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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Distinct localisation of lipids in the ovarian follicular environment

Tawiwan Pantasri A D , Linda L. Wu A , M. Louise Hull A B , Thomas R. Sullivan C , Michael Barry B , Robert J. Norman A B and Rebecca L. Robker A E
+ Author Affiliations
- Author Affiliations

A The Robinson Research Institute, School of Paediatrics & Reproductive Health, University of Adelaide, Adelaide, SA 5005, Australia.

B Fertility SA, St Andrew’s Hospital, Adelaide, SA, 5000, Australia.

C School of Population Health, University of Adelaide, Adelaide, SA 5005, Australia.

D Present address: Department of Obstetrics and Gynaecology, Chiangmai University, Chiang Mai, Thailand.

E Corresponding author. Email: rebecca.robker@adelaide.edu.au

Reproduction, Fertility and Development 27(4) 593-601 https://doi.org/10.1071/RD14321
Submitted: 29 August 2014  Accepted: 8 January 2015   Published: 10 March 2015

Abstract

Obesity is associated with decreased pregnancy rates due, in part, to compromised oocyte quality. The aim of the present cross-sectional study of 84 women undergoing oocyte aspiration was to: (1) compare insulin, lipids and glucose in follicular fluid with serum; (2) determine whether increased body mass index (BMI) and waist circumference, hyperinsulinaemia, dyslipidaemia or metabolic syndrome altered follicular fluid metabolites; and (3) determine relative lipid content in oocytes to reveal any influence of these parameters on oocyte quality and IVF outcomes. Insulin, glucose, triglyceride and free fatty acids were lower in follicular fluid than blood and not strictly correlated between compartments. Insulin, glucose and triglyceride positively correlated with increasing BMI and waist circumference in blood and follicular fluid. Insulin increased in follicular fluid in association with metabolic syndrome. Free fatty acid composition analysis showed saturated fatty acids, particularly palmitic and stearic acid, to be more prevalent in follicular fluid than blood. There were no associations between follicular fluid metabolites or oocyte lipid content and clinical outcomes; however, oocyte immaturity correlated with follicular fluid glucose and fatty acid levels, as well as metabolic syndrome. The present study confirms that the human ovarian follicular environment surrounding the oocyte exhibits a unique metabolite profile compared with blood, with distinct localisation of lipids within follicular fluid and oocytes.

Additional keywords: fatty acid, glucose, insulin, oocyte.


References

Alberti, K. G., Zimmet, P., and Shaw, J. (2005). The metabolic syndrome: a new worldwide definition. Lancet 366, 1059–1062.
The metabolic syndrome: a new worldwide definition.Crossref | GoogleScholarGoogle Scholar | 16182882PubMed |

Awartani, K. A., Nahas, S., Al Hassan, S. H., Al Deery, M. A., and Coskun, S. (2009). Infertility treatment outcome in sub groups of obese population. Reprod. Biol. Endocrinol. 7, 52.
Infertility treatment outcome in sub groups of obese population.Crossref | GoogleScholarGoogle Scholar | 19473499PubMed |

Brewer, C. J., and Balen, A. H. (2010). The adverse effects of obesity on conception and implantation. Reproduction 140, 347–364.
The adverse effects of obesity on conception and implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Cnu7fI&md5=60a335247c8d5c417a5d658e5d3075cdCAS | 20395425PubMed |

Chen, S. J., Chuang, L. T., and Chen, S. N. (2014). Incorporation of eicosatrienoic acid exerts mild anti-inflammatory properties in murine RAW264.7 cells. Inflammation , .
Incorporation of eicosatrienoic acid exerts mild anti-inflammatory properties in murine RAW264.7 cells.Crossref | GoogleScholarGoogle Scholar |

Cordeiro, F. B., Cataldi, T. R., do Vale Teixeira da Costa, L., de Lima, C. B., Stevanato, J., Zylbersztejn, D. S., Ferreira, C. R., Eberlin, M. N., Cedenho, A. P., and Turco, E. G. (2014). Follicular fluid lipid fingerprinting from women with PCOS and hyper response during IVF treatment. J. Assist. Reprod. Genet. , .
Follicular fluid lipid fingerprinting from women with PCOS and hyper response during IVF treatment.Crossref | GoogleScholarGoogle Scholar | 25374394PubMed |

