Skip to main content
Erschienen in: Journal of Assisted Reproduction and Genetics 11/2010

01.11.2010 | Fertility Preservation

Cryo-survival, fertilization and early embryonic development of vitrified oocytes derived from mice of different reproductive age

verfasst von: Jie Yan, Joao Suzuki, Xiaomin Yu, Frederick W. K. Kan, Jie Qiao, Ri-Cheng Chian

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 11/2010

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To evaluate the effect of female reproductive age on oocyte cryo-survival, fertilization and the subsequent embryonic development following vitrification using the mouse model in order to address the question of how maternal reproductive age is related to fertility preservation.

Methods

Oocytes were collected from mice of different reproductive age: (1) 8–10 weeks, (2) 16–20 weeks, (3) 32–36 weeks, and (4) 44–48 weeks. Following vitrification and warming, the oocytes in each group were assessed for cryo-survival, fertilization and embryonic development as well as for the quality of blastocysts. Fresh oocytes without undergoing vitrification were used in each age group as controls.

Results

The mean number of oocytes retrieved following superovulation was found to reduce significantly (P < 0.05) in mice from 32–36 weeks of age (18.1 ± 8.5) compared with 8–10 weeks of age (26.8 ± 9.8) and 16–20 weeks of age (23.9 ± 4.2) respectively. The cryo-survival rate of oocytes was reduced significantly (P < 0.05) in mice of 44–48 weeks of age (90.4% ± 7.9) compared with the other 3 groups (98.8% ± 2.1, 98.0% ± 3.3 and 98.5% ± 2.2, respectively). The cleavage rate of vitrified oocytes declined significantly following the increase in maternal age in mice of 32–36 weeks of age (69.7% ± 20.8) forward (63.6% ± 9.2). However, no significant difference in the cleavage rate was found among the control groups of different maternal ages. The rate of embryo development to the blastocyst stage in the vitrified oocytes also significantly declined following the increase in maternal age (71.8% ± 8.8, 66.4% ± 10.7, 64.2% ± 17.4 and 4.1% ± 8.3 respectively). There were no such differences in the rates of embryo development to the blastocyst stage among the control groups following the increase in maternal age (75.9% ± 12.2, 79.5% ± 28.9, 70.2% ± 17.4 and 69.3% ± 19.0 respectively). However, the quality of blastocysts produced from 32–36 weeks and 44–48 weeks of ages was significantly poor in term of total cell numbers and the ratio of inner cell mass(ICM) / trophectoderm (TE) compared to younger age in both vitrified and control groups

