Negative effects of zearalenone on reproductive productivity in dairy cattle

Year 2022, Volume: 1 Issue: 1, 42 - 57, 30.06.2022

Veysel Dogan , Sevval Damla Dal

Abstract

Mycotoxins, which are produced by different fungi reproduced in feed materials worldwide, have adverse effects on animal and human health. Zearalenone (ZEN) is a common mycotoxin, secreted from Fusarium spp. that may cause reproductive problems in animal species due to its non-steroidal estrogenic feature. The sensitivity of livestock to ZEN differs based on the species and sexuality. Cows are considered less sensitive to ZEN, however, there is limited information about adverse effects caused by ZEN. In this article, we aimed to review the effects of ZEN on cows in negative energy balance.

Keywords

Zearalenone, -zearalenol -zearalenol, negative energy balance, dairy cattle

References

• Alassane-Kpembi, I., Puel, O., & Oswald, I. P. (2015). Toxicological interactions between the mycotoxins deoxynivalenol, nivalenol, and their acetylated derivatives in intestinal epithelial cells. Archives of Toxicology, 89, 1337-1346. https://doi.org/10.1007/s00204- 014-1309-4
• Bauman, D. E., & Currie, W. B. (1980). Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis and homeorhesis. Journal of Dairy Science, 63(9), 1514-1529. https://doi.org/10.3168/jds.S0022-0302(80)83111-0
• Bloomquist, C., Davidson, J, & Person, E. (1983). Toxicology, metabolism, and physiological effects of aflatoxin in the bovine. In: U. L. Diener, R. L. Asquith, & J. W. Dickens, (Eds.), Aflatoxin and Aspergillus flavus in Corn. Alabama Agric. Exp. Sta. Auburn University.
• Castro, N., Kawashima, C., Van Dorland, H. A., Morel, I., Miyamoto, A., & Bruckmaier, R. M. (2012). Metabolic and energy status during the dry period is crucial for the resumption of ovarian activity postpartum in dairy cows. Journal of Dairy Science, 95(10), 5804-5812. https://doi.org/10.3168/jds.2012-5666
• Civelek, T., Aydin, I., Cingi, C. C., Yilmaz, O., & Kabu, M. (2011). Serum non-esterified fatty acids and beta-hydroxybutyrate in dairy cows with retained placenta. Pakistan Veterinary Journal, 31(4), 341-344.
• Coppock, R. W., Mostrom, M. S., Sparling, M. S., Jacobsen, B., & Ross, S. C. (1990). Apparent zearalenone intoxication in a dairy herd from feeding spoiled acid-treated corn. Veterinary and Human Toxicology, 32(3), 246-248.
• Danicke, S., & Winkler J. (2015). Invited review: Diagnosis of zearalenone (ZEN) exposure of farm animals and transfer of its residues into edible tissues (carry over). Food and Chemical Toxicology, 84, 225-249. https://doi.org/10.1016/j.fct.2015.08.009
• Danicke, S., Matthaus, K., Lebzien, P., Valenta, H., Stemm, K., Ueberschar, K. H., Razzazi- Fazeli, E., Böhm, J., & Flachowsky, G. (2005). Effects of Fusarium toxin-contaminated wheat grain on nutrient turnover, microbial protein synthesis, and metabolism of deoxynivalenol and zearalenone in the rumen of dairy cows. Journal of Animal Physiology and Animal Nutrition, 89(9-10), 303-315. https://doi.org/10.1111/j.1439- 0396.2005.00513.x
• Desjardins, A. E, & Proctor, R. H. (2007). Molecular biology of Fusarium mycotoxins. International Journal of Food Microbiology, 119(1-2), 47-50.
• Edite Bezerra da Rocha, M., da Freire, F. C. O., Erlan Feitosa Maia, F., Guedes, M. I. F., & Rondina, D. 2014. Mycotoxins and their effect on human and animal health. Food Control, 36, 159-165. https://doi.org/10.1016/j.foodcont.2013.08.021
• EFSA CONTAM. (2017). Panel Scientific opinion on risk for animal health related to the presence of zearalenone and its modified forms in feed. EFSA Journal, 15, 4851.
• EFSA. (2016). Panel on Contaminants in the Food Chain. Scientific opinion on the appropriateness to set a group helath-based guidance value for zearalenone and its modified forms. EFSA Journal, 14, 4425.
