Assessment of selected immunological parameters in dairy cows with naturally occurring mycotoxicosis before and after the application of a mycotoxin deactivator

Brodzki, Piotr; Marczuk, Jan; Lisiecka, Urszula; Krakowski, Leszek; Szczubiał, Marek; Dąbrowski, Roman; Bochniarz, Mariola; Kulpa, Katarzyna; Brodzki, Nikodem; Wolniaczyk, Karolina

doi:10.2478/jvetres-2023-0002

Abstract

Introduction

Mycotoxins in dairy cows can cause many non-specific symptoms often resulting from immune system overreaction. The study assessed the concentration of selected cytokines and acute phase proteins (APP) in cows with natural mycotoxicosis before and after using a mycotoxin neutraliser. The cytokines were tumour necrosis factor alpha (TNF-α), interleukin 6 (IL-6) and interleukin 10 (IL-10), and the APP were serum amyloid A (SAA) and haptoglobin (Hp).

Material and Methods

The research was carried out on an experimental group (Exp) of 10 herdmate Holstein-Friesian cows with mycotoxicosis. The control group (Con) was 10 healthy cows of the same breed from a different herd. Cows in the Exp group were administered the mycotoxin deactivator Mycofix for three months. Blood was drawn from Exp cows once before administering Mycofix and a second time after three months of its use. Blood was also drawn from Con cows at the same times. Serum levels of TNF-α, IL-6, IL-10, SAA and Hp were assessed using ELISA.

Results

The concentrations of all cytokines and Hp in Exp cows were higher before treatment (P < 0.001) than those in Con cows. After three months of administering Mycofix, the concentrations of TNF-α and IL-6 were significantly lower than their pre-treatment levels (P < 0.001). The concentrations of IL-6, IL-10, and Hp were still significantly higher than those in the Con group (P < 0.001). In cows with mycotoxicosis, simultaneous stimulation of antagonistic processes was noted: a pro-inflammatory process in the upregulation of TNF-α and IL-6, and an anti-inflammatory one in the upregulation of IL-10.

Conclusion

Despite the absorbent’s use and the resolution of clinical symptoms in Exp cows, high levels of IL-10 and Hp and IL-6 were maintained. Assessment of the level of cytokines and APP appears to be a useful and precise tool for the evaluation and application of the appropriate dose of the mycotoxin absorbent or the evaluation of its effectiveness.

