Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 2/2015

01-02-2015 | Reproductive Physiology and Disease

Effect of induced peritoneal endometriosis on oocyte and embryo quality in a mouse model

Authors: J. Cohen, A. Ziyyat, I. Naoura, N. Chabbert-Buffet, S. Aractingi, E. Darai, B. Lefevre

Published in: Journal of Assisted Reproduction and Genetics | Issue 2/2015

Login to get access

Abstract

Purpose

To assess the impact of peritoneal endometriosis on oocyte and embryo quality in a mouse model.

Methods

Peritoneal endometriosis was surgically induced in 33 B6CBA/F1 female mice (endometriosis group, N = 17) and sham-operated were used as control (sham group, N = 16). Mice were superovulated 4 weeks after surgery and mated or not, to collect E0.5-embryos or MII-oocytes. Evaluation of oocyte and zygote quality was done by immunofluorescence under spinning disk confocal microscopy.

Results

Endometriosis-like lesions were observed in all mice of endometriosis group. In both groups, a similar mean number of MII oocytes per mouse was observed in non-mated mice (30.2 vs 32.6), with a lower proportion of normal oocytes in the endometriosis group (61 vs 83 %, p < 0.0001). Abnormalities were incomplete extrusion or division of the first polar body and spindle abnormalities. The mean number of zygotes per mouse was lower in the endometriosis group (21 vs 35.5, p = 0.02) without difference in embryo quality.

