The DOI matches its Crossref record; 29 of the 29 references it cites were found in a registry or an index.
Superovulation of female mice delays embryonic and fetal development
Abstract
Mouse and human embryos, cultured in vitro, undergo a delay in development compared with those grown in vivo. This delay can be caused by suboptimal culture conditions, but possible influences of ovarian stimulation cannot be excluded. The objective of this study was to test the hypothesis that both in vitro and in vivo, preimplantation embryonic development and postimplantation fetal development are impaired in superovulated female mice when compared with naturally cycling controls. A delay in in-vitro blastocyst hatching and in-vivo blastocyst formation (P < 0.03 and P < 0.0001 respectively) and a 40% fetal growth retardation (P < 0.0001) were observed after superovulation in comparison with naturally cycling controls. After transfer to non-stimulated foster mothers, blastocysts from stimulated females had a lower implantation rate (P < 0.005), and developed into fewer living fetuses (P < 0.02), more resorption sites (P < 0.02) and had more pronounced growth retardation (P < 0.0001) when compared with blastocysts from naturally cycling controls. In conclusion, superovulation in the mouse causes a delayed embryonic development in vitro and in vivo, an increased abnormal blastocyst formation, a pronounced fetal growth retardation, and an increased number of resorption sites. If this observation in mice can be extrapolated to humans, it may offer an explanation for the delay in embryonic development and the low birth weight observed after IVF.
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Healthy viable pups are routinely born to wildtype females after superovulation protocols.
“The literature suggests healthy viable pups are routinely born to wildtype females after superovulation protocols”
From Conditional loss of ERK1 and ERK2 results in abnormal placentation and delayed parturition in the mouse (2019) · cites this paper as [17]
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Cites
Quinn, P. M., Kerin, J. F., & Warnes, G. M. (1985) · Fertility and Sterility · doi:10.1016/s0015-0282(16)48918-1 · Cited by 847
Embryo implantation after human in vitro fertilization: importance of endometrial receptivity
Paulson, R. J., Sauer, M. V., & Løbo, R. A. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53524-9 · Cited by 293
Edwards, R. G., & Gates, A. H. (1959) · Journal of Endocrinology · doi:10.1677/joe.0.0180292 · Cited by 255
Biology of the Laboratory Mouse.
(1941) · Annals of Internal Medicine · doi:10.7326/0003-4819-15-6-1121 · Cited by 237
The relation of mating, ovulation and the estrous smear in the house mouse to time of day
Snell, G. D., Fekete, E., Hummel, K. P., et al. (1940) · The Anatomical Record · doi:10.1002/ar.1090760105 · Cited by 142
FIVNAT (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57850-9 · Cited by 141
Adverse effects of gonadotrophin treatment on pre- and postimplantation development in mice
Ertzeid, G., & Storeng, R. (1992) · Reproduction · doi:10.1530/jrf.0.0960649 · Cited by 121
Ovarian hyperstimulation inhibits embryo implantation in the mouse
Fossum, G., Davidson, A., & Paulson, R. J. (1989) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf01134574 · Cited by 104
der Auwera, I. V., Pijnenborg, R., & Koninckx, P. R. (1999) · Human Reproduction · doi:10.1093/humrep/14.10.2570 · Cited by 66
Treatment with gonadotropins impaired implantation and fetal development in mice
Ertzeid, G., Storeng, R., & Lyberg, T. (1993) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf01204944 · Cited by 65
BEAUMONT, H. M., & SMITH, A. F. (1975) · Reproduction · doi:10.1530/jrf.0.0450437 · Cited by 64
McKiernan, S. H., & Bavister, B. D. (1998) · Human Reproduction · doi:10.1093/humrep/13.3.724 · Cited by 56
Romero, A., Villamayor, F., Grau, M. T., et al. (1992) · Reproductive Toxicology · doi:10.1016/0890-6238(92)90009-i · Cited by 53
