Toxicity of high uranium doses in broilers and protection with mineral adsorbents

  • Branislava MitrovićEmail author
  • Mirjana Stojanović
  • Živko Sekulić
  • Velibor Andrić
  • Mihajlo Vićentijević
  • Borjana Vranješ
Original Article


The aim of this study was to determine the uranium distribution and histopathological changes in broiler organs (kidney, liver, and brain) and muscle after 7 days of contamination with high doses of uranyl nitrate hexahydrate (UN), and the protective efficiency of three different mineral adsorbents (organobentonite, organozeolite, and sepiolite). During the 7 days, the UN administration was 50 mg per day, and administration of adsorbents was 2 g per day immediately after UN. In control group where broilers received only UN, histopathological changes such as necrosis of intestinal villi, oedema, vacuolisation and abruption of epithelial cells in renal tubules, oedema and vacuolisation of the cytoplasm of hepatocytes, and dystrophic changes in the neurons of the medulla oblongata were observed. In contrast, when the adsorbents organobentonite, organozeolite, and sepiolite were administered, no histopathological changes were observed in liver and brain. The investigated adsorbents showed the highest protective effects in liver (80–92%), compared to the kidney (77–86%), brain (37–64%), and meat (31–63%).


Uranyl nitrate Broilers Toxicity Histopathological changes Adsorbents 



This paper was part of the projects “Development of technology and products based on mineral raw materials and biomass for protecting the food resources” (No. TR31003) and “Development of technological processes for obtaining of ecological materials based on non-metallic minerals” (No. TR034013) financed by the Ministry of Education, Science and Technological Development of the Republic of Serbia (2011–2019).

Compliance with ethical standards

Conflict of interest

Al authors declare that they have no conflict of interest.