Conclusions

Our results support that induced peritoneal endometriosis in a mouse model is associated with a decrease in oocyte quality and embryo number. This experimental model allows further studies to understand mechanisms of endometriosis-associated infertility.
Literature
1.
go back to reference Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility. Fertil Steril. 2004;82 Suppl 1:S40–5. Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility. Fertil Steril. 2004;82 Suppl 1:S40–5.
2.
go back to reference Witz CA, Burns WN. Endometriosis and infertility: is there a cause and effect relationship? Gynecol Obstet Investig. 2002;53 Suppl 1:2–11.CrossRef Witz CA, Burns WN. Endometriosis and infertility: is there a cause and effect relationship? Gynecol Obstet Investig. 2002;53 Suppl 1:2–11.CrossRef
3.
go back to reference Porpora MG, Pultrone DC, Bellavia M, Franco C, Crobu M, Cosmi EV. Reproductive outcome after laparoscopic treatment of endometriosis. Clin Exp Obstet Gynecol. 2002;29:271–3.PubMed Porpora MG, Pultrone DC, Bellavia M, Franco C, Crobu M, Cosmi EV. Reproductive outcome after laparoscopic treatment of endometriosis. Clin Exp Obstet Gynecol. 2002;29:271–3.PubMed
4.
go back to reference Jacobson TZ, Duffy JM, Barlow D, Farquhar C, Koninckx PR, Olive D. Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev. 2010: CD001398. Jacobson TZ, Duffy JM, Barlow D, Farquhar C, Koninckx PR, Olive D. Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev. 2010: CD001398.
5.
go back to reference Marcoux S, Maheux R, Berube S. Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian collaborative group on endometriosis. N Engl J Med. 1997;337:217–22.CrossRefPubMed Marcoux S, Maheux R, Berube S. Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian collaborative group on endometriosis. N Engl J Med. 1997;337:217–22.CrossRefPubMed
6.
go back to reference Parazzini F. Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo studio dell’Endometriosi. Hum Reprod. 1999;14:1332–4.CrossRefPubMed Parazzini F. Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo studio dell’Endometriosi. Hum Reprod. 1999;14:1332–4.CrossRefPubMed
7.
go back to reference Halme J, Becker S, Hammond MG, Raj MH, Raj S. Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol. 1983;145:333–7.PubMed Halme J, Becker S, Hammond MG, Raj MH, Raj S. Increased activation of pelvic macrophages in infertile women with mild endometriosis. Am J Obstet Gynecol. 1983;145:333–7.PubMed
8.
go back to reference Rana N, Braun DP, House R, Gebel H, Rotman C, Dmowski WP. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis. Fertil Steril. 1996;65:925–30.PubMed Rana N, Braun DP, House R, Gebel H, Rotman C, Dmowski WP. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis. Fertil Steril. 1996;65:925–30.PubMed
9.
go back to reference Wang Y, Sharma RK, Falcone T, Goldberg J, Agarwal A. Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril. 1997;68:826–30.CrossRefPubMed Wang Y, Sharma RK, Falcone T, Goldberg J, Agarwal A. Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril. 1997;68:826–30.CrossRefPubMed
10.
go back to reference Oosterlynck DJ, Meuleman C, Waer M, Vandeputte M, Koninckx PR. The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil Steril. 1992;58:290–5.PubMed Oosterlynck DJ, Meuleman C, Waer M, Vandeputte M, Koninckx PR. The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis. Fertil Steril. 1992;58:290–5.PubMed
11.
go back to reference Yoshida S, Harada T, Iwabe T, Taniguchi F, Mitsunari M, Yamauchi N, et al. A combination of interleukin-6 and its soluble receptor impairs sperm motility: implications in infertility associated with endometriosis. Hum Reprod. 2004;19:1821–5.CrossRefPubMed Yoshida S, Harada T, Iwabe T, Taniguchi F, Mitsunari M, Yamauchi N, et al. A combination of interleukin-6 and its soluble receptor impairs sperm motility: implications in infertility associated with endometriosis. Hum Reprod. 2004;19:1821–5.CrossRefPubMed
