Original Scientific Article
Impact of body condition score on oxidative stress status in cow’s reproductive tract
Amel Khaled ,
Sofiane Boudjellaba ,
Takfarinas Idres ,
Yuva Bellik * ,
Mohammed Nait Mouloud ,
Mokrane Iguer-Ouada

Mac Vet Rev 2020; 43 (2): 93 - 101

10.2478/macvetrev-2020-0021

Received: 17 October 2019

Received in revised form: 08 April 2020

Accepted: 25 May 2020

Available Online First: 02 July 2020

Published on: 15 October 2020

Correspondence: Yuva Bellik, y.bellik@univ-bba.dz
PDF HTML

Abstract

It is well known in cattle that reproductive disorders are intimately associated with low or high body condition score (BCS). However, little is known concerning the relationship between BCS and oxidative stress, particularly in the reproductive tract. Thus, the aim of the present study was to investigate the oxidative stress biomarkers according to cows BCS values in the plasma, ovaries, oviductal, follicular and uterine fluids. The study was conducted on 58 cows classified in four classes (1, 2, 3 and 4) of BCS varying from1-1.5, 2-2.5, 3-3.5 and 4-4.5, respectively. The genital tracts and plasma were collected from slaughtered cows and processed within 5h after slaughtering. The number of ovarian follicles was measured using ultrasonography and the oxidative stress was assessed by considering total antioxidant status (TAS), catalase activity (CAT), and thiobarbituric acid-reactive substances (TBARS). The results showed that follicles number was significantly affected by BCS; cows with medium BCS (3) presented higher number of follicles than cows with low or high BCS (<3 or >3). Overall, BCS affects significantly the oxidative stress status at different levels of the reproductive tract. Cows with medium BCS (3) showed the best oxidative status than those with low or high values (BCS <3 or >3). In conclusion, the current results suggest that reproductive disorders observed in cows with low or high BCS values could be mediated through oxidative stress affecting consequently the reproductive tract and finally compromising fertility outputs.

Keywords: BCS, oxidative status, follicles number, reproductive tract, reproduction


