Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0124
Animal Reproduction (AR)
ORIGINAL ARTICLE

Cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid gastric administration during the pregestational and gestational periods does not influence the follicular endowment of the progeny

Danielle Storino de Freitas; Guilherme Antonio de Gouvêa Lopes; Barbara Rodrigues Nascimento; Ana Paula Madureira; Paulo Henrique Almeida Campos-Junior

Downloads: 0
Views: 276

Abstract

Abstract: Fetal programming suggests that maternal stimulation and nutrition during the period of fetal development can program the progeny. Conjugated linoleic acid (CLA), an isomer of linoleic acid, has been characterized in several aspects, but few studies have been performed on its involvement in reproduction and fetal programming. The aim of this study was to evaluate the F1, F2 and F3 progeny of female mice supplemented with CLA during the pregestational and gestational periods with respect to biometric and reproductive parameters, as well as ovarian morphophysiology. The F1 progeny of mothers supplemented with CLA exhibited stable weight gain, while the F2 progeny showed no effects (P=0.0187 and P=0.0245, respectively). A reduction in Lee's Index was observed in both generations at the second post-weaning evaluation week in the animals treated with CLA (P=0.0100 and P=0.0078, respectively). The F2 generation showed an increase in the anogenital index in both sexes of the animals treated with CLA (P= 0.0114 and P<0.0001, female and male respectively). CLA administration to mothers did not affect any of the following in their progeny: ovarian follicle mobilization (P>0.05), follicle number (P>0.05) and the integrated density of the lipid content of oocytes included in antral follicles (P>0.05). This study evaluated the use of CLA in mothers and found that it did not affect the progeny regarding murine reproductive performance, suggesting that this supplement can be used safely.

Keywords

fertility, fetal programming, folliculogenesis, nutrition, CLA

References

Abazarikia AH, Zhandi M, Shakeri M, Towhid A, Yousefi, AR. In vitro supplementation of trans-10, cis-12 conjugated linoleic acid ameliorated deleterious effect of heat stress on bovine oocyte developmental competence. Theriogenology. 2020;142:296-302. http://dx.doi.org/10.1016/j.theriogenology.2019.10.028. PMid:31708194.

Abodi M, De Cosmib V, Parazzini F, Agostoni C. Omega-3 fatty acids dietary intake for oocyte quality in women undergoing assisted reproductive techniques: a systematic review. Eur J Obstet Gynecol Reprod Biol. 2022;275:97-105. http://dx.doi.org/10.1016/j.ejogrb.2022.06.019. PMid:35779332.

Bach A. La reproducción del vacuno lechero: nutrición y fisiología. In: XVII Curso de Especialización FEDNA. Purina: FEDNA; 2003. 24 p.

Barker MJ, Greenwood KM, Jackson M, Crowe S. Persistence of cognitive effects after withdrawal from long-term benzodiazepine use: a meta-analysis. Arch Clin Neuropsychol. 2004;19(3):437-54. http://dx.doi.org/10.1016/S0887-6177(03)00096-9. PMid:15033227.

Basak S, Duttaroy AK. Conjugated linoleic acid and its beneficial effects in obesity, cardiovascular disease, and cancer. Nutrients. 2020;12(7):1913. http://dx.doi.org/10.3390/nu12071913. PMid:32605287.

Bayat AR, Razzaghi M, Sari M, Kairenius P, Tröscher E, Trevisi J, Vilkki L. The effect of dietary rumen-protected trans-10,cis-12 conjugated linoleic acid or a milk fat-depressing diet on energy metabolism, inflammation, and oxidative stress of dairy cows in early lactation. J Dairy Sci. 2022;105(4):3032-48. http://dx.doi.org/10.3168/jds.2021-20543. PMid:35123782.

Bernardis LL. Prediction of carcass fat, water and lean body mass from Lee’s “nutritive ratio” in rats with hypothalamic obesity. Experientia. 1970;26(7):789-90. http://dx.doi.org/10.1007/BF02232553. PMid:4914444.

