Generic placeholder image

Current Drug Metabolism


ISSN (Print): 1389-2002
ISSN (Online): 1875-5453

Research Article

Effects of Montmorillonite on Growth Performance, Serum Biochemistry and Oxidative Stress of Red-Crowned Crane (Grus japonensis) Fed Mycotoxin-Contaminated Feed

Author(s): Dawei Liu, Qinghua Wu, Hongyi Liu, Changhu Lu, Chao Gu, Kamil Kuca* and Wenda Wu*

Volume 21, Issue 8, 2020

Page: [626 - 632] Pages: 7

DOI: 10.2174/1389200221666200726221126

Price: $65


Background: The red-crowned crane (Grus japonensis) is one of the most vulnerable bird species in the world. Mycotoxins are toxic secondary metabolites produced by fungi and considered naturally unavoidable contaminants in animal feed. Our recent survey indicated that the mycotoxins had the potential to contaminate redcrowned crane’s regular diets in China.

Objective: This experiment was conducted to investigate the protective effects of mycotoxin binder montmorillonite (Mont) on growth performance, serum biochemistry and oxidative stress parameters of the red-crowned crane.

Methods: 16 red-crowned cranes were divided into four groups and fed one of the following diets; a selected diet, regular diet, or the selected diet or regular diet with 0.5% montmorillonite added to the diets. The cranes' parameters of performance, hematology, serum biochemistry and serum oxidative stress were measured.

Results: Consuming regular diets decreased the average daily feed intake (ADFI), levels of haemoglobin (Hb), platelet count (PLT), superoxide dismutase (SOD), glutathione peroxidase (GSH-Px) and catalase (CAT), but increased the activities of aspartate aminotransferase (AST), alanine aminotransferase (ALT), creatine kinase (CK) and lactate dehydrogenase (LDH). The supplementation of 0.5% Mont provided protection for the red-crowned crane in terms of feed intake, serum biochemistry and oxidative stress. Moreover, Mont supplementation had no adverse effect on the health of red-crowned crane.

Conclusions: Taken together, these findings suggested that the addition of dietary Mont is effective in improving the health of red-crowned crane.

Keywords: Montmorillonite, red-crowned crane, mycotoxicosis, oxidative stress, growth performance, serum biochemistry, protective effect.