Depalo, R., Garruti, G., Totaro, I., Panzarino, M., Vacca, M. P., Giorgino, F., and Selvaggi, L. E. (2011). Oocyte morphological abnormalities in overweight women undergoing in vitro fertilization cycles. Gynecol. Endocrinol. 27, 880–884.
Oocyte morphological abnormalities in overweight women undergoing in vitro fertilization cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlWms77L&md5=43d7b37c4faf2e60d7d28899b109546cCAS | 21500991PubMed |

Dunning, K. R., Russell, D. L., and Robker, R. L. (2014). Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation. Reproduction 148, R15–R27.
Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyrtrnE&md5=165dea5bbc533770beafa05b87509710CAS | 24760880PubMed |

Expert Panel on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults (1998). Executive summary of the clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults. Arch. Intern. Med. 158, 1855–1867.
Executive summary of the clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults.Crossref | GoogleScholarGoogle Scholar | 9759681PubMed |

Ferlitsch, K., Sator, M. O., Gruber, D. M., Rucklinger, E., Gruber, C. J., and Huber, J. C. (2004). Body mass index, follicle-stimulating hormone and their predictive value in in vitro fertilization. J. Assist. Reprod. Genet. 21, 431–436.
Body mass index, follicle-stimulating hormone and their predictive value in in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 15704518PubMed |

Gesink Law, D. C., Maclehose, R. F., and Longnecker, M. P. (2007). Obesity and time to pregnancy. Hum. Reprod. 22, 414–420.
Obesity and time to pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s%2FhvFCktA%3D%3D&md5=966bdebbb8cb4113612832f837afb92fCAS | 17095518PubMed |

Grodstein, F., Goldman, M. B., and Cramer, D. W. (1994). Body mass index and ovulatory infertility. Epidemiology 5, 247–250.
Body mass index and ovulatory infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3islWltg%3D%3D&md5=a308f79227ad05649e30b9cb89ffe145CAS | 8173001PubMed |

Hohmann, F. P., Macklon, N. S., and Fauser, B. C. (2003). A randomized comparison of two ovarian stimulation protocols with gonadotropin-releasing hormone (GnRH) antagonist cotreatment for in vitro fertilization commencing recombinant follicle-stimulating hormone on cycle Day 2 or 5 with the standard long GnRH agonist protocol. J. Clin. Endocrinol. Metab. 88, 166–173.
A randomized comparison of two ovarian stimulation protocols with gonadotropin-releasing hormone (GnRH) antagonist cotreatment for in vitro fertilization commencing recombinant follicle-stimulating hormone on cycle Day 2 or 5 with the standard long GnRH agonist protocol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVertA%3D%3D&md5=678ba1ff77b8dcf236d104a417163223CAS | 12519847PubMed |

Igosheva, N., Abramov, A. Y., Poston, L., Eckert, J. J., Fleming, T. P., Duchen, M. R., and McConnell, J. (2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE 5, e10074.
Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes.Crossref | GoogleScholarGoogle Scholar | 20404917PubMed |

Jensen, T. K., Scheike, T., Keiding, N., Schaumburg, I., and Grandjean, P. (1999). Fecundability in relation to body mass and menstrual cycle patterns. Epidemiology 10, 422–428.
Fecundability in relation to body mass and menstrual cycle patterns.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzivVejtw%3D%3D&md5=944dbd93291423e5ea0eb397c1740fa5CAS | 10401878PubMed |

Jungheim, E. S., Macones, G. A., Odem, R. R., Patterson, B. W., Lanzendorf, S. E., Ratts, V. S., and Moley, K. H. (2011). Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization. Fertil. Steril. 95, 1970–1974.
Associations between free fatty acids, cumulus oocyte complex morphology and ovarian function during in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFymt7s%3D&md5=76d9b420ab9daf852b82db55d5d51d58CAS | 21353671PubMed |

Kassi, E., Pervanidou, P., Kaltsas, G., and Chrousos, G. (2011). Metabolic syndrome: definitions and controversies. BMC Med. 9, 48.
Metabolic syndrome: definitions and controversies.Crossref | GoogleScholarGoogle Scholar | 21542944PubMed |

Legro, R. S., Castracane, V. D., and Kauffman, R. P. (2004). Detecting insulin resistance in polycystic ovary syndrome: purposes and pitfalls. Obstet. Gynecol. Surv. 59, 141–154.
Detecting insulin resistance in polycystic ovary syndrome: purposes and pitfalls.Crossref | GoogleScholarGoogle Scholar | 14752302PubMed |

