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Effects of cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid supplementation on maternal reproductive parameters

Published online by Cambridge University Press:  23 September 2022

Danielle Storino de Freitas ,
Guilherme Antonio de Gouvêa Lopes ,
Barbara Rodrigues Nascimento ,
Breno Augusto Magalhães Open the ORCID record for Breno Augusto Magalhães [Opens in a new window] ,
Ana Paula Madureira  and
Paulo Henrique Almeida Campos-Junior Open the ORCID record for Paulo Henrique Almeida Campos-Junior [Opens in a new window]
Danielle Storino de Freitas
Affiliation:
Laboratório de Pesquisa em Reprodução e Desenvolvimento, Universidade Federal de São João del Rei. São João del-Rei, Minas Gerais, Brazil
Guilherme Antonio de Gouvêa Lopes
Affiliation:
Laboratório de Pesquisa em Reprodução e Desenvolvimento, Universidade Federal de São João del Rei. São João del-Rei, Minas Gerais, Brazil
Barbara Rodrigues Nascimento
Affiliation:
Laboratório de Pesquisa em Reprodução e Desenvolvimento, Universidade Federal de São João del Rei. São João del-Rei, Minas Gerais, Brazil
Breno Augusto Magalhães
Affiliation:
Laboratório de Pesquisa em Reprodução e Desenvolvimento, Universidade Federal de São João del Rei. São João del-Rei, Minas Gerais, Brazil
Ana Paula Madureira
Affiliation:
Laboratório de Pesquisa em Reprodução e Desenvolvimento, Universidade Federal de São João del Rei. São João del-Rei, Minas Gerais, Brazil
Paulo Henrique Almeida Campos-Junior*
Affiliation:
Laboratório de Pesquisa em Reprodução e Desenvolvimento, Universidade Federal de São João del Rei. São João del-Rei, Minas Gerais, Brazil
*
Author for correspondence: Paulo Henrique Almeida Campos-Junior. Universidade Federal de São João del Rei. Praça Dom Helvécio, 74 – Dom Bosco, São João del-Rei, MG, 36301-160, Brazil. E-mail: paulohenrique@ufsj.edu.br
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Summary

Conjugated linoleic acid (CLA) is a mixture of positional isomers of linoleic acid found in ruminant products and meat. The diet supplementing with CLA is an emerging area, requiring studies to elucidate its effects on animals and human reproduction, as well as its side effects. Therefore, the aim of this study was to evaluate the effects of CLA gastric administration, during the pregestational and gestational period in biometric and reproductive parameters, as well as in ovarian morphophysiology. Animals were distributed in three groups: (1) control (n = 10); (2) fish oil (n = 10); and (3) CLA (n = 10), that daily received, by gavage, phosphate-buffered saline, fish oil and CLA, respectively, carried out over 50 days (before mating, mating and pregnancy). There was an increment in the nasoanal distance and Lee index of the CLA and fish oil-treated groups during the first weeks (P > 0.05). CLA administration did not affect the ovarian follicle mobilization (P > 0.05), the number of follicles (P > 0.05) and the integrated density of lipid content of oocytes included in antral follicles (P > 0.05). There was no effect of CLA administration on the litter weight (P > 0.05; F2 and F3), however, an increment (P < 0.05) in the number of pups per litter (F2) was observed. Overall, this study demonstrated the absence of side effects of the CLA gastric administration on mice reproductive performance and suggests that this treatment would transgenerationally enhance fertility in this species.

