Original Scientific Article
Metabolic profile comparison between follicular fluid and serum in normal cows and those affected by ovarian cysts
Nora Mimoune * ,
Rachid Kaidi ,
Mohammed Hocine Benaissa ,
Mohamed Wail Bahouh ,
Ratiba Baazizi ,
Mohamed Yassine Azzouz

Mac Vet Rev 2019; 42 (1): 51 - 59

10.2478/macvetrev-2018-0030

Received: 02 March 2018

Received in revised form: 12 July 2018

Accepted: 18 September 2018

Available Online First: 30 December 2018

Published on: 15 March 2019

Correspondence: Nora Mimoune, nora.mimoune@gmail.com
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Abstract

The aim of this study was to carry out the metabolic profile comparison between follicular fluid and serum in normal cows and those affected by ovarian cysts (OC). After slaughtering, blood samples and follicular fluids from normal and cystic animals were collected and assayed using commercial kits to determine the concentrations of metabolites (glucose, total protein, total cholesterol, cortisol, triglycerides, urea, creatinine and insulin) and the liver enzymes activity. Data showed that OC were characterized by low levels of glucose, total protein, cholesterol and cortisol in cystic fluid, while urea concentrations were high compared to normal follicular fluid (P<0.001). On the other hand, serum assays of cystic animals revealed very low values of insulin and urea, whereas cortisol levels were relatively high in comparison with the serum of normal cows (P<0.001). Significant correlations between the serum and follicular fluid concentrations of normal cows were found for glucose (r=0.49), total cholesterol (r=0.31), cortisol (r=0.38) and total protein (r=0.63). The highest correlation was found for urea (r=0.86). On contrary, weak correlations were observed between metabolites concentrations in cystic fluid and in serum for normal and cystic cows. In conclusion, OC grow and persist in a metabolic environment, which differs from follicular fluid to blood. These changes may act together and/or separately to ensure the continuous development of OC. To understand a part of the mechanism, the authors propose a deep study about blood-follicle-barrier.