  1. ATSDR (2013) Toxicological profile for Uranium. U.S. Department of Health and Human Services, Washington DCGoogle Scholar
  2. Ayed MH, Zghal I, Rekik B (2011) Effect of sepiolite supplementation on broiler growth performance and carcass yield. Res Opin Anim Vet Sci 1:375–378Google Scholar
  3. Bolt AM, Medina S, Lauer FT, Xu H, Ali AM, Liu KJ, Burchiel SW (2018) Minimal uranium accumulation in lymphoid tissues following an oral 60-day uranyl acetate exposure in male and female C57BL/6 J mice. PLoS One 13:e0205211CrossRefGoogle Scholar
  4. Carraro A, De Giacomo A, Giannossi ML, Medici L, Muscarella M, Palazzo L, Quaranta V, Summa V, Tateo F (2014) Clay minerals as adsorbents of aflatoxin M1 from contaminated milk and effects on milk quality. Appl Clay Sci 88–89:92–99CrossRefGoogle Scholar
  5. Chkuaseli A, Khutsishvili-Maisuradze M, Chagelishvili A, Natsvaladze K, Lashkarashvili T, Chagelishvili G, Maisuradze N (2016) Application of new mycotoxin adsorbent-bentonite clay “Askangel” in poultry feed. Ann Agrar Sci 14:295–298CrossRefGoogle Scholar
  6. Di Gregorio MC, De Neeff DV, Jager AV, Corassin CH, Carão ÁCDP, De Albuquerque R, De Azevedo AC, Oliveira CAF (2014) Mineral adsorbents for prevention of mycotoxins in animal feeds. Toxin Rev 33:125–135CrossRefGoogle Scholar
  7. Diamond GL, Morrow PE, Panner BJ, Gelein RM, Baggs RB (1989) Reversible uranyl fluoride nephrotoxicity in the Long Evans rat. Fundam Appl Toxicol 13:65–78CrossRefGoogle Scholar
  8. Dublineau I, Grison S, Baudelin C, Dudoignon N, Souidi M, Marquette C, Paquet F, Aigueperse J, Gourmelon P (2005) Absorption of uranium through the entire gastrointestinal tract of the rat. Int J Radiat Biol 81:473–482CrossRefGoogle Scholar
  9. Dublineau I, Souidi M, Gueguen Y, Lestaevel P, Bertho JM, Manens L, Delissen O, Grison S, Paulard A, Monin A, Kern Y, Rouas C, Loyen J, Gourmelon P, Aigueperse J (2014) unexpected lack of deleterious effects of uranium on physiological systems following a chronic oral intake in adult rat. Biomed Res Int 2014:1–24CrossRefGoogle Scholar
  10. EFSA (2010) Scientific opinion on the safety and efficacy of bentonite as a technological feed additive for all species. EFSA J 10:2787Google Scholar
  11. Fesenko S, Isamov N, Howard BJ, Voigt G, Beresford NA, Sanzharova N (2007) Review of Russian language studies on radionuclide behavior in agricultural animals: part 1. Gut absorption. J Environ Radioact 98:85–103CrossRefGoogle Scholar
  12. Fesenko S, Isamov N, Howard BJ, Sanzharova N, Wells C (2018) Review of Russian language studies on radionuclide behaviour in agricultural animals: transfer to animal tissues. J Environ Radioact 192:233–249CrossRefGoogle Scholar
  13. Fitsanakis VA, Erikson KM, Garcia SJ, Evje L, Syversen T, Aschner M (2006) Brain accumulation of depleted uranium in rats following 3- or 6-month treatment with implanted depleted uranium pellets. Biol Trace Elem Res 111:185–197CrossRefGoogle Scholar
  14. Ghosh S, Kumar A, Pandey BN, Mishra KP (2007) Acute exposure of uranyl nitrate causes lipid peroxidation and histopathological damage in brain and bone of Wistar rat. J Environ Pathol Toxicol Oncol 26:255–261CrossRefGoogle Scholar
  15. Gilman AP, Villeneuve DC, Secours VE, Yagminas AP, Tracy BL, Quinn JM, Valli VE, Moss MA (1998a) Uranyl nitrate: 91-day toxicity studies in the New Zealand white rabbit. Toxicol Sci 41:129–137CrossRefGoogle Scholar
  16. Gilman AP, Villeneuve DC, Secours VE, Yagminas AP, Tracy BL, Quinn JM, Valli VE, Willes RJ, Moss MA (1998b) Uranyl nitrate: 28-day and 91-day toxicity studies in the Sprague-Dawley rat. Toxicol Sci 41:117–128Google Scholar
  17. Gupta R (2015) Handbook of toxicology of chemical warfare agents. Elsevier, AmsterdamGoogle Scholar
  18. Houpert P, Lestaevel P, Bussy C, Paquet F, Gourmelon P (2005) Enriched but not depleted uranium affects central nervous system in long-term exposed rat. Neurotoxicology 26:1015–1020CrossRefGoogle Scholar
  19. Houpert P, Frelon S, Monleau M, Bussy C, Chazel V, Paquet F (2007) Heterogeneous accumulation of uranium in the brain of rats. Radiat Prot Dosim 127:86–89CrossRefGoogle Scholar
  20. Howard BJ, Beresford NA, Voigt G (2001) Countermeasures for animal products: a review of effectiveness and potential usefulness after an accident. J Environ Radioact 56:115–137CrossRefGoogle Scholar
  21. IAEA (2010) Handbook of parameter values for the prediction of radionuclide transfer in terrestrial and freshwater environments. Technical reports series No 472, ViennaGoogle Scholar
  22. ICRP (1995) Age-dependent doses to the members of the public from Intake of Radionuclides—part 5 compilation of ingestion and inhalation coefficients. ICRP Publication. Annals of the ICRP, vol 72. Pergamon Press, OxfordGoogle Scholar
  23. ICRP (1996) International Commission for Radiation Protection. Age-dependent doses to members of the public from Intake of Radionuclides: Part 4. Inhalation dose coefficients. Publication. Annals of the ICRP, vol 72. Pergamon Press, OxfordGoogle Scholar
  24. Konietzka R (2015) Gastrointestinal absorption of uranium compounds—a review. Regul Toxicol Pharmacol 71:125–133CrossRefGoogle Scholar
  25. La Touche YD, Willis DL, Dawydiak OI (1987) Absorption and biokinetics of U in rats following an oral administration of uranyl nitrate solution. Health Phys 53:147–162CrossRefGoogle Scholar
  26. Leggett RW, Harrison JD (1995) Fractional absorption of ingested uranium in humans. Health Phys 68:484–498CrossRefGoogle Scholar
  27. Leggett RW, Pellmar TC (2003) The biokinetics of uranium migrating from embedded DU fragments. J Environ Radioact 64:205–225CrossRefGoogle Scholar
