Skip to main content
Log in

An Evaluation of the Supplementation of Dietary-Modified Palygorskite on Growth Performance, Zearalenone Residue, Serum Metabolites, and Antioxidant Capacities in Broilers Fed a Zearalenone-Contaminated Diet

  • Published:
Clays and Clay Minerals

Abstract

–Zearalenone (ZEA), a common contaminant in food and feedstuffs, threatens human and animal health. The present study aimed to investigate the protective effects of modified palygorskite (MPal), a ZEA-targeted adsorbent, on broilers (young chickens) fed a ZEA-contaminated diet. Broilers were subjected to one of three treatments for a period of 42 days: a basal diet (control group), a ZEA- contaminated diet, and a ZEA-contaminated diet supplemented with 1 g/kg of MPal. Blood was collected for serum metabolite assay, and liver and kidney were sampled to determine ZEA residue and antioxidant- related parameters, using commercial spectrophotometric kits. Compared with the basal diet, the ZEA- contaminated diet resulted in compromised growth performance (reduced daily gain and feed intake during finisher period), disordered relative liver weight (decreased at 21 days but increased at 42 days), increased ZEA residue in liver and kidney, abnormal serum metabolites (decreased total protein content but increased alanine aminotransferase activity at 21 and 42 days, reduced albumin content at 21 days, and elevated aspartate aminotransferase activity at 42 days), and disrupted antioxidant capacities of broilers (increased total superoxide dismutase (T-SOD) activity in liver at 21 and 42 days, decreased T-SOD activity in kidney at 21 and 42 days, and in serum at 42 days, greater malondialdehyde accumulation in liver and kidney at 42 days, and lower glutathione content in kidney at 21 days). The adverse consequences resulting from the ZEA-contaminated diet were relieved by the supplementation of MPal (except albumin concentration in serum and T-SOD activity in liver at 21 days), with the values of growth-performance parameters, liver weight, renal ZEA accumulation, total protein content, transaminase activity at 42 days, and antioxidant indexes being similar to those in the control group. These results suggested that MPal supplementation could promote growth performance, attenuate liver damage, and improve the antioxidant abilities of broilers fed ZEA-contaminated diet by reducing ZEA accumulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbès, S., Ouanes, Z., Salah-Abbès, J.B., Houas, Z., Oueslati, R., Bacha, H., and Othman, O. (2006) The protective effect of hydrated sodium calcium aluminosilicate against haematological, biochemical and pathological changes induced by Zearalenone in mice. Toxicon, 47, 567–574.

    Article  Google Scholar 

  • Abidessefi, S., Ouanes, Z., Hassen, W., Baudrimont, I., Creppy, E., and Bacha, H. (2004) Cytotoxicity, inhibition of DNA and protein syntheses and oxidative damage in cultured cells exposed to zearalenone. Toxicology in Vitro, 18, 467–474.

    Article  Google Scholar 

  • Allen, N.K., Mirocha, C.J., Aakhus-Allen, S., Bitgood, J.J., Weaver, G., and Bates, F. (1981a) Effect of dietary zearalenone on reproduction of chickens. Poultry Science, 60, 1165–1174.

    Article  Google Scholar 

  • Allen, N.K., Mirocha, C.J., Weaver, G., Aakhusallen, S., and Bates, F. (1981b) Effects of dietary zearalenone on finishing broiler chickens and young turkey poults. Poultry Science, 60, 124–131.

    Article  Google Scholar 

  • Allen, N.K., Peguri, A., Mirocha, C.J., and Newman, J.A. (1983) Effects of fusarium cultures, T-2 toxin, and zearalenone on reproduction of turkey females. Poultry Science, 62, 282–289.

    Article  Google Scholar 

  • AQSIQ (2017) GB/T 13078-2017. Hygienical Standard for Feeds. General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China.

    Google Scholar 

  • Aravind, K.L., Patil, V.S., Devegowda, G.B., Umakantha, B., and Ganpule, S.P. (2003) Efficacy of esterified glucomannan to counteract mycotoxicosis in naturally contaminated feed on performance and serum biochemical and hematological parameters in broilers. Poultry Science, 82, 571–576.

    Article  Google Scholar 

  • Ben, S.I., Boussabbeh, M., Helali, S., Abid-Essefi, S., and Bacha, H. (2015) Protective effect of Crocin against zearalenone-induced oxidative stress in liver and kidney of Balb/c mice. Environmental Science and Pollution Research, 22, 19069–19076.

    Article  Google Scholar 

  • Bergaya, F. and Lagaly, G., editors (2013) Handbook of Clay Science. 2nd edition. Developments in Clay Science, 5. Elsevier, Amsterdam.