References

Ametaj B.N., Bradford B.J., Bobe G., Nafikov R.A., Lu Y., Young J.W., Beitz D.C.: Strong relationships between mediators of the acute phase response and fatty liver in dairy cows. Can J Anim Sci 2005, 85, 165–175, doi: 10.4141/A04-043.
Open DOI Search in Google Scholar Back to article
Antonissen G., Martel A., Pasmans F., Ducatelle R., Verbrugghe E., Vandenbroucke V., Li S., Haesebrouck F., Van Immerseel F., Croubels S.: The Impact of Fusarium Mycotoxins on Human and Animal Host Susceptibility to Infectious Diseases. Toxins 2014, 6, 430–452, doi: 10.3390/toxins6020430.
Open DOI Search in Google Scholar Back to article
Brodzki P., Brodzki A., Krakowski L., Dąbrowski R., Szczubiał M., Bochniarz M.: Levels of selected cytokines and acute-phase proteins in the serum of dairy cows with cystic ovarian disease and those in follicular and luteal phases of normal ovarian cycle. Res Vet Sci 2019, 123, 20–25, doi: 10.1016/j.rvsc.2018.12.007.
Open DOI Search in Google Scholar Back to article
Brodzki P., Kostro K., Brodzki A., Wawron W., Marczuk J., Kurek Ł.: Inflammatory cytokines and acute-phase proteins concentrations in the peripheral blood and uterus of cows that developed endometritis during early postpartum. Theriogenology 2015, 84, 11–18, doi: 10.1016/j.theriogenology.2015.02.006.
Open DOI Search in Google Scholar Back to article
Bryła M., Waśkiewicz A., Podolska G., Szymczyk K., Jędrzejczak R., Damaziak K., Sułek A.: Occurrence of 26 mycotoxins in the grain of cereals cultivated in Poland. Toxins 2016, 8, 160, doi: 10.3390/toxins8060160.
Open DOI Search in Google Scholar Back to article
Calabrese E.J.: Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 2005, 138, 378–411, doi: 10.1016/j.envpol.2004.10.001.
Open DOI Search in Google Scholar Back to article
Cheli F., Campagnoli A., Dell’Orto V.: Fungal populations and mycotoxins in silages: From occurrence to analysis. Anim Feed Sci Technol 2013, 183, 1–16, doi: 10.1016/j.anifeedsci. 2013.01.013.
Open DOI Search in Google Scholar Back to article
Devreese M., De Backer P., Croubels S.: Different methods to counteract mycotoxin production and its impact on animal health. Vlaams Diergeneeskd Tijdschr 2013, 82, 181–190, doi: 10.21825/vdt.v82i4.16695.
Open DOI Search in Google Scholar Back to article
Fink-Gremmels J.: The role of mycotoxins in the health and performance of dairy cows. Vet J 2008, 176, 84–92, doi: 10.1016/j.tvjl.2007.12.034.
Open DOI Search in Google Scholar Back to article
Frizzell C., Ndossi D., Verhaegen S., Dahl E., Eriksen G., Sřlie M., Ropstad E., Muller M., Elliott C.T., Connolly L.: Endocrine disrupting effects of zearalenone, alpha- and beta-zearalenol at the level of nuclear receptor binding and steroidogenesis. Toxicol Lett 2011, 206, 210–217, doi: 10.1016/j.toxlet.2011.07.015.
Open DOI Search in Google Scholar Back to article
Gajęcka M., Gajęcki M.T.: Could mycotoxins be inhibitory substances in milk? Innowacyjne Mleczarstwo 2014, 2, 22–29.
Search in Google Scholar Back to article
Gajęcka M., Otrocka-Domagała I.: Immunocyto-chemical expression of 3β- and 17β-hydroxysteroid dehydrogenase in bitch ovaries exposed to low doses of zearalenone. Pol J Vet Sci 2013, 16, 55–62.
Search in Google Scholar Back to article
Gajęcka M., Zielonka Ł., Dąbrowski M., Mróz M., Gajęcki M.T.: The effect of low doses of zearalenone and its metabolites on progesterone and 17β-estradiol concentrations in blood of pre-pubertal female Beagle dogs. Toxicon 2013, 76, 260–269, doi: 10.1016/j.toxicon.2013.08.060.
Open DOI Search in Google Scholar Back to article
Gajęcki M.T., Gajęcka M., Zielonka Ł.: The Presence of Mycotoxins in Feed and Their Influence on Animal Health. Toxins 2020, 12, 663, doi: 10.3390/toxins12100663.
Open DOI Search in Google Scholar Back to article
Gallo A., Minuti A., Bani P., Bertuzzi T., Piccioli Cappelli F., Doupovec B., Faas J., Schatzmayr D., Trevisi E.: A mycotoxin-deactivating feed additive counteracts the adverse effects of regular levels of Fusarium mycotoxins in dairy cows. J Dairy Sci 2020, 103, 11314–11331, doi: 10.3168/jds.2020-18197.
Open DOI Search in Google Scholar Back to article
Grenier B., Applegate T.J.: Modulation of Intestinal Functions Following Mycotoxin Ingestion: Meta-Analysis of Published Experiments in Animals. Toxins 2013, 5, 396-430, doi: 10.3390/toxins502039.
Open DOI Search in Google Scholar Back to article