Graphical Abstract
IUCN (International Union for Conservation of Nature). IUCN Red List of Threatened Species.., 2014. Available at:;
Snyder, N.F.; Derrickson, S.R.; Beissinger, S.R.; Wiley, J.W.; Smith, T.B.; Toone, W.D.; Miller, B. Limitations of captive breeding in endangered species recovery. Conserv. Biol., 2002, 10, 338-348.
Liu, D.W.; Liu, H.Y.; Zhang, H.B.; Cao, M.C.; Sun, Y.; Wu, W.D.; Lu, C.H. Potential natural exposure of endangered red-crowned crane (Grus japonensis) to mycotoxins aflatoxin B1, deoxynivalenol, zearalenone, T-2 toxin, and ochratoxin A. J. Zhejiang Univ. Sci. B, 2016, 17(2), 158-168.
[] [PMID: 26834016]
Liu, D.W.; Zhou, Y.W.; Fei, Y.L.; Xie, C.P.; Liu, H.Y.; Lu, C.H.; Hou, S.L. A survey on the occurrence of mycotoxins in the feeds of captive red-crowned cranes (Grus japonensis) in some areas of China. J. Sichuan Agr. U., 2019, 37, 868-875.
Neme, K.; Mohammed, A. Mycotoxin occurrence in grains and the role of postharvest management as a mitigation strategies. A review. Food Control, 2017, 78, 412-425.
Wu, W.; Flannery, B.M.; Sugita-Konishi, Y.; Watanabe, M.; Zhang, H.; Pestka, J.J. Comparison of murine anorectic responses to the 8-ketotrichothecenes 3-acetyldeoxynivalenol, 15-acetyldeoxynivalenol, fusarenon X and nivalenol. Food Chem. Toxicol., 2012, 50(6), 2056-2061.
[] [PMID: 22465835]
Marin, S.; Ramos, A.J.; Cano-Sancho, G.; Sanchis, V. Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem. Toxicol., 2013, 60, 218-237.
[] [PMID: 23907020]
Smith, B.J.; Higgins, K.F.; Tucker, W.L. Precipitation, waterfowl densities and mycotoxins: their potential effect on avian cholera epizootics in the Nebraska rainwater basin area. Transactions of the North American Wildlife and Natural Resource Conference, 1990, pp. 269-282.
Windingstad, R.M.; Cole, R.J.; Nelson, P.E.; Roffe, T.J.; George, R.R.; Dorner, J.W. Fusarium mycotoxins from peanuts suspected as a cause of sandhill crane mortality. J. Wildl. Dis., 1989, 25(1), 38-46.
[] [PMID: 2915402]
Olsen, G.H.; Carpenter, J.W.; Gee, G.F.; Thomas, N.J.; Dein, F.J. Mycotoxin-induced disease in captive whooping cranes (Grus americana) and sandhill cranes (Grus canadensis). J. Zoo Wildl. Med., 1995, 26, 569-576.
Higgins, K.F.; Barta, R.M.; Neiger, R.D.; Rottinghaus, G.E.; Sterry, R.I. Mycotoxin occurrence in waste field corn and ingesta of wild geese in the northern Great Plains. Prairie Nat., 1992, 24, 31-37.
Moore, D.L.; Henke, S.E.; Fedynich, A.M.; Laurenz, J.C.; Morgan, R. Acute effects of aflatoxin on northern bobwhites (Colinus virginianus). J. Wildl. Dis., 2013, 49(3), 568-578.
[] [PMID: 23778606]
Huwig, A.; Freimund, S.; Käppeli, O.; Dutler, H. Mycotoxin detoxication of animal feed by different adsorbents. Toxicol. Lett., 2001, 122(2), 179-188.
[] [PMID: 11439224]
Zeng, L.; Wang, S.P. Adsorption of zearalenone by montmorillonite. Adv. Mat. Res., 2013, 683, 343-347.
Ahmed, O.S.; Dutta, D.K. Generation of metal nanoparticles on montmorillonite K10 and their characterization. Langmuir, 2003, 19, 5540-5541.
Bekci, Z.M.; Antep, M.K.; Merdivan, M.; Yurdakoç, K. Zearalenone removal in synthetic media and aqueous part of canned corn by montmorillonite K10 and pillared montmorillonite K10. J. Food Prot., 2011, 74(6), 954-959.
[] [PMID: 21669073]
Wang, J.P.; Chi, F.; Kim, I.H. Effects of montmorillonite clay on growth performance, nutrient digestibility, vulva size, faecal microflora, and oxidative stress in weaning gilts challenged with zearalenone. Anim. Feed Sci. Technol., 2012, 178, 158-166.
Yang, L.; Zhao, Z.; Deng, Y.; Zhou, Z.; Hou, J. Toxicity induced by F. poae-contaminated feed and the protective effect of Montmorillonite supplementation in broilers. Food Chem. Toxicol., 2014, 74, 120-130.
[] [PMID: 25296281]
