Abstract
Indiscriminate small-scale artisanal gold mining activities were reported to have caused anthropogenic heavy metal environmental pollution in Zamfara State, north-western Nigeria. There is little or no information on the neurotoxic effects and related neuropathological lesions due to environmental pollution in the animal population. Therefore, this work investigated the concentration of heavy metal and associated lesions in the brain of goats around an artisanal mining site in Zamfara. Brain samples were collected from 40 goats at slaughter slabs in Bagega (Zamfara State) while 15 goats with the same demography but without a history of environmental exposure at the time of this study served as controls. The concentration of lead and cadmium in brain tissue and histopathologic changes were assessed using atomic absorption spectrophotometry, histology and immunohistochemistry. The metal concentrations were significantly higher in exposed goats than in the unexposed animals. Cresyl violet staining and glial fibrillary acidic protein (GFAP) immunohistochemistry indicated chromatolysis and increased astrocytic activity respectively in the exposed goats. This study is of epidemiological importance as it shows a generalised increase of the metal concentrations in the brain of goats exposed to artisanal mining in Zamfara, north-western Nigeria. This could have health effects on the animals associated with nervous co-ordination, growth and development and as a good sentinel for pathogenesis of the heavy metal exposure.
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Aguilera de Benzo Z, Fraile R, Carrion N, Loreto D (1989) Determination of lead in whole blood by electrothermal atomization atomic absorption spectrometry using tube and platform atomizers and dilution with Triton X-100. J Anal Atom Spectrometry 4:397–400
Ahmed RG, Walaa GH, Asmaa FS (2018) Suppressive effects of neonatal bisphenol A on the neuroendocrine system. Toxicol Ind Health 34(6):397–407
Anetor JI (2012) Rising environmental cadmium levels in developing countries: threat to genome stability and health. Environ Anal Toxicol 2:140
Argos M, Ahsan H, Raziano JH (2012) Arsenic and human health: epidemiologic progress and public health implications. Rev Environ Health 27(4):191–195
Ashafaq M, Tabassum H, Vishnoi S, Salman M, Raisuddin S, Parvez S (2016) Tannic acid alleviates lead acetate-induced neurochemical perturbations in rat brain. Neuroscilett 617:94–100
Ayannuga OA, Oyekunle JAO, Ijomone OM, Ibeachusim BI (2015) Cadmium and lead toxicity, modulating roles of age and trace metals on Wistar rat cortical cells. Environ Pollut 4(3):51
Bello O, Naidu R, Rahman MM, Liu Y, Dong Z (2016) Lead concentration in the blood of the general population living near a lead–zinc mine site, Nigeria: Exposure pathways. Sci Total Environ 542:908–914
Betancourt O, Narvaez A, Roulet M (2005) Small-scale gold mining in the Puango river basin, southern Ecuador: a study of environmental impacts and human exposures. Ecohealth 2(4):323–332
Bihaqi SW, Huang H, Wu J, Zawia NH (2011) Infant exposure to lead (Pb) and epigenetic modifications in the aging primate brain: implications for Alzheimer’s disease. Int J Alzheimers Dis 27(4):819–833
Biswas S, Prabhu RK, Hussain KJ, Selvanayagam M, Satpathy KK (2012) Heavy metals concentration in edible fishes from coastal region of Kalpakkam, southeastern part of India. Environ Monit Assess 184:5097–5104
