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Albendazole in environment: faecal concentrations in lambs and impact on lower development stages of helminths and seed germination

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Abstract

Albendazole (ABZ), widely used benzimidazole anthelmintic, administered to animals enters via excrements into environment and may impact non-target organisms. Moreover, exposure of lower development stages of helminths to anthelmintics may also encourage the development of drug-resistant strains of helminths. In present project, the kinetics of ABZ (10 mg kg−1 p.o.) and its metabolite (ABZ.SO, ABZSO2) elimination in faeces from treated Texel lambs were studied using UHPLC/MS/MS with the aim to find out their concentrations achievable in the environment. Consequently, the effect of these compounds on lower development stages of Barber’s pole worm (Haemonchus contortus) and on germination of white mustard (Sinapis alba) seeds was evaluated. The results showed that ABZ concentrations in faeces excreted in 4–60 h after treatment were above the concentrations lethal for H. contortus eggs. Moreover, pre-incubation with sub-lethal doses of ABZ and ABZ.SO did not increase the resistance of H. contortus eggs and larvae to anthelmintics. On the other hand, concentrations of ABZ and ABZ.SO in faeces are so high that might have negative influence on non-target soil invertebrates. As neither ABZ nor its metabolites affect the germination of mustard seeds, phytoremediation could be considered as potential tool for detoxification of ABZ in the environment.

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References

  • Baggot JD (1977) Principles of drug disposition in domestic animals: the basis of veterinary clinical pharmacology. W.B. Saunders, Philadelphia

    Google Scholar 

  • Capece BPS, Castells G, Pérez F, Arboix M, Cristòfol C (2000) Pharmacokinetic behaviour of albendazole sulphoxide enantiomers in male and female sheep. Vet Res Commun 24:339–348. doi:10.1023/A:1006496122684

    Article  CAS  Google Scholar 

  • Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, Waller PJ (1992) World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44:35–44. doi:10.1016/0304-4017(92)90141-U

    Article  CAS  Google Scholar 

  • Coles GC, Jackson F, Pomroy WE, Prichard RK, von Samson-Himmelstjerna G, Silvestre A, Taylor MA, Vercruysse J (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 136:167–85. doi:10.1016/j.vetpar.2005.11.019

    Article  CAS  Google Scholar 

  • Cooper KM, McMahon C, Fairweather I, Elliott CT (2015) Potential impacts of climate change on veterinary medicinal residues in livestock produce: an island of Ireland perspective††This paper is one of a series of reviews on “Climate Change and Food Safety—an Island of Ireland perspective”. Trends Food Sci Technol 44:21–35. doi:10.1016/j.tifs.2014.03.007

    Article  CAS  Google Scholar 

  • Cvilink V, Lamka J, Skálová L (2009a) Xenobiotic metabolizing enzymes and metabolism of anthelminthics in helminths. Drug Metab Rev 41:8–26. doi:10.1080/03602530802602880

    Article  CAS  Google Scholar 

  • Cvilink V, Szotáková B, Krízová V, Lamka J, Skálová L (2009b) Phase I biotransformation of albendazole in lancet fluke (Dicrocoelium dendriticum). Res Vet Sci 86:49–55. doi:10.1016/j.rvsc.2008.05.006

    Article  CAS  Google Scholar 

  • Dobson RJ, Griffiths DA, Donald AD, Waller PJ (1987) A genetic model describing the evolution of levamisole resistance in Trichostrongylus colubriformis, a nematode parasite of sheep. Mathematical Med Biol 4:279–293. doi:10.1093/imammb/4.4.279

    Article  CAS  Google Scholar 

  • Fisher PMJ, Scott R (2008) Evaluating and controlling pharmaceutical emissions from dairy farms: a critical first step in developing a preventative management approach. J Clean Prod 16:1437–1446. doi:10.1016/j.jclepro.2008.04.024

    Article  Google Scholar 

  • Gokbulut C, Akar F, McKellar QA (2006) Plasma disposition and faecal excretion of oxfendazole, fenbendazole and albendazole following oral administration to donkeys. Vet J 172:166–72. doi:10.1016/j.tvjl.2005.02.022

    Article  CAS  Google Scholar 

  • Gokbulut C, Cirak VY, Senlik B, Yildirim F, McKellar QA (2009) Pharmacological assessment of netobimin as a potential anthelmintic for use in horses: plasma disposition, faecal excretion and efficacy. Res Vet Sci 86:514–520. doi:10.1016/j.rvsc.2008.10.001

