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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Steroid hormone concentrations and body mass are differently affected by polyunsaturated fatty acids during the oestrous cycle in guinea pigs

Matthias Nemeth A D , Bernard Wallner A B , Carina Siutz A , Elisabeth Pschernig A , Karl-Heinz Wagner C and Eva Millesi A
+ Author Affiliations
- Author Affiliations

A Department of Behavioural Biology, University of Vienna, Faculty of Life Sciences, Althanstrasse 14, 1090 Vienna, Austria.

B Department of Anthropology, University of Vienna, Faculty of Life Sciences, Althanstrasse 14, 1090 Vienna, Austria.

C Department of Nutritional Sciences, University of Vienna, Faculty of Life Sciences, Althanstrasse 14, 1090 Vienna, Austria.

D Corresponding author. Email: matthias.nemeth@univie.ac.at

Reproduction, Fertility and Development 30(8) 1077-1086 https://doi.org/10.1071/RD17242
Submitted: 28 June 2017  Accepted: 4 December 2017   Published: 8 January 2018

Abstract

Reproductive functions in female mammals can be significantly affected by the actions of dietary polyunsaturated fatty acids (PUFAs) on steroid hormone secretion rates. Nevertheless, the effects of plasma free PUFAs on the oestrous cycle have seldom been considered. Therefore, in the present study, the diet of domestic guinea pigs was supplemented with high concentrations of different PUFAs and the effects of altered plasma PUFA patterns on steroid hormone concentrations, measured non-invasively, and body mass during oestrus and dioestrus were analysed. The oestrous cycle was characterised by increased oestrogen and cortisol concentrations in oestrus, corroborated by lowest bodyweight, whereas progesterone concentrations were highest in dioestrus. Plasma concentrations of the long-chain PUFAs docosahexaenoic acid (DHA; 22:6 ω3) and arachidonic acid (AA; 20:5 ω6) affected steroid hormone concentrations differently in oestrus and dioestrus. DHA positively affected oestrogen and progesterone concentrations and diminished cortisol concentrations only in oestrus. In contrast, AA negatively affected oestrogen and stimulated cortisol concentrations in oestrus and reduced progesterone concentrations in general. These findings imply selective and opposite contributions of DHA and AA to ovarian functions during different stages of the oestrous cycle, indicating a high biological relevance of plasma free PUFAs in female reproductive function.

Additional keywords: enzyme-linked immunoassay, linoleic acid, α-linolenic acid.


References

Abayasekara, D. R. E., and Wathes, D. C. (1999). Effects of altering dietary fatty acid composition on prostaglandin synthesis and fertility. Prostaglandins Leukot. Essent. Fatty Acids 61, 275–287.
Effects of altering dietary fatty acid composition on prostaglandin synthesis and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltF2gtw%3D%3D&md5=0b962e9383d824c7d22550602b98dfb0CAS |

Barbadoro, P., Annino, I., Ponzio, E., Romanelli, R. M. L., D’Errico, M. M., Prospero, E., and Minelli, A. (2013). Fish oil supplementation reduces cortisol basal levels and perceived stress: a randomized, placebo-controlled trial in abstinent alcoholics. Mol. Nutr. Food Res. 57, 1110–1114.
Fish oil supplementation reduces cortisol basal levels and perceived stress: a randomized, placebo-controlled trial in abstinent alcoholics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVOgsbc%3D&md5=bac4adc0cf7c07ee8b4fde2802fb31dbCAS |

Bauer, B., Palme, R., Machatschke, I. H., Dittami, J., and Huber, S. (2008). Non-invasive measurement of adrenocortical and gonadal activity in male and female guinea pigs (Cavia aperea f. porcellus). Gen. Comp. Endocrinol. 156, 482–489.
Non-invasive measurement of adrenocortical and gonadal activity in male and female guinea pigs (Cavia aperea f. porcellus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsF2qs7Y%3D&md5=cd202ac2a56f7c17702a550c5a776646CAS |