Bornschein RL, Succop PA, Krafft KM, Clark CS, Peace B, Hammond PB (1986) Exterior surface dust lead, interior house dust lead and childhood lead exposure in an urban environment. In: Hemphill D (ed) Trace substances in environmental health. University of Missouri, Columbia, pp 322–332
Calderón-Garcidueñas L, Torres-Jardón R, Kulesza RJ, Su-Bin P, D’Angiulli A (2014) Air pollution and detrimental effects on children’s brain. The need for a multidisciplinary approach to the issue complexity and challenges. Front Hum Neurosci 8:613
Carocci A, Catalano A, Lauria G, Sinicropi MS, Genchi G (2016) Lead toxicity, antioxidant defense and environment. Rev Environ Contam Toxicol 238:45–67 Springer, Cham
Casjens S, Pesch B, van Thriel C, Zschiesche W, Behrens T, Weiss T, Pallapies D, Arendt M, Dragano N, Moebus S, Jöckel KH (2018) Associations between blood lead, olfaction and fine-motor skills in elderly men: results from the Heinz Nixdorf Recall Study. Neurotoxicology 68:66–72
Center for Disease Control and Prevention Guidelines, CDC (1997) Preventing lead poisoning in young children U.S. Department of Health and Human Services, Public Health Service
Chander K, Vaibhav K, Ejaz Ahmed M, Javed H, Tabassum R, Khan A, Siddiqui MS (2014) Quercetin mitigates lead acetate-induced behavioural and histological alterations via suppression of oxidative stress, Hsp-70, Bak and upregulation of Bcl-2. Food Chem Toxicol 68:297–306
Charlet L, Chapron Y, Faller P, Kirsch R, Stone AT, Baveye PC (2012) Neurodegenerative diseases and exposure to the environmental metals Mn, Pb, and Hg. Coord Chem Rev 256:2147–2163
Corkhill CL, Vaughan DJ (2009) Arsenopyrite oxidation – a review. Appl Geochem 24:2342–2361
Cortés JL, Bautista F, Delgado C, Quintana P, Aguilar D, García A, Figueroa C Gogichaishvili A (2017) Spatial distribution of heavy metals in urban dust from Ensenada, Baja California, Mexico. RevistaChapingo. SerieCienciasForestales y delAmbiente 23(1)
Costa LG, Chang YC, Cole TB (2017) Developmental neurotoxicity of traffic-related air pollution: focus on autism. Curr Environ Health Rep 4(2):156–165 Curr Environ Health Rep
da Silva WAM, de Oliveira Mendes B, Guimarães ATB, Rabelo LM, de Oliveira Ferreira R, e Silva BC, de Souza JM, de Menezes IPP, de Lima Rodrigues AS, Malafaia G (2016) Dermal exposure to tannery effluent causes neurobehavioral changes in C57Bl/6J and Swiss mice. Chemosphere 160:237–243
Darmanto W, Inouye M, Takagishi Y, Ogawa M, Mikoshiba K, Murata Y (2000) Derangement of Purkinje cells in the rat cerebellum following prenatal exposure to X-irradiation: decreased reelin level is a possible cause. J Neuropathol Exp Neurol 59(3):251–262
Dhimal M, Karki KB, Aryal KK, Dhimal B, Joshi HD, Puri S, Pandey AR, Dhakal P, Sharma AK, Raya GB, Ansari I (2017) High blood levels of lead in children aged 6-36 months in Kathmandu Valley, Nepal: a cross-sectional study of associated factors. PLoS One 12(6):e0179233
Dhuria SV, Hanson LR, Frey WH (2010) II Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J Pharm Sci 99:1654–1673
Dooyema CA, Neri A, Lo YC, Durant J, Dargan PI, Swarthout T (2012) Outbreak of fatal childhood lead poisoning related to artisanal gold mining in northwestern Nigeria, 2010. Environ Health Perspect 120:601–607
Ebrahimzadeh-Bideskan AR, Hami J, Alipour F, Haghir H, Fazel AR, Sadeghi A (2016) Protective effects of ascorbic acid and garlic extract against lead-induced apoptosis in developing rat hippocampus. Metab Brain Dis 31(5):1123–1132