Keywords: ovarian cyst, follicular fluid, serum, metabolic profile


References

1. Ghoneim, I.M., Waheed, M.M., El-Bahr, S.M., Alhaider, A.K., Al-Eknah, M.M. (2013). Comparison of some biochemical and hormonal constituents of oversized follicles and preovulatory follicles in camels (Camelus dromedarius). Theriogenology 79, 647–652. https://doi.org/10.1016/j.theriogenology.2012.11.019 PMid:23290312
2. Aller, J.F., Callejas, S.S., Alberio, R.H. (2013). Biochemical and steroid concentrations in follicular fluid and blood plasma in different follicular waves of the estrous cycle from normal and superovulated beef cows. Anim Reprod Sci. 142, 113-120. https://doi.org/10.1016/j.anireprosci.2013.09.009 PMid:24139762
3. Leroy, J.L.M.R., Vanholder, T., Delanghe, J.R., Opsomer, G., Van Soom, A., Bols, P.E.J., 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. https://doi.org/10.1016/S0378-4320(03)00173-8
4. Murayama, C., Yamasaki, E., Miyamoto, A., Shimizu, T. (2015). Effect in dedicator of cytokinesis 6 (DOCK6) on steroid production in theca cells of follicular cysts. Biochem Biophys Res Commun. 462, 415-419. https://doi.org/10.1016/j.bbrc.2015.05.005 PMid:25976676
5. Diaz, P.U., Stangaferro, M.L., Matiller, V., Salvetti, N.R., Gareis, N.C., et al. (2015). Characterization of persistent follicles induced by prolonged treatment with progesterone in dairy cows:An experimental model for the study of ovarian follicular cysts. Theriogenology 84, 1149–1160. https://doi.org/10.1016/j.theriogenology.2015.06.015 PMid:26187329
6. Kaneko J.J., Harvey H.W., Bruss M.L. (1997). Clinical biochemistry of domestic animals. In:Kaneko J.J., Harvey H.W., Bruss M.L. (Eds.), (p.932), San Diego:Academic Press.
7. Spicer, L.J., Chamberlain, C.S. (1998). Influence of cortisol on insulin- and insulin-like growth factor 1 (IGF-1)- induced steroid production and on IGF-1 receptors in cultured bovine granulosa cells and thecal cells. Endocrine 9 (2) :153–161. https://doi.org/10.1385/ENDO:9:2:153
8. Iwata, H., Inoue, J., Kimura, K., Kuge, T., Kuwayama, T., Monji, Y. (2006). Comparison between the characteristics of follicular fluid and the developmental competence of bovine oocytes. Anim Reprod Sci. 91, 215–223. https://doi.org/10.1016/j.anireprosci.2005.04.006 PMid:15961265
9. Bellier, S. (2010). Interpretation and usual values of blood parameters in veterinary clinical biochemistry. Revue Francophone Des Laboratoires 420.
10. Acar, Baki, D., Birdane, M.K., Dogan, N., Gurler, H. (2013). Effect of the stage of estrous cycle on follicular population, oocyte yield and quality, and biochemical composition of serum and follicular fluid in Anatolian water buffalo. Anim Reprod Sci. 137, 8-14. https://doi.org/10.1016/j.anireprosci.2012.12.004 PMid:23317849
11. Alves, B.G., Alves, K.A., Lúcio, A.C., Martins, M.C., Silva, T.H., Alves, B.G., et al. (2014). Ovarian activity and oocyte quality associated with the biochemical profile of serum and follicular fluid from Girolando dairy cows postpartum. Anim Reprod Sci. 146, 117–125. https://doi.org/10.1016/j.anireprosci.2014.02.019 PMid:24674823
12. Duffield, T.F. (2000). Subclinical ketosis in lactating dairy cattle. Vet Clin North Am Food Anim Pract. 16, 231-253. https://doi.org/10.1016/S0749-0720(15)30103-1
13. Yousefdoost, S., Samadi, F., Moghaddam, G., Hassani, S., Jafari Ahangari, Y. (2012). A comparison of hormonal, metabolite and mineral profiles between Holstein cows with and without ovarian cysts. IJAS. 2 (12):1107-1115.
14. Probo, M., Comin, A., Cairoli, F., Faustini, M., Kindahl, H., De Amicis, I., Veronesi, M.C. (2011). Selected metabolic and hormonal profiles during maintenance of spontaneous ovarian cysts in dairy cows. Reprod Dom Anim. 46, 448–454. https://doi.org/10.1111/j.1439-0531.2010.01688.x PMid:20825583
15. Brugère-Picoux, J. (1995). Metabolic diseases and clinical biochemistry of the dairy cow. La dépêche technique. 46, 30.
16. Yotov, S.A., Atanasov, A.S., Georgiev, G.B., Dineva, J.D., Palova, N.A. (2014). Investigation on some biochemical parameters and effect of hormonal treatment in anoestrous dairy cows with cystic ovarian follicle. Asian Pac J Reprod. 3 (1):41-45. https://doi.org/10.1016/S2305-0500(13)60183-9
17. Bender, K., Walsh, S., Evans, A.C.O., Fair, T., Brennan, L. (2010). Metabolite concentrations in follicular fluid may explain differences in fertility between heifers and lactating cows. Reproduction 139, 1047–1055. https://doi.org/10.1530/REP-10-0068 PMid:203ↂ2
18. Sun, Y.L., Ping, Z.G., Li, G.J., Sun, Y.F., Yi, K.L., Chen, L., Li, X.Y., Wang, X.L., Zhou, X. (2011). Comparative proteomic analysis of follicular fluids from normal and cystic follicles in sows. Reprod Dom Anim. 46, 889–895. https://doi.org/10.1111/j.1439-0531.2011.01760.x PMid:21366716
19. Fahiminiya, S., Gérard, N. (2010). Follicular fluid in mammals. Gynecol Obstet Fertil. 38, 402–404. https://doi.org/10.1016/j.gyobfe.2010.04.010 PMid:20576551
20. Khan, F.A., Das, G.K., Pande, M., Pathak, M.K., Sarkar, M. (2011). Biochemical and hormonal composition of follicular cysts in water buffalo (Bubalus bubalis). Anim Reprod Sci. 124, 61–64. https://doi.org/10.1016/j.anireprosci.2011.02.020 PMid:21392901
21. Arshad, H.M., Ahmad, N., Ziaur, R., Samad, H.A., Akhtar, N., Ali, S. (2005). Studies on some biochemical constituents of ovarian follicular fluid and peripheral blood in buffaloes. Pak Vet J. 25 (4):155-158.