  28. Macháček M, Večerek V, Mas N, Suchý P, Straková E, Šerman V, Herzig I (2010) Effect of the feed additive clinoptilolite (zeofeed) on nutrient metabolism and production performance of laying hens. Acta Vet Brno 79:S29–S34CrossRefGoogle Scholar
  29. Mallek Z, Fendri I, Khannous L, Ben Hassena A, Traore AI, Ayadi M-A, Gdoura R (2012) Effect of zeolite (clinoptilolite) as feed additive in Tunisian broilers on the total flora, meat texture and the production of omega 3 polyunsaturated fatty acid. Lipids Health Dis 11:35CrossRefGoogle Scholar
  30. Matijašević S, Daković A, Tomašević-Čanović M, Stojanović M, Ileš D (2006) Uranium(VI) adsorption on surfactant modified heulandite/clinoptilolite rich tuff. J Serb Chem Soc 71:1323–1331CrossRefGoogle Scholar
  31. Miazzo R, Peralta MF, Magnoli C, Salvano M, Ferrero S, Chiacchiera SM, Carvalho ECQ, Rosa CAR, Dalcero A (2005) Efficacy of sodium bentonite as a detoxifier of broiler feed contaminated with aflatoxin and fumonisin. Poult Sci 84:1–8CrossRefGoogle Scholar
  32. Mitrović B, Vitorović G, Jovanović M, Lazarević-Macanović M, Andrić V, Stojanović M, Daković A, Vitorović D (2014) Uranium distribution in broiler organs and possibilities for protection. Radiat Environ Biophys 53:151–157CrossRefGoogle Scholar
  33. Mitrović BM, Jovanović M, Lazarević-Macanović M, Dj Janaćković, Krstić N, Stojanović M, Mirilović M (2015) Efficiency of sepiolite in broilers diet as uranium adsorbent. Radiat Environ Biophys 54:217–224CrossRefGoogle Scholar
  34. National Research Council (NRC) (2005) Mineral tolerance of animals. 2nd edn. The National Academies Press, Washington, D.C.
  35. Official Journal of the European Communities (OJEU) (1986) Council directive of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purpose (86/609/EEC)Google Scholar
  36. Ortatatli M, Oǧuz H, Hatipoǧlu F, Karaman M (2005) Evaluation of pathological changes in broilers during chronic aflatoxin (50 and 100 ppb) and clinoptilolite exposure. Res Vet Sci 78:61–68CrossRefGoogle Scholar
  37. Osman A (2011) Experimental simulation for accidental exposure to uranium pollutants in drinking water: a histological study on the possible impact on cerebral cortex of adult albino rats. Int J Health Sci (Qassim) 5:8–9Google Scholar
  38. Papaioannou D, Katsoulos PD, Panousis N, Karatzias H (2005) The role of natural and synthetic zeolites as feed additives on the prevention and/or the treatment of certain farm animal diseases: a review. Microporous Mesoporous Mater 84:161–170CrossRefGoogle Scholar
  39. Pellmar TC, Fuciarelli AF, Ejnik JW, Hamilton M, Hogan J, Strocko S, Emond C, Mottaz HM, Landauer MR (1999) Distribution of uranium in rats implanted with depleted uranium pellets. Toxicol Sci 49:29–39CrossRefGoogle Scholar
  40. Prasai TP, Walsh KB, Midmore DJ, Jones BEH, Bhattarai SP (2018) Manure from biochar, bentonite and zeolite feed supplemented poultry: moisture retention and granulation properties. J Environ Manage 216:82–88CrossRefGoogle Scholar
  41. Stojanović M, Stevanović D, Milojković J, Grubišić M, Ileš D (2010) Phytotoxic effect of the uranium on the growing up and development the plant of corn. Water Air Soil Pollut 209:401–410ADSCrossRefGoogle Scholar
  42. Sullivan MF, Ruemmler PS, Ryan JL, Buschbom RL (1986) Influence of oxidizing or reducing agents on gastrointestinal absorption of U, Pu, Am, Cm and Pm by rats. Health Phys 50:223–232CrossRefGoogle Scholar
  43. Trailović JN, Stefanović S, Trailović SM (2013) In vitro and in vivo protective effects of three mycotoxin adsorbents against ochratoxin A in broiler chickens. Br Poult Sci 54:515–523CrossRefGoogle Scholar
  44. UNSCEAR (1988) Sources, effects and risks of ionizing radiation. Report to the general assembly with scientific annexes. New YorkGoogle Scholar
  45. UNSCEAR (2017) Sources, effects and risks of ionizing radiation. Report to the general assembly with scientific annexes 2016. New YorkGoogle Scholar
  46. Vićentijević MČ, Pantelić GK, Vuković DŽ, Vuković JV, Mitrović MB, Živanov ZD (2013) The effect of radioprotectors protection ability in pheasants after alimentary radio-contamination with137Cs. Nucl Technol Radiat Prot 28:232–236CrossRefGoogle Scholar
  47. Wawrzyniak A, Kapica M, Stępień-Pyśniak D, Łuszczewska-Sierakowska I, Szewerniak R, Jarosz Ł (2017) The effect of dietary supplementation of transcarpathian zeolite on intestinal morphology in female broiler chickens. J Appl Poult Res 26:421–430CrossRefGoogle Scholar
  48. Wu QJ, Wang QY, Wang T, Zhou YM (2015) Effects of clinoptilolite (zeolite) on attenuation of lipopolysaccharide-induced stress, growth and immune response in broiler chickens. Ann Anim Sci 15:681–697CrossRefGoogle Scholar
  49. Yalçın S, Yalçın S, Gebeş ES, Şahin A, Duyum HM, Escribano F, Ceylan A (2017) Sepiolite as a feed supplement for broilers. Appl Clay Sci 148:95–102CrossRefGoogle Scholar
  50. Zhu G, Xiang X, Chen X, Wang L, Hu H, Weng S (2009) Renal dysfunction induced by long-term exposure to depleted uranium in rats. Arch Toxicol 83:37–46CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Branislava Mitrović
    • 1
    Email author
  • Mirjana Stojanović
    • 2
  • Živko Sekulić
    • 2
  • Velibor Andrić
    • 1
  • Mihajlo Vićentijević
    • 3
  • Borjana Vranješ
    • 1
  1. 1.Faculty of Veterinary MedicineBelgradeSerbia
  2. 2.Institute for Technology of Nuclear and Other Mineral Row MaterialsUniversity of BelgradeBelgradeSerbia
  3. 3.Science Institute of Veterinary Medicine of SerbiaBelgradeSerbia

Personalised recommendations