Skip to main content

Advertisement

Log in

Subchronic exposure to leachate activates key markers linked with neurological disorder in Wistar male rat

Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The linking of various environmental chemicals exposure to neurodegenerative disorders is current. This study was undertaken to elucidate the toxic effects and the underlying biochemical mechanism of leachate obtained from Elewi Odo municipal battery recycling site (EOMABRL) using key markers of neuronal damage in rat via an oral route. Analysis of the concentrations of heavy metals showed that lead, cadmium, nickel, chromium, manganese, and iron were higher than the acceptable limits set by the regulatory authority—the World Health Organization. Whereas, copper, zinc, and cobalt were lower than permissible limits. EOMABRL was administered at 0, 20, 40, 60, 80, and 100 % concentrations to adult male rats for 60 days. An in vitro study was also carried out in the cerebellum to assess cholinesterase biochemistry assays. Following exposure, brain was collected to determine the antioxidant status. EOMABRL administration significantly increased superoxide dismutase (SOD) and catalase (CAT) activities, and a sequential decrease in reduced glutathione (GSH) level with a concomitant increase in the accumulation of hydrogen peroxide (H2O2) and malondialdehyde (MDA) level was observed, when compared with the control. The treated rat had a significant (P < 0.05) increase in the activities of acetycholinesterase (AChE) and butyrylcholinesterase (BuChE). Taken together, these findings conclude that some possible mechanisms by which EOMABRL elicits neuronal disorder in male rat could be through the activation of AChE and BuChE and induction of oxidative stress with necrosis of neuronal cells.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  • Agency for Toxic Substances and Disease Registry, ATSDR (2008) ToxFAQs. Retrieved March 2009 from http://www.atsdr.cdc.gov/toxfaq.html

  • Ahmad M, Sharif T, Javed AA, Zabta M, Jeelani B (2008) Alamgeer Bioavailability study of oral 5-fluorouracil in colorectal cancer patients. Pharmacol Online 3:100–109

  • Akintunde JK, Oboh G (2012) In vitro oxidative damage induced in livers, hearts and kidneys of rats treated with leachate from battery recycling site: evidence for environmental contamination and tissue damage. J Clin Exp Pathol 2:129

    Google Scholar 

  • Akintunde JK, Oboh G (2013a) Municipal auto-battery recycling-site leachate activates key enzymes linked to non-insulin dependent diabetes mellitus (NIDDM) and hypertension. J Diabetes Metab 4:235

    Google Scholar 

  • Akintunde JK, Oboh G (2013b) Exposure to leachate from municipal battery recycling site: implication as key inhibitor of steroidogenic enzymes and risk factor of prostate damage in rats. Rev Environ Health 28(4):203–213. doi:10.1515/reveh-2013-0009

    Article  CAS  Google Scholar 

  • Akintunde JK, Oboh G (2015) Depletion of cellular adenosine triphosphate and hepatocellular damage in rat after subchronic exposure to leachate from anthropogenic recycling site. Hum Exp Toxicol. 0960327115569809 (in press)

  • Akintunde JK, Oboh G, Akindahunsi AA (2015) Inhibition of key markers linked with spermatogenesis and cellular ATP by sub-chronic exposure to leachate in a rat model. Arch Environ Contam Toxicol 68(2):68–79

    Google Scholar 

  • Aleksandra D, Urszula B (2008) The impact of nickel on human health. J Elem 13(4):685–696

  • American Society for Testing Material (1992) Standard method for shake extraction of solid waste with water, ASTM designation D3987-85. ASTM, West Conshohocken, p 4

    Google Scholar 

  • AOAC (1991) Official methods of analysis, 5th edn. Association of official analytical chemists, Washington

    Google Scholar 

  • Ariel MT, Maya K, Ronit A, Yanina G (2005) Vitamin B12, demyelination, remyelination and repair in multiple sclerosis. J Neurol Sci 233(1-2):93–97