12.
go back to reference Mansour G, Aziz N, Sharma R, Falcone T, Goldberg J, Agarwal A. The impact of peritoneal fluid from healthy women and from women with endometriosis on sperm DNA and its relationship to the sperm deformity index. Fertil Steril. 2009;92:61–7.CrossRefPubMed Mansour G, Aziz N, Sharma R, Falcone T, Goldberg J, Agarwal A. The impact of peritoneal fluid from healthy women and from women with endometriosis on sperm DNA and its relationship to the sperm deformity index. Fertil Steril. 2009;92:61–7.CrossRefPubMed
13.
go back to reference Perdichizzi A, Nicoletti F, La Vignera S, Barone N, D’Agata R, Vicari E, et al. Effects of tumour necrosis factor-alpha on human sperm motility and apoptosis. J Clin Immunol. 2007;27:152–62.CrossRefPubMed Perdichizzi A, Nicoletti F, La Vignera S, Barone N, D’Agata R, Vicari E, et al. Effects of tumour necrosis factor-alpha on human sperm motility and apoptosis. J Clin Immunol. 2007;27:152–62.CrossRefPubMed
14.
go back to reference Mansour G, Sharma RK, Agarwal A, Falcone T. Endometriosis-induced alterations in mouse metaphase II oocyte microtubules and chromosomal alignment: a possible cause of infertility. Fertil Steril. 2010;94:1894–9.CrossRefPubMed Mansour G, Sharma RK, Agarwal A, Falcone T. Endometriosis-induced alterations in mouse metaphase II oocyte microtubules and chromosomal alignment: a possible cause of infertility. Fertil Steril. 2010;94:1894–9.CrossRefPubMed
16.
go back to reference Piromlertamorn W, Saeng-anan U, Vutyavanich T. Effects of ovarian endometriotic fluid exposure on fertilization rate of mouse oocytes and subsequent embryo development. Reprod Biol Endocrinol. 2013;11:4.CrossRefPubMedCentralPubMed Piromlertamorn W, Saeng-anan U, Vutyavanich T. Effects of ovarian endometriotic fluid exposure on fertilization rate of mouse oocytes and subsequent embryo development. Reprod Biol Endocrinol. 2013;11:4.CrossRefPubMedCentralPubMed
17.
go back to reference Moon CE, Bertero MC, Curry TE, London SN, Muse KN, Sharpe KL, et al. The presence of luteinized unruptured follicle syndrome and altered folliculogenesis in rats with surgically induced endometriosis. Am J Obstet Gynecol. 1993;169:676–82.CrossRefPubMed Moon CE, Bertero MC, Curry TE, London SN, Muse KN, Sharpe KL, et al. The presence of luteinized unruptured follicle syndrome and altered folliculogenesis in rats with surgically induced endometriosis. Am J Obstet Gynecol. 1993;169:676–82.CrossRefPubMed
18.
go back to reference Stilley JA, Woods-Marshall R, Sutovsky M, Sutovsky P, Sharpe-Timms KL. Reduced fecundity in female rats with surgically induced endometriosis and in their daughters: a potential role for tissue inhibitors of metalloproteinase 1. Biol Reprod. 2009;80:649–56.CrossRefPubMedCentralPubMed Stilley JA, Woods-Marshall R, Sutovsky M, Sutovsky P, Sharpe-Timms KL. Reduced fecundity in female rats with surgically induced endometriosis and in their daughters: a potential role for tissue inhibitors of metalloproteinase 1. Biol Reprod. 2009;80:649–56.CrossRefPubMedCentralPubMed
19.
go back to reference Pal AK, Biswas S, Goswami SK, Kabir SN. Effect of pelvic endometrial implants on overall reproductive functions of female rats. Biol Reprod. 1999;60:954–8.CrossRefPubMed Pal AK, Biswas S, Goswami SK, Kabir SN. Effect of pelvic endometrial implants on overall reproductive functions of female rats. Biol Reprod. 1999;60:954–8.CrossRefPubMed
20.
go back to reference Vernon MW, Wilson EA. Studies on the surgical induction of endometriosis in the rat. Fertil Steril. 1985;44:684–94.PubMed Vernon MW, Wilson EA. Studies on the surgical induction of endometriosis in the rat. Fertil Steril. 1985;44:684–94.PubMed
21.