Broughton KS, Rule DC, Ye Y, Zhang X, Driscoll M, Culver B. Dietary omega-3 fatty acids differentially influence ova release and ovarian cyclooxygenase-1 and cyclooxygenase-2 expression in rats. Clin Nutr Res. 2009;29(3):197-205. http://dx.doi.org/10.1016/j.nutres.2009.01.007. PMid:19358934.

Campos-Junior PHA, Assunção CM, Carvalho BC, Batista RIP, Garcia RMG, Viana JHM. Follicular populations, recruitment and atresia in the ovaries of different strains of mice. Reprod Biol. 2012;12(1):41-55. http://dx.doi.org/10.1016/S1642-431X(12)60076-X. PMid:22472939.

Cardoso RC, Puttabyatappa M, Padmanabhan V. Steroidogenic versus metabolic programming of reproductive neuroendocrine, Ovarian and Metabolic Dysfunctions. Neuroendocrinology. 2015;102(3):226-37. http://dx.doi.org/10.1159/000381830. PMid:25832114.

Castañeda-Gutierrez E, Benefield BC, Veth MJ, Santos NR, Gilbert RO, Butler WR, Bauman DE. Evaluation of mechanism of action of conjugated linoleic acid isomers on reproduction in dairy cows. J Dairy Sci. 2007;90(9):4253-64. http://dx.doi.org/10.3168/jds.2007-0117. PMid:17699044.

Childs S, Lynch CO, Hennessy AA, Stanton C, Whates DC, Sreenan JM, Diskin MG, Kenn DA. Effect of dietary enrichment with either n-3 or n-6 fatty acids on systemic metabolite and hormone concentration and ovarian function in heifers. Animal. 2008;2(6):883-93. http://dx.doi.org/10.1017/S1751731108002115. PMid:22443668.

Csillik Z, Faigl V, Keresztes M, Galamb E, Hammon HM, Tröscher A, Fébel H, Kulcsár M, Husvéth F, Huszenicza G, Butler WR. Effect of pré and postpartum supplementation with lipid encapsulated conjugated linoleic acid on reproductive performance and the growth hormone insulin-like growth factor-I axis in multiparous high-producing dairy cows. J Dairy Sci. 2017;100(7):5888-98. http://dx.doi.org/10.3168/jds.2016-12124. PMid:28456404.

Dean A, Sharpe RM. Anogenital distance or digit length ratio as measures of fetal androgen exposure: relationship to male reproductive development and its disorders. J Clin Endocrinol Metab. 2013;98(6):2230-8. http://dx.doi.org/10.1210/jc.2012-4057. PMid:23569219.

Federici S, Goggi G, Giovanelli L, Cangiano B, Persani L, Bonomi M, Quinton R. Pharmacological induction of puberty. Comprehensive Pharmacology. 2022;2022:75-93. http://dx.doi.org/10.1016/B978-0-12-820472-6.00101-8.

Freitas DS, Lopes GAG, Nascimento BR, Magalhães BA, Madureira AP, Campos-Junior PHA. Effects of cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid supplementation on maternal reproductive parameters. Zygote. 2022;30(6):863-871. http://dx.doi.org/10.1017/S0967199422000405. PMid:36148787.

Freitas DS, Lopes GAG, Nascimento BR, Pereira LC, Batista RI, Campos-Junior PHA. Ácido linoleico conjugado como potencial bioativo para modulação e criotolerância de gametas e embriões. Cienc Anim Bras. 2020;21. http://dx.doi.org/10.1590/1809-6891v21e-63574.

Funston RN, Martin JL, Adams DC, Larson EDM. Effects of winter grazing system and supplementation during late gestation on performance of beef cows and progeny. Amer Soci of Ani Sci. 2008;59:102-5. http://dx.doi.org/10.2527/jas.2008-1323.

Gaullier JM, Halse J, Hoye L, Kristiansen K, Fagertun H, Vik H, Gudmundsen O. Conjugated linoleic acid supplementation for 1 year reduces body fat mass in healthy overweight humans. Am J Clin Nutr. 2004;79(6):1118-25. http://dx.doi.org/10.1093/ajcn/79.6.1118. PMid:15159244.