Keywords

CLAFertilityFolliculogenesisNutritionOvary
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 863 - 871
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Abazarikia, A. H., Zhandi, M., Shakeri, M., Towhidi, A. and Yousefi, A. R. (2020). In vitro supplementation of trans-10, cis-12 conjugated linoleic acid ameliorated deleterious effect of heat stress on bovine oocyte developmental competence. Theriogenology, 142, 296–302. doi: 10.1016/j.theriogenology.2019.10.028 CrossRefGoogle ScholarPubMed
Ávila, G., Catozzi, C., Pravettoni, D., Sala, G., Martino, P., Meroni, G., Lecchi, C. and Ceciliani, F. (2020). In vitro effects of conjugated linoleic acid (CLA) on inflammatory functions of bovine monocytes. Journal of Dairy Science, 103(9), 8554–8563. doi: 10.3168/jds.2020-18659 CrossRefGoogle ScholarPubMed
Azain, M. J., Hausman, D. B., Sisk, M. B., Flatt, W. P. and Jewell, D. E. (2000). Dietary conjugated linoleic acid reduces rat adipose tissue cell size rather than cell number. Journal of Nutrition, 130(6), 1548–1554. doi: 10.1093/jn/130.6.1548 CrossRefGoogle ScholarPubMed
Basak, S. and Duttaroy, A. K. (2020). Conjugated linoleic acid and its beneficial effects in obesity, cardiovascular disease, and cancer. Nutrients, 12(7), 1913. doi: 10.3390/nu12071913 CrossRefGoogle ScholarPubMed
Batista, R. I. T. P., Raposo, N. R. B., Campos-Junior, P. H. A., Pereira, M. M., Camargo, L. S. A., Gama, M. A. S. and Viana, J. H. M. (2014). Trans-10, cis-12 conjugated linoleic acid reduces neutral lipid content and may affect cryotolerance of in vitro-produced crossbred bovine embryos. Journal of Animal Science and Biotechnology 33. doi:10.1186/2049–1891–5-33CrossRefGoogle Scholar
Bauman, D. E., Perfield, J. W., Harvatine, K. J. and Baumgard, L. H. (2008). Regulation of fat synthesis by conjugated linoleic acid: Lactation and the ruminant model. Journal of Nutrition, 138(2), 403–409. doi: 10.1093/jn/138.2.403 CrossRefGoogle ScholarPubMed
Bee, G. (2000). Dietary conjugated linoleic acid consumption during pregnancy and lactation influences growth and tissue composition in weaned pigs. Journal of Nutrition, 130(12), 2981–2989. doi: 10.1093/jn/130.12.2981 CrossRefGoogle ScholarPubMed
Bernardis, L. L. (1970). Prediction of carcass fat, water and lean body mass from Lee’s “nutritive ratio” in rats with hypothalamic obesity. Experientia, 26(7), 789–790. doi: 10.1007/BF02232553 CrossRefGoogle ScholarPubMed
Butler, W. R. (2000). Nutritional interactions with reproductive performance in dairy cattle. Animal Reproduction Science, 60–61, 449–457. doi: 10.1016/s0378-4320(00)00076-2 CrossRefGoogle ScholarPubMed
Campos-Junior, P. H., Marinho Assuncao, C., Carvalho, B. C., Batista, R. I., Garcia, R. M. and Viana, J. H. (2012). Follicular populations, recruitment and atresia in the ovaries of different strains of mice. Reproductive Biology, 12(1), 41–55. doi: 10.1016/s1642-431x(12)60076-x CrossRefGoogle ScholarPubMed
Castañeda-Gutiérrez, E., Benefield, B. C., de Veth, M. J., Santos, N. R., Gilbert, R. O., Butler, W. R. and Bauman, D. E. (2007). Evaluation of mechanism of action of conjugated linoleic acid isomers on reproduction in dairy cows. Journal of Dairy Science, 90(9), 4253–4264. doi: 10.3168/jds.2007-0117 CrossRefGoogle ScholarPubMed
Chin, S. F., Storkson, J. M., Albright, K. J., Cook, M. E. and Pariza, M. W. (1994). Conjugated linoleic acid is a growth factor for rats as shown by enhanced weight gain and improved feed efficiency. Journal of Nutrition, 124(12), 2344–2349. doi: 10.1093/jn/124.12.344 CrossRefGoogle ScholarPubMed
Cordoba-Chacon, J., Sugasini, D., Poorna, C. R., Apoorva, Y., Zachary, T., White, C. and Subbaiah, P. V. (2020). Tissue-dependent effects of cis-9,trans-11- and trans-10,cis-12-CLA isomers on glucose and lipid metabolism in adult male mice. Journal of Nutritional Biochemistry, 67, 90–100. htps:. doi: 10.1016/j.jnutbio.2019.01.020 CrossRefGoogle Scholar