go back to reference Barragan JC, Brotons J, Ruiz JA, Acien P. Experimentally induced endometriosis in rats: effect on fertility and the effects of pregnancy and lactation on the ectopic endometrial tissue. Fertil Steril. 1992;58:1215–9.PubMed Barragan JC, Brotons J, Ruiz JA, Acien P. Experimentally induced endometriosis in rats: effect on fertility and the effects of pregnancy and lactation on the ectopic endometrial tissue. Fertil Steril. 1992;58:1215–9.PubMed
22.
go back to reference Furukubo M, Fujino Y, Umesaki N, Ogita S. Effects of endometrial stromal cells and peritoneal fluid on fertility associated with endometriosis. Osaka City Med J. 1998;44:43–54.PubMed Furukubo M, Fujino Y, Umesaki N, Ogita S. Effects of endometrial stromal cells and peritoneal fluid on fertility associated with endometriosis. Osaka City Med J. 1998;44:43–54.PubMed
23.
go back to reference Umezawa M, Saito Y, Tanaka-Hattori N, Takeda K, Ihara T, Sugamata M. Expression profile of extracellular matrix and adhesion molecules in the development of endometriosis in a mouse model. Reprod Sci. 2012;19:1365–72.CrossRefPubMed Umezawa M, Saito Y, Tanaka-Hattori N, Takeda K, Ihara T, Sugamata M. Expression profile of extracellular matrix and adhesion molecules in the development of endometriosis in a mouse model. Reprod Sci. 2012;19:1365–72.CrossRefPubMed
24.
go back to reference Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, Qin J, et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18:1102–11.CrossRefPubMedCentralPubMed Han SJ, Hawkins SM, Begum K, Jung SY, Kovanci E, Qin J, et al. A new isoform of steroid receptor coactivator-1 is crucial for pathogenic progression of endometriosis. Nat Med. 2012;18:1102–11.CrossRefPubMedCentralPubMed
25.
go back to reference Laschke MW, Giebels C, Nickels RM, Scheuer C, Menger MD. Endothelial progenitor cells contribute to the vascularization of endometriotic lesions. Am J Pathol. 2011;178:442–50.CrossRefPubMedCentralPubMed Laschke MW, Giebels C, Nickels RM, Scheuer C, Menger MD. Endothelial progenitor cells contribute to the vascularization of endometriotic lesions. Am J Pathol. 2011;178:442–50.CrossRefPubMedCentralPubMed
26.
go back to reference Becker CM, Beaudry P, Funakoshi T, Benny O, Zaslavsky A, Zurakowski D, et al. Circulating endothelial progenitor cells are up-regulated in a mouse model of endometriosis. Am J Pathol. 2011;178:1782–91.CrossRefPubMedCentralPubMed Becker CM, Beaudry P, Funakoshi T, Benny O, Zaslavsky A, Zurakowski D, et al. Circulating endothelial progenitor cells are up-regulated in a mouse model of endometriosis. Am J Pathol. 2011;178:1782–91.CrossRefPubMedCentralPubMed
27.
go back to reference Fang Z, Yang S, Gurates B, Tamura M, Simpson E, Evans D, et al. Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue. J Clin Endocrinol Metab. 2002;87:3460–6.CrossRefPubMed Fang Z, Yang S, Gurates B, Tamura M, Simpson E, Evans D, et al. Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue. J Clin Endocrinol Metab. 2002;87:3460–6.CrossRefPubMed
28.
go back to reference Rudzitis-Auth J, Menger MD, Laschke MW. Resveratrol is a potent inhibitor of vascularization and cell proliferation in experimental endometriosis. Hum Reprod. 2013;28:1339–47.CrossRefPubMed Rudzitis-Auth J, Menger MD, Laschke MW. Resveratrol is a potent inhibitor of vascularization and cell proliferation in experimental endometriosis. Hum Reprod. 2013;28:1339–47.CrossRefPubMed
29.
go back to reference Pelch KE, Sharpe-Timms KL, Nagel SC. Mouse model of surgically-induced endometriosis by auto-transplantation of uterine tissue. J Vis Exp. 2012: e3396. Pelch KE, Sharpe-Timms KL, Nagel SC. Mouse model of surgically-induced endometriosis by auto-transplantation of uterine tissue. J Vis Exp. 2012: e3396.
30.
go back to reference Eroglu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertil Steril. 1998;69:944–57.CrossRefPubMed Eroglu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertil Steril. 1998;69:944–57.CrossRefPubMed
31.