Bhatti, S.A.; Khan, M.Z.; Saleemi, M.K.; Saqib, M.; Khan, A.; Ul-Hassan, Z. Protective role of bentonite against aflatoxin B1- and ochratoxin A-induced immunotoxicity in broilers. J. Immunotoxicol., 2017, 14(1), 66-76.
[] [PMID: 28094577]
National Feed Safety Standards of China. Tolerance limits for ochratoxin A and zearalenone in feeds, Hygienical standard for feeds. GB13078.2–2006. China’s Ministry of Health; China's General Administration of Quality Supervision, Inspection and Quarantine, 2006.
National Feed Safety Standards of China. Tolerance limits for deoxynivalenol in formula feed, Hygienicalstandard for feeds. GB13078; China's General Administration of Quality Supervision, Inspection and Quarantine, 2007.
National Feed Safety Standards of China. Hygienical standard for feeds. GB13078–2001. China’s Ministry of Health; China's General Administration of Quality Supervision, Inspection and Quarantine, 2011.
Pestka, J.J. Toxicological mechanisms and potential health effects of deoxynivalenol and nivalenol. World Mycotoxin J., 2010, 3, 323-347.
Wu, W.; Zhang, H. Role of tumor necrosis factor-α and interleukin-1β in anorexia induction following oral exposure to the trichothecene deoxynivalenol (vomitoxin) in the mouse. J. Toxicol. Sci., 2014, 39(6), 875-886.
[] [PMID: 25392278]
Flannery, B.M.; Clark, E.S.; Pestka, J.J. Anorexia induction by the trichothecene deoxynivalenol (vomitoxin) is mediated by the release of the gut satiety hormone peptide YY. Toxicol. Sci., 2012, 130(2), 289-297.
[] [PMID: 22903826]
Wu, W.; He, K.; Zhou, H.R.; Berthiller, F.; Adam, G.; Sugita-Konishi, Y.; Watanabe, M.; Krantis, A.; Durst, T.; Zhang, H.; Pestka, J.J. Effects of oral exposure to naturally-occurring and synthetic deoxynivalenol congeners on proinflammatory cytokine and chemokine mRNA expression in the mouse. Toxicol. Appl. Pharmacol., 2014, 278(2), 107-115.
[] [PMID: 24793808]
Wu, W.D.; Zhou, H.R.; He, K.; Pan, X.; Sugita-Konishi, Y.; Watanabe, M.; Zhang, H. Role of cholecystokinin in anorexia induction following oral exposure to the 8-ketotrichothecenes deoxynivalenol, 15-acetyldeoxynivalenol, 3-acetyldeoxynivalenol, fusarenon x, and nivalenol. Toxicol. Sci., 2014, 138, 278-289.
Plata-Salamán, C.R. Cytokines and anorexia: a brief overview. Semin. Oncol., 1998, 25(1)(Suppl. 1), 64-72.
[PMID: 9482542]
Ebenezer, I.S.; de la Riva, C.; Baldwin, B.A. Effects of the CCK receptor antagonist MK-329 on food intake in pigs. Physiol. Behav., 1990, 47(1), 145-148.
[] [PMID: 2326329]
Batterham, R.L.; Cowley, M.A.; Small, C.J.; Herzog, H.; Cohen, M.A.; Dakin, C.L.; Wren, A.M.; Brynes, A.E.; Low, M.J.; Ghatei, M.A.; Cone, R.D.; Bloom, S.R. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature, 2002, 418(6898), 650-654.
[] [PMID: 12167864]
Kelley, K.W.; Bluthé, R.M.; Dantzer, R.; Zhou, J.H.; Shen, W.H.; Johnson, R.W.; Broussard, S.R. Cytokine-induced sickness behavior. Brain Behav. Immun., 2003, 17(Suppl. 1), S112-S118.
[] [PMID: 12615196]
Saminathan, M.; Selamat, J.; Abbasi Pirouz, A.; Abdullah, N.; Zulkifli, I. Effects of nano-composite adsorbents on the growth performance, serum biochemistry, and organ weights of broilers fed with aflatoxin-contaminated feed. Toxins (Basel), 2018, 10(9)E345
[] [PMID: 30150553]
Dänicke, S.; Ueberschär, K.H.; Valenta, H.; Matthes, S.; Matthäus, K.; Halle, I. Effects of graded levels of fusarium-toxin-contaminated wheat in Pekin duck diets on performance, health and metabolism of deoxynivalenol and zearalenone. Br. Poult. Sci., 2004, 45(2), 264-272.
[] [PMID: 15222424]
Raju, M.V.; Devegowda, G. Influence of esterified-glucomannan on performance and organ morphology, serum biochemistry and haematology in broilers exposed to individual and combined mycotoxicosis (aflatoxin, ochratoxin and T-2 toxin). Br. Poult. Sci., 2000, 41(5), 640-650.
