Heijnen CJ, de Sousa Lopes SM C, Kuijk EW: Cell lineage specific distribution of H3K27 trimethylation accumulation in an in vitro model for human implantation. PLoS One. 2012, 7: e32701-PubMedCentralCrossRefPubMed Teklenburg G, Weimar CH, Fauser BC, Macklon N, Geijsen N, Heijnen CJ, de Sousa Lopes SM C, Kuijk EW: Cell lineage specific distribution of H3K27 trimethylation accumulation in an in vitro model for human implantation. PLoS One. 2012, 7: e32701-PubMedCentralCrossRefPubMed
46.
go back to reference Migeon BR: Why females are mosaics, X-chromosome inactivation, and sex differences in disease. Gend Med. 2007, 4: 97-105.CrossRefPubMed Migeon BR: Why females are mosaics, X-chromosome inactivation, and sex differences in disease. Gend Med. 2007, 4: 97-105.CrossRefPubMed
47.
go back to reference Renault NK, Pritchett SM, Howell RE, Greer WL, Sapienza C, Orstavik KH, Hamilton DC: Human X-chromosome inactivation pattern distributions fit a model of genetically influenced choice better than models of completely random choice. Eur J Hum Genet. 2013, 21: 1396-1402.PubMedCentralCrossRefPubMed Renault NK, Pritchett SM, Howell RE, Greer WL, Sapienza C, Orstavik KH, Hamilton DC: Human X-chromosome inactivation pattern distributions fit a model of genetically influenced choice better than models of completely random choice. Eur J Hum Genet. 2013, 21: 1396-1402.PubMedCentralCrossRefPubMed
48.
go back to reference Brown CJ, Greally JM: A stain upon the silence: genes escaping X inactivation. Trends Genet. 2003, 19: 432-438.CrossRefPubMed Brown CJ, Greally JM: A stain upon the silence: genes escaping X inactivation. Trends Genet. 2003, 19: 432-438.CrossRefPubMed
49.
go back to reference Aiken CE, Ozanne SE: Sex differences in developmental programming models. Reproduction. 2013, 145: R1-13.CrossRefPubMed Aiken CE, Ozanne SE: Sex differences in developmental programming models. Reproduction. 2013, 145: R1-13.CrossRefPubMed
50.
go back to reference Hemberger M: The role of the X chromosome in mammalian extra embryonic development. Cytogenet Genome Res. 2002, 99: 210-217. ç45CrossRefPubMed Hemberger M: The role of the X chromosome in mammalian extra embryonic development. Cytogenet Genome Res. 2002, 99: 210-217. ç45CrossRefPubMed
51.
go back to reference Schulz EG, Heard E: Role and control of X chromosome dosage in mammalian development. Curr Opin Genet Dev. 2013, 23: 109-115.CrossRefPubMed Schulz EG, Heard E: Role and control of X chromosome dosage in mammalian development. Curr Opin Genet Dev. 2013, 23: 109-115.CrossRefPubMed
52.
go back to reference Lengner CJ, Gimelbrant AA, Erwin JA, Cheng AW, Guenther MG, Welstead GG, Alagappan R, Frampton GM, Xu P, Muffat J, Santagata S, Powers D, Barrett CB, Young RA, Lee JT, Jaenisch R, Mitalipova M: Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell. 2010, 141: 872-883. ç48CrossRefPubMed Lengner CJ, Gimelbrant AA, Erwin JA, Cheng AW, Guenther MG, Welstead GG, Alagappan R, Frampton GM, Xu P, Muffat J, Santagata S, Powers D, Barrett CB, Young RA, Lee JT, Jaenisch R, Mitalipova M: Derivation of pre-X inactivation human embryonic stem cells under physiological oxygen concentrations. Cell. 2010, 141: 872-883. ç48CrossRefPubMed
53.
go back to reference Bontekoe S, Mantikou E, van Wely M, Seshadri S, Repping S, Mastenbroek S: Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev. 2012, 7: CD008950 Bontekoe S, Mantikou E, van Wely M, Seshadri S, Repping S, Mastenbroek S: Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev. 2012, 7: CD008950
54.
go back to reference Oliveira CS, Saraiva NZ, Cruz MH, Mazeti B, Oliveira LZ, Lopes FL, Garcia JM: HDAC inhibition decreases XIST expression on female IVP bovine blastocysts. Reproduction. 2013, 145: 9-17.CrossRefPubMed Oliveira CS, Saraiva NZ, Cruz MH, Mazeti B, Oliveira LZ, Lopes FL, Garcia JM: HDAC inhibition decreases XIST expression on female IVP bovine blastocysts. Reproduction. 2013, 145: 9-17.CrossRefPubMed
55.
go back to reference Shen Y, Matsuno Y, Fouse SD, Rao N, Root S, Xu R, Pellegrini M, Riggs AD, Fan G: X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc Natl Acad Sci U S A. 2008, 105: 4709-4714.PubMedCentralCrossRefPubMed Shen Y, Matsuno Y, Fouse SD, Rao N, Root S, Xu R, Pellegrini M, Riggs AD, Fan G: X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc Natl Acad Sci U S A. 2008, 105: 4709-4714.PubMedCentralCrossRefPubMed
56.
go back to reference Glujovsky D, Blake D, Farquhar C, Bardach A: Cleavage stage versus blastocyst stage embryo transfer in assisted reproductive technology. Cochrane Database Syst Rev. 2012, 7: CD002118 Glujovsky D, Blake D, Farquhar C, Bardach A: Cleavage stage versus blastocyst stage embryo transfer in assisted reproductive technology. Cochrane Database Syst Rev. 2012, 7: CD002118
57.