go back to reference Schatten G, Simerly C, Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc Natl Acad Sci U S A. 1985;82:4152–6.CrossRefPubMedCentralPubMed Schatten G, Simerly C, Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc Natl Acad Sci U S A. 1985;82:4152–6.CrossRefPubMedCentralPubMed
32.
go back to reference Boiso I, Marti M, Santalo J, Ponsa M, Barri PN, Veiga A. A confocal microscopy analysis of the spindle and chromosome configurations of human oocytes cryopreserved at the germinal vesicle and metaphase II stage. Hum Reprod. 2002;17:1885–91.CrossRefPubMed Boiso I, Marti M, Santalo J, Ponsa M, Barri PN, Veiga A. A confocal microscopy analysis of the spindle and chromosome configurations of human oocytes cryopreserved at the germinal vesicle and metaphase II stage. Hum Reprod. 2002;17:1885–91.CrossRefPubMed
33.
go back to reference Choi WJ, Banerjee J, Falcone T, Bena J, Agarwal A, Sharma RK. Oxidative stress and tumor necrosis factor-alpha-induced alterations in metaphase II mouse oocyte spindle structure. Fertil Steril. 2007;88:1220–31.CrossRefPubMed Choi WJ, Banerjee J, Falcone T, Bena J, Agarwal A, Sharma RK. Oxidative stress and tumor necrosis factor-alpha-induced alterations in metaphase II mouse oocyte spindle structure. Fertil Steril. 2007;88:1220–31.CrossRefPubMed
34.
go back to reference Tarin JJ, Vendrell FJ, Ten J, Blanes R, van Blerkom J, Cano A. The oxidizing agent tertiary butyl hydroperoxide induces disturbances in spindle organization, c-meiosis, and aneuploidy in mouse oocytes. Mol Hum Reprod. 1996;2:895–901.CrossRefPubMed Tarin JJ, Vendrell FJ, Ten J, Blanes R, van Blerkom J, Cano A. The oxidizing agent tertiary butyl hydroperoxide induces disturbances in spindle organization, c-meiosis, and aneuploidy in mouse oocytes. Mol Hum Reprod. 1996;2:895–901.CrossRefPubMed
35.
go back to reference Richter HE, Holley RL, Andrews WW, Owen J, Miller KB. The association of interleukin 6 with clinical and laboratory parameters of acute pelvic inflammatory disease. Am J Obstet Gynecol. 1999;181:940–4.CrossRefPubMed Richter HE, Holley RL, Andrews WW, Owen J, Miller KB. The association of interleukin 6 with clinical and laboratory parameters of acute pelvic inflammatory disease. Am J Obstet Gynecol. 1999;181:940–4.CrossRefPubMed
36.
go back to reference Bedaiwy MA, Falcone T, Sharma RK, Goldberg JM, Attaran M, Nelson DR, et al. Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum Reprod. 2002;17:426–31.CrossRefPubMed Bedaiwy MA, Falcone T, Sharma RK, Goldberg JM, Attaran M, Nelson DR, et al. Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum Reprod. 2002;17:426–31.CrossRefPubMed
37.
go back to reference Ebner T, Moser M, Yaman C, Feichtinger O, Hartl J, Tews G. Elective transfer of embryos selected on the basis of first polar body morphology is associated with increased rates of implantation and pregnancy. Fertil Steril. 1999;72:599–603.CrossRefPubMed Ebner T, Moser M, Yaman C, Feichtinger O, Hartl J, Tews G. Elective transfer of embryos selected on the basis of first polar body morphology is associated with increased rates of implantation and pregnancy. Fertil Steril. 1999;72:599–603.CrossRefPubMed
38.
go back to reference De Santis L, Cino I, Rabellotti E, Calzi F, Persico P, Borini A, et al. Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod BioMed Online. 2005;11:36–42.CrossRefPubMed De Santis L, Cino I, Rabellotti E, Calzi F, Persico P, Borini A, et al. Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod BioMed Online. 2005;11:36–42.CrossRefPubMed
39.
go back to reference Rienzi L, Ubaldi FM, Iacobelli M, Minasi MG, Romano S, Ferrero S, et al. Significance of metaphase II human oocyte morphology on ICSI outcome. Fertil Steril. 2008;90:1692–700.CrossRefPubMed Rienzi L, Ubaldi FM, Iacobelli M, Minasi MG, Romano S, Ferrero S, et al. Significance of metaphase II human oocyte morphology on ICSI outcome. Fertil Steril. 2008;90:1692–700.CrossRefPubMed
40.