    Article  CAS  Google Scholar 

  • Gothwal R, Shashidhar T (2015) Antibiotic pollution in the environment: a review. CLEAN - Soil, Air, Water 43:479–489. doi:10.1002/clen.201300989

    Article  CAS  Google Scholar 

  • Grovum WL, Williams VJ (1973) Rate of passage of digesta in sheep. Br J Nutr 30:313. doi:10.1079/BJN19730036

    Article  CAS  Google Scholar 

  • Gyurik RJ, Chow AW, Zaber B, Brunner EL, Miller JA, Villani AJ, Petka LA, Parish RC (1981) Metabolism of albendazole in cattle, sheep, rats and mice. Drug Metab Dispos: Biol Fate Chem 9:503–8

    CAS  Google Scholar 

  • Hennessy DR, Steel JW, Lacey E, Eagleson GK, Prichard RK (1989) The disposition of albendazole in sheep. J Vet Pharmacol Ther 12:421–429. doi:10.1111/j.1365-2885.1989.tb00693.x

    Article  CAS  Google Scholar 

  • Hernando MD, Mezcua M, Fernández-Alba AR, Barceló D (2006) Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 69:334–42. doi:10.1016/j.talanta.2005.09.037

    Article  CAS  Google Scholar 

  • Hunt K, Taylor M (1989) Use of the egg hatch assay on sheep faecal samples for the detection of benzimidazole resistant nematodes. Vet Rec 125:153–154. doi:10.1136/vr.125.7.153

    Article  CAS  Google Scholar 

  • Jackson F, Coop RL (2000) The development of anthelmintic resistance in sheep nematodes. Parasitology 120:95–107

    Article  Google Scholar 

  • Lanusse CE, Prichard RK (1990) Pharmacokinetic behaviour of netobimin and its metabolites in sheep. J Vet Pharmacol Ther 13:170–8

    Article  CAS  Google Scholar 

  • Lanusse CE, Prichard RK (1993) Clinical pharmacokinetics and metabolisms of benzimidazole anthelmintics in ruminants. Drug Metab Rev 25:235–79

    Article  CAS  Google Scholar 

  • Lanusse CE, Gascon LH, Prichard RK (1993) Gastrointestinal distribution of albendazole metabolites following netobimin administration to cattle: relationship with plasma disposition kinetics. J Vet Pharmacol Ther 16:38–47

    Article  CAS  Google Scholar 

  • Lumaret JP, Errouissi F, Floate K, Römbke J, Wardhaugh K (2012) A review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments. Curr Pharm Biotechnol 13:1004–60

    Article  CAS  Google Scholar 

  • Lutterbeck CA, Kern DI, Machado ÊL, Kümmerer K (2015) Evaluation of the toxic effects of four anti-cancer drugs in plant bioassays and its potency for screening in the context of waste water reuse for irrigation. Chemosphere 135:403–10. doi:10.1016/j.chemosphere.2015.05.019

    Article  CAS  Google Scholar 

  • Marriner SE, Bogan JA (1980) Pharmacokinetics of albendazole in sheep. Am J Vet Res 41:1126–9

    CAS  Google Scholar 

  • Moroni P, Buronfosse T, Longin-Sauvageon C, Delatour P, Benoit E (1995) Chiral sulfoxidation of albendazole by the flavin adenine dinucleotide-containing and cytochrome P450-dependent monooxygenases from rat liver microsomes. Drug Metab Dispos 23:160–165

    CAS  Google Scholar 

  • Podlipná R, Skálová L, Seidlová H, Szotáková B, Kubíček V, Stuchlíková L, Jirásko R, Vaněk T, Vokřál I (2013) Biotransformation of benzimidazole anthelmintics in reed (Phragmites australis) as a potential tool for their detoxification in environment. Bioresour Technol 144:216–24. doi:10.1016/j.biortech.2013.06.105

    Article  Google Scholar 

  • Prchal L, Vokřál I, Kašný M, Rejšková L, Zajíčková M, Lamka J, Skálová L, Lecová L, Szotáková B (2015) Metabolism of drugs and other xenobiotics in giant liver fluke (Fascioloides magna). Xenobiotica 1–9. doi:10.3109/00498254.2015.1060370

  • Prichard RK (1985) Interaction of host physiology and efficacy of antiparasitic drugs. Vet Parasitol 18:103–110. doi:10.1016/0304-4017(85)90060-3