Conclusions

Cryo-survival of oocytes following vitrification and warming procedures is associated with female reproductive age. There is a more negative impact on the oocytes following vitrification and warming with the increase of maternal age.
Literatur
1.
Zurück zum Zitat van Noord-Zaadstra BM, Looman CW, Alsbach H, Habbema JD, te Velde ER, Karbaat J. Delaying childbearing: effect of age on fecundity and outcome of pregnancy. BMJ. 1991;302:1361–5.PubMedCrossRef van Noord-Zaadstra BM, Looman CW, Alsbach H, Habbema JD, te Velde ER, Karbaat J. Delaying childbearing: effect of age on fecundity and outcome of pregnancy. BMJ. 1991;302:1361–5.PubMedCrossRef
2.
Zurück zum Zitat Ottolenghi C, Uda M, Hamatani T, Crisponi L, Garcia JE, Ko M, et al. Aging of oocyte, ovary, and human reproduction. Ann NY Acad Sci. 2004;1034:117–31.PubMedCrossRef Ottolenghi C, Uda M, Hamatani T, Crisponi L, Garcia JE, Ko M, et al. Aging of oocyte, ovary, and human reproduction. Ann NY Acad Sci. 2004;1034:117–31.PubMedCrossRef
3.
Zurück zum Zitat Armstrong DT. Effects of maternal age on oocyte developmental competence. Theriogenology. 2001;55:1303–22.PubMedCrossRef Armstrong DT. Effects of maternal age on oocyte developmental competence. Theriogenology. 2001;55:1303–22.PubMedCrossRef
4.
Zurück zum Zitat Klein J, Sauer MV. Assessing fertility in women of advanced reproductive age. Am J Obstet Gynecol. 2001;185:758–70.PubMedCrossRef Klein J, Sauer MV. Assessing fertility in women of advanced reproductive age. Am J Obstet Gynecol. 2001;185:758–70.PubMedCrossRef
5.
Zurück zum Zitat Schwartz D, Mayaux MJ. Female fecundity as a function of age: results of artificial insemination in 2193 nulliparous women with azoospermic husbands. Federation CECOS. N Engl J Med. 1982;306:404–6.PubMedCrossRef Schwartz D, Mayaux MJ. Female fecundity as a function of age: results of artificial insemination in 2193 nulliparous women with azoospermic husbands. Federation CECOS. N Engl J Med. 1982;306:404–6.PubMedCrossRef
6.
Zurück zum Zitat van Kooij RJ, Looman CW, Habbema JD, Dorland M, te Velde ER. Age-dependent decrease in embryo implantation rate after in vitro fertilization. Fertil Steril. 1996;66:769–75.PubMed van Kooij RJ, Looman CW, Habbema JD, Dorland M, te Velde ER. Age-dependent decrease in embryo implantation rate after in vitro fertilization. Fertil Steril. 1996;66:769–75.PubMed
7.
Zurück zum Zitat te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef
8.
Zurück zum Zitat Navot D, Drews MR, Bergh PA, Guzman I, Karstaedt A, Scott Jr RT, et al. Age-related decline in female fertility is not due to diminished capacity of the uterus to sustain embryo implantation. Fertil Steril. 1994;61:97–101.PubMed Navot D, Drews MR, Bergh PA, Guzman I, Karstaedt A, Scott Jr RT, et al. Age-related decline in female fertility is not due to diminished capacity of the uterus to sustain embryo implantation. Fertil Steril. 1994;61:97–101.PubMed
9.
Zurück zum Zitat Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet. 1991;337:1375–7.PubMedCrossRef Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet. 1991;337:1375–7.PubMedCrossRef
10.
Zurück zum Zitat Volarcik K, Sheean L, Goldfarb J, Woods L, Abdul-Karim FW, Hunt P. The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum Reprod. 1998;13:154–60.PubMedCrossRef Volarcik K, Sheean L, Goldfarb J, Woods L, Abdul-Karim FW, Hunt P. The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum Reprod. 1998;13:154–60.PubMedCrossRef
11.
Zurück zum Zitat Krisher RL. The effect of oocyte quality on development. J Anim Sci. 2004;82(E-Suppl):E14–23.PubMed Krisher RL. The effect of oocyte quality on development. J Anim Sci. 2004;82(E-Suppl):E14–23.PubMed
12.
Zurück zum Zitat Huang JY, Tulandi T, Holzer H, Tan SL, Chian RC. Combining ovarian tissue cryobanking with retrieval of immature oocytes followed by in vitro maturation and vitrification: an additional strategy of fertility preservation. Fertil Steril. 2008;89:567–72.PubMedCrossRef Huang JY, Tulandi T, Holzer H, Tan SL, Chian RC. Combining ovarian tissue cryobanking with retrieval of immature oocytes followed by in vitro maturation and vitrification: an additional strategy of fertility preservation. Fertil Steril. 2008;89:567–72.PubMedCrossRef