go back to reference Choi T, Fukasawa K, Zhou R, Tessarollo L, Borror K, Resau J, et al. The Mos/mitogen-activated protein kinase (MAPK) pathway regulates the size and degradation of the first polar body in maturing mouse oocytes. Proc Natl Acad Sci U S A. 1996;93:7032–5.CrossRefPubMedCentralPubMed Choi T, Fukasawa K, Zhou R, Tessarollo L, Borror K, Resau J, et al. The Mos/mitogen-activated protein kinase (MAPK) pathway regulates the size and degradation of the first polar body in maturing mouse oocytes. Proc Natl Acad Sci U S A. 1996;93:7032–5.CrossRefPubMedCentralPubMed
41.
go back to reference Zhang H, Zhang Y, Zhao H, Zhang Y, Chen Q, Peng H, et al. Hormonal regulation of ovarian bursa fluid in mice and involvement of aquaporins. PLoS One. 2013;8:e63823.CrossRefPubMedCentralPubMed Zhang H, Zhang Y, Zhao H, Zhang Y, Chen Q, Peng H, et al. Hormonal regulation of ovarian bursa fluid in mice and involvement of aquaporins. PLoS One. 2013;8:e63823.CrossRefPubMedCentralPubMed
42.
go back to reference Rodriguez A, Catalan V, Gomez-Ambrosi J, Garcia-Navarro S, Rotellar F, Valenti V, et al. Insulin- and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade. J Clin Endocrinol Metab. 2011;96:E586–97.CrossRefPubMed Rodriguez A, Catalan V, Gomez-Ambrosi J, Garcia-Navarro S, Rotellar F, Valenti V, et al. Insulin- and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade. J Clin Endocrinol Metab. 2011;96:E586–97.CrossRefPubMed
43.
go back to reference Shahine LK, Burney RO, Behr B, Milki AA, Westphal LM, Lathi RB. Embryo quality before and after surgical treatment of endometriosis in infertile patients. J Assist Reprod Genet. 2009;26:69–73.CrossRefPubMedCentralPubMed Shahine LK, Burney RO, Behr B, Milki AA, Westphal LM, Lathi RB. Embryo quality before and after surgical treatment of endometriosis in infertile patients. J Assist Reprod Genet. 2009;26:69–73.CrossRefPubMedCentralPubMed
44.
go back to reference Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC. Increased incidence of aberrant morphological phenotypes in human embryogenesis–an association with endometriosis. J Assist Reprod Genet. 1995;12:106–12.CrossRefPubMed Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC. Increased incidence of aberrant morphological phenotypes in human embryogenesis–an association with endometriosis. J Assist Reprod Genet. 1995;12:106–12.CrossRefPubMed
45.
go back to reference Pellicer A, Oliveira N, Ruiz A, Remohi J, Simon C. Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod. 1995;10 Suppl 2:91–7.CrossRefPubMed Pellicer A, Oliveira N, Ruiz A, Remohi J, Simon C. Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod. 1995;10 Suppl 2:91–7.CrossRefPubMed
46.
47.
go back to reference Colette S, Donnez J. Animal models in endometriosis experimental research. Gynecol Obstet Fertil. 2012;40:494–6.CrossRefPubMed Colette S, Donnez J. Animal models in endometriosis experimental research. Gynecol Obstet Fertil. 2012;40:494–6.CrossRefPubMed
48.
go back to reference Ertzeid G, Storeng R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod. 2001;16:221–5.CrossRefPubMed Ertzeid G, Storeng R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod. 2001;16:221–5.CrossRefPubMed
49.
go back to reference Rajkumar K, Schott PW, Simpson CW. The rat as an animal model for endometriosis to examine recurrence of ectopic endometrial tissue after regression. Fertil Steril. 1990;53:921–5.PubMed Rajkumar K, Schott PW, Simpson CW. The rat as an animal model for endometriosis to examine recurrence of ectopic endometrial tissue after regression. Fertil Steril. 1990;53:921–5.PubMed
Metadata
Title
Effect of induced peritoneal endometriosis on oocyte and embryo quality in a mouse model
Authors
J. Cohen
A. Ziyyat
I. Naoura
N. Chabbert-Buffet
S. Aractingi
E. Darai
B. Lefevre
Publication date
01-02-2015
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 2/2015
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-014-0390-1

Other articles of this Issue 2/2015

Journal of Assisted Reproduction and Genetics 2/2015 Go to the issue