Bilby, T. R., Block, J., Do Amaral, B. C., Sa Filho, O., Silvestre, F. T., Hansen, P. J., Staples, C. R., and Thatcher, W. W. (2006). Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer. J. Dairy Sci. 89, 3891–3903.
Effects of dietary unsaturated fatty acids on oocyte quality and follicular development in lactating dairy cows in summer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVWgsb%2FO&md5=2d04b1742747bd9cf058cc40b19c0173CAS |

Blatchley, F. R., and Donovan, B. T. (1969). Luteolytic effect of prostaglandin in the guinea-pig. Nature 221, 1065–1066.
Luteolytic effect of prostaglandin in the guinea-pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXptlKmug%3D%3D&md5=78b89437e7fa24ec7b2b3d8de69a910aCAS |

Blatchley, F. R., Donovan, B. T., Poyser, N. L., Horton, E. W., Thompson, C. J., and Los, M. (1971). Identification of prostaglandin F2α in the utero-ovarian blood of guinea-pig after treatment with oestrogen. Nature 230, 243–244.
Identification of prostaglandin F in the utero-ovarian blood of guinea-pig after treatment with oestrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXhtlGku7c%3D&md5=47bc479add1f6a4e81fa17a35e24ad0bCAS |

Blatchley, F. R., Donovan, B. T., and Ter Haar, M. B. (1976). Plasma progesterone and gonadotrophin levels during the estrous cycle of the guinea pig. Biol. Reprod. 15, 29–38.
Plasma progesterone and gonadotrophin levels during the estrous cycle of the guinea pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlvFSjt7o%3D&md5=06cff7dd7ea2cd337c736bd19e3068d6CAS |

Broughton, K. S., Bayes, J., and Culver, B. (2010). High α-linolenic acid and fish oil ingestion promotes ovulation to the same extent in rats. Nutr. Res. 30, 731–738.
High α-linolenic acid and fish oil ingestion promotes ovulation to the same extent in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2gt7fL&md5=aba2144c6e0c2f8a19b15d8c2795e376CAS |

Bruning, P. F., and Bonfrer, J. M. G. (1986). Free fatty acid concentrations correlated with the available fraction of estradiol in human plasma. Cancer Res. 46, 2606–2609.
| 1:CAS:528:DyaL28Xit1akt78%3D&md5=e73b36439a0054bbd895114b7804ed47CAS |

Calder, P. C. (2006). Polyunsaturated fatty acids and inflammation. Prostaglandins Leukot. Essent. Fatty Acids 75, 197–202.
Polyunsaturated fatty acids and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFChtrc%3D&md5=476bc8156050599ebcc0cb9428ac1053CAS |

Coyral-Castel, S., Ramé, C., Fatet, A., and Dupont, J. (2010). Effects of unsaturated fatty acids on progesterone secretion and selected protein kinases in goat granulosa cells. Domest. Anim. Endocrinol. 38, 272–283.
Effects of unsaturated fatty acids on progesterone secretion and selected protein kinases in goat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFClsLo%3D&md5=08969a1912deecddbe37f52ebdf70115CAS |

Czaja, J. A., and Goy, R. W. (1975). Ovarian hormones and food intake in female guinea pigs and rhesus monkeys. Horm. Behav. 6, 329–349.
Ovarian hormones and food intake in female guinea pigs and rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XoslCgsA%3D%3D&md5=5aad1e43337d64f2d0b93ae495d26160CAS |

Espey, L. L. (1980). Ovulation as an inflammatory reaction: a hypothesis. Biol. Reprod. 22, 73–106.
Ovulation as an inflammatory reaction: a hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVCnsbs%3D&md5=07e49dc41e7ef3afbfb03e7080caf263CAS |

Fenske, M. (1997). The use of salivary cortisol measurements for the non-invasive assessment of adrenal cortical function in guinea pigs. Exp. Clin. Endocrinol. Diabetes 105, 163–168.
The use of salivary cortisol measurements for the non-invasive assessment of adrenal cortical function in guinea pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVSjs7k%3D&md5=6f106036837ddccc47426fbf56f3b958CAS |

Fink, G., Pfaff, D., and Levine, J. (2012). ‘Handbook of Neuroendocrinology.’ (Academic Press, Elsevier: London.)