• Eskola, M., Kos, G., Elliott, C. T., Hajslova, J., Maya, S., & Krska, R. 2020. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25. Critical Reviews in Food Science and Nutrition, 60(16), 2773-2786. https://doi.org/10.1080/10408398.2019.1658570
• Fenwick, M. A., Llewellyn, S., Fitzpatrick, R., Kenny, D. A., Murphy, J. J., Patton, J., & Wathes, D. C. (2008). Negative energy balance in dairy cows is associated with specific changes in IGF-binding protein expression in oviduct. Reproduction, 135(1), 63-75. https://doi.org/10.1530/REP-07-0243
• Fiedler, K., Schutz, E., & Geh, S. (2001). Detection of microbial volatile organic compounds (MVOCs) produced by moulds on various materials. International Hygiene and Environmental Health, 204(2-3), 111-121. https://doi.org/10.1078/1438-4639-00094
• Fink-Gremmels, J. (2008). The role of mycotoxins in the health and performance of dairy cows. The Veterinary Journal, 176, 84-92. https://doi.org/10.1016/j.tvjl.2007.12.034
• Fushimi, Y., Takagi, M., Monniaux, D., Uno, S., Kokushi, E., Shinya, U., Kawashima, C., Otoi, T., Deguchi, E., & Fink-Gremmels, J. (2015). Effects of dietary contamination by zearalenone and its metabolites on serum anti-müllerian hormone: Impact on the reproductive performance of breeding cows. Reproduction in Domestic Animals, 50(5), 834-839. https://doi.org/10.1111/rda.12599
• Gromadzka, K., Waskiewicz, A., Chelkowski, J., & Golinski, P. (2008). Zearalenone and its metabolites: Ocuurance, detection, toxicity and guidelines. World Mycotoxin Journal, 1(2), 209-220. https://doi.org/10.3920/WMJ2008.x015
• Grummer, R. R., Mashek, D. G., & Hayirli, A. (2004). Dry matter intake and energy balance in the transition period. Veterinary Clinics of North America: Food Animal Practice, 20(3), 447-470. https://doi.org/10.1016/j.cvfa.2004.06.013
• Harcarova, M., Conkova, E., Proskovcova, M., & Falis, M. (2020). In vivo assessment of zearalenone toxicity. Folia Veterinaria, 64(2), 60-65. https://doi.org/10.2478/fv-2020- 0018
• Hayirli, A., Grummer, R. R., Nordehim, E. V., & Crump, P. M. (2002). Animal and dietary factors affecting feed intake during the prefresh transition period in Holsteins. Journal of Dairy Science, 85(12), 3430-3443. https://doi.org/10.3168/jds.S0022-0302(02)74431-7
• Huzzey, J. M., Mann, S., Nydam, D. V., Grant, R. J., & Overton, T. R. (2015). Associations of peripartum markers of stress and inflammation with milk yield and reproductive performance in Holstein dairy cows. Preventive Veterinary Medicine, 120(3-4), 291- 2917. https://doi.org/10.1016/j.prevetmed.2015.04.011
• Kallela, K., & Ettala, E. (1984). The oestrogenic Fusarium toxin (zearalenone) in hay as a cause of early abortions in the cow. Nordisk Veterinaer Medicine, 36(9-10), 305-309.
• Kiessling, K. H., Pettersson, H., Sandholm, K., & Olsen, M. (1984). Metabolism of aflatoxin, ochratoxin, zearalenone, and three trichothecenes by intact rumen fluid, rumen protozoa, and rumen bacteria. Applied and Environmental Microbiology, 47(5), 1070- 1073. https://doi.org/10.1128/aem.47.5.1070-1073.1984
• King, R. R., McQueen, R. E., Levesque, D., & Greenhalgh, R. (1984). Transformation of deoxynivalenol (vomitoxin) by rumen microorganisms. Journal of Agricultural and Food Chemistry, 32(5), 1181-1183. https://doi.org/10.1021/jf00125a061
• Kinoshita, A., Keese, C., Meyer, U., Starke, A., Wrenzycki, C., Danicke, S., & Rehage, J. (2018). Chronic effects of Fusarium mycotoxins in rations with or without increased concentrate proportion on the insulin sensitivity in lactating dairy cows. Toxins, 10(5), 188. https://doi.org/10.3390/toxins10050188
• Kramer, R. 1997. Zearalenone in Pasture and its Effects on Reproduction in Ewes. MApplSc thesis, Masset University, Parmerston North, New Zealand.