Miller, B. G., & Armstrong, D. T. (1981) · Biology of Reproduction · doi:10.1095/biolreprod25.2.261 · Cited by 53
Perinatal outcome after in vitro fertilisation
Petersen, K., HORNNES, P. J., Ellingsen, S., et al. (1995) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349509008921 · Cited by 49
Miller, B. G., & Armstrong, D. T. (1981) · Biology of Reproduction · doi:10.1095/biolreprod25.2.253 · Cited by 45
CHECK, J. H., O'Shaughnessy, A., Lurie, D., et al. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a135840 · Cited by 44
Poromaa, I. S., Ildgruben, A., & Högberg, U. (1997) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/j.1600-0412.1997.tb07852.x · Cited by 41
Walton, E. A., & Armstrong, D. T. (1981) · Biology of Reproduction · doi:10.1095/biolreprod25.2.272 · Cited by 37
Superovulation-induced intrauterine growth retardation in mice
Evans, M. I., Schulman, J. D., Golden, L., et al. (1981) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(81)90607-4 · Cited by 35
Oocyte normality after superovulation in immature rats
Walton, E. A., & Armstrong, D. T. (1983) · Reproduction · doi:10.1530/jrf.0.0670309 · Cited by 35
CLEAVAGE RATE OF MOUSE EGGS FROM INDUCED AND SPONTANEOUS OVULATION
ALLEN, J., & McLaren, A. L. D. (1971) · Reproduction · doi:10.1530/jrf.0.0270137 · Cited by 31
der Auwera, I. V., Meuleman, C., & Koninckx, P. R. (1994) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138748 · Cited by 30
Possible Causes of Implantation Failure in Superovulated Immature Rats12
Walton, E. A., Huntley, S., Kennedy, T. G., et al. (1982) · Biology of Reproduction · doi:10.1095/biolreprod27.4.847 · Cited by 29
Maternal factors influencing development of embryos from mice superovulated with gonadotropins
Elmazar, M. M., Vogel, R. W., & Spielmann, H. (1989) · Reproductive Toxicology · doi:10.1016/0890-6238(89)90047-6 · Cited by 22
Infertility in Superovulated Immature Rats: Role of Ovarian Steroid Hypersecretion12
Miller, B. G., & Armstrong, D. T. (1982) · Biology of Reproduction · doi:10.1095/biolreprod26.5.861 · Cited by 18
Champlin, A. K., Kuzia, S. J., Rice, B. A., et al. (1987) · Biology of Reproduction · doi:10.1095/biolreprod36.2.439 · Cited by 14
Wetzels, A. M. M., Artz, M. T., Goverde, H. J. M., et al. (1995) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf02212904 · Cited by 6
P-146. The impact of ovarian hyperstimulation on implantation and fetal development in mice
Ertzeid, G., Storeng, R., Tanbo, T., et al. (1999) · Human Reproduction · doi:10.1093/humrep/14.suppl_3.214 · Cited by 3
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Brown, J. L., Sones, J. L., Angulo, C. N., Abbott, K., Miller, A. D., Boehm, U., & Roberson, M. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-45997-0 · Cited by 13
Metadata
- Authors
- Van der Auwera, I.
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2001-06-01
- Volume
- 16
- Issue
- 6
- Pages
- 1237-1243
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2099401496
- Cited by
- 224
- References
- 29
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 10 · 2023: 10 · 2022: 11 · 2021: 11 · 2020: 8 · 2019: 15 · 2018: 8 · 2017: 9 · 2016: 4 · 2015: 10 · 2014: 16 · 2013: 7 · 2012: 14
- FWCI
- 6.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Assisted Reproductive Technology and Twin Pregnancy
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Health and Technologies
- Keywords
- superovulation, ovulation induction, preimplantation embryo development, blastocyst development, blastocyst hatching, fetal growth restriction, implantation rate, embryo resorption, embryo culture, low birth weight, in vitro fertilization, mouse model
- MeSH terms
- Animals, Blastocyst, Female, Embryonic and Fetal Development, Fetal Growth Retardation, Chorionic Gonadotropin, Mice, Inbred CBA, Mice, Inbred C57BL, Embryo Implantation, Placebos, Pregnancy, Superovulation, Culture Techniques, Embryonic Development, Mice
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