Csillik, Z., Faigl, V., Keresztes, M., Galamb, E., Hammon, H. M., Tröscher, A. and Butler, W. R. (2017). Effect of pre- 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. Journal of Dairy Science, 100, 1–11. doi: 10.3168/jds.2016-12124 CrossRefGoogle ScholarPubMed
Dahiya, D. K. and Puniya, A. K. (2018). Conjugated linoleic acid enriched skim milk prepared with Lactobacillus fermentum DDHI27 endorsed antiobesity in mice. Future Microbiology, 13, 1007–1020. doi: 10.2217/fmb-2017-0280 CrossRefGoogle ScholarPubMed
de Veth, M. J., Bauman, D. E., Koch, W., Mann, G. E., Pfeiffer, A. M. and Butler, W. R. (2009). Efficacy of conjugated linoleic acid for improving reproduction: A multi-study analysis in early-lactation dairy cows. Journal of Dairy Science, 92(6), 2662–2669. doi: 10.3168/jds.2008-1845 CrossRefGoogle ScholarPubMed
Den Hartigh, L. J. (2019). Conjugated linoleic acid effects on cancer, obesity, and atherosclerosis: A review of pre-clinical and human trials with current perspectives. Nutrients, 11(2), 370. doi: 10.3390/nu11020370 CrossRefGoogle ScholarPubMed
Fontana, R. and Torre, S. (2016). The deep correlation between energy metabolism and reproduction: A view on the effects of nutrition for women fertility. Nutrients, 6, 8. doi: 10.3390/nu8020087 Google Scholar
Fouladi-Nashta, A. A., Gutierrez, C. G., Gong, J. G., Garnsworthy, P. C. and Webb, R. (2007). Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biology of Reproduction, 77(1), 9–17. doi: 10.1095/biolreprod.106.058578 CrossRefGoogle ScholarPubMed
Freitas, D. S., Lopes, G. A. G., Nascimento, B. R., Pereira, L. C., Batista, R. I. and Campos-Junior, P. H. A. (2020). Ácido linoleico conjugado como potencial bioativo para modulação e criotolerância de gametas e embriões. Ciência Animal Brasileira, 21. doi: 10.1590/1809-6891v21e-63574 Google Scholar
Gaullier, J. M., Halse, J., Høye, K., Kristiansen, K., Fagertun, H., Vik, H. and Gudmundsen, O. (2004). Conjugated linoleic acid supplementation for 1 y reduces body fat mass in healthy overweight humans. American Journal of Clinical Nutrition, 79(6), 1118–1125. doi: 10.1093/ajcn/79.6.1118 CrossRefGoogle ScholarPubMed
González-Serrano, A. F., Ferreira, C. R., Pirro, V., Lucas-Hahn, A., Heinzmann, J., Hadeler, K. G., Baulain, U., Aldag, P., Meyer, U., Piechotta, M., Jahreis, G., Dänicke, S., Cooks, R. G. and Niemann, H. (2015). Effects of long-term dietary supplementation with conjugated linoleic acid on bovine oocyte lipid profile. Reproduction, Fertility, and Development, 28, 1326–1339. doi: 10.1071/RD14352 CrossRefGoogle Scholar
Harris, M. A., Hansen, R. A., Vidsudhiphan, P., Koslo, J. L., Thomas, J. B., Watkins, B. A. and Allen, K. G. D. (2001). Effects of conjugated linoleic acids and docosahexaenoic acid on rat liver and reproductive tissue fatty acids, prostaglandins and matrix metalloproteinase production. Prostaglandins, Leukotrienes, and Essential Fatty Acids, 65(1), 23–29. doi: 10.1054/plef.2001.0283 CrossRefGoogle ScholarPubMed
Jazwiec, P. A. and Sloboda, D. M. (2019). Nutritional adversity, sex and reproduction: 30 years of DOHaD and what have we learned? Journal of Endocrinology, 51, 68. doi: 10.1530/JOE-19-0048 Google Scholar
Khajeh, M., Rahbarghazi, R., Nouri, M. and Darabi, M. (2017). Potential role of polyunsaturated fatty acids, with particular regard to the signaling pathways of arachidonic acid and its derivatives in the process of maturation of the oocytes: Contemporary review. Biomedicine and Pharmacotherapy, 94, 458–467. doi: 10.1016/j.biopha.2017.07.140 CrossRefGoogle Scholar
Kim, J. H., Kim, Y., Kim, Y. J. and Park, Y. (2016). Conjugated linoleic acid: Potential health benefits as a functional food ingredient. Annual Review of Food Science and Technology, 7, 221–244. doi: 10.1146/annurev-food-041715-033028 CrossRefGoogle ScholarPubMed