Fu, Z., and Sinclair, A. J. (2000). Increased α-linolenic acid intake increases tissue α-linolenic acid content and apparent oxidation with little effect on tissue docosahexaenoic acid in the guinea pig. Lipids 35, 395–400.
Increased α-linolenic acid intake increases tissue α-linolenic acid content and apparent oxidation with little effect on tissue docosahexaenoic acid in the guinea pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjt1Gisr4%3D&md5=8d51ddfa88e25486dfba238a35468e99CAS |

Garris, D. R. (1986). The ovarian–adrenal axis in the guinea pig: effects of photoperiod, cyclic state and ovarian steroids on serum cortisol levels. Horm. Metab. Res. 18, 34–37.
The ovarian–adrenal axis in the guinea pig: effects of photoperiod, cyclic state and ovarian steroids on serum cortisol levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhvVSgurs%3D&md5=9660d40120dc00837d046e6e6f65b9daCAS |

Gulliver, C. E., Friend, M. A., King, B. J., and Clayton, E. H. (2012). The role of omega-3 polyunsaturated fatty acids in reproduction of sheep and cattle. Anim. Reprod. Sci. 131, 9–22.
The role of omega-3 polyunsaturated fatty acids in reproduction of sheep and cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1alu7Y%3D&md5=8aeba4d368aa18bd92f853e6f544f3ffCAS |

Hennebelle, M., Balasse, L., Latour, A., Champeil-Potokar, G., Denis, S., Lavialle, M., Gisquet-Verrier, P., Denis, I., and Vancassel, S. (2012). Influence of omega-3 fatty acid status on the way rats adapt to chronic restraint stress. PLoS One 7, e42142.
Influence of omega-3 fatty acid status on the way rats adapt to chronic restraint stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCnsLrI&md5=42ef42f485608ab6d14960e0434835e8CAS |

Hughes, J., Kwong, W. Y., Li, D., Salter, A. M., Lea, R. G., and Sinclair, K. D. (2011). Effects of omega-3 and-6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism. Reproduction 141, 105–118.
Effects of omega-3 and-6 polyunsaturated fatty acids on ovine follicular cell steroidogenesis, embryo development and molecular markers of fatty acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs7k%3D&md5=b9d9616eb8890b8e56a0633875d6908bCAS |

Ishii, O. (1920). Observations on the sexual cycle of the guinea pig. Biol. Bull. 38, 237–250.
Observations on the sexual cycle of the guinea pig.Crossref | GoogleScholarGoogle Scholar |

Joshi, H. S., Watson, D. J., and Labhsetwar, A. P. (1973). Ovarian secretion of oestradiol, oestrone, 20 dihydroprogesterone and progesterone during the oestrous cycle of the guinea pig. J. Reprod. Fertil. 35, 177–181.
Ovarian secretion of oestradiol, oestrone, 20 dihydroprogesterone and progesterone during the oestrous cycle of the guinea pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXhtlWlsg%3D%3D&md5=2728aaf3b57a7ce5bc47c3da3e7d5994CAS |

Kapoor, A., and Matthews, S. G. (2008). Prenatal stress modifies behavior and hypothalamic–pituitary–adrenal function in female guinea pig offspring: effects of timing of prenatal stress and stage of reproductive cycle. Endocrinology 149, 6406–6415.
Prenatal stress modifies behavior and hypothalamic–pituitary–adrenal function in female guinea pig offspring: effects of timing of prenatal stress and stage of reproductive cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVGltrnI&md5=5dc17619a4c8a2e8e9a135b07242e0d1CAS |

Lopes, A. S., Butler, S. T., Gilbert, R. O., and Butler, W. R. (2007). Relationship of pre-ovulatory follicle size, estradiol concentrations and season to pregnancy outcome in dairy cows. Anim. Reprod. Sci. 99, 34–43.
Relationship of pre-ovulatory follicle size, estradiol concentrations and season to pregnancy outcome in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1GmsL8%3D&md5=e6e4f36a468ba36641417fa3a3b36d04CAS |

Lunn, J., and Theobald, H. E. (2006). The health effects of dietary unsaturated fatty acids. Nutr. Bull. 31, 178–224.
The health effects of dietary unsaturated fatty acids.Crossref | GoogleScholarGoogle Scholar |