    Article  CAS  Google Scholar 

  • Prichard RK, Hennessy DR (1981) Effect of oesophageal groove closure on the pharmacokinetic behaviour and efficacy of oxfendazole in sheep. Res Vet Sci 30:22–7

    CAS  Google Scholar 

  • Renwick AG, Strong HA, George CF (1986) The role of the gut flora in the reduction of sulphoxide containing drugs. Biochem Pharmacol 35:64. doi:10.1016/0006-2952(86)90557-5

    Article  CAS  Google Scholar 

  • Sangster N, Gill J (1999) Pharmacology of anthelmintic resistance. Parasitol Today 15:141–146. doi:10.1016/S0169-4758(99)01413-1

    Article  CAS  Google Scholar 

  • Várady M, Čudeková P, Čorba J (2007) In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Vet Parasitol 149:104–110. doi:10.1016/j.vetpar.2007.07.011

    Article  Google Scholar 

  • Virkel G, Lifschitz A, Soraci A, Sansinanea A, Lanusse C (2000) Enantioselective liver microsomal sulphoxidation of albendazole in cattle: effect of nutritional status. Xenobiotica 30:381–393. doi:10.1080/004982500237579

    Article  CAS  Google Scholar 

  • Wagil M, Białk-Bielińska A, Puckowski A, Wychodnik K, Maszkowska J, Mulkiewicz E, Kumirska J, Stepnowski P, Stolte S (2015) Toxicity of anthelmintic drugs (fenbendazole and flubendazole) to aquatic organisms. Environ Sci Pollut Res 22:2566–2573. doi:10.1007/s11356-014-3497-0

    Article  CAS  Google Scholar 

  • Wang Y, Tang Y, Xu L, Diao X (2009) 书书书阿苯哒唑对蚯蚓的生态毒理效应 [Ecotoxicolgical effects of albendazole on Eisenia fetida]. Ying yong sheng tai xue bao = The journal of applied ecology / Zhongguo sheng tai xue xue hui, Zhongguo ke xue yuan Shenyang ying yong sheng tai yan jiu suo zhu ban 20:2296–300

    CAS  Google Scholar 

  • Wolstenholme AJ, Fairweather I, Prichard R, von Samson-Himmelstjerna G, Sangster NC (2004) Drug resistance in veterinary helminths. Trends Parasitol 20:469–76. doi:10.1016/j.pt.2004.07.010

    Article  CAS  Google Scholar 

  • Zhang Y, Huo M, Zhou J, Xie S (2010) PKSolver: an add-in program for pharmacokinetic and pharmacodynamic data analysis in Microsoft Excel. Comput Methods Prog Biomed 99:306–14. doi:10.1016/j.cmpb.2010.01.007

    Article  Google Scholar 

Download references

Acknowledgments

L3 larvae of H. contortus were kind gift of Dr. Várady, Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia.

This project was supported by Czech Science Foundation, grant No. 15-05325S and by Charles University in Prague (research project SVV 260 294).

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Authors and Affiliations

  1. Department of Biochemical Sciences, Faculty of Pharmacy in Hradec Králové, Charles University, Heyrovského 1203, CZ-50005, Hradec Králové, Czech Republic

    Lukáš Prchal, Tereza Dědková, Lenka Skálová, Lenka Lecová & Barbora Szotáková

  2. Laboratory of Plant Biotechnologies, Institute of Experimental Botany, Czech Academy of Sciences, Praha 6, Czech Republic

    Radka Podlipná & Tomáš Vaněk

  3. Department of Pharmacology and Toxicology, Faculty of Pharmacy in Hradec Králové, Charles University, Hradec Králové, Czech Republic

    Jiří Lamka & Ivan Vokřál

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  1. Lukáš Prchal
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  2. Radka Podlipná
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  3. Jiří Lamka
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  4. Tereza Dědková
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  5. Lenka Skálová
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  9. Barbora Szotáková
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Correspondence to Barbora Szotáková.

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Compliance with ethical standards

All experimental procedures were undertaken in accordance with the Czech guidelines for the care and use of farm and experimental animals and were performed under the supervision of Ethical Committee of the Charles University, Faculty of Pharmacy in Hradec Králové (Protection of Animals from Cruelty Act No. 246/92, Czech Republic).

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Responsible editor: Philippe Garrigues

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Prchal, L., Podlipná, R., Lamka, J. et al. Albendazole in environment: faecal concentrations in lambs and impact on lower development stages of helminths and seed germination. Environ Sci Pollut Res 23, 13015–13022 (2016). https://doi.org/10.1007/s11356-016-6472-0

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