    Google Scholar 

  • Binder, E.M., Tan, L.M., Chin, L.J., Handl, J., and Richard, J. (2007) Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Animal Feed Science and Technology, 137, 265–282.

    Article  Google Scholar 

  • Bočarovstančić, A., Adamovic, M., Salma, N., Bodrozasolarov, M., Vučković, J., and Pantić, V. (2011) In vitro efficacy of mycotoxins’ adsorption by natural mineral adsorbents. Biotechnology in Animal Husbandry, 27, 1241–1251.

    Article  Google Scholar 

  • Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  Google Scholar 

  • Buranatragool, K., Poapolathep, S., Isariyodom, S., Imsilp, K., Klangkaew, N., and Poapolathep, A. (2015) Dispositions and tissue residue of zearalenone and its metabolites α-zearalenol and β-zearalenol in broilers. Toxicology Reports, 2, 351–356.

    Article  Google Scholar 

  • Cavret, S. and Lecoeur, S. (2006) Fusariotoxin transfer in animal. Food and Chemistry Toxicology, 44, 444–453.

    Article  Google Scholar 

  • Chalvatzi, S., Arsenos, G., Tserveni-Goussi, A., and Fortomaris, P. (2014) Tolerance and efficacy study of palygorskite incorporation in the diet of laying hens. Applied Clay Science, 101, 643–647.

    Article  Google Scholar 

  • Che, Z., Liu, Y., Wang, H., Zhu, H., Hou, Y., and Ding, B. (2011) The protective effects of different mycotoxin adsorbents against blood and liver pathological changes induced by mold-contaminated feed in broilers. Asian-Australasian Journal of Animal Science, 24, 250–257.

    Article  Google Scholar 

  • Chowdhury, S.R. and Smith, T.K. (2007) Effects of feed-borne Fusarium mycotoxins on performance, plasma chemistry and hepatic fractional protein synthesis rates of turkeys. Canadian Journal of Animal Science, 87, 543–551.

    Article  Google Scholar 

  • Čonkovaá, E., Laciakovaá A., Paástorovaá B., Seidel H., and Kovaác G. (2001) The effect of zearalenone on some enzymatic parameters in rabbits. Toxicology Letters, 121, 145–149.

    Article  Google Scholar 

  • Daković, A., Matijašević, S., Rottinghaus, G.E., Dondur, V., Pietrass, T., and Clewett, C.F. (2007) Adsorption of zearalenone by organomodified natural zeolitic tuff, Jounal of Colloid and Interface Science, 311, 8–13.

    Article  Google Scholar 

  • Daković, A., Matijasevic, S., Rottinghaus, G.E., Ledoux, D.R., Butkeraitis, P., and Sekulic, Z. (2008) Aflatoxin B1 adsorption by natural and copper modified montmorillonite. Colloids and Surfaces B: Biointerfaces, 66, 20–25.

    Article  Google Scholar 

  • Daković, A., Kragović, M., Rottinghaus, G.E., Ledoux, D.R., Butkeraitis, P., Vojislavljević, D.Z., Zarić, S.D., and Stamenić, L. (2012) Preparation and characterization of zinc-exchanged montmorillonite and its effectiveness as aflatoxin B1 adsorbent. Materials Chemistry and Physics, 137, 213–220.

    Article  Google Scholar 

  • Daänicke, S., Ueberschaär, K.H., Halle, I., Matthes, S., Valenta, H., and Flachowsky, G. (2002) Effect of addition of a detoxifying agent to laying hen diets containing uncontaminated or Fusarium toxin-contaminated maize on performance of hens and on carryover of zearalenone. Poultry Science, 81, 1671–1680.

    Article  Google Scholar 

  • Daänicke, S., Matthes, S., Halle, I., Ueberschaär, K.H., Döll, S., and Valenta, H. (2003) Effects of graded levels of Fusarium toxin-contaminated wheat and of a detoxifying agent in broiler diets on performance, nutrient digestibility and blood chemical parameters. British Poultry Science, 44, 113–126.

    Article  Google Scholar 

  • Denli, M., Blandon, J.C., Salado, S., Guynot, M.E., and Pérez, J.F. (2017) Effect of dietary zearalenone on the performance, reproduction tract and serum biochemistry in young rats. Journal of Applied Animal Research, 45, 619–622.

    Article  Google Scholar 

  • D’Mello, J.P.F., Placinta, C.M., and Macdonald, A.M.C. (1999) Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Animal Feed Science and Technology, 80, 183–205.