Martin, M. E., Vranckx, R., Benassayag, C., and Nunez, E. A. (1986). Modifications of the properties of human sex steroid-binding protein by nonesterified fatty acids. J. Biol. Chem. 261, 2954–2959.
| 1:CAS:528:DyaL28XhsVant7s%3D&md5=d3305a27df9e4a8853aed77802304ec7CAS |

Mohn, C. E., Fernandez-Solari, J., De Laurentiis, A., Prestifilippo, J. P., De La Cal, C., Funk, R., Bornstein, S. R., McCann, S. M., and Rettori, V. (2005). The rapid release of corticosterone from the adrenal induced by ACTH is mediated by nitric oxide acting by prostaglandin E2. Proc. Natl Acad. Sci. USA 102, 6213–6218.
The rapid release of corticosterone from the adrenal induced by ACTH is mediated by nitric oxide acting by prostaglandin E2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1ClsLk%3D&md5=9f97c5e2677482c15598364175df3931CAS |

Nemeth, M., Millesi, E., Wagner, K. H., and Wallner, B. (2014). Effects of diets high in unsaturated fatty acids on socially induced stress responses in guinea pigs. PLoS One 9, e116292.
Effects of diets high in unsaturated fatty acids on socially induced stress responses in guinea pigs.Crossref | GoogleScholarGoogle Scholar |

Nemeth, M., Millesi, E., Wagner, K. H., and Wallner, B. (2015). Sex-specific effects of diets high in unsaturated fatty acids on spatial learning and memory in guinea pigs. PLoS One 10, e0140485.
Sex-specific effects of diets high in unsaturated fatty acids on spatial learning and memory in guinea pigs.Crossref | GoogleScholarGoogle Scholar |

Nemeth, M., Pschernig, E., Wallner, B., and Millesi, E. (2016). Non-invasive cortisol measurements as indicators of physiological stress responses in guinea pigs. PeerJ 4, e1590.
Non-invasive cortisol measurements as indicators of physiological stress responses in guinea pigs.Crossref | GoogleScholarGoogle Scholar |

Palme, R., and Möstl, E. (1993). Biotin–streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. In ‘Proceedings of the 5th Symposium on the Analysis of Steroids’. (Ed. S. Görög.) pp. 111–117. (Akademiai Kiado: Budapest.)

Palme, R., and Möstl, E. (1997). Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Zeitschrift fur Saugetierkunde. 62, 192–197.

Robinson, R. S., Pushpakumara, P. G. A., Cheng, Z., Peters, A. R., Abayasekara, D. R. E., and Wathes, D. C. (2002). Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows. Reproduction 124, 119–131.
Effects of dietary polyunsaturated fatty acids on ovarian and uterine function in lactating dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtFaksLo%3D&md5=3d460a8a1234698509c277fc60111bf1CAS |

Sachser, N., and Pröve, E. (1984). Short-term effects of residence on the testosterone responses to fighting in alpha male guinea pigs. Aggress. Behav. 10, 285–292.
Short-term effects of residence on the testosterone responses to fighting in alpha male guinea pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXls1CitA%3D%3D&md5=af26911c5e611edd745416bcd1264ad0CAS |

Santos, J. E. P., Bilby, T. R., Thatcher, W. W., Staples, C. R., and Silvestre, F. T. (2008). Long chain fatty acids of diet as factors influencing reproduction in cattle. Reprod. Domest. Anim. 43, 23–30.
Long chain fatty acids of diet as factors influencing reproduction in cattle.Crossref | GoogleScholarGoogle Scholar |

Sapolsky, R. M., Romero, L. M., and Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55–89.
How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs12hu78%3D&md5=49121026b8f25ba314c3ce3c32a3881dCAS |

Schwarzenberger, F., Tomášová, K., Holečková, D., Matern, B., and Möstl, E. (1996). Measurement of fecal steroids in the black rhinoceros (Diceros bicornis) using group-specific enzyme immunoassays for 20-oxo-pregnanes. Zoo Biol. 15, 159–171.
Measurement of fecal steroids in the black rhinoceros (Diceros bicornis) using group-specific enzyme immunoassays for 20-oxo-pregnanes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtVaju7k%3D&md5=1d432b001c8f250b45cef72cd94fc658CAS |