    Article  Google Scholar 

  • Bechan S, Shweta S, Nikhat JS (2014) Biomedical implications of heavy metals induced imbalances in redox systems. BioMed Res Int 2014(640754):26. doi:10.1155/2014/640754

    Google Scholar 

  • Benarroch EE (2009) Brain iron homeostasis and neurodegenerative disease. Neurology 72:1436–1440

    Article  Google Scholar 

  • Bitanihirwe BK, Cunningham MG (2009) Zinc: the brain’s dark horse. Synapse 63:1029

    Article  CAS  Google Scholar 

  • Bo W, Yanli D (2013) Cadmium and its neurotoxic effects. Oxidative Med Cell Longev 2013(898034):12. doi:10.1155/2013/898034

    Google Scholar 

  • Bornhorst J, Wehe CA, Hüwel S, Karst U, Galla HJ, Schwerdtle T (2012) Impact of manganese on and transfer across blood-brain and blood-cerebrospinal fluid barrier in vitro. J Biol Chem 287(21):17140–17151

    Article  CAS  Google Scholar 

  • Brusick D (1980) Bone marrow cytogenic analysis in rats. In: Principles of genetics toxicology. Plenum, New York, p. 235–239

  • Centres for Disease Control and Prevention (CDCP) (2009). Fourth report on human exposure to environmental chemicals. CDCP, Atlanta, GA. http://www.cdc.gov/exposurereport/pdf/fourthreport.pdf. Accessed 17 Sep 2012

  • Cesar VB, Jack B, Naoki T, Christine ES, Nathan LW, Hideki S, Paul RS, Dwaine FE, Yuji K, Harry RV (2013) Epidemiological survey-based formulae to approximate incidence and prevalence of neurological disorders in the United States: a meta-analysis. Plos One 8(10), e78490

    Article  Google Scholar 

  • Chiou SY, Wu YG, Lin YF, Lin LY, Lin G (2007) Substrate activation of butyrylcholinesterase and substrate inhibition of acetylcholinesterase by 3,3-dimethylbutyl-N-n-butylcarbamate and 2-trimethylsilyl-ethyl-N-n-butylcarbamate. J Biochem Mol Toxicol 21(1):24–31

    Article  CAS  Google Scholar 

  • Chow ESH, Hui MNY, Lin CC, Cheng SH (2008) Cadmium inhibits neurogenesis in zebrafish embryonic brain development. Aquat Toxicol 87(3):157–169

    Article  CAS  Google Scholar 

  • Clairborne A (1995) Catalase activity. In: Greewald AR (ed) Handbook of methods for oxygen radical research. CRC, Florida, pp 237–242

    Google Scholar 

  • Dandlen SA, Miguel MG, Duarte J, Faleiro ML, Sousa MJ, Lima AS, Figueiredo AC, Barroso JG, Pedro LG (2011) Acetylcholinesterase inhibition activity of Portuguese Thymus species essential oils. J Essent Oil Bear Pl 14:140–150

    Article  CAS  Google Scholar 

  • FAO/WHO (2010) The summary report of the 73rd JECFA meeting, Tech. Rep., WHO, Geneva, Switzerland

  • Farombi EO, Akintunde JK, Nsute N, Adedara IA, Arojojoye O (2011) Municipal landfill leachate induces hepatotoxicity and oxidative stress in rats. J Toxicol Ind Health 28(6):532–541

    Article  Google Scholar 

  • Ferrari B, Radetski CM, Veber AM, Ferard JF (1999) Ecotoxicological assessment of solid wastes: a combined liquid- and solid-phase testing approach using a battery of bioassays and biomarkers. Environ Toxicol Chem 18:1195–1202

    CAS  Google Scholar 

  • Fujiwara M, Yagi N, Miyazawa M (2010) Acetylcholinesterase inhibitory activity of volatile oil from Peltophorum dasyrachis Kurz ex Bakar (Yellow Batai) and bisabolene-type sesquiterpenoids. J Agric Food Chem 58:2824–2829