go back to reference van der Gaast MH, Classen-Linke I, Krusche CA, Beier-Hellwig K, Fauser BC, Beier HM, Macklon NS: Impact of ovarian stimulation on mid-luteal endometrial tissue and secretion markers of receptivity. Reprod Biomed Online. 2008, 17: 553-563.CrossRefPubMed van der Gaast MH, Classen-Linke I, Krusche CA, Beier-Hellwig K, Fauser BC, Beier HM, Macklon NS: Impact of ovarian stimulation on mid-luteal endometrial tissue and secretion markers of receptivity. Reprod Biomed Online. 2008, 17: 553-563.CrossRefPubMed
58.
go back to reference Bourgain C, Devroey P: The endometrium in stimulated cycles for IVF. Hum Reprod Update. 2003, 9: 515-522.CrossRefPubMed Bourgain C, Devroey P: The endometrium in stimulated cycles for IVF. Hum Reprod Update. 2003, 9: 515-522.CrossRefPubMed
59.
go back to reference Shapiro BS, Daneshmand ST, Restrepo H, Garner FC: Serum HCG measured in the peri-implantation period predicts IVF cycle outcomes. Reprod Biomed Online. 2012, 25: 248-253.CrossRefPubMed Shapiro BS, Daneshmand ST, Restrepo H, Garner FC: Serum HCG measured in the peri-implantation period predicts IVF cycle outcomes. Reprod Biomed Online. 2012, 25: 248-253.CrossRefPubMed
60.
go back to reference Poikkeus P, Hiilesmaa V, Tiitinen A: Serum HCG 12 days after embryo transfer in predicting pregnancy outcome. Hum Reprod. 2002, 17: 1901-1905.CrossRefPubMed Poikkeus P, Hiilesmaa V, Tiitinen A: Serum HCG 12 days after embryo transfer in predicting pregnancy outcome. Hum Reprod. 2002, 17: 1901-1905.CrossRefPubMed
61.
go back to reference Eiben B, Bartels I, Bähr-Porsch S, Borgmann S, Gatz G, Gellert G, Goebel R, Hammans W, Hentemann M, Osmers R, Rauskolb R, Hansmannt I: Cytogenetic analysis of 750 spontaneous abortions with the direct-preparation method of chorionic villi and its implications for studying genetic causes of pregnancy wastage. Am J Hum Genet. 1990, 47: 656-663.PubMedCentralPubMed Eiben B, Bartels I, Bähr-Porsch S, Borgmann S, Gatz G, Gellert G, Goebel R, Hammans W, Hentemann M, Osmers R, Rauskolb R, Hansmannt I: Cytogenetic analysis of 750 spontaneous abortions with the direct-preparation method of chorionic villi and its implications for studying genetic causes of pregnancy wastage. Am J Hum Genet. 1990, 47: 656-663.PubMedCentralPubMed
62.
go back to reference Yusuf RZ, Naeem R: Cytogenetic abnormalities in products of conception: a relationship revisited. Am J Reprod Immunol. 2004, 52: 88-96.CrossRefPubMed Yusuf RZ, Naeem R: Cytogenetic abnormalities in products of conception: a relationship revisited. Am J Reprod Immunol. 2004, 52: 88-96.CrossRefPubMed
63.
go back to reference Huether CA, Martin RL, Stoppelman SM, D’Souza S, Bishop JK, Torfs CP, Lorey F, May KM, Hanna JS, Baird PA, Kelly JC: Sex ratios in fetuses and liveborn infants with autosomal aneuploidy. Am J Med Genet. 1996, 63: 492-500.CrossRefPubMed Huether CA, Martin RL, Stoppelman SM, D’Souza S, Bishop JK, Torfs CP, Lorey F, May KM, Hanna JS, Baird PA, Kelly JC: Sex ratios in fetuses and liveborn infants with autosomal aneuploidy. Am J Med Genet. 1996, 63: 492-500.CrossRefPubMed
64.
go back to reference Dumoulin JC, Derhaag JG, Bras M, Van Montfoort AP, Kester AD, Evers JL, Geraedts JP, Coonen E: Growth rate of human preimplantation embryos is sex dependent after ICSI but not after IVF. Hum Reprod. 2005, 20: 484-491.CrossRefPubMed Dumoulin JC, Derhaag JG, Bras M, Van Montfoort AP, Kester AD, Evers JL, Geraedts JP, Coonen E: Growth rate of human preimplantation embryos is sex dependent after ICSI but not after IVF. Hum Reprod. 2005, 20: 484-491.CrossRefPubMed
65.
go back to reference James WH: The human sex ratio part 1: a review of the literature. Hum Biol. 1987, 59: 721-752.PubMed James WH: The human sex ratio part 1: a review of the literature. Hum Biol. 1987, 59: 721-752.PubMed
66.
go back to reference James WH: The variation of the probability of a son within and across couples. Hum Reprod. 2000, 15: 1184-1188.CrossRefPubMed James WH: The variation of the probability of a son within and across couples. Hum Reprod. 2000, 15: 1184-1188.CrossRefPubMed
Metadata
Title
Changes in sex ratio from fertilization to birth in assisted-reproductive-treatment cycles
Authors
Juan J Tarín
Miguel A García-Pérez
Carlos Hermenegildo
Antonio Cano
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-56

Other articles of this Issue 1/2014

Reproductive Biology and Endocrinology 1/2014 Go to the issue