    Article  Google Scholar 

  • Feng, J., Shan, M., Du, H., Han, X., and Xu, Z. (2008) In vitro adsorption of zearalenone by cetyltrimethyl ammonium bromide-modified montmorillonite nanocomposites. Microporous and Mesoporous Materials, 113, 99–105.

    Article  Google Scholar 

  • Ferrer, E., Juan-García, A., Font, G., and Ruiz, M. (2009) Reactive oxygen species induced by beauvericin, patulin and zearalenone in CHO-K1 cells. Toxicology in Vitro, 23, 1504–1509.

    Article  Google Scholar 

  • Girish, C.K., Smith, T.K., Boermans, H.J., and Karrow, N.A. (2005) Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on performance, hematology, metabolism, and immunocompetence of turkeys. Poultry Science, 84, 1179–1185.

    Article  Google Scholar 

  • Glenn, A.E. (2007) Mycotoxigenic Fusarium species in animal feed. Animal Feed Science and Technology, 137, 213–240.

    Article  Google Scholar 

  • Hassen, W., Ayed-Boussema, I., Oscoz, A.A., Lopez, A.C., and Bacha, H. (2007) The role of oxidative stress in zearale-none-mediated toxicity in Hep G2 cells: Oxidative DNA damage, gluthatione depletion and stress proteins induction. Toxicology, 232, 294–302.

    Article  Google Scholar 

  • Hestbjerg, H., Nielsen, K.F., Thrane, U., and Elmholt, S. (2002) Production of trichothecenes and other secondary metabolites by Fusarium culmorum and Fusarium equiseti on common laboratory media and a soil organic matter agar: an ecological interpretation. Journal of Agricultural and Food Chemistry, 50, 7593–7599.

    Article  Google Scholar 

  • Homolka, J. (1969) Clinic Biochemistry. Publishing House SZN, Prague, Czech Republic.

    Google Scholar 

  • Jia, Z., Liu, M., Qu, Z., Zhang, Y., Yin, S., and Shan, A. (2014) Toxic effects of zearalenone on oxidative stress, inflammatory cytokines, biochemical and pathological changes induced by this toxin in the kidney of pregnant rats. Environmental Toxicology and Pharmacology, 37, 580–591.

    Article  Google Scholar 

  • Jiang, S.Z., Yang, Z.B., Yang, W.R., Yao, B.Q., Zhao, H., Liu, F.X., Chen, C.C., and Chi, F. (2010) Effects of feeding purified zearalenone contaminated diets with or without clay enterosorbent on growth, nutrient availability, and genital organs in post-weaning female pigs. Asian-Australasian Journal of Animal Science, 23, 74–81.

    Article  Google Scholar 

  • Jiang, S.Z., Yang, Z.B., Yang, W.R., Gao, J., Liu, F.X., Broomhead, J., and Chi, F. (2011) Effects of purified zearalenone on growth performance, organ size, serum metabolites, and oxidative stress in postweaning gilts. Journal of Animal Science, 89, 3008–3015.

    Article  Google Scholar 

  • Jiang, S.Z., Yang, Z.B., Yang, W.R., Wang, S.J., Wang, Y., Broomhead, J., Johnston, S. L., and Chi, F. (2012) Effect on hepatonephric organs, serum metabolites and oxidative stress in post-weaning piglets fed purified zearalenone-contaminated diets with or without Calibrin-Z. Journal of Animal Physiology and Animal Nutrition, 96, 1147–1156.

    Article  Google Scholar 

  • Jiang, S.Z., Li, Z., Wang, G.Y., Yang, Z.B., Yang, W.R., Zhang, G.G., and Wu, Y.B. (2014) Effects of Fusarium mycotoxins with yeast cell wall absorbent on hematology, serum biochemistry, and oxidative stress in broiler chickens. Journal of Applied Poultry Research, 23, 165–173.

    Article  Google Scholar 

  • Koraichi, F., Videmann, B., Mazallon, M., Benahmed, M., Prouillac, C., and Lecoeur, S. (2012) Zearalenone exposure modulates the expression of ABC transporters and nuclear receptors in pregnant rats and fetal liver. Toxicology Letters, 211, 246–256.

    Article  Google Scholar 

  • Kouadio, J.H., Mobio, T.A., Baudrimont, I., Moukha, S., Dano, S.D., and Creppy, E.E. (2005) Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology, 213, 56–65.

    Article  Google Scholar 

  • Kramer, R.A., Zakher, J., and Kim, G. (1988) Role of the glutathione redox cycle in acquired and de novo multidrug resistance. Science, 241, 694–697.