Gromadzka K., Waskiewicz A., Chełkowski J., Goliński P.: Zearalenone and its metabolites: Occurrence, detection, toxicity and guidelines. World Mycotoxin J 2008, 1, 209–220, doi: 10.3920/WMJ2008.x015.
Open DOI Search in Google Scholar Back to article
Hoek A., Rutten V.P.M.G., Kool J., Arkesteijn G.J.A., Bouwstra R.J., Van Rhijn I., Koets A.: Subpopulations of bovine WC1+γδ T cells rather than CD4+CD25high Foxp3 T cells act as immune regulatory cells ex vivo. Vet Res 2009, 40, 6, doi: 10.1051/vetres:2008044.
Open DOI Search in Google Scholar Back to article
Hussein H.S., Brasel J.M.: Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 2001, 167, 101– 134, doi: 10.1016/S0300-483X(01)00471-1.
Open DOI Search in Google Scholar Back to article
Jovaisiene J., Bakutis B., Baliukoniene V., Gerulis G.: Fusarium and Aspergillus mycotoxins effects on dairy cow health, performance and the efficacy of anti-mycotoxin additive. Pol J Vet Sci 2016, 19, 79–87, doi: 10.1515/pjvs-2016-0011.
Open DOI Search in Google Scholar Back to article
Kim I.H., Kang H.G., Jeong J.K., Hur T.Y., Jung Y.H.: Inflammatory cytokine concentrations in uterine flush and serum samples from dairy cows with clinical or subclinical endometritis. Theriogenology 2014, 82, 427–432, doi: 10.1016/j.theriogenology.2014.04.022.
Open DOI Search in Google Scholar Back to article
Korosteleva S.N., Smith T.K., Boermans H.J.: Effects of feed naturally contaminated with Fusarium mycotoxins on metabolism and immunity of dairy cows. J. Dairy Sci 2009, 92, 1585–1593, doi: 10.3168/jds.2007-0162.
Open DOI Search in Google Scholar Back to article
Kushibiki S., Hodate K., Shingu H., Obara Y., Touno E., Shinoda M., Yokomizo Y.: Metabolic and lactational responses during recombinant bovine tumor necrosis factor-α treatment in lactating cows. J Dairy Sci 2003, 86, 819–827, doi: 10.3168/jds.S0022-0302(03)73664-9.
Open DOI Search in Google Scholar Back to article
Liao Y., Peng Z., Chen L., Nüssler A.K., Liu L., Yang W.: Deoxynivalenol, gut microbiota and immunotoxicity: A potential approach? Food Chem Toxicol 2018 Feb, 112, 342–354, doi: 10.1016/j.fct.2018.01.013.
Open DOI Search in Google Scholar Back to article
Loor J.J., Everts R.E., Bionaz M., Dann H.M., Morin D.E., Oliveira R., Rodriguez-Zas S.L., Drackley J.K., Lewin H.A.: Nutrition-induced ketosis alters metabolic and signaling gene networks in liver of periparturient dairy cows. Physiol Genomics 2007, 32, 105–116, doi: 10.1152/physiolgenomics.00188.2007.
Open DOI Search in Google Scholar Back to article
Macri A., Schollenberger M., Drochner W., Tafaj M., Morar M.V.: Investigation on the "In vitro" degradation of zearalenone in rumen fluid. Mycotoxin Research 2005, 21, 65– 67, doi: 10.1007/bf02954821.
Open DOI Search in Google Scholar Back to article
Marczuk J., Obremski K., Lutnicki K., Gajęcka M., Gajęcki M.: Zearalenone and deoxynivalenol mycotoxicosis in dairy cattle herds. Pol J Vet Sci 2012, 15, 365–372, doi: 10.2478/v10181-012-0055-x.
Open DOI Search in Google Scholar Back to article
Maresca M., Fantini J.: Some food-associated mycotoxins as potential risk factors in humans predisposed to chronic intestinal inflammatory diseases. Toxicon 2010, 56, 282–294, doi: 10.1016/j.toxicon.2010.04.016.
Open DOI Search in Google Scholar Back to article
Morgavi D., Boudra H., Jouany J., Graviou D.: Prevention of patulin toxicity on rumen microbial fermentation by SH-containing reducing agents. J Agric Food Chem 2003, 51, 6906– 6910, doi: 10.1021/jf034505v.
Open DOI Search in Google Scholar Back to article
Obremski K., Podlasz P., Żmigrodzka M., Winnicka A., Woźny M., Brzuzan P., Jakimiuk E., Wojtacha P., Gajęcka M., Zielonka Ł., Gajęcki M.: The effect of T-2 toxin on percentages of CD4+,CD8+, CD4+CD8+ and CD21+ lymphocytes, and mRNA expression levels of selected cytokines in porcine ileal Peyer’s patches. Pol J Vet Sci 2013, 16, 341–349, doi: 10.2478/pjvs-2013-0046.
Open DOI Search in Google Scholar Back to article
Ohtsuka H., Koiwa M., Hatsugaya A., Kudo K., Hoshi F., Itoh N., Yokota H., Okada H., Kawamura S.: Relationship between serum TNF activity and insulin resistance in dairy cows affected with naturally occurring fatty liver. J Vet Med Sci 2001, 63, 1021–1025, doi: 10.1292/jvms.15-0583.
Open DOI Search in Google Scholar Back to article