Leroy, J. L., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., and Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 130, 485–495.
Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFent7rJ&md5=16ddfb8af1de3a55f051d7e88b361557CAS | 16183866PubMed |

Luke, B., Brown, M. B., Missmer, S. A., Bukulmez, O., Leach, R., and Stern, J. E. (2011a). The effect of increasing obesity on the response to and outcome of assisted reproductive technology: a national study. Fertil. Steril. 96, 820–825.
The effect of increasing obesity on the response to and outcome of assisted reproductive technology: a national study.Crossref | GoogleScholarGoogle Scholar | 21821244PubMed |

Luke, B., Brown, M. B., Stern, J. E., Missmer, S. A., Fujimoto, V. Y., and Leach, R. (2011b). Female obesity adversely affects assisted reproductive technology (ART) pregnancy and live birth rates. Hum. Reprod. 26, 245–252.
Female obesity adversely affects assisted reproductive technology (ART) pregnancy and live birth rates.Crossref | GoogleScholarGoogle Scholar | 21071489PubMed |

Luzzo, K. M., Wang, Q., Purcell, S. H., Chi, M., Jimenez, P. T., Grindler, N., Schedl, T., and Moley, K. H. (2012). High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS ONE 7, e49217.
High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKjtrvN&md5=9bc77d7bb0f30a2e41cdb8f2da55d9a2CAS | 23152876PubMed |

Machtinger, R., Combelles, C. M., Missmer, S. A., Correia, K. F., Fox, J. H., and Racowsky, C. (2012). The association between severe obesity and characteristics of failed fertilized oocytes. Hum. Reprod. 27, 3198–3207.
The association between severe obesity and characteristics of failed fertilized oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFKmu7vM&md5=edd16e47b7f314bf31e945ad56e75f72CAS | 22968161PubMed |

Matorras, R., Ruiz, J. I., Mendoza, R., Ruiz, N., Sanjurjo, P., and Rodriguez-Escudero, F. J. (1998). Fatty acid composition of fertilization-failed human oocytes. Hum. Reprod. 13, 2227–2230.
Fatty acid composition of fertilization-failed human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmt1Wjsb4%3D&md5=17985be599ba6465a0daebf4b50a1ba2CAS | 9756301PubMed |

McCormick, B., Thomas, M., Maxwell, R., Williams, D., and Aubuchon, M. (2008). Effects of polycystic ovarian syndrome on in vitro fertilization–embryo transfer outcomes are influenced by body mass index. Fertil. Steril. 90, 2304–2309.
Effects of polycystic ovarian syndrome on in vitro fertilization–embryo transfer outcomes are influenced by body mass index.Crossref | GoogleScholarGoogle Scholar | 18191852PubMed |

McKeegan, P. J., and Sturmey, R. G. (2012). The role of fatty acids in oocyte and early embryo development. Reprod. Fertil. Dev. 24, 59–67.
The role of fatty acids in oocyte and early embryo development.Crossref | GoogleScholarGoogle Scholar |

Niu, Z., Lin, N., Gu, R., Sun, Y., and Feng, Y. (2014). Associations between insulin resistance, free fatty acids, and oocyte quality in polycystic ovary syndrome during in vitro fertilization. J. Clin. Endocrinol. Metab. 99, E2269–E2276.
Associations between insulin resistance, free fatty acids, and oocyte quality in polycystic ovary syndrome during in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFGhsr7P&md5=70f382a73a6b01118e36e88185aa0df0CAS | 24694334PubMed |

O’Gorman, A., Wallace, M., Cottell, E., Gibney, M. J., McAuliffe, F. M., Wingfield, M., and Brennan, L. (2013). Metabolic profiling of human follicular fluid identifies potential biomarkers of oocyte developmental competence. Reproduction 146, 389–395.
Metabolic profiling of human follicular fluid identifies potential biomarkers of oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1ygtr3K&md5=4cd68703a2b42043e3e1bb14b7e86ff1CAS | 23886995PubMed |

Piñero-Sagredo, E., Nunes, S., de los Santos, M. J., Celda, B., and Esteve, V. (2010). NMR metabolic profile of human follicular fluid. NMR Biomed. 23, 485–495.
NMR metabolic profile of human follicular fluid.Crossref | GoogleScholarGoogle Scholar | 20336675PubMed |