22. El-Bahr, S.M., Ghoneim, I.M., Waheed, M.M. (2015). Biochemical and hormonal analysis of follicular fluid and serum of female dromedary camels (Camelus dromedarius) with different sized ovarian follicles. Anim Reprod Sci. 159, 98–103. https://doi.org/10.1016/j.anireprosci.2015.06.002 PMid:26077770
23. Sutton-McDowall, M.L., Yelland, R., MacMillan, K.L., Robker, R.L., Thompson, J.G. A. (2014). Study relating the composition of follicular fluid and blood plasma from individual Holstein dairy cows to the in vitro developmental competence of pooled abattoir-derived oocytes. Theriogenology 82, 95-103. https://doi.org/10.1016/j.theriogenology.2014.03.011 PMid:24746097
24. Zhao, H., Zhao, Y., Li, T., Li, M., Li, J., Li, R., Liu, P., Yu, Y., Qiao, J. (2015). Metabolism alteration in follicular niche:The nexus among intermediary metabolism, mitochondrial function, and classic polycystic ovary syndrome. Free Radic Biol Med 86, 295 –307. https://doi.org/10.1016/j.freeradbiomed.2015.05.013 PMid:26057937
25. Nandi, S., Girish, K.V., Manjunatha, B.M., Gupta, P.S.P. (2007). Biochemical composition of ovine follicular fluid in relation to follicle size. Dev Growth Differ. 49, 61–66.
https://doi.org/10.1111/j.1440-169X.2007.00901.x PMid:17227345
26. Wise, T. (1987). Biochemical analysis of bovine follicular fluid:albumin, total protein, lysosomal enzymes, ions, steroids and ascorbic acid content in relation to follicular size, rank, atresia classification and day of estrous cycle. J Anim Sci. 64, 1153-1169. https://doi.org/10.2527/jas1987.6441153x PMid:3571024
27. Maniwa, J., Izumi, S., Isobe, N., Terada, T. (2005). Studies on substantially increased proteins in follicular fluid of bovine ovarian follicular cysts using 2-D PAGE and MALDI-TOF MS. Reprod Biol Endocrinol. 3, 23. https://doi.org/10.1186/1477-7827-3-23 PMid:15941490 PMCid:PMC1177988
28. Isobe, N., Yoshimura, Y. (2000). Localization of apoptotic cells in the cystic ovarian follicles of cows:a DNA-end labelling histochemical study. Theriogenology 53, 897–904. https://doi.org/10.1016/S0093-691X(00)00238-7
29. Braw-Tal, R., Pen, S., Roth, Z. (2009). Ovarian cysts in high-yielding dairy cows. Theriogenology 72, 690–698. https://doi.org/10.1016/j.theriogenology.2009.04.027 PMid:19559473
30. Hudson, N.L., Berg, M.C., Green, M.P., Back, P.J., Thorstensen, E.B., Peterson, A.J., Pitman, J.L., McNatty, K.P. (2014). The microenvironment of the ovarian follicle in the postpartum dairy cows:Effects on reagent transfer from cumulus cells to oocytes in vitro. Theriogenology 82, 563–573. https://doi.org/10.1016/j.theriogenology.2014.05.016 PMid:2495↻
31. Ménézo, Y., Guérin, P. (2001). In:C. Thibault, Levasseur, M.C. (Eds.), Reproduction in mammals and humans (pp.410-421). Paris:Co-ed INRA-Ellipses.
32. Rabiee, A.R., Lean, I.J. (2000). Uptake of glucose and cholesterol by the ovary of sheep and cattle and the influence of arterial LH concentrations. Anim Reprod Sci. 64, 199-209. https://doi.org/10.1016/S0378-4320(00)00208-6
33. Hein, G.J., Panzani, C.G., Rodríguez, F.M., Salvetti, N.R., Díaz, P.U., Gareisa, N.C., Benítez, G.A., Ortega, H.H., Rey, F. (2015). Impaired insulin signaling pathway in ovarian follicles of cows with cystic ovarian disease. Anim Reprod Sci. 156, 64–74. https://doi.org/10.1016/j.anireprosci.2015.02.010 PMid:25813700
34. Vanholder, T., Leroy, J.L.M.R., Dewulf, J., Duchateau, L., Coryn, M., De Kruif, A., Opsomer, G. (2005). Hormonal and metabolic profiles of high-yielding dairy cows prior to ovarian cyst formation or first ovulation post-partum. Reprod Dom Anim. 40, 460 –467. https://doi.org/10.1111/j.1439-0531.2005.00601.x  PMid:16149953
35. Amweg, A.N., Salvetti, N.R., Stangaferro, M.L., Paredes, A.H., Lara, H.H., Rodríguez, F.M., Ortega, H.H. (2013). Ovarian localization of 11β-hydroxysteroid dehydrogenase (11βHSD):effects of ACTH stimulation and its relationship with bovine cystic ovarian disease. Domest Anim Endocrinol. 45, 126–140. https://doi.org/10.1016/j.domaniend.2013.07.001 PMid:23972491
36. Spicer, L.J., Zinn, S.A. (1987). Relationship between concentrations of cortisol in ovarian follicular fluid and various biochemical markers of follicular differentiation in cyclic and anovulatory cows. J Reprod Fert. 81, 221-226. https://doi.org/10.1530/jrf.0.0810221
37. Peter, A.T., Peter, I., Simon, J.E., Luker C.W., Bosu, W.T.K. (1990). Site of action for endotoxin-induced cortisol release in the suppression of preovulatory luteinizing hormone surges. Theriogenology 33 (3):637-643. https://doi.org/10.1016/0093-691X(90)90540-A
38. Kawate, N., Inaba, T., Mori, J. (1993). Effects of cortisol on the amounts of estradiol-17βand progesterone secreted and the number of luteinizing hormone receptors in cultured bovine granulosa cells. Anim Reprod Sci. 32 (15):15-25. https://doi.org/10.1016/0378-4320(93)90054-U
39. Sunak, N., Green, D.F., Abeydeera, L.R., Thurston, L.M., Michael, A.E. (2007). Implication of cortisol and 11b-hydroxysteroid dehydrogenase enzymes in the development of porcine (Sus scrofa domestica) ovarian follicles and cysts. Reproduction 133, 1149–1158. https://doi.org/10.1530/REP-07-0003 PMid:17636169


Copyright

© 2018 Mimoune N. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Acknowledgment

The authors are grateful to the staff of Nuclear Research Laboratory, Pathological Anatomy Laboratory of Douera (Algiers, Algeria) for their kind assistance during all analyses.

Conflict of Interest Statement

The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 42, Issue 1, Pages 51-59, p-ISSN 1409-7621, e-ISSN 1857-7415, DOI: 10.2478/macvetrev-2018-0030, 2018