[] [PMID: 11201446]
Balogh, K.; Hausenblasz, J.; Weber, M.; Erdélyi, M.; Fodor, J.; Mézes, M. Effects of ochratoxin A on some production traits, lipid peroxide and glutathione redox status of weaned piglets. Acta Vet. Hung., 2007, 55(4), 463-470.
[] [PMID: 18277705]
Desheng, Q.; Fan, L.; Yanhu, Y.; Niya, Z. Adsorption of aflatoxin B1 on montmorillonite. Poult. Sci., 2005, 84(6), 959-961.
[] [PMID: 15971538]
Thrall, M.A. Veterinary hematology and clinical chemistry; Lippincott Williams & Wikins: Philadelphia, PA, 2004.
Yang, L.; Yang, W.; Feng, Q.; Huang, L.; Zhang, G.; Liu, F.; Jiang, S.; Yang, Z. Effects of purified zearalenone on selected immunological measurements of blood in post-weaning gilts. Anim Nutr, 2016, 2(3), 142-148.
[] [PMID: 29767104]
Abdel-Wahhab, M.A.; Nada, S.A.; Amra, H.A. Effect of aluminosilicates and bentonite on aflatoxin-induced developmental toxicity in rat. J. Appl. Toxicol., 1999, 19(3), 199-204.
[<199:AID-JAT558>3.0.CO;2-D] [PMID: 10362271]
Harvey, R.B.; Kubena, L.F.; Elissalde, M.H.; Corrier, D.E.; Phillips, T.D. Comparison of two hydrated sodium calcium aluminosilicate compounds to experimentally protect growing barrows from aflatoxicosis. J. Vet. Diagn. Invest., 1994, 6(1), 88-92.
[] [PMID: 8011787]
Van, V.J.F.; Ferrans, V.J. Etiologic factors and pathologic alterations in selenium-vitamin E deficiency and excess in animals and humans. Biol. Trace Elem. Res., 1992, 33, 1-21.
Cheng, Y.H.; Shen, T.F.; Pang, V.F.; Chen, B.J. Effects of aflatoxin and carotenoids on growth performance and immune response in mule ducklings. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2001, 128(1), 19-26.
[] [PMID: 11166670]
Chen, F.; Ma, Y.; Xue, C.; Ma, J.; Xie, Q.; Wang, G.; Bi, Y.; Cao, Y. The combination of deoxynivalenol and zearalenone at permitted feed concentrations causes serious physiological effects in young pigs. J. Vet. Sci., 2008, 9(1), 39-44.
[] [PMID: 18296887]
Giannini, E.G.; Testa, R.; Savarino, V. Liver enzyme alteration: a guide for clinicians. CMAJ, 2005, 172(3), 367-379.
[] [PMID: 15684121]
Andres, R.H.; Ducray, A.D.; Schlattner, U.; Wallimann, T.; Widmer, H.R. Functions and effects of creatine in the central nervous system. Brain Res. Bull., 2008, 76(4), 329-343.
[] [PMID: 18502307]
Jiang, S.Z.; Yang, Z.B.; Yang, W.R.; Gao, J.; Liu, F.X.; Chen, C.C.; Chi, F. Physiopathological effects of zeralenone in post-weaning female piglets with or without montmorillonite clay adsorbent. Livest. Sci., 2010, 131, 130-136.
Mary, V.S.; Theumer, M.G.; Arias, S.L.; Rubinstein, H.R. Reactive oxygen species sources and biomolecular oxidative damage induced by aflatoxin B1 and fumonisin B1 in rat spleen mononuclear cells. Toxicology, 2012, 302(2-3), 299-307.
[] [PMID: 22981896]
Ermak, G.; Davies, K.J. Calcium and oxidative stress: from cell signaling to cell death. Mol. Immunol., 2002, 38(10), 713-721.
[] [PMID: 11841831]
Sies, H. Glutathione and its role in cellular functions. Free Radic. Biol. Med., 1999, 27(9-10), 916-921.
[] [PMID: 10569624]
Dvorska, J.E.; Pappas, A.C.; Karadas, F.; Speake, B.K.; Surai, P.F. Protective effect of modified glucomannans and organic selenium against antioxidant depletion in the chicken liver due to T-2 toxin-contaminated feed consumption. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2007, 145(4), 582-587.
[] [PMID: 17350343]
Jiang, S.Z.; Yang, Z.B.; Yang, W.R.; Gao, J.; Liu, F.X.; Broomhead, J.; Chi, F. Effects of purified zearalenone on growth performance, organ size, serum metabolites, and oxidative stress in postweaning gilts. J. Anim. Sci., 2011, 89(10), 3008-3015.
[] [PMID: 21531849]

Rights & Permissions Print Export Cite as
© 2023 Bentham Science Publishers | Privacy Policy