Lapa, M., Marques, C. C., Baptista, M., Vasques, M. I., Horta, A., Portugal, P. V. and Pereira, R. M. (2005). Fatty acid profile of oocytes and blastocysts during in vitro bovine embryo production. Reproduction in Domestic Animals, 40, 365. doi: 10.1111/j.1439–0531.2011.01762.x Google Scholar
Lapa, M., Marques, C., Alves, S. P., Vasques, M., Baptista, M., Carvalhais, I. and Pereira, R. M. (2011). Effect of trans-10 cis-12 conjugated linoleic acid on bovine oocyte competence and fatty acid composition. Animals, 46, 904–910. doi: 10.1111/j.1439-0531.2011.01762.x Google ScholarPubMed
Leite, A. C., Andrade, V. B., Silva, E. B. M. and Borges, A. M. (2017). Effect of conjugated linoleic acid addition in in vitro culture medium in F1 Holstein ´ Zebu embryo survival post vitrification. Arquivos Brasileiro de Medicina Veterinária e Zootecnia, 69, 1385–1392. doi: 10.1590/1678–4162–9238 CrossRefGoogle Scholar
Medeiros, S. R., Oliveira, D. E., Aroeira, L. J., McGuire, M. A., Bauman, D. E. and Lanna, D. P. (2010). Effects of dietary supplementation of rumen-protected conjugated linoleic acid to grazing cows in early lactation. Journal of Dairy Science, 93(3), 1126–1137. doi: 10.3168/jds.2009-2645 CrossRefGoogle ScholarPubMed
Mostafa, A. F., Samir, S. M. and Nagib, R. M. (2018). Omega-3 polyunsaturated fatty acid docosahexaenoic acid and its role in exhaustive-exercise-induced changes in female rat ovulatory cycle. Canadian Journal of Physiology and Pharmacology, 96(4), 395–403. doi: 10.1139/cjpp-2017-0354 CrossRefGoogle ScholarPubMed
Novelli, E. L., Diniz, Y. S., Galhardi, C. M., Ebaid, G. M., Rodrigues, H. G., Mani, F., Fernandes, A. A., Cicogna, A. C. and Novelli Filho, J. L. (2007). Anthropometrical parameters and markers of obesity in rats. Laboratory Animals, 41(1), 111–119. doi: 10.1258/002367707779399518 CrossRefGoogle ScholarPubMed
NRC (National Research Council (US) Subcommittee on laboratory animal nutrition) (1995). Nutrient requirements of laboratory animals: Fourth revised edition. doi: 10.17226/4758. National Academies Press, USA.Google Scholar
Oliveira, D. E., Urio, M. and Sandri, E. C. (2018). Effect of trans-10, cis-12 conjugated linoleic acid (CLA) on expression of lipogenic genes is related to amount of trans-10, cis-12 CLA per unit of metabolic weight in lactating dairy ewes. Small Ruminant Research, 169, 42–45. doi: 10.1016/j.smallrumres.2018.10.009 CrossRefGoogle Scholar
Park, Y., Albright, K. J., Storkson, J., Cook, M. E. and Pariza, M. W. (1997). Effect of conjugated linoleic acid on body composition in mice. Lipids, 32, 853–858. doi: 10.1007/s11745–997–0109-x CrossRefGoogle ScholarPubMed
Penedo, L. A., Nunes, J. C., Gama, M. A., Leite, P. E., Quirico-Santos, T. F. and Torres, A. G. (2013). Intake of butter naturally enriched with cis9,trans11 conjugated linoleic acid reduces systemic inflammatory mediators in healthy young adults. Journal of Nutritional Biochemistry, 24(12), 2144–2151. doi: 10.1016/j.jnutbio.2013.08.006 CrossRefGoogle ScholarPubMed
Peng, Y., Ren, F., Yin, J. D., Fang, Q., Li, F. N. and Li, D. F. (2010). 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. Journal of Animal Science, 88(5), 1741–1751. doi: 10.2527/jas.2009-2354 CrossRefGoogle ScholarPubMed
Pires, J. A. A. and Grummer, R. R. (2008). Specific fatty acids as metabolic modulators in the dairy cow. Revista Brasileira de Zootecnia, 37(spe), 287–298. doi: 10.1590/S1516-35982008001300033 CrossRefGoogle Scholar
Poulos, S. P., Sisk, M., Hausman, D. B., Azain, M. J. and Hausman, G. J. (2001). Pre- and postnatal dietary conjugated linoleic acid alters adipose development, body weight gain and body composition in Sprague-Dawley rats. Journal of Nutrition, 131(10), 2722–2731. doi: 10.1093/jn/131.10.2722 CrossRefGoogle ScholarPubMed