13.
Zurück zum Zitat Oktay K, Cil AP, Bang H. Efficiency of oocyte cryopreservation: a meta-analysis. Fertil Steril. 2006;86:70–80.PubMedCrossRef Oktay K, Cil AP, Bang H. Efficiency of oocyte cryopreservation: a meta-analysis. Fertil Steril. 2006;86:70–80.PubMedCrossRef
14.
Zurück zum Zitat Cobo A, Kuwayama M, Perez S, Ruiz A, Pellicer A, Remohi J. Comparison of concomitant outcome achieved with fresh and cryopreserved donor oocytes vitrified by the Cryotop method. Fertil Steril. 2008;89:1657–64.PubMedCrossRef Cobo A, Kuwayama M, Perez S, Ruiz A, Pellicer A, Remohi J. Comparison of concomitant outcome achieved with fresh and cryopreserved donor oocytes vitrified by the Cryotop method. Fertil Steril. 2008;89:1657–64.PubMedCrossRef
15.
Zurück zum Zitat Wei YH, Wu SB, Ma YS, Lee HC. Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med J. 2009;32:113–32.PubMed Wei YH, Wu SB, Ma YS, Lee HC. Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med J. 2009;32:113–32.PubMed
16.
Zurück zum Zitat Practice Committee of American Society for Reproductive Medicine, Practice Committee of Society for Assisted Reproductive Technology. Ovarian tissue and oocyte cryopreservation. Fertil Steril. 2008;90:S241–6. Practice Committee of American Society for Reproductive Medicine, Practice Committee of Society for Assisted Reproductive Technology. Ovarian tissue and oocyte cryopreservation. Fertil Steril. 2008;90:S241–6.
18.
Zurück zum Zitat Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab. 2007;18:58–65.PubMedCrossRef Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC. Female reproductive ageing: current knowledge and future trends. Trends Endocrinol Metab. 2007;18:58–65.PubMedCrossRef
19.
Zurück zum Zitat Mosher WD, Pratt WF. Fecundity and infertility in the United States: incidence and trends. Fertil Steril. 1991;56:192–3.PubMed Mosher WD, Pratt WF. Fecundity and infertility in the United States: incidence and trends. Fertil Steril. 1991;56:192–3.PubMed
20.
Zurück zum Zitat Huang JY, Chen HY, Park JY, Tan SL, Chian RC. Comparison of spindle and chromosome configuration in in vitro- and in vivo-matured mouse oocytes after vitrification. Fertil Steril. 2008;90:1424–32.PubMedCrossRef Huang JY, Chen HY, Park JY, Tan SL, Chian RC. Comparison of spindle and chromosome configuration in in vitro- and in vivo-matured mouse oocytes after vitrification. Fertil Steril. 2008;90:1424–32.PubMedCrossRef
21.
Zurück zum Zitat Kimura Y, Yanagimachi R. Intracytoplasmic sperm injection in the mouse. Biol Reprod. 1995;52:709–20.PubMedCrossRef Kimura Y, Yanagimachi R. Intracytoplasmic sperm injection in the mouse. Biol Reprod. 1995;52:709–20.PubMedCrossRef
22.
Zurück zum Zitat Handyside AH, Hunter S. A rapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocysts in situ using polynucleotide-specific fluorochromes. J Exp Zool. 1984;231:429–34.PubMedCrossRef Handyside AH, Hunter S. A rapid procedure for visualising the inner cell mass and trophectoderm nuclei of mouse blastocysts in situ using polynucleotide-specific fluorochromes. J Exp Zool. 1984;231:429–34.PubMedCrossRef
23.
Zurück zum Zitat Rugh R. The mouse. Its reproduction and development. Oxford University Press; 1990, P5. Rugh R. The mouse. Its reproduction and development. Oxford University Press; 1990, P5.
24.
Zurück zum Zitat Tarin JJ, Perez-Albala S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod. 2001;65:141–50.PubMedCrossRef Tarin JJ, Perez-Albala S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod. 2001;65:141–50.PubMedCrossRef
25.
Zurück zum Zitat Lass A, Silye R, Abrams DC, Krausz T, Hovatta O, Margara R, et al. Follicular density in ovarian biopsy of infertile women: a novel method to assess ovarian reserve. Hum Reprod. 1997;12:1028–31.PubMedCrossRef Lass A, Silye R, Abrams DC, Krausz T, Hovatta O, Margara R, et al. Follicular density in ovarian biopsy of infertile women: a novel method to assess ovarian reserve. Hum Reprod. 1997;12:1028–31.PubMedCrossRef