Park Y.H., Joo Y.S., Park J.Y., Moon J.S., Kim S.H., Kwon N.H., Ahn J.S., Davis W.C., Davies C.J.: Characterization of lymphocyte subpopulations and major histocompatibility complex haplotypes of mastitis-resistant and susceptible cows. J Vet Sci 2004, 5, 29–39.
Search in Google Scholar Back to article
Pestka J.J., Zhou H.R., Moon Y., Chung Y.J.: Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol Lett 2004, 153, 61–73, doi: 10.1016/j.toxlet.2004.04.023.
Open DOI Search in Google Scholar Back to article
Petersen H.H., Nielsen J.P., Heegaard P.M.H.: Application of acute phase protein measurements in veterinary clinical chemistry. Vet Res 2004, 35, 163–187, doi: 10.1051/vetres:2004002.
Open DOI Search in Google Scholar Back to article
Piotrowska M., Śliżewska K., Nowak A., Zielonka Ł., Żakowska Z., Gajęcka M., Gajęcki M.: The effect of experimental Fusarium mycotoxicosis on microbiota diversity in porcine ascending colon contents. Toxins 2014, 6, 2064-2081, doi: 10.3390/toxins6072064.
Open DOI Search in Google Scholar Back to article
Popa C., Netea M.G., van Riel P.L.C.M., van der Meer J.W.M., Stalenhoef A.F.H.: The role of TNF-α in chronic inflammatory conditions, intermediary metabolism, and cardiovascular risk. J Lipid Res 2007, 48, 751–762, doi: 10.1194/jlr.R600021-JLR200.
Open DOI Search in Google Scholar Back to article
Roche J.R., Friggens N.C., Kay J.K., Fisher M.W., Stafford K.J., Berry D.P.: Invited review: Body condition score and its association with dairy cow productivity, health, and welfare. J Dairy Sci 2009, 92, 5769–5801, doi: 10.3168/jds.2009-2431.
Open DOI Search in Google Scholar Back to article
Schatzmayr G., Zehner F., Schatzmayr D., Töaubel M., Binder E.M.: Microbiologicals for deactivating mycotoxins in contaminated feed. Mol Nutr Food Res 2006, 50, 543–551, doi: 10.1002/mnfr.200500181.
Open DOI Search in Google Scholar Back to article
Shafer-Weaver K.A., Sordillo L.M.: Bovine CD8+ suppressor lymphocytes alter immune responsiveness during the post-partum period. Vet Immunol Immunopath 1997, 56, 53–64, doi: 10.1016/S0165-2427(96)05725-X.
Open DOI Search in Google Scholar Back to article
Sheldon I.M., Cronin J.G., Bromfield J.J.: Tolerance and Innate Immunity Shape the Development of Postpartum Uterine Disease and the Impact of Endometritis in Dairy Cattle. Annu Rev Anim Biosci 2019, 7, 361–384, doi: 10.1146/annurev-animal-020518-115227.
Open DOI Search in Google Scholar Back to article
Tothova C.S., Nagy O., Seidel H., Kovac G.: Acute phase proteins in relation to various inflammatory diseases of calves. Comp Clin Pathol 2012, 21, 1037–1042, doi: 10.1007/s00580-011-1224-5.
Open DOI Search in Google Scholar Back to article
Trevisi E., Amadori M., Cogrossi S., Razzuoli E., Bertoni G.: Metabolic stress and inflammatory response in high-yielding, periparturient dairy cows. Res Vet Sci 2012, 93, 695–704, doi: 10.1016/j.rvsc.2011.11.008.
Open DOI Search in Google Scholar Back to article
Vekiru E., Fruhauf S., Sahin M., Ottner F., Schatzmayr G., Krska R.: Investigation of various adsorbents for their ability to bind aflatoxin B1. Mycotoxin Res 2007, 23, 27–33, doi: 10.1007/BF02946021.
Open DOI Search in Google Scholar Back to article
Wang Y., Chai T., Lu G., Quan C., Duan H., Yao M., Zucker B., Schlenker G.: Simultaneous detection of airborne Aflatoxin, Ochratoxin and Zearalenone in a poultry house by immunoaffinity clean-up and high-performance liquid chromatography. Environ Res 2008, 107, 139, doi: 10.1016/j.envres.2008.01.008.
Open DOI Search in Google Scholar Back to article
Winnicka A.: Wartości referencyjne podstawowych badań laboratoryjnych w weterynarii (Reference values for basic veterinarian laboratory assays – in Polish) Wydanie VII, Wydawnictwo SGGW, Warszawa, 2021.
Search in Google Scholar Back to article
Woźniak B., Minta M., Stypuła-Trębas S., Radko L., Żmudzki J.: Evaluation of estrogenic activity in animal diets using in vitro assay. Toxicol in Vitro 2014, 28, 70–75, doi: 10.1016/j.tiv.2013.10.005.
Open DOI Search in Google Scholar Back to article
Zachariasova M., Dzuman Z., Veprikova Z., Hajkova K., Jiru M., Vaclavikova M., Zachariasova A., Pospichalova M., Florian M., Hajslova J.: Occurrence of multiple mycotoxins in European feedingstuffs, assessment of dietary intake by farm animals. Anim Feed Sci Technol 2014, 193, 124–140, doi: 10.1016/j.anifeedsci.2014.02.007.
Open DOI Search in Google Scholar Back to article