• Kuiper-Goodman, T., Scott, P. M., & Watanabe, H. (1987). Risk assessment of the mycotoxin zearalenone. Regulatory Toxicology and Pharmacology, 7(3), 253-306. https://doi.org/10.1016/0273-2300(87)90037-7
• Kuiper-Goodman, T., Scott, P. M., & Watanabe, H. (1987). Risk assessment of the mycotoxin zearalenone. Regulatory Toxicology and Pharmacology, 7(3), 253-306. https://doi.org/10.1016/0273-2300(87)90037-7
• Kumari, S., Prasad, S., Patbandha, T. K., Pathak, R., Kumerasan, A., Boro, P., Maniamaran, A., & Mohanty, T. K. (2016). Metabolic indicators for retention of fetal membranes in Zebu and crossbred dairy cattle. Animal Production Science, 56(7), 1113-1120. https://doi.org/10.1071/AN14941
• Li, Y., Zhang, B., He, X., Cheng, W. H., Xu, W., Luo, Y., Liang, R., Luo, H., &Huang, K. (2014). Analysis of individual and combined effects of ochratoxin A and zearalenone on HepG2 and KK-1 cells with methematical models. Toxins, 6(4), 1177-1192. https://doi.org/10.3390/toxins6041177
• Li. L., Zhang, T., Ren, X., Li, B., & Wang, S. (2021). Male reproductive toxicity of zearalenone-meta-analysis with mechanism review. Ecotoxicolgy and Environmental Safety, 221, 112457. https://doi.org/10.1016/j.ecoenv.2021.112457
• Malekinejad, H., Colenbrander, B., & Fink-Gremmels, J. (2006). Hydroxstreoid dehydrogenases in bovine and porcine granulosa cells convert zearalenone into its hydroxylated metabolites -zearalenol and -zearalenol. Veterinary Research Communications, 30, 445-453. https://doi.org/10.1007/s11259-006-3325-1
• Marquardt, J. P., Horst, R. L., & Jorgensen, N. A. (1977). Effect of parity on dry matter intake at parturition in dairy cattle. Journal of Dairy Science, 60(6), 929-934. https://doi.org/10.3168/jds.S0022-0302(77)83965-9
• Martins, C., Torres, D., Lopes, C., Correia, D., Goios, A., Assunçao, R., Alvito, P., Vidal, A., De Boevre, M., De Saeger, S., & Nunes, C. (2020). Food consumption data as a tool to estimate exposure to mycoestrogens. Toxins, 12, 118. https://doi.org/10.3390/toxins12020118
• Metzler, M., Pfeiffer, E., & Hildebrand, A. (2010). Zearalenone and its metabolites as endocrine disrupting chemicals. World Mycotoxin Journal, 3(4), 385-401. https://doi.org/10.3920/WMJ2010.1244
• Minervini, F., Dell’Aquilla, M. E., Maritato, F., Minoia, P., & Visconti, A. (2001). Toxic effect of the mycotoxin zearalenone and its derivatives on in vitro maturation of bovine oocytes and 17-estradiol levels in mural granulosa cell cultures. Toxicology in Vitro, 15(4-5), 489-495. https://doi.org/10.1016/S0887-2333(01)00068-6
• Mirocha, C. J., Harrison, J., Nichols, A. A., & McClintock, M. (1968). Detection of a fungal estrogen (F-2) in hay associated with infertility in dairy cattle. Applied Microbiology, 16(5), 797. https://doi.org/10.1128/am.16.5.797-798.1968
• Mirocha, C. J., Weaver, G., Gustafsson, B., Chi, M., Pathre, S. V., Robinson, T. S., & Bates, F. (1978a). Pharmacological and Toxicological Studies on Zearalenone in Food Producing Animals. Food and Drug Administration. Washington, DC.
• Mirocha, C. J., Pathre, S. V., Behrens, J., & Schaueramer, B. (1978b). Uterotropic activity of cis and trans isomers of zearalenone an zearalenol. Applied and Environmental Microbiology, 35(5), 986-987. https://doi.org/10.1128/aem.35.5.986-987.1978
• Monniaux, D., Clement, F., Dalbies-Tran, R., Estienne, A., Fabre, S., Mansanet, C., & Monget, P. (2014). The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link? Biology of Reproduction, 90(4), 1-11. https://doi.org/10.1095/biolreprod.113.117077
• Monniaux, D., Drouilhet L., Rico, C., Estienne, A., Jarrier, P., Touze, J. L., Sapa, J., Phocas, F., Dupont, J., Dalbies-Tran, R., & Fabre, S. (2013). Regulation of anti-Müllerian hormone production in domestic animals. Reproduction, Fertility and Development, 25(1), 1-16. https://doi.org/10.1071/RD12270
• Moretti, P., Probo, M., Cantoni, A., Paltrinieri, S., & Giordano, A. (2016). Fluctation of neutrophil counts around parturition in Holstein dairy cows with and without retained placenta. Research in Veterinary Science, 107, 207-212. https://doi.org/10.1016/j.rvsc.2016.06.015
• Mostrom., M. S. (2012). Zearalenone. In: R. C. Gupta (Ed.), Veterinary Toxicology. London, Elsevier.