Guerrero-Bosagna C, Sabat P, Valladares L. Environmental signaling and evolutionary change: can exposure of pregnant mammals to environmental estrogens lead to epigenetically induced evolutionary changes in embryos? Evol Dev. 2005;7(4):341-50. http://dx.doi.org/10.1111/j.1525-142X.2005.05033.x. PMid:15982371.

Ideraabdullah FY, Zeisel SH. Dietary modulation of the epigenome. Physiol Veg. 2018;98(2):667-95. http://dx.doi.org/10.1152/physrev.00010.2017. PMid:29442595.

Iwasa T, Matsuzaki T, Murakami M, Kinouchi R, Gereltsetseg G, Yamamoto S, Kuwahara A, Yasui T, Irahara M. Delayed puberty in prenatally glucocorticoid administered female rats occurs independently of the hypothalamic Kiss1-Kiss1r-GnRH. Int J Dev Neurosci. 2011;29(2):183-8. http://dx.doi.org/10.1016/j.ijdevneu.2010.11.001. PMid:21074602.

Klein JL, Machado DS, Adams SM, Alves DC Fo, Brodani IL. Effects of maternal nutrition on pregnancy on progeny quality - a review. Res Soc Dev. 2021;10:e45710212654. http://dx.doi.org/10.33448/rsd-v10i2.12654.

Langley-Evans SC. Developmental programming of health and disease. Proc Nutr Soc. 2006;65(1):97-105. http://dx.doi.org/10.1079/PNS2005478. PMid:16441949.

Leite AC, Andrade VB, Silva EBM, Borges AM. Effect of conjugated linoleic acid addition in in vitro culture medium in F1 Holstein X Zebu embryo survival post vitrification. Arq Bras Med Vet Zootec. 2017;69:1385-92. http://dx.doi.org/10.1590/1678-4162-9238.

Lucy MC. Regulation of ovarian follicular function by somatotropin and insulin-like growth factors in cattle. J Dairy Sci. 2000;83(7):1635-47. http://dx.doi.org/10.3168/jds.S0022-0302(00)75032-6. PMid:10908067.

Maamar BM, King SE, Nilsson E, Beck D, Skinner MK. Epigenetic transgenerational inheritance of parent-of-origin allelic transmission of outcross pathology and sperm epimutations. Dev Biol. 2020;458(1):106-19. http://dx.doi.org/10.1016/j.ydbio.2019.10.030. PMid:31682807.

McCarrey JR. Distinctions between transgenerational and non-transgenerational epimutations. Mol Cell Endocrinol. 2014;398(1-2):13-23. http://dx.doi.org/10.1016/j.mce.2014.07.016. PMid:25079508.

Mendiola J, Roca M, Mínguez-Alarcón L, Mira-Escolano MP, Lopez-Espin J, Barrett E, Swan S, Torres-Cantero A. Anogenital distance is related to ovarian follicular number in young Spanish women: a cross-sectional study. Environ Health. 2012;11(1):90. http://dx.doi.org/10.1186/1476-069X-11-90. PMid:23217457.

Mira-Escolano MP, Mendiola J, Mínguez-Alarcón L, Melgarejo M, Cutillas-Tolín A, Roca M, López-Espín JJ, Noguera-Velasco JÁ, Torres-Cantero AM. Longer anogenital distance is associated with higher testosterone levels in women: a cross-sectional study. Int. J. Obstet. Gynaecol. 2014;121(11):1359-64. http://dx.doi.org/10.1111/1471-0528.12627. PMid:25250921.

Ohajuruka OA, Wu ZG, Palmquist DL. Ruminal metabolism, fiber, and protein digestion by lactating cows fed calcium soap or animal-vegetable fat. J Dairy Sci. 1991;74(8):2601-9. http://dx.doi.org/10.3168/jds.S0022-0302(91)78438-5. PMid:1655844.