26.
Zurück zum Zitat Gosden RG, Laing SC, Felicio LS, Nelson JF, Finch CE. Imminent oocyte exhaustion and reduced follicular recruitment mark the transition to acyclicity in aging C57BL/6J mice. Biol Reprod. 1983;28:255–60.PubMedCrossRef Gosden RG, Laing SC, Felicio LS, Nelson JF, Finch CE. Imminent oocyte exhaustion and reduced follicular recruitment mark the transition to acyclicity in aging C57BL/6J mice. Biol Reprod. 1983;28:255–60.PubMedCrossRef
27.
Zurück zum Zitat Faddy MJ, Gosden RG. A mathematical model of follicle dynamics in the human ovary. Hum Reprod. 1995;10:770–5.PubMed Faddy MJ, Gosden RG. A mathematical model of follicle dynamics in the human ovary. Hum Reprod. 1995;10:770–5.PubMed
28.
Zurück zum Zitat Levran D, Ben-Shlomo I, Dor J, Ben-Rafael Z, Nebel L, Mashiach S. Aging of endometrium and oocytes: observations on conception and abortion rates in an egg donation model. Fertil Steril. 1991;56:1091–4.PubMed Levran D, Ben-Shlomo I, Dor J, Ben-Rafael Z, Nebel L, Mashiach S. Aging of endometrium and oocytes: observations on conception and abortion rates in an egg donation model. Fertil Steril. 1991;56:1091–4.PubMed
29.
Zurück zum Zitat Balmaceda JP, Bernardini L, Ciuffardi I, Felix C, Ord T, Sueldo CE, et al. Oocyte donation in humans: a model to study the effect of age on embryo implantation rate. Hum Reprod. 1994;9:2160–3.PubMed Balmaceda JP, Bernardini L, Ciuffardi I, Felix C, Ord T, Sueldo CE, et al. Oocyte donation in humans: a model to study the effect of age on embryo implantation rate. Hum Reprod. 1994;9:2160–3.PubMed
30.
Zurück zum Zitat Faddy MJ, Gosden RG. A model conforming the decline in follicle numbers to the age of menopause in women. Hum Reprod. 1996;11:1484–6.PubMed Faddy MJ, Gosden RG. A model conforming the decline in follicle numbers to the age of menopause in women. Hum Reprod. 1996;11:1484–6.PubMed
31.
Zurück zum Zitat Munne S, Alikani M, Tomkin G, Grifo J, Cohen J. Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil Steril. 1995;64:382–91.PubMed Munne S, Alikani M, Tomkin G, Grifo J, Cohen J. Embryo morphology, developmental rates, and maternal age are correlated with chromosome abnormalities. Fertil Steril. 1995;64:382–91.PubMed
32.
Zurück zum Zitat Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod. 1996;11:2217–22.PubMed Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod. 1996;11:2217–22.PubMed
33.
Zurück zum Zitat Lopes FL, Fortier AL, Darricarrere N, Chan D, Arnold DR, Trasler JM. Reproductive and epigenetic outcomes associated with aging mouse oocytes. In: Hum Mol Genet, vol. 18; 2009: 2032–2044. Lopes FL, Fortier AL, Darricarrere N, Chan D, Arnold DR, Trasler JM. Reproductive and epigenetic outcomes associated with aging mouse oocytes. In: Hum Mol Genet, vol. 18; 2009: 2032–2044.
34.
Zurück zum Zitat Wang Y, Ock SA, Chian RC. Effect of gonadotrophin stimulation on mouse oocyte quality and subsequent embryonic development in vitro. Reprod Biomed Online. 2006;12:304–14.PubMedCrossRef Wang Y, Ock SA, Chian RC. Effect of gonadotrophin stimulation on mouse oocyte quality and subsequent embryonic development in vitro. Reprod Biomed Online. 2006;12:304–14.PubMedCrossRef
35.
Zurück zum Zitat Fujino Y, Ozaki K, Yamamasu S, Ito F, Matsuoka I, Hayashi E, et al. DNA fragmentation of oocytes in aged mice. Hum Reprod. 1996;11:1480–3.PubMed Fujino Y, Ozaki K, Yamamasu S, Ito F, Matsuoka I, Hayashi E, et al. DNA fragmentation of oocytes in aged mice. Hum Reprod. 1996;11:1480–3.PubMed
36.
Zurück zum Zitat Bouquet M, Selva J, Auroux M. Cryopreservation of mouse oocytes: mutagenic effects in the embryo? Biol Reprod. 1993;49:764–9.PubMedCrossRef Bouquet M, Selva J, Auroux M. Cryopreservation of mouse oocytes: mutagenic effects in the embryo? Biol Reprod. 1993;49:764–9.PubMedCrossRef
37.
Zurück zum Zitat Men H, Monson RL, Parrish JJ, Rutledge JJ. Detection of DNA damage in bovine metaphase II oocytes resulting from cryopreservation. Mol Reprod Dev. 2003;64:245–50.PubMedCrossRef Men H, Monson RL, Parrish JJ, Rutledge JJ. Detection of DNA damage in bovine metaphase II oocytes resulting from cryopreservation. Mol Reprod Dev. 2003;64:245–50.PubMedCrossRef