• Nakamura, U., Rudolf, F. O., Pandey, K., & Kadokawa, H. (2015). The non-streoidal mycoestrogen zeranol suppresses luteinizing hormone secretion from the anterior pituitary of cattle via the estradiol receptor GPR30 in a rapid, non-genomic manner. Animal Reproduction Science, 156, 118-127. https://doi.org/10.1016/j.anireprosci.2015.03.009
• Overton, T. R., & Waldron, M. R. (2004). Nutritional management of transition dairy cows: Strategies to optimize metabolic health. Journal of Dairy Science, 87, 105-119. https://doi.org/10.3168/jds.S0022-0302(04)70066-1
• Pizzo, F., Caloni, F., Schreiber, N. B., Cortinovis, C., & Spicer, L. J. (2016). In vitro effects of deoxynivalenol and zearalenone major metabolites alone and combined, on cell proliferation, steroid production and gene expression in bovine small-follicle granulosa cells. Toxicon, 109, 70-83. https://doi.org/10.1016/j.toxicon.2015.11.018
• Ricciardi, C., Castagna, R., Ferrante, I., Frascella, F., Marasso, S. L., Ricci, A., Canavese, G., Lore, A., Prelle, A., Gullino, M. L., & Spadora, D. (2013). Development of a microcantilever-based immunosensing method for mycotoxin detection. Biosensor & Bioelectronics, 40(1), 233-239. https://doi.org/10.1016/j.bios.2012.07.029
• Rico, C., Fabre, S., Medigue, C., di Clemente, N., Clement, F., Bontoux, M., Touze, J. L., Dupont, M., Briant, E., Reny, B., Beckers, J. F., & Monniaux, D. (2009). Anti- Müllerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biology of Reproduction, 80(1), 50-59. https://doi.org/10.1095/biolreprod.108.072157
• Roine, K., Korpinen, E. L., & Kallela, L. (1971). Mycotoxicosis as the probable cause of infertility in dairy cows. Nordisk Veterinaer Medicin, 23(12): 628-633
• Ropejko, K., & Twaruzek, M. (2021). Zearalenone and its metabolites- General overview, occurrence, and toxicity. Toxins, 13, 35. https://doi.org/10.3390/toxins13010035
• Rudolf, F. O., & Kadokawa, H. (2014). Expression of estradiol receptor, GPR30, in bovine anterior pituitary and effects of GPR30 agonist on GnRH-induced LH secretion. Animal Reproduction Science, 139(1-4), 9-17. https://doi.org/10.1016/j.anireprosci.2013.04.003
• Schatzmayr, G., Zehner, F., Taubel, M. Schatzmayr, D., Klimitsch, A., Loibner, A. P., & Binder, E. M. (2006). Microbiologicals for deactivating mycotoxins. Molecular Nutrition & Food Research, 50(6), 543-551. https://doi.org/10.1002/mnfr.200500181
• Seeling, K., Boguhn, J., Strobel, E., Danicke, S., Valenta, H., Ueberschar, K. H., & Rodehutscord, M. (2006). On the effects of Fusarium toxin contaminated wheat and wheat chaff on nutrient utilization and turnover of deoxynivalenol and zearalenone in vitro. Toxicology in Vitro, 20, 703-711. https://doi.org/10.1016/j.tiv.2005.10.006
• Shin, E. K., Jeong, J. K., Choi, I. S., Kang, H. G., Hur, T. Y., Jung, Y. H., & Kim, I. H. (2015). Relationship among ketosis, serum metabolites, body condition, and reproductive outcomes in dairy cows. Theriogenology, 84(2), 252-260. https://doi.org/10.1016/j.theriogenology.2015.03.014
• Silva, L. A., Mello, M. R. B., Piao, D. O., Silenciato, L. N., Quadros, T. C. O., Souza, A. H., & Barbero, R. P. (2021). Effects of experimental exposure to zearalenone on reproductive system morphometry, plasma oestrogen levels, and oocyte quality of beef heifer. Reproduction in Domestic Animals, 56(5), 775-782. https://doi.org/10.1111/rda.13917
• Takagi, M., Mukai, S., Kuriyagawa, T., Takagaki, K., Uno, S., Kokushi, E., Otoi, T., Budiyanto, A., Shirasuna, K., Miyamoto, A., Kawamura, O., Okamoto, K., & Deguchi, E. (2008). Detection of zearalenone and its metabolites in naturally contaminated follicular fluids by using LC/MS/MS and in vitro effects of zearalenone on oocyte maturation in cattle. Reproductive Toxicology, 26(2), 164-169. https://doi.org/10.1016/j.reprotox.2008.08.006
• Taylor, V. J., Beever, D. E., & Wathes, D. C. (2003). Physiological adaptations to milk production that affect fertility in high-yielding dairy cows. British Society of Animal Science Occasional Publication, vol 29, (pp. 37-71). Nottingham, UK: Nottingham University Press.