Prates, E. G., Nunes, J. T., and Pereira, R. M. (2014). A role of lipid metabolism during cumulus–oocyte complex maturation: impact of lipid modulators to improve embryo production. Mediat. Inflamm. 2014, 692067.
A role of lipid metabolism during cumulus–oocyte complex maturation: impact of lipid modulators to improve embryo production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cnosFSmug%3D%3D&md5=9c449ca018f77de3a65dc4e4445e6bd7CAS |

Rich-Edwards, J. W., Spiegelman, D., Garland, M., Hertzmark, E., Hunter, D. J., Colditz, G. A., Willett, W. C., Wand, H., and Manson, J. E. (2002). Physical activity, body mass index, and ovulatory disorder infertility. Epidemiology 13, 184–190.
Physical activity, body mass index, and ovulatory disorder infertility.Crossref | GoogleScholarGoogle Scholar | 11880759PubMed |

Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., and Norman, R. J. (2009). Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J. Clin. Endocrinol. Metab. 94, 1533–1540.
Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVCqtrw%3D&md5=ad9fc9f21f34fed2964925dd65571412CAS | 19223519PubMed |

Rodgers, R. J., and Irving-Rodgers, H. F. (2010). Formation of the ovarian follicular antrum and follicular fluid. Biol. Reprod. 82, 1021–1029.
Formation of the ovarian follicular antrum and follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVCgtrs%3D&md5=15aaf4594527f38881e4f8662e28d35aCAS | 20164441PubMed |

Shalgi, R., Kraicer, P., Rimon, A., Pinto, M., and Soferman, N. (1973). Proteins of human follicular fluid: the blood–follicle barrier. Fertil. Steril. 24, 429–434.
| 1:CAS:528:DyaE3sXksVSmt7g%3D&md5=675008b348769aed3742df1b6d935635CAS | 4122802PubMed |

Song, Y., Manson, J. E., Tinker, L., Howard, B. V., Kuller, L. H., Nathan, L., Rifai, N., and Liu, S. (2007). Insulin sensitivity and insulin secretion determined by homeostasis model assessment and risk of diabetes in a multiethnic cohort of women: the Women’s Health Initiative Observational Study. Diabetes Care 30, 1747–1752.
Insulin sensitivity and insulin secretion determined by homeostasis model assessment and risk of diabetes in a multiethnic cohort of women: the Women’s Health Initiative Observational Study.Crossref | GoogleScholarGoogle Scholar | 17468352PubMed |

Styne-Gross, A., Elkind-Hirsch, K., and Scott, R. T. (2005). Obesity does not impact implantation rates or pregnancy outcome in women attempting conception through oocyte donation. Fertil. Steril. 83, 1629–1634.
Obesity does not impact implantation rates or pregnancy outcome in women attempting conception through oocyte donation.Crossref | GoogleScholarGoogle Scholar | 15950629PubMed |

Sutton, M. L., Gilchrist, R. B., and Thompson, J. G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update 9, 35–48.
Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVelt7Y%3D&md5=75859ff3ff369af7cc6bb67f34275966CAS | 12638780PubMed |

The Rotterdam ESHRE/ASRM-sponsored PCOS Consensus Workshop Group (2004). Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum. Reprod. 19, 41–47.
Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS).Crossref | GoogleScholarGoogle Scholar | 14688154PubMed |

Tian, L., Shen, H., Lu, Q., Norman, R. J., and Wang, J. (2007). Insulin resistance increases the risk of spontaneous abortion after assisted reproduction technology treatment. J. Clin. Endocrinol. Metab. 92, 1430–1433.
Insulin resistance increases the risk of spontaneous abortion after assisted reproduction technology treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVSrt7c%3D&md5=63cc00b59efb1e1d452b9100d265bc1cCAS | 17244790PubMed |

Valckx, S. D., De Pauw, I., De Neubourg, D., Inion, I., Berth, M., Fransen, E., Bols, P. E., and Leroy, J. L. (2012). BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality. Hum. Reprod. 27, 3531–3539.
BMI-related metabolic composition of the follicular fluid of women undergoing assisted reproductive treatment and the consequences for oocyte and embryo quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKrsLrL&md5=36e8e2c48e7445163a84e1ab94e8a470CAS | 23019302PubMed |

Valckx, S. D., Arias-Alvarez, M., De Pauw, I., Fievez, V., Vlaeminck, B., Fransen, E., Bols, P. E., and Leroy, J. L. (2014). Fatty acid composition of the follicular fluid of normal weight, overweight and obese women undergoing assisted reproductive treatment: a descriptive cross-sectional study. Reprod. Biol. Endocrinol. 12, 13.
Fatty acid composition of the follicular fluid of normal weight, overweight and obese women undergoing assisted reproductive treatment: a descriptive cross-sectional study.Crossref | GoogleScholarGoogle Scholar | 24498875PubMed |