    Article  CAS  Google Scholar 

  • Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150

    Article  CAS  Google Scholar 

  • Hambidge KM, Krebs NF (2007) Zinc deficiency: a special challenge. J Nutr 137:1101–1105

    CAS  Google Scholar 

  • Hyman MS (2011) Neurodegeneration with brain iron accumulation—clinical syndromes and neuroimaging. Biochim Biophys Acta 1822(3):350–360

    Google Scholar 

  • IIhami GI, Haci AA, Mehmet C (2005) Chem Pharm Bull 53(3):281

    Article  Google Scholar 

  • Ip PS, Tsim KW, Chan K, Bauer R (2012) Application of complementary and alternative medicine on neurodegenerative disorders: current status and future prospects. Evid Based Complement Alternat Med, l2012. doi:10.1155/2012/930908, 1–2

  • Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene induced liver necrosis: protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11:151–169

    Article  CAS  Google Scholar 

  • Kanter M, Unsal C, Aktas C, Erboga M (2013) Neuroprotective effect of quercetin against oxidative damage and neuronal apoptosis caused by cadmium in hippocampus. Toxicol Ind Health. doi:10.1177/0748233713504810

  • Li X, Jankovic J, Le W (2011) Iron chelation and neuroprotection in neurodegenerative diseases. J Neural Transm 118:473–477

    Article  CAS  Google Scholar 

  • Ling-Mei T, To-Jung T, Tien-Hui L, Dong-Zong H, Chin-Chuan S, Cheng-Chieh Y, Yi-Chang S, Chun-Fa H, Shing-Hwa L, Ya-Wen C (2012) Cadmium-induced oxidative stress damage causes neuron cells apoptosis through JNK/mitochondria-dependent/endoplasmic reticulum stress pathways

  • Longe EO, Balogun MR (2010) Groundwater quality assessment near a municipal landfill, Lagos, Nigeria. Res J Appl Sci Eng Technol 2(1):39–44

    CAS  Google Scholar 

  • Mahomoodally MF, Vidooshi B, Geerjanand C (2013) Complementary and alternative medicines use against neurodegenerative diseases. Adv Pharmacol Pharm 1(3):103–123. doi:10.13189/app.2013.010301

    Google Scholar 

  • Martin SE, Griswold W (2009) Human health effects of heavy metals. Environmental Science and Technology Briefs for Citizens 1:1–6

    Google Scholar 

  • Matthew S, Claudius M, Udochukwu O, Wolff M (2011) Iron, zinc and copper in the Alzheimer’s disease brain: a quantitative meta-analysis. Some insight on the influence of citation bias on scientific opinion. Prog Neurobiol. 94(3): 296–306

  • Mead MN (2010) Cadmium confusion do consumers need protection? Environ Health Perspect 118(12):A528–A534

    Article  CAS  Google Scholar 

  • Menichini F, Tundis R, Loizzo MR, Bonesi M, Marreli M, Statti GA, Menichini F, Conforti F (2009) Acetylcholinesterase and butyrylcholinesterase inhibition of ethanolic extract and monoterpenes from Pimpinella anisoides V Brig. (Apiaceae). Fitoterapia 80:297–300

    Article  CAS  Google Scholar 

  • Miguel MG (2010) Antioxidant activity of medicinal and aromatic plants. A review. Flavour Fragr J 25:291–312

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1989) The role of superoxide anion in the auto-oxidation of epinephrine and a simple assay of superoxide dismutase. Toxicol Biol Chem 2417:3170

    Google Scholar 

  • Mohamed ME, Artef EA (2008) Effect of dietary iron overload in rat brain: oxidative stress, neurotransmitter level and serum metal ion in relation to neurodegenerative disorder. Indian J Exp Biol 46:855–858

    Google Scholar 

  • Nakashima AS, Dyck RH (2009) Zinc and cortical plasticity. Brain Res Rev 59:347

    Article  CAS  Google Scholar 

  • Nduka JK, Orisakwe EO (2010) Assessment of environmental distribution of lead in some municipalities of south-eastern Nigeria. Int J Environ Res Public Health 7(6):2501–2513