Prates, E. G., Marques, C. C., Baptista, M. C., Vasques, M. I., Carolino, N., Horta, A. E., Charneca, R., Nunes, J. T. and Pereira, R. M. (2013). Fat area and lipid droplet morphology of porcine oocytes during in vitro maturation with trans-10, cis-12 conjugated linoleic acid and forskolin. Animal, 7(4), 602–609. doi: 10.1017/S1751731112001899 CrossRefGoogle ScholarPubMed
Ramakrishnan, U., Grant, F., Goldenberg, T., Zongrone, A. and Martorell, R. (2012). Effect of women’s nutrition before and during early pregnancy on maternal and infant outcomes: A systematic review. Paediatric and Perinatal Epidemiology, 26, 285–301. doi: 10.1111/j.1365–3016.2012.01281.x CrossRefGoogle ScholarPubMed
Reynolds, C. M., Vickers, M. H., Harrison, C. J., Segovia, S. A. and Gray, C. (2014). High fat and/or high salt intake during pregnancy alters maternal meta-inflammation and offspring growth and metabolic profiles. Physiological Reports, 2(8), 12399. doi: 10.14814/phy2.12110 CrossRefGoogle ScholarPubMed
Sandri, E. C., Camêra, M., Sandri, E. M., Harvatine, K. J. and De Oliveira, D. E. (2018). Peroxisome proliferator-activated receptor gamma (PPARγ) agonist fails to overcome trans-10, cis-12 conjugated linoleic acid (CLA) inhibition of milk fat in dairy sheep. Animal, 12(7), 1405–1412. doi: 10.1017/S1751731117002956 CrossRefGoogle ScholarPubMed
Sudano, M. J., Santos, V. G., Tata, A., Ferreira, C., Paschoal, D. M., Machado, R. and Landim-Alvarenga, F. C. (2012). Phosphatidylcholine and sphingomyelin profiles vary in Bos taurus indicus and Bos taurus taurus in vitro- and in vivo-produced blastocysts. Biology of Reproduction, 87, 1–11. doi: 10.1095/biolreprod.112.102897 CrossRefGoogle ScholarPubMed
Taylor, J. S., Williams, S. R., Rhys, R., James, P. and Frenneaux, M. P. (2006). Conjugated linoleic acid impairs endothelial function. Arteriosclerosis, Thrombosis, and Vascular Biology, 26(2), 307–312. doi: 10.1161/01.ATV.0000199679.40501.ac CrossRefGoogle ScholarPubMed
Ticiani, E., Urio, M., Ferreira, R., Harvatine, K. J. and De Oliveira, D. E. (2016). Transcriptional regulation of acetyl-CoA carboxylase a isoforms in dairy ewes during conjugated linoleic acid induced milk fat depression. Animal, 10(10), 1677–1683. doi: 10.1017/S1751731116000677 CrossRefGoogle ScholarPubMed
Uti, D. E., Atangwho, I. J., Eyong, E. U., Umoru, G. U., Egbung, G. E., Nna, V. U. and Udeozor, P. A. (2020). African walnuts attenuate ectopic fat accumulation and associated peroxidation and oxidative stress in monosodium glutamate-obese Wistar rats. Biomedicine and Pharmacotherapy, 124, 109879. doi: 10.1016/j.biopha.2020.109879 CrossRefGoogle ScholarPubMed
Yeganeh, A., Zahradka, P. and Taylor, C. G. (2017). Trans-10,cis-12 conjugated linoleic acid (t10-c12 CLA) treatment and caloric restriction differentially affect adipocyte cell turnover in obese and lean mice. Journal of Nutritional Biochemistry, 49, 123–132. doi: 10.1016/j.jnutbio.2017.08.003 CrossRefGoogle ScholarPubMed
Yi, D., Zeng, S. and Guo, Y. (2012). A diet rich in n-3 polyunsaturated fatty acids reduced prostaglandin biosynthesis, ovulation rate, and litter size in mice. Theriogenology, 78(1), 28–38. doi: 10.1016/j.theriogenology.2012.01.013 CrossRefGoogle Scholar
Zeng, Y., Liu, P., Yang, X., Li, H., Li, H., Guo, Y., Meng, X. and Liu, X. (2020). The dietary c9, t11-conjugated linoleic acid enriched from butter reduces breast cancer progression in vivo. Journal of Food Biochemistry, 44(4), e13163. doi: 10.1111/jfbc.13163 CrossRefGoogle ScholarPubMed
Zhai, F., Ma, X., Yan, L. and Qiao, J. (2019). The molecular genetics of oogenesis. In: Leung, Peter C.K. and Qiao, Jie (eds), Human Reproductive and Prenatal Genetics, pp. 155–172. Academic Press.CrossRefGoogle Scholar