References

  1. Buckley, F., O'Sullivan, K., Mee, J.F., Evans, R.D., Dillon, P. (2003). Relationships among milk yield, body condition, cow weight, and reproduction in spring-calved Holstein-Friesians. J Dairy Sci. 86 (7):2308-2319. https://doi.org/10.3168/jds.S0022-0302(03)73823-5
  2. Houghton, P.L., Lemenager, R.P., Moss, G.E., Hendrix, K.S. (1990). Prediction of postpartum beef cow body composition using weight to height ratio and visual body condition score. J Anim Sci. 68 (5):1428-1437. https://doi.org/10.2527/1990.6851447x PMid:2365655        
  3. Gillund, P., Reksen, O., Gröhn, Y., Karlberg, K. (2001). Body condition related to ketosis and reproductive performance in Norwegian dairy cows. J Dairy Sci. 84 (6):1390-1396. https://doi.org/10.3168/jds.S0022-0302(01)70170-1
  4. Gearhart, M., Curtis, C., Erb, H., et al. (1990). Relationship of changes in condition score to cow health in Holsteins. J Dairy Sci. 73 (11):3132-3140. https://doi.org/10.3168/jds.S0022-0302(90)79002-9
  5. Edmonson, A.J., Lean, I.J., Weaver, L.D., Farver, T., Webster, G. (1989). A body condition scoring chart for Holstein dairy cows. J Dairy Sci. 72 (1):68-78. https://doi.org/10.3168/jds.S0022-0302(89)79081-0
  6. Stagg, K., Spicer, L., Roche, J.F., Diskin, M.G. (1998). Effect of calf isolation on follicullar wave dynamics, gonadotrophin, and metabolic changes, and interval to first ovulation in beef cows fed either of tow energy levels postpartum. Biol Reprod. 59 (4):777-783. https://doi.org/10.1095/biolreprod59.4.777 PMid:9746725
  7. Overton, T.R., Waldron, M.R. (2004). Nutritional management of transition dairy cows: Strategies to optimize metabolic health. J Dairy Sci. 87 (Suppl):105-119. https://doi.org/10.3168/jds.S0022-0302(04)70066-1
  8. Celi, P. (2011). Biomarkers of oxidative stress in ruminant medicine. Immunopharmacol Immunotoxicol. 33 (2):233-240. doi:10.3109/08923973.2010.514917 https://doi.org/10.3109/08923973.2010.514917 PMid:20849293    
  9. Ferguson, J., Galligan D., Thomsen, N. (1994). Principal descriptors of body condition in Holstein dairy cattle. J Dairy Sci. 77 (9):2695-2703. https://doi.org/10.3168/jds.S0022-0302(94)77212-X
  10. Aebi, H. (1984). Catalase in Vitro. Methods Enzymol. 105, 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3
  11. Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M., Rice-Evans, C. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med. 26 (9-10):1231-1237. https://doi.org/10.1016/S0891-5849(98)00315-3
  12. Stocks, J., Dormandy, T.L. (1971). The autoxidation of human red cell lipids induced by hydrogen peroxide. Br J Haematol. 20 (1):95-111. https://doi.org/10.1111/j.1365-2141.1971.tb00790.x PMid:5540044        
  13. Wright, I.A., Rhind, S.M., Russel, A.J.F., Whyte, T.K., McBean, A.J., McMillen, S.R. (1987). Effects of body condition, food intake and temporary calf separation on the duration of the post-partum anoestrus period and associated LH, FSH and prolactin concentrations in beef cows. Anim Prod. 45 (3):395-402. https://doi.org/10.1017/S0003356100002889
  14. Galina, C., Arthur, G. (1989). Review of cattle reproduction in the tropics. 3. Puerperium. In: Anim. Breed. Abstr. 57, 889-910.
  15. Polak, G., Koziol-Montewka, M., Gogacz, M., Blaszkowska, I., Kotarski, J. (2001). Total antioxidant status of peritoneal fluid in infertile women. Eur J Obstet Gynecol Reprod Biol. 94 (2):261-263. https://doi.org/10.1016/S0301-2115(00)00352-3
  16. Combelles, C.M., Gupta, S., Agarwal, A. (2009). Could oxidative stress influence the in-vitro maturation of oocytes?. Reprod Biomed Online. 18 (6):864-880. https://doi.org/10.1016/S1472-6483(10)60038-7
  17. Al-Gubory, K., Fowler, P.A., Garrel, C. (2010). The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol. 42 (10):1634-1650. https://doi.org/10.1016/j.biocel.2010.06.001 PMid:20601089          
  18. Bernal, A., Vickers, M., Hampton, M., Poynton, R., Sloboda, D. (2010). Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One. 5 (12):155-158. https://doi.org/10.1371/journal.pone.0015558 PMid:21179452 PMCid:PMC3001490           
  19. Anderson, K., Nisenblat, V., Norman, R. (2010). Lifestyle factors in people seeking infertility treatment. Aust N Z J Obs Gynaecol. 50(1):8-20. https://doi.org/10.1111/j.1479-828X.2009.01119.x PMid:20218991     
  20. Butler, W. (2000). Nutritional interactions with reproductive performance in dairy cattle. Anim Reprod Sci. 60-61, 449-457. https://doi.org/10.1016/S0378-4320(00)00076-2
  21. Diskin, M.G., Mackey, D.R., Roche, J.F., Sreenan, J. (2003). Effects of nutrition and metabolic status on circulating hormone and ovarian follicle development in cattle. Anim Reprod Sci. 78 (3-4):345-370. https://doi.org/10.1016/S0378-4320(03)00099-X
  22. Bernabucci, U., Ronchi, B., Lacetera, N., Nardone, A. (2005). Influence of body condition score on relationships between betabolic status and oxidative stress in periparturient dairy cows. J Dairy Sci. 88 (6):2017-2026. doi:10.3168/jds.S0022-0302(05)72878-2 https://doi.org/10.3168/jds.S0022-0302(05)72878-2