    Article  CAS  Google Scholar 

  • Nnorom IC, Osibanjo O (2009) Heavy metal characterization of waste portable rechargeable batteries used in mobile phones. Int J Environ Sci Tech 6(4):641–650

    Article  CAS  Google Scholar 

  • Oboh G, Rocha JBT (2007) Distribution and antioxidant activity of polyphenols in ripe and unripe tree pepper (Capsicum pubescens). J Food Biochem 31:456–473

    Article  CAS  Google Scholar 

  • Oboh G, Ademiluyi A, Akinyemi A (2010) Inhibition of acetylcholinesterase activities and some pro-oxidants induced lipid peroxidation in rat brain by two varieties of ginger (Zingiber officiriale). Exp Toxicol Pathol. doi:10.1016/j.etp.2010.09.004

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  • Olesen J, Leonardi M (2003) The burden of brain diseases in Europe. Eur.J. Neurol., 10, 471–477

  • Pamphlett R, Kum JS (2013) Uptake of inorganic mercury by human locus ceruleus and corticomotor neurons: implications for amyotrophic lateral sclerosis. Acta Neuropathol Commun 1(1):13. doi:10.1186/2051-5960-1-13

    Article  Google Scholar 

  • Paul SI, Karl WT, Kelvin C, Rudolf B (2012) Application of complementary and alternative medicine on neurodegenerative disorders: current status and future prospects. Evid Based Complement Alternat Med 2012:930908. doi:10.1155/2012/930908

    Google Scholar 

  • Perry NS, Houghton PJ, Theobal DA, Jenner P, Perry EK (2000) In vitro activity of S. lavan-dulaefolia (Spanish sage) relevant to treatment of Alzheimer’s disease. J Pharm Pharmacol 52:895–902

    Article  CAS  Google Scholar 

  • Rivera-Mancia S, Perez-Neri I, Rios C, Tristan-Lopez L, Rivera-Espinosa L, Montes S (2010) The transition metals copper and iron in neurodegenerative disease. J Chem Biol Interact 186:184–199

    Article  CAS  Google Scholar 

  • Robert B, Siena L, Dylan P, Nicholas S, Diane Z, Allan A (2008) The cellular effect of lead poisoning and its clinical picture. GUJHS, 5(2)

  • Roger P, Stephen KJ (2013) Heavy metals in locus ceruleus and motor neurons in motor neuron disease. Acta Neuropathol Commun 1:81

    Article  Google Scholar 

  • Scheiber I, Dringen R, Mercer JFB (2013) Chapter 11. Copper: effects of deficiency and overload. In: Sigel A, Sigel H, Sigel RKO (eds) Interrelations between essential metal ions and human diseases. Metal ions in life sciences 13. Springer, pp 359–387. doi:10.1007/978-94-007-7500-8_11

  • Schipper HM (2009) Metal accumulation during aging. In: Squire LR (ed) Encyclopedia of Neuroscience. Academic, Oxford. 123:811–818

  • Shahat AA, Ibrahim AY, Hendawy SF, Omer EA, Hammouda FM, Abdel-Rahman F, Saleh MA (2011) Chemical composition, antimicrobial and antioxidant activities of essential oils from organically cultivated fennel cultivars. Molecules 16:1366–1377

    Article  CAS  Google Scholar 

  • Siddique HR, Gupta SC, Dhawan A, Murthy RC, Saxena DK, Chowdhuri DK (2005) Genotoxicity of industrial solid waste leachates in Drosophila melanogaster. Environ Mol Mutagen 46:189–197

    Article  CAS  Google Scholar 

  • Small A, Badia L, Maria M (2011) Antioxidant and anti-acetylcholinesterase activities of some commercial essential oils and their major compounds. Molecules 16:7672–7690, 3390/molecules 16097672

    Article  Google Scholar 

  • Smita S, Pico C (2011) Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 71(1):35–48