    Article  Google Scholar 

  • Lemke, S.L., Mayura, K., Reeves, W.R., Wang, N., Fickey, C., and Phillips, T.D. (2001) Investigation of organophilic montmorillonite clay inclusion in zearalenone-contaminated diets using the mouse uterine weight bioassay. Journal of Toxicology and Environmental Health, Part A, 62, 243–258.

    Article  Google Scholar 

  • Li, Z., Yang, Z.B., Yang, W.R., Wang, S.J., Jiang, S.Z., and Wu, Y.B. (2012) Effects of feed-borne Fusarium mycotoxins with or without yeast cell wall adsorbent on organ weight, serum biochemistry, and immunological parameters of broiler chickens. Poultry Science, 91, 2487–2495.

    Article  Google Scholar 

  • Liu, M., Gao, R., Meng, Q., Zhang, Y., Bi, C., and Shan, A. (2014) Toxic effects of maternal zearalenone exposure on intestinal oxidative stress, barrier function, immunological and morphological changes in rats. PLoS One, 9, e106412.

  • Malekinejad, H., Maas-Bakker, R., and Fink-Gremmels, J. (2006) Species differences in the hepatic biotransformation of zearalenone. The Veterinary Journal, 172, 96–102.

    Article  Google Scholar 

  • Marin, D.E., Pistol, G.C., Neagoe, I.V., Calin, L., and Taranu, I. (2013) Effects of zearalenone on oxidative stress and inflammation in weanling piglets. Food and Chemical Toxicology, 58, 408–415.

    Article  Google Scholar 

  • Meister, A. (1994) Glutathione-ascorbic acid antioxidant system in animals. Journal of Biological Chemistry, 269, 9397–9400.

    Google Scholar 

  • Mirocha, C.J., Robison, T.S., Pawlosky, R.J., and Allen, N.K. (1982) Distribution and residue determination of [3H] zearalenone in broilers. Toxicology and Applied Pharmacology, 66, 77–87.

    Article  Google Scholar 

  • Nesic, K., Pupavac S., and Sinovec, Z.J. (2005) Efficacy of different adsorbents in alleviating zearalenone effects on performance of pigs. Zbornik Matice Srpske Za Prirodne Nauke, 108, 173–179.

    Article  Google Scholar 

  • NRC (1994) Nutrient Requirements of Poultry. 9th edition. National Academy Press, Washington, DC.

    Google Scholar 

  • Othmen, O.B., Golli, E.E., Abid-Essefi, S., and Bacha, H. (2008) Cytotoxicity effects induced by Zearalenone meta-bolites, alpha Zearalenol and beta Zearalenol, on cultured Vero cells. Toxicology, 252, 72–77.

    Article  Google Scholar 

  • Ouanes, Z., Abid, S., Ayed, I., Anane, R., Mobio, T., Creppy, E.E., and Bacha, H. (2003) Induction of micronuclei by Zearalenone in Vero monkey kidney cells and in bone marrow cells of mice: protective effect of Vitamin E. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 538, 63–70.

    Article  Google Scholar 

  • Schell, T., Lindemann, M., Kornegay, E., Blodgett, D., and Doerr, J. (1993) Effectiveness of different types of clay for reducing the detrimental effects of aflatoxin-contaminated diets on performance and serum profiles of weanling pigs. Journal of Animal Science, 71, 1226–1231.

    Article  Google Scholar 

  • Seong, H., Whang, H.S., and Ko, S. (2000) Synthesis of a quaternary ammonium derivative of chito-oligosaccharide as antimicrobial agent for cellulosic fibers. Journal of Applied Polymer Science, 76, 2009–2015.

    Article  Google Scholar 

  • Sies, H. (1991) Oxidative stress: from basic research to clinical application. American Journal of Medicine, 91, 31S–38S.

    Article  Google Scholar 

  • Šperanda, M., Liker, B., Šperanda, T., Šerić, V., Antunović, Z., Grabarević, Ž., and Steiner, Z. (2006) Haematological and biochemical parameters of weaned piglets fed on fodder mixture contaminated by zearalenone with addition of clinoptilolite. Acta Veterinaria, 6, 121–136.

    Google Scholar 

  • Swamy, H., Smith, T., Cotter, P., Boermans, H., and Sefton, A. (2002a) Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on production and metabolism in broilers. Poultry Science, 81, 966–975.

    Article  Google Scholar 

  • Swamy, H.V., Smith, T.K., MacDonald, E.J., Boermans, H.J., and Squires, E.J. (2002b) Effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on swine performance, brain regional neurochemistry, and serum chemistry and the efficacy of a polymeric glucomannan mycotoxin adsorbent. Journal of Animal Science, 80, 3257–3267.