Van Blerkom, J., and Henry, G. (1992). Oocyte dysmorphism and aneuploidy in meiotically mature human oocytes after ovarian stimulation. Hum. Reprod. 7, 379–390.
| 1:STN:280:DyaK383mvValtA%3D%3D&md5=a4ae4b633bc7ca753fe170ea9970c1f5CAS | 1587948PubMed |

van der Steeg, J. W., Steures, P., Eijkemans, M. J., Habbema, J. D., Hompes, P. G., Burggraaff, J. M., Oosterhuis, G. J., Bossuyt, P. M., van der Veen, F., and Mol, B. W. (2008). Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women. Hum. Reprod. 23, 324–328.
Obesity affects spontaneous pregnancy chances in subfertile, ovulatory women.Crossref | GoogleScholarGoogle Scholar | 18077317PubMed |

Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E., and Leroy, J. L. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS ONE 6, e23183.
Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKmsLjM&md5=b6eb69e3072d782b967fdaef51eb2625CAS | 21858021PubMed |

Van Hoeck, V., Leroy, J. L., Arias Alvarez, M., Rizos, D., Gutierrez-Adan, A., Schnorbusch, K., Bols, P. E., Leese, H. J., and Sturmey, R. G. (2013). Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 145, 33–44.
Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGisb8%3D&md5=2e22f5e936a1f5d16f80b6bbb94a824bCAS | 23108110PubMed |

Wang, J. X., Davies, M., and Norman, R. J. (2000). Body mass and probability of pregnancy during assisted reproduction treatment: retrospective study. BMJ 321, 1320–1321.
Body mass and probability of pregnancy during assisted reproduction treatment: retrospective study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FmsVKjtA%3D%3D&md5=6f4f801bd0a4bd73141c04be569cde05CAS | 11090515PubMed |

Wise, L. A., Rothman, K. J., Mikkelsen, E. M., Sorensen, H. T., Riis, A., and Hatch, E. E. (2010). An Internet-based prospective study of body size and time-to-pregnancy. Hum. Reprod. 25, 253–264.
An Internet-based prospective study of body size and time-to-pregnancy.Crossref | GoogleScholarGoogle Scholar | 19828554PubMed |

Wu, L. L., Dunning, K. R., Yang, X., Russell, D. L., Lane, M., Norman, R. J., and Robker, R. L. (2010). High-fat diet causes lipotoxicity responses in cumulus–oocyte complexes and decreased fertilization rates. Endocrinology 151, 5438–5445.
High-fat diet causes lipotoxicity responses in cumulus–oocyte complexes and decreased fertilization rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKks7bL&md5=eefe18c6b932287de00f82f7d18fd452CAS | 20861227PubMed |

Yang, Y. J., Zhang, Y. J., and Li, Y. (2009). Ultrastructure of human oocytes of different maturity stages and the alteration during in vitro maturation. Fertil. Steril. 92, 396.e1–396.e6.
Ultrastructure of human oocytes of different maturity stages and the alteration during in vitro maturation.Crossref | GoogleScholarGoogle Scholar |

Yang, X., Wu, L. L., Chura, L. R., Liang, X., Lane, M., Norman, R. J., and Robker, R. L. (2012). Exposure to lipid-rich follicular fluid is associated with endoplasmic reticulum stress and impaired oocyte maturation in cumulus-oocyte complexes. Fertil. Steril. 97, 1438–1443.
Exposure to lipid-rich follicular fluid is associated with endoplasmic reticulum stress and impaired oocyte maturation in cumulus-oocyte complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktlChsbs%3D&md5=86e359977edd7ce09a76e8239914f8f8CAS | 22440252PubMed |

Zhang, D., Zhu, Y., Gao, H., Zhou, B., Zhang, R., Wang, T., Ding, G., Qu, F., Huang, H., and Lu, X. (2010). Overweight and obesity negatively affect the outcomes of ovarian stimulation and in vitro fertilisation: a cohort study of 2628 Chinese women. Gynecol. Endocrinol. 26, 325–332.
Overweight and obesity negatively affect the outcomes of ovarian stimulation and in vitro fertilisation: a cohort study of 2628 Chinese women.Crossref | GoogleScholarGoogle Scholar | 20192898PubMed |