Simopoulos, A. P. (2002). The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 56, 365–379.
The importance of the ratio of omega-6/omega-3 essential fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVKrtbY%3D&md5=3956ac4b54d7b6711aa9aa442f84dc1aCAS |

Song, C., Li, X., Leonard, B. E., and Horrobin, D. F. (2003). Effects of dietary n-3 or n-6 fatty acids on interleukin-1β-induced anxiety, stress, and inflammatory responses in rats. J. Lipid Res. 44, 1984–1991.
Effects of dietary n-3 or n-6 fatty acids on interleukin-1β-induced anxiety, stress, and inflammatory responses in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXos1Giu7Y%3D&md5=8d6dec3f6cf148e6c57deb6cf4eca7adCAS |

Trujillo, E. P., and Broughton, K. S. (1995). Ingestion of n-3 polyunsaturated fatty acids and ovulation in rats. J. Reprod. Fertil. 105, 197–203.
Ingestion of n-3 polyunsaturated fatty acids and ovulation in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjslShuw%3D%3D&md5=d49c43fa4351cd6ffee3fcaa6ce68e4bCAS |

Wathes, D. C., Abayasekara, D. R. E., and Aitken, R. J. (2007). Polyunsaturated fatty acids in male and female reproduction. Biol. Reprod. 77, 190–201.
Polyunsaturated fatty acids in male and female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1OnsL0%3D&md5=b1d435f9fb8504ce8d4bcdaa10dde610CAS |

Wathes, D. C., Cheng, Z., Mareiy, W., and Fouladi-Nashta, A. (2013). Polyunsaturated fatty acids and fertility in female mammals: An update. CAB Rev. 8, 041.
Polyunsaturated fatty acids and fertility in female mammals: An update.Crossref | GoogleScholarGoogle Scholar |

Weir, B. J. (1970). The management and breeding of some more hystricomorph rodents. Lab. Anim. 4, 83–97.
The management and breeding of some more hystricomorph rodents.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c7ht1arsw%3D%3D&md5=3ce2b233ad9eb29902177bb28e708875CAS |

Widmaier, E. P., Margenthaler, J., and Sarel, I. (1995). Regulation of pituitary–adrenocortical activity by free fatty acids in vivo and in vitro. Prostaglandins Leukot. Essent. Fatty Acids 52, 179–183.
Regulation of pituitary–adrenocortical activity by free fatty acids in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXktVSqtr4%3D&md5=f2dae9e4ac1d15b40f8726662b961775CAS |

Wiltbank, M. C., Souza, A. H., Carvalho, P. D., Bender, R. W., and Nascimento, A. B. (2012). Improving fertility to timed artificial insemination by manipulation of circulating progesterone concentrations in lactating dairy cattle. Reprod. Fertil. Dev. 24, 238–243.
Improving fertility to timed artificial insemination by manipulation of circulating progesterone concentrations in lactating dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Wolfram, M., Bellingrath, S., and Kudielka, B. M. (2011). The cortisol awakening response (CAR) across the female menstrual cycle. Psychoneuroendocrinology 36, 905–912.
The cortisol awakening response (CAR) across the female menstrual cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVeiur0%3D&md5=96e751f1fdbb2ca5edf4ada21e6906a5CAS |

Wonnacott, K. E., Kwong, W. Y., Hughes, J., Salter, A. M., Lea, R. G., Garnsworthy, P. C., and Sinclair, K. D. (2010). Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos. Reproduction 139, 57–69.
Dietary omega-3 and -6 polyunsaturated fatty acids affect the composition and development of sheep granulosa cells, oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWnug%3D%3D&md5=84b56c2efe9f3c2b2d97331653943b4bCAS |

Zachut, M., Arieli, A., Lehrer, H., Argov, N., and Moallem, U. (2008). Dietary unsaturated fatty acids influence preovulatory follicle characteristics in dairy cows. Reproduction 135, 683–692.
Dietary unsaturated fatty acids influence preovulatory follicle characteristics in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Wquro%3D&md5=9caca3b6bc91e3bd58f18d8f81f8011cCAS |