Peng Y, Ren F, Yin JD, Fang Q, Li FN, Li DF. Transfer of conjugated linoleic acid from sows to their offspring and its impact on the fatty acid profiles of plasma, muscle, and subcutaneous fat in piglets. J Anim Sci. 2010;88(5):1741-51. http://dx.doi.org/10.2527/jas.2009-2354. PMid:20081085.

Pires JAA, Grummer RR. Specific fatty acids as metabolic modulators in the dairy cow. Ver Bras Zoot. 2008;37(spe):287-98. http://dx.doi.org/10.1590/S1516-35982008001300033.

Poulos SP, Sisk M, Hausman D, Azain MJ, Hausman GJ. Pre- and postnatal dietary conjugated linoleic acid alters adipose development, body weight gain and body composition in sprague-dawley rats. Nutr Metab. 2001;131(10):2722-31. http://dx.doi.org/10.1093/jn/131.10.2722. PMid:11584096.

Reynolds C, Vickers M, Harrison C, Segovia AS, Gray C. High fat and/or high salt intake during pregnancy alters maternal meta-inflammation and offspring growth and metabolic profiles. Physiol Rep. 2014;2(8):e12110. http://dx.doi.org/10.14814/phy2.12110. PMid:25096554.

Sudano MJ, Santos VG, Tata A, Ferreira CR, Paschoal DM, Machado R, Buratini J, Landim-Alvarenga FC. Phosphatidylcholine and sphingomyelin profiles vary in bos taurus indicus and bos taurus taurus in vitro- and in vivo-produced blastocysts. Biol Reprod. 2012;87(6):130. http://dx.doi.org/10.1095/biolreprod.112.102897. PMid:23053436.

Thankamony A, Pasterski V, Ong KK, Hughes IA. Anogenital distance as a marker of androgen exposure in humans. Andrology. 2016;4(4):616-25. http://dx.doi.org/10.1111/andr.12156. PMid:26846869.

Vaisar T, Wang S, Omer M, Irwin A, Storey C, Tang C, DenHartigh L. 10,12-conjugated linoleic acid supplementation improves HDL composition and function on mice. J Lipid Res. 2022;63(8):100241. http://dx.doi.org/10.1016/j.jlr.2022.100241. PMid:35714730.

van den Driesche S, Scott HH, MacLeod DJ, Fisken M, Walker M, Sharpe RM. Relative importance of prenatal and postnatal androgen action in determining growth of the penis and anogenital distance in the rat before, during and after puberty. Int J Androl. 2011;34(6 Pt 2):e578-86. http://dx.doi.org/10.1111/j.1365-2605.2011.01175.x. PMid:21631528.

Veldhuis J, Alleva JM, Bij de Vaate AJ. Me, my selfie, and I: the relations between selfie behaviors, body image, self-objectification, and self-esteem in young women. Psychol Pop Media Cult. 2020;9(1):3-13. http://dx.doi.org/10.1037/ppm0000206.

Welsh M, Saunders PT, Fisken M, Scott HM, Hutchison GR, Smith LB, Sharpe RM. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest. 2008;118(4):1479-90. http://dx.doi.org/10.1172/JCI34241. PMid:18340380.

Yeganeh A, Zahradka P, Taylor CG. Trans-10, cis-12 conjugated linoleic acid (t10- c12 CLA) treatment and caloric restriction differentially affect adipocyte cell turnover in obese and lean mice. J Nutr Biochem. 2017;49:123-32. http://dx.doi.org/10.1016/j.jnutbio.2017.08.003. PMid:28945993.

Yi D, Zeng S, Guo Y. A diet rich in n-3 polyunsaturated fatty acids reduced prostaglandin biosynthesis, ovulation rate, and litter size in mice. Theriogenology. 2012;78(1):28-38. http://dx.doi.org/10.1016/j.theriogenology.2012.01.013. PMid:22460154.
 


Submitted date:
11/28/2022

Accepted date:
06/29/2023

6504470ca953957f44381842 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections