Metabolic stress and negative energy balance (NEB) are typical undesirable accompanying phenomena of the postpartum period in dairy cattle. They negatively affect not only milk production but also the reproductive abilities of the cow, and it is therefore desirable to recognize NEB early to prevent its development. Metabolic stress markers are traditionally total cholesterol (tChol), nonesterified fatty acids (NEFA), beta-hydroxybutyrate (BHB), and triacylglycerols (TAGs). The aim of this work was to determine whether the level of the aforementioned markers in the blood correlates with the ability of a primiparous dairy cow to conceive soon after the first calving. Therefore, oocytes were collected from the monitored cows shortly after calving using the ovum pick-up method, and their quality was subsequently determined. We observed cumulus cell expansion, oocytes quality, maturation rate, and the amount and distribution of lipids within the oocyte. In addition to the mentioned markers, we also monitored the effect of the season in which aspiration was performed to assess its impact on the reproductive indicators of the monitored cows. We observed a negative correlation between higher TAGs and oocyte maturation rate, while the number of aspirated oocytes per cow and the fertilization capability were positively associated with TAGs. Additionally, higher BHB levels in the blood were linked to enhanced fertilization capability. The higher levels of TAGs, BHB, and NEFA in blood were associated with increased lipid intensity, and higher lipid content was positively correlated with both the quality of cumulus cells and oocytes. In summary, we found that NEFA, BHB, and TAGs are the most reliable markers of a cow's readiness to become pregnant after her first calving. The use of tChol, however, remains very controversial. Moreover, primiparous cows are more prepared for re-pregnancy in the warmer season.

After giving birth to a calf, cows, like other mammals, experience a period of very high energy expenditure, which is often associated with negative energy balance (NEB) or metabolic stress. NEB, among others, decreases the reproductive ability of the cow. In dairy cattle, it is required that both a high milk yield is achieved, and the cow is able to conceive again as soon as possible. Thus, the levels of markers of metabolic stress, namely total cholesterol (tChol), nonesterified fatty acids (NEFA), beta-hydroxybutyrate (BHB), and triacylglycerols (TAGs), were monitored to see whether their level correlate with the reproduction capability of primiparous dairy cows and whether these molecules can be used as markers of readiness of the cow to conceive. It was shown that there is high correlation between NEFA, BHB, and TAGs levels and reproduction capability of the primiparous dairy cow. On the other hand, the impact of tChol is very ambiguous.

Department of Animal Science Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Prague Czech Republic

Laboratory of Developmental Biology Institute of Animal Physiology and Genetics CAS Liběchov Czech Republic

Zobrazit více v PubMed

Aardema, H., Vos P. L. A. M., Lolicato F., Roelen B. A. J., Knijn H. M., Vaandrager A. B., Helms J. B., and Gadella B. M... 2011. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biol. Reprod. 85:62–69. doi: https://doi.org/ 10.1095/biolreprod.110.088815 PubMed DOI

Bartková, A. R., Němcová L., Kinterová V., Radová D., Strejček F., Toralová T., Laurinčík J., and Procházka R... 2024. Meiotic and developmental competence of growing pig oocytes derived from small antral follicles is enhanced in culture medium containing FGF2, LIF, and IGF1 (FLI medium). J. Ovarian Res. 17:54. doi: https://doi.org/ 10.1186/s13048-024-01360-0 PubMed DOI PMC

Benesova, V., Kinterova V., Kanka J., and Toralova T... 2017. Potential involvement of SCF-complex in zygotic genome activation during early bovine embryo development. Methods Mol. Biol. 1605:245–257. doi: https://doi.org/ 10.1007/978-1-4939-6988-3_17 PubMed DOI

Beran, J., Stádník L., Ducháček J., Okrouhlá M., Doležalová M., Kadlecová V., and Ptáček M... 2013. Relationships among the cervical mucus urea and acetone, accuracy of insemination timing, and sperm survival in Holstein cows. Anim. Reprod. Sci. 142:28–34. doi: https://doi.org/ 10.1016/j.anireprosci.2013.09.005 PubMed DOI

Bezdíček, J., Nesvadbová A., Ducháček J., Sekaninová J., Stádník L., and Janků M... 2024. Changes in the oxidative – biochemical status in dairy cows during the transition period affecting reproductive and health parameters. Czech J. Ani. Sci. 69:345–355. doi: https://doi.org/ 10.17221/128/2024-cjas DOI

Britt, J. H. 2008. Oocyte development in cattle: physiological and genetic aspects. R. Bras. Zootec 37:110–115. doi: https://doi.org/ 10.1590/s1516-35982008001300013 DOI

Chen, L., Thorup V. M., Kudahl A. B., and Østergaard S... 2024. Effects of heat stress on feed intake, milk yield, milk composition, and feed efficiency in dairy cows: a meta-analysis. J. Dairy Sci. 107:3207–3218. doi: https://doi.org/ 10.3168/jds.2023-24059 PubMed DOI

De Bie, J., Marei W. F. A., Maillo V., Jordaens L., Gutierrez-Adan A., Bols P. E. J., and Leroy J. L. M. R... 2017. Differential effects of high and low glucose concentrations during lipolysis-like conditions on bovine in vitro oocyte quality, metabolism and subsequent embryo development. Reprod. Fertil. Dev. 29:2284–2300. doi: https://doi.org/ 10.1071/RD16474 PubMed DOI

Dunning, K. R., Russell D. L., and Robker R. L... 2014. Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation. Reproduction 148:R15–R27. doi: https://doi.org/ 10.1530/REP-13-0251 PubMed DOI

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. doi: https://doi.org/ 10.1016/j.fertnstert.2011.01.154 PubMed DOI PMC

Kawashima, C., Sakaguchi M., Suzuki T., Sasamoto Y., Takahashi Y., Matsui M., and Miyamoto A... 2007. Metabolic profiles in ovulatory and anovulatory primiparous dairy cows during the first follicular wave postpartum. J. Reprod. Dev. 53:113–120. doi: https://doi.org/ 10.1262/jrd.18105 PubMed DOI

Leroy, J. L. M. R., Vanholder T., Delanghe J. R., Opsomer G., Van Soom A., Bols P. E. J., and de Kruif A... 2004. Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Anim. Reprod. Sci. 80:201–211. doi: https://doi.org/ 10.1016/S0378-4320(03)00173-8 PubMed DOI

Leroy, J. L. M. R., Van Soom A., Opsomer G., and Bols P. E. J... 2008a. The consequences of metabolic changes in high-yielding dairy cows on oocyte and embryo quality. Animal 2:1120–1127. doi: https://doi.org/ 10.1017/S1751731108002383 PubMed DOI

Leroy, J. L. M. R., Opsomer G., Van Soom A., Goovaerts I. G. F., and Bols P. E. J... 2008b. Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part I. The importance of negative energy balance and altered corpus luteum function to the reduction of oocyte and embryo quality in high-yielding dairy cows. Reprod. Domest. Anim. 43:612–622. doi: https://doi.org/ 10.1111/j.1439-0531.2007.00960.x PubMed DOI

Leroy, J. L. M., Sturmey R.G., Van Hoeck V., De Bie J., Mckeegan P., and Bols P... 2013. Dietary lipid supplementation on cow reproductive performance and oocyte and embryo viability: a real benefit? Anim. Reprod. 10:258–267.

Leroy, J. L. M. R., De Bie J., Jordaens L., Desmet K., Smits A., Marei W. F., and Van Hoeck V... 2018. Negative energy balance and metabolic stress in relation to oocyte and embryo quality: an update on possible pathways reducing fertility in dairy cows. Anim. Reprod. 14:497–506. doi: https://doi.org/ 10.21451/1984-3143-AR992 DOI

Martinez, C. A., Rizos D., Rodriguez-Martinez H., and Funahashi H... 2023. Oocyte-cumulus cells crosstalk: new comparative insights. Theriogenology 205:87–93. doi: https://doi.org/ 10.1016/j.theriogenology.2023.04.009 PubMed DOI

Matoba, S., O’Hara L., Carter F., Kelly A. K., Fair T., Rizos D., and Lonergan P... 2012. The association between metabolic parameters and oocyte quality early and late postpartum in Holstein dairy cows. J. Dairy Sci. 95:1257–1266. doi: https://doi.org/ 10.3168/jds.2011-4649 PubMed DOI

Menéndez, L. G., Fernández A. L., Enguix A., Ciriza C., and Amador J... 2001. Effect of storage of plasma and serum on enzymatic determination of non-esterified fatty acids. Ann. Clin. Biochem. 38:252–255. doi: https://doi.org/ 10.1258/0004563011900470 PubMed DOI

Nemcova, L., Bartkova A. R., Kinterova V., and Toralova T.. 2023. Importance of Supplementation during In Vitro Production of Livestock Animals. UK: IntechOpen. doi: 10.5772/intechopen.112008 DOI

Renaville, B., Bacciu N., Comin A., Motta M., Poli I., Vanini G., and Prandi A... 2010. Plasma and follicular fluid fatty acid profiles in dairy cows. Reprod. Domest. Anim. 45:118–121. doi: https://doi.org/ 10.1111/j.1439-0531.2008.01264.x PubMed DOI

Sarentonglaga, B., Ogata K., Taguchi Y., Kato Y., and Nagao Y... 2013. The developmental potential of oocytes is impaired in cattle with liver abnormalities. J. Reprod. Dev. 59:168–173. doi: https://doi.org/ 10.1262/jrd.2012-163 PubMed DOI PMC

Song, Y., Wang Z., Zhao C., Bai Y., Xia C., and Xu C... 2021. Effect of negative energy balance on plasma metabolites, minerals, hormones, cytokines and ovarian follicular growth rate in holstein dairy cows. J. Vet. Res. 65:361–368. doi: https://doi.org/ 10.2478/jvetres-2021-0035 PubMed DOI PMC

Stádník, L., Ducháček J., Beran J., Toušová R., and Ptáček M... 2015. Relationships between milk fatty acids composition in early lactation and subsequent reproductive performance in Czech Fleckvieh cows. Anim. Reprod. Sci. 155:75–79. doi: https://doi.org/ 10.1016/j.anireprosci.2015.02.002 PubMed DOI

Stádník, L., Ducháček J., Pytlík J., Gašparík M., Codl R., and Vrhel M... 2022. Cow metabolic status assessed from fat/protein ratio in milk affected ovarian response and number of transferable embryos after superovulation. Czech J. Anim. Sci. 67:39–46. doi: https://doi.org/ 10.17221/187/2021-cjas DOI

Stádník, L., Kinterová V., Šichtař J., Ducháček J., Gašparík M., Němcová L., Procházka R., and Codl R... 2024. Comparison of selected data acquisition models using on-farm production records on qualitative parameters of oocytes in dairy cows. Czech J. Anim. Sci. 69:1–10. doi: https://doi.org/ 10.17221/156/2023-cjas DOI

Štolcová, M., Bartoň L., and Řehák D... 2024. Milk components as potential indicators of energy status in early lactation Holstein dairy cows from two farms. Animal 18:101235. doi: https://doi.org/ 10.1016/j.animal.2024.101235 PubMed DOI

Su, Y. -Q., Sugiura K., Wigglesworth K., O’Brien M. J., Affourtit J. P., Pangas S. A., Matzuk M. M., and Eppig J. J... 2008. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135:111–121. doi: https://doi.org/ 10.1242/dev.009068 PubMed DOI

Takahashi, T., Mori A., Oda H., Murayama I., Kouno M., and Sako T... 2021. Comparison of cholesterol levels among lipoprotein fractions separated by anion-exchange high-performance liquid chromatography in periparturient Holstein-Friesian dairy cows. J. Vet. Med. Sci. 83:260–266. doi: https://doi.org/ 10.1292/jvms.20-0361 PubMed DOI PMC

Tessari, R., Berlanda M., Morgante M., Badon T., Gianesella M., Mazzotta E., Contiero B., and Fiore E... 2020. Changes of plasma fatty acids in four lipid classes to understand energy metabolism at different levels of non-esterified fatty acid (NEFA) in dairy cows. Animals (Basel) 10:1410. doi: https://doi.org/ 10.3390/ani10081410 PubMed DOI PMC

Tufarelli, V., Puvača N., Glamočić D., Pugliese G., and Colonna M. A... 2024. The most important metabolic diseases in dairy cattle during the transition period. Animals (Basel) 14:816. doi: https://doi.org/ 10.3390/ani14050816 PubMed DOI PMC

Valckx, S. D. M., De Pauw I., De Neubourg D., Inion I., Berth M., Fransen E., Bols P. E. J., and Leroy J. L. M. R... 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. doi: https://doi.org/ 10.1093/humrep/des350 PubMed DOI

Yehia, S. G., Ramadan E. S., Megahed E. A., and Salem N. Y... 2020. Effect of parity on metabolic and oxidative stress profiles in Holstein dairy cows. Vet World 13:2780–2786. doi: https://doi.org/ 10.14202/vetworld.2020.2780-2786 PubMed DOI PMC