    Article  Google Scholar 

  • Tian, G., Wang, W., Mu, B., Kang, Y., and Wang, A. (2015) Facile fabrication of carbon/attapulgite composite for bleaching of palm oil. Journal of the Taiwan Institute of Chemical Engineers, 50, 252–258.

    Article  Google Scholar 

  • Trailović, J.N., Stefanović, S., and Trailović, S.M. (2013) In vitro and in vivo protective effects of three mycotoxin adsorbents against ochratoxin a in broiler chickens. British Poultry Science, 54, 515.

    Article  Google Scholar 

  • Turcotte, J.C., Hunt, P.J.B., and Blaustein, J.D. (2005) Estrogenic effects of zearalenone on the expression of progestin receptors and sexual behavior in female rats. Hormones and Behavior, 47, 178–184.

    Article  Google Scholar 

  • Vaca, C.E., Wilhelm, J., and Harmsringdahl, M. (1988) Interaction of lipid peroxidation products with DNA: A review. Mutation Research/Reviews in Genetic Toxicology, 195, 137–149.

    Article  Google Scholar 

  • Wang, D.F., Zhang, N.Y., Peng, Y.Z., and Qi, D.S. (2010) Interaction of zearalenone and soybean isoflavone on the development of reproductive organs, reproductive hormones and estrogen receptor expression in prepubertal gilts. Animal Reproduction Science, 122, 317–323.

    Article  Google Scholar 

  • Wang, D.F., Zhang, N.Y., Peng, Y.Z., and Qi, D.S. (2012) Interaction of zearalenone and soybean isoflavone in diets on the growth performance, organ development and serum parameters in prepubertal gilts. Journal of Animal Physiology and Animal Nutrition, 96, 939–946.

    Article  Google Scholar 

  • Wang, D.F., Zhou, H.L., Hou, G.Y., Qi, D.S., and Zhang, N.Y. (2013) Soybean isoflavone reduces the residue of zearalenone in the muscle and liver of prepubertal gilts. Animal, 7, 699–703.

    Article  Google Scholar 

  • Wang, W., Tian, G., Zhang, Z., and Wang, A. (2015) A simple hydrothermal approach to modify palygorskite for high-efficient adsorption of Methylene blue and Cu(II) ations. Chemical Engineering Journal, 265, 228–238.

    Article  Google Scholar 

  • Yegani, M., Smith, T.K., Leeson, S., and Boermans, H.J. (2006) Effects of feeding grains naturally contaminated with Fusarium mycotoxins on performance and metabolism of broiler breeders. Poultry Science, 85, 1541.

    Article  Google Scholar 

  • Yiannikouris, A., Kettunen, H, Apajalahti, J., Pennala, E., and Moran, C.A. (2013) Comparison of the sequestering properties of yeast cell wall extract and hydrated sodium calcium aluminosilicate in three in vitro models accounting for the animal physiological bioavailability of zearalenone. Food Additives and Contaminants Part A: Chemistry Analysis Control Exposure and Risk Assessment, 30, 1641–1650.

    Article  Google Scholar 

  • Zelko, I.N., Mariani, T.J., and Folz, R.J. (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radical Biology and Medicine, 33, 337–349.

    Article  Google Scholar 

  • Zhang, L., Yan, R., Zhang, R., Wen, C., and Zhou, Y. (2017) Effect of different levels of palygorskite inclusion on pellet quality, growth performance and nutrient utilization in broilers. Animal Feed Science and Technology, 223, 73–81.

    Article  Google Scholar 

  • Zinedine, A., Soriano, J.M., Moltó, J.C., and Mañes, J. (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food and Chemical Toxicology, 45, 1–18.

    Article  Google Scholar 

  • Zourgui, L., Golli, E.E., Bouaziz, C., Bacha, H., and Hassen, W. (2008) Cactus (Opuntia ficus-indica) cladodes prevent oxidative damage induced by the mycotoxin zearalenone in Balb/C mice. Food and Chemical Toxicology, 46, 1817–1824.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yanmin Zhou.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Q., Chen, Y., Cheng, Y. et al. An Evaluation of the Supplementation of Dietary-Modified Palygorskite on Growth Performance, Zearalenone Residue, Serum Metabolites, and Antioxidant Capacities in Broilers Fed a Zearalenone-Contaminated Diet. Clays Clay Miner. 66, 474–484 (2018). https://doi.org/10.1346/CCMN.2018.064113

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1346/CCMN.2018.064113

Key Words

Navigation