38.
Zurück zum Zitat Stachowiak EM, Papis K, Kruszewski M, Iwanenko T, Bartlomiejczyk T, Modlinski JA. Comparison of the level(s) of DNA damage using Comet assay in bovine oocytes subjected to selected vitrification methods. Reprod Domest Anim. 2009;44:653–8.PubMedCrossRef Stachowiak EM, Papis K, Kruszewski M, Iwanenko T, Bartlomiejczyk T, Modlinski JA. Comparison of the level(s) of DNA damage using Comet assay in bovine oocytes subjected to selected vitrification methods. Reprod Domest Anim. 2009;44:653–8.PubMedCrossRef
39.
Zurück zum Zitat Fuku E, Xia L, Downey BR. Ultrastructural changes in bovine oocytes cryopreserved by vitrification. Cryobiology. 1995;32:139–56.PubMedCrossRef Fuku E, Xia L, Downey BR. Ultrastructural changes in bovine oocytes cryopreserved by vitrification. Cryobiology. 1995;32:139–56.PubMedCrossRef
40.
Zurück zum Zitat Boonkusol D, Faisaikarm T, Dinnyes A, Kitiyanant Y. Effects of vitrification procedures on subsequent development and ultrastructure of in vitro-matured swamp buffalo (Bubalus bubalis) oocytes. Reprod Fertil Dev. 2007;19:383–91.PubMedCrossRef Boonkusol D, Faisaikarm T, Dinnyes A, Kitiyanant Y. Effects of vitrification procedures on subsequent development and ultrastructure of in vitro-matured swamp buffalo (Bubalus bubalis) oocytes. Reprod Fertil Dev. 2007;19:383–91.PubMedCrossRef
41.
Zurück zum Zitat Gualtieri R, Iaccarino M, Mollo V, Prisco M, Iaccarino S, Talevi R. Slow cooling of human oocytes: ultrastructural injuries and apoptotic status. Fertil Steril. 2009;91:1023–34.PubMedCrossRef Gualtieri R, Iaccarino M, Mollo V, Prisco M, Iaccarino S, Talevi R. Slow cooling of human oocytes: ultrastructural injuries and apoptotic status. Fertil Steril. 2009;91:1023–34.PubMedCrossRef
42.
Zurück zum Zitat Rho GJ, Kim S, Yoo JG, Balasubramanian S, Lee HJ, Choe SY. Microtubulin configuration and mitochondrial distribution after ultra-rapid cooling of bovine oocytes. Mol Reprod Dev. 2002;63:464–70.PubMedCrossRef Rho GJ, Kim S, Yoo JG, Balasubramanian S, Lee HJ, Choe SY. Microtubulin configuration and mitochondrial distribution after ultra-rapid cooling of bovine oocytes. Mol Reprod Dev. 2002;63:464–70.PubMedCrossRef
43.
Zurück zum Zitat Valojerdi MR, Salehnia M. Developmental potential and ultrastructural injuries of metaphase II (MII) mouse oocytes after slow freezing or vitrification. J Assist Reprod Genet. 2005;22:119–27.PubMedCrossRef Valojerdi MR, Salehnia M. Developmental potential and ultrastructural injuries of metaphase II (MII) mouse oocytes after slow freezing or vitrification. J Assist Reprod Genet. 2005;22:119–27.PubMedCrossRef
44.
Zurück zum Zitat de Bruin JP, Dorland M, Spek ER, Posthuma G, van Haaften M, Looman CW, et al. Age-related changes in the ultrastructure of the resting follicle pool in human ovaries. Biol Reprod. 2004;70:419–24.PubMedCrossRef de Bruin JP, Dorland M, Spek ER, Posthuma G, van Haaften M, Looman CW, et al. Age-related changes in the ultrastructure of the resting follicle pool in human ovaries. Biol Reprod. 2004;70:419–24.PubMedCrossRef
45.
Zurück zum Zitat Parmegiani L, Cognigni GE, Bernardi S, Ciampaglia W, Pocognoli P, Filicori M. Birth of a baby conceived from frozen oocytes of a 40-year-old woman. Reprod Biomed Online. 2009;18:795–8.PubMedCrossRef Parmegiani L, Cognigni GE, Bernardi S, Ciampaglia W, Pocognoli P, Filicori M. Birth of a baby conceived from frozen oocytes of a 40-year-old woman. Reprod Biomed Online. 2009;18:795–8.PubMedCrossRef
Metadaten
Titel
Cryo-survival, fertilization and early embryonic development of vitrified oocytes derived from mice of different reproductive age
verfasst von
Jie Yan
Joao Suzuki
Xiaomin Yu
Frederick W. K. Kan
Jie Qiao
Ri-Cheng Chian
Publikationsdatum
01.11.2010
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 11/2010
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-010-9450-3

Weitere Artikel der Ausgabe 11/2010

Journal of Assisted Reproduction and Genetics 11/2010 Zur Ausgabe

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.