• Tola, M., & Kebede, B. (2016). Occurrence, importance and control of mycotoxins: A review. Cogent Food & Agriculture, 2(1), 1191103. https://doi.org/10.1080/23311932.2016.1191103
• Towers, N. R., & Sprosen, J.M. (1993). Zearalenone-induced fertility in sheep and cattle in New Zealend. New Zealend Veterinary Journal, 41, 223-224.
• Valenta, H., & Vemmer, H. (1996). In vitro-Unterschungen zum Metabolismus von Zearalenon bei Inkubation mit Pansensaft; Proceedings of the 18 Mykotoxin-Workshop; Kulmbach, Germany. 10-12 June 1996 [(accessed on 14 May 2022)]. (pp, 10-12).
• Visser, J.A., & Themmen, A. P. (2014). Role of anti-Müllerian hormone and bone morphogenetic proteins in the regulation of FSH sensitivity. Molecular and Cellular Endocrinology, 382(1), 460-465. https://doi.org/10.1016/j.mce.2013.08.012
• Wankhade, P. R., Manimaran, A., Kumerasan, A., Jeyakumar, S., Ramesha, K. P., Sejian, V., Rajendran, D., & Varghese, M. R. (2017). Metabolic and immunological changes in transition dairy cows: A review. Veterinary World, 10, 1367-1377. https://doi. org/10.14202/vetworld.2017.1367-1377
• Weaver, G. A., Kurtz, H. J., Behrens, J. C., Robinson, T. C., Sequin, B.E., Bates, F. Y., & Mirocha, C. J. (1986). Effect of zearalenone on fertility of virgin dairy heifers. American Journal of Veterinary Research, 47(6):1395-1397.
• Winkler, J., Kersten, S., Meyer, U., Stinshoff, H., Locher, L., Rehage, J., Wrenzycki, C., Engelhardt, U.H., & Danicke, S. (2015). Diagnostic opportunities for evaluation of the exposure of dairy cows to the mycotoxins deoxynivalenol (DON) and zearalenone (ZEN): reliability of blood plasma, bile and follicular fluid as indicators. Journal of Animal Physiology and Animal Nutrition, 99(5), 847-855. https://doi.org/10.1111/jpn.12285
• Yang, F., Li, L., Chen, K., Li, C., Wang, Y., & Wang, G. (2019). Melatonin alleviates - zearalenol and HT-2 toxin-induced apoptosis and oxidative stress in bovine ovarian granulosa cells. Environmental Toxicology and Pharmacology, 68, 52-60. https://doi.org/10.1016/j.etap.2019.03.005
• Zhang, G. L., Feng, Y. L., Song. J. L., & Zhou, X. S. (2018). Zearalenone: A mycotoxin with different toxic effect in domestic and laboratory animlas’ granulosa cells. Frontier in Genetics, 9, 667. https://doi.org/10.3389/fgene.2018.00667
• Zheng, N., Gao, Y. N., Liu, J., Wang, H. W., &Wang, Q. J. (2018). Individual and combined cytotoxicity assessment of zearalenone with ochratoxin A or -zearalenol by full factorial design. Food Science Biotechnology, 27(1), 251-259. https://doi.org/10.1007/s10068-017-0197-9
• Zhu, L., Yuan, H., Guo, C., Lu, Y., Deng, S., Yang, Y., Wei, Q., & Wen, H. (2012). Zearalenone induces apoptosis and necrosis in porcine granulosa cells via a caspase-3-and caspase-9-dependent mitochondrial signaling pathway. Journal of Cellular Physiology, 227, 1814-1820. https://doi.org/10.1002/jcp.22906