    Article  Google Scholar 

  • Soudani N, Troudi A, Amara IB, Bouaziz H, Boudawara T, Zeghal N (2012) Ameliorating effect of selenium on chromium (VI)-induced oxidative damage in the brain of adult rats. Physiol Biochem 68(3):397–409

    Article  CAS  Google Scholar 

  • Stephen DA, Christopher DM, William TC, Corby KM, Sandra C, Paula G, Hongmei H, Christy LW, Donald AW (2008) Effects of chromium picolinate on food intake and satiety. Diabetes Technol Ther 10(5):405–412

    Article  Google Scholar 

  • Stewart W, Schwartz B (2007) Effects of lead on the adult brain: a 15-year exploration. Am J Ind Med 50:729–739

    Article  CAS  Google Scholar 

  • Theodore IL, Jay SS (2003) Lead neurotoxicity in children: basic mechanisms and clinical correlates. J Neurol 126(1):5–19

    Google Scholar 

  • Topal A, Atamanalp M, Oruç E, Halıcı MB, Şişecioğlu M, Erol HS, Gergit A, Yılmaz B (2015) Neurotoxic effects of nickel chloride in the rainbow trout brain: assessment of c-Fos activity, antioxidant responses, acetylcholinesterase activity, and histopathological changes. Fish Physiol Biochem 41(3):625–634

    Article  CAS  Google Scholar 

  • Torben M, Evan HM (2004) The metabolism of neuronal iron and its pathogenic role in neurological disease: review. Ann NY Acad Sci 1012:14–26

    Article  Google Scholar 

  • U.S. Environmental Protection Agency (2008). Protect your family from lead in your home. Accessed on February 5, http://www.epa.gov/lead/pubs/leadpdfe.pdf

  • Unsal C, Kanter M, Aktas C, Erboga M (2013) Role of quercetin in cadmium-induced oxidative stress, neuronal damage, and apoptosis in rats. Toxicol Ind Health. doi:10.1177/0748233713504810

    Google Scholar 

  • Uttara B, Singh AV, Zamboni P, Mahajan RT (2009) Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 7(1):65–74

    Article  CAS  Google Scholar 

  • Vahid YB, Leila S, Kobra S, Ali AM, Mohammad R (2014) The toxic effect of manganese on the acetylcholinesterase activity in rat brains. J Toxicol 2014(946372):4. doi:10.1155/2014/946372

    Google Scholar 

  • Vest KE, Hashemi HF, Cobine PA (2013) Chapter 13. The copper metallome in eukaryotic cells. In: Banci L (ed) Metallomics and the cell. Metal ions in life sciences 12. Springer. doi:10.1007/978-94-007-5561-10_12. ISBN 978-94-007-5560-4.electronic-book ISBN 978-94-007-5561-1 ISSN 1559-0836 electronic-ISSN 1868-0402

  • Wojcik D, Godfrey ME, Christie D, Haley BE (2006) Mercury toxicity presenting as chronic fatigue, memory impairment and depression: diagnosis, treatment, susceptibility and outcomes in a New Zealand general practice setting (1994–2006). Neuro Endocrinol Lett 27(4):415–423

    CAS  Google Scholar 

  • World Health Organization (2008) International year of fresh water. General Assembly Resolution A/RES/55/196. www.wateryear2003.org. Accessed 13 Mar 2011

  • Xia W (2010) Exploring Alzheimer’s disease in zebrafish. J Alzheimers Dis 20:981–990

    CAS  Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, p 620

    Google Scholar 

  • Zhao W, Beers DR, Henkel JS, Zhang W, Urushitani M, Julien JP, Appel SH (2010) Extracellular mutant SOD1 induces microglial-mediated motoneuron injury. Glia 58:231–243

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. K. Akintunde.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akintunde, J.K., Oboh, G. Subchronic exposure to leachate activates key markers linked with neurological disorder in Wistar male rat. Environ Sci Pollut Res 22, 18541–18553 (2015). https://doi.org/10.1007/s11356-015-5327-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-5327-4

Keywords

Navigation