  23. Santos, J.E.P., Cerri, R.L.A., Sartori, R. (2008). Nutritional management of the donor cow. Theriogenology. 69 (1): 88-97. https://doi.org/10.1016/j.theriogenology.2007.09.010 PMid:17959235     
  24. Bage, R., Awasthi, H., Saravia, F., Rodriguez-Martinez, H. (2007). Excessive lipid contents in immature oocytes from repeat breeder dairy heifers. Reprod Domest Anim. 42(2): 67.
  25. Igosheva, N., Abramov, A.Y., Poston, L., et al. (2010). Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One. 5 (4):e10074. doi:10.1371/journal.pone.0010074 https://doi.org/10.1371/journal.pone.0010074 PMid:20404917 PMCid:PMC2852405
  26. Lord, T., Aitken, R.J. (2013). Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 146 (6), R217-R227. doi:10.1530/REP-13-0111 https://doi.org/10.1530/REP-13-0111 PMid:23950493     
  27. Revelli, A., Piane, L.D., Casano, S., Molinari, E., Massobrio, M., Rinaudo, P. (2009) Follicular fluid content and oocyte quality: from single biochemical markers to metabolomics. Reprod Biol Endocrinol. 7 (40): 874-878. doi:10.1186/1477-7827-7-40 https://doi.org/10.1186/1477-7827-7-40 PMid:19413899 PMCid:PMC2685803          
  28. Gupta, S., Choi, A., Yu, H.Y., et al. (2011). Fluctuations in total antioxidant capacity, catalase activity, and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis. Reprod Fertil Dev. 23 (5):673-680. doi:10.1071/RD10270. https://doi.org/10.1071/RD10270 PMid:21635816 PMCid:PMC3235527           
  29. Pasqualotto, E., Agarwal, A., Sharma, R., et al. (2004). Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril. 81 (4):973-976. https://doi.org/10.1016/j.fertnstert.2003.11.021 PMid:15066450   
  30. Pasqualotto, E., Lara, L., Salvador, M., Sobreiro, B., Borges, E., Pasqualotto, F. (2009). The role of enzymatic antioxidants detected in the follicular fluid and semen of infertile couples undergoing assisted reproduction. Hum Fertil. 12 (3):166-171. https://doi.org/10.1080/14647270903207941 PMid:19925327     
  31. Kazemi, A., Ramezanzadeh, F., Nasr Esfahani, M.H., Saboor-Yaraghi, A.A., Nejat, S., Rahimi-Foroshani, A. (2014). Relationship between energy expenditure related factors and oxidative stress in follicular fluid. Int J Fertil Steril. 8 (2):175-182.            
  32. Walter I. (1995). Culture of bovine oviduct epithelial cells (BOEC). Anat Rec. 243 (3), 347-356. https://doi.org/10.1002/ar.1092430309 PMid:8579254       
  33. Murray, M., De Souza, M., Messinger, S. (1995). Oviduct during early pregnancy: hormonal regulation and interactions with the fertilized ovum. Microsc Res Tech. 31 (6):497-506. https://doi.org/10.1002/jemt.1070310606 PMid:8527850  
  34. Arganaraz, M.E., Apichela, S.A., Miceli, D.C. (2012). LEFTY2 expression and localization in rat oviduct during early pregnancy. Zygote. 20 (1):53-60. https://doi.org/10.1017/S0967199410000602 PMid:21205391     
  35. Cheong, A.W.Y., Lee, Y., Liu, W., Yeung, W.S.B., Lee, K. (2009). Oviductal microsomal epoxide hydrolase ( EPHX1 ) reduces reactive oxygen species ( ROS ) level and enhances preimplantation mouse embryo development. Biol Reprod. 81 (1):126-132. doi:10.1095/biolreprod.108.071449 https://doi.org/10.1095/biolreprod.108.071449 PMid:19321813     
  36. Agarwal, A., Saleh, R.A., Bedaiwy, M.A. (2003). Modern trends role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 79 (4):829-843. doi:10.1016/S0015-0282(02)04948-8 https://doi.org/10.1016/S0015-0282(02)04948-8
  37. Al-Gubory, K.H., Arianmanesh, M., Garrel, C., Bhattacharya, S., Cash, P., Fowler, P.A. (2014). Proteomic analysis of the sheep caruncular and intercaruncular endometrium reveals changes in functional proteins crucial for the establishment of pregnancy. Reproduction. 147 (5):599-614. doi:10.1530/REP-13-0600 https://doi.org/10.1530/REP-13-0600 PMid:24446454     
  38. Yoon, S., Choi, S., Sim, B., et al. (2014). Developmental competence of bovine early embryos depends on the coupled response between oxidative and endoplasmic reticulum stress. Biol Reprod. 90 (5):104. doi:10.1095/biolreprod.113.113480 https://doi.org/10.1095/biolreprod.113.113480 PMid:24695629     
  39. Kim, I.H., Suh, G.H. (2003). Effect of the amount of body condition loss from the dry to near calving periods on the subsequent body condition change, occurrence of postpartum diseases, metabolic parameters and reproductive performance in Holstein dairy cows. Theriogenology. 60(8): 1445-1456. https://doi.org/10.1016/S0093-691X(03)00135-3


Copyright

© 2020 Bellik Y. 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.

Conflict of Interest Statement

The authors have declared that no competing interests exist.

Citation Information

Macedonian Veterinary Review. Volume 43, Issue 2, Pages 93-101, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2020-0021, 2020