El-Amier YA, Elnaggar AA, El-Alfy MA (2017) Evaluation and mapping spatial distribution of bottom sediment heavy metal contamination in Burullus Lake, Egypt. Egypt J Basic Appl Sci 4(1):55–66
Ettinger AS, Roy A, Amarasiriwardena CJ, Smith D, Lupoli N, Mercado-García A, Lamadrid-Figueroa H, Tellez-Rojo MM, Hu H, Hernández-Avila M (2013) Maternal blood, plasma, and breast milk lead: lactational transfer and contribution to infant exposure. Environ Health Perspect 122(1):87–92
Ferreira MCDF, Zucki F, Duarte JL, Iano FG, Ximenes VF, Buzalaf MAR, Oliveira RCD (2017) Influence of iron on modulation of the antioxidant system in rat brains exposed to lead. Environ Toxicol 32(3):813–822
Florio M, Leto K, Muzio L, Tinterri A, Badaloni A, Croci L, Zordan P, Barili V, Albieri I, Guillemot F (2012) Neurogenin 2 regulates progenitor cell-cycle progression and Purkinje cell dendritogenesis in cerebellar development. Development 139(1):2308–2320
Folarin OR, Snyder AM, Peters DG, Olopade F, Connor JR, Olopade JO (2017) Brain metal distribution and neuro-inflammatory profiles after chronic vanadium administration and withdrawal in mice. Front Neurosci 11:58
Ghani SA (2015) Trace metals in seawater, sediments and some fish species from Marsa Matrouh Beahes in north western Mediterranean coast, Egypt. Egypt J Aquat Res 41(2):145–154
Goyer RA (1993) Lead toxicity: current concerns. Environ Health Perspect 100:177–187
Guzmán-Morales J, Morton-Bermea O, Hernández-Álvarez, Rodríguez-Salazar MT, García-Arreola ME, Tapia-Cruz V (2011) Assessment of atmospheric metal pollution in the urban area of mexico city, using Ficusbenjamina as Biomonitor. Bull Environ Contam Toxicol 86(5):495–500
Hammond PB, Aronson AL (1964) Lead poisoning in cattle and horses in the vicinity of a smelter. Ann N Y Acad Sci 111:595–611
Hanson K, Seibel G, Allard S, Wortman G, Kozak A (2010) AMEC nova gold resources Inc. Donlin Creek Gold Project, Alaska, US ANI Technical Report. 43-101
Hernández JA, López-Sánchez RC, Rendón-Ramírez A (2016) Lipids and oxidative stress associated with ethanol-induced neurological damage. Oxidative Med Cell Longev 2016
Heusinkveld HJ, Wahle T, Campbell A, Westerink RH, Tran L, Johnston H, Stone V, Cassee FR, Schins RP (2016) Neurodegenerative and neurological disorders by small inhaled particles. Neurotoxicology 56:94–106
Høgåsen HR, Ørnsrud R, Knutsen HK, Bernhoft A (2016) Lead intoxication in dogs: risk assessment of feeding dogs trimmings of lead-shot game. BMC Vet Res 12(1):152
Hopkins LE, Laing EA, Peake JL, Uyeminami D, Mack SM1, Li X, Smiley-Jewell S, Pinkerton KE (2018) Repeated Iron-Soot Exposure and Nose-to-brain Transport of Inhaled Ultrafine Particles.ToxicolPathol. 46(1):75–84
Igado OO, Olopade JO, Onwuka SK, Chukwudi AC, Daramola OA, Ajufo UE (2008) Evidence of environmental pollution in caprine brains obtained from a relatively unindustrialized area in Nigeria. Afr J Biomed Res 11:305–309
Inomi OE, Chukwuji OD, Ogisi OD, Oyaide WJ (2006) Alleviating rural poverty: what role for small-holder livestock production in delta state, Nigeria. Agricconspecsci 72(2):159–164
Ionescu P, Deak GYORGY, Diacu E, Radu VM (2016) Assessment of heavy metals levels in water, sediments and fish from Plumbuita Lake, Romania. Rev Chim 67(11):2148–2150
Ivanova J, Petrova E, Kamenova K, Gluhcheva Y (2017) Comparative effects of meso-2, 3-dimercaptosuccinic acid, monensin, and salinomycin on cadmium-induced brain dysfunction in cadmium intoxicated mice. InterdiscipToxicol 10(3):107–113
Jin X, Tian X, Liu Z, Hu H, Li X, Deng Y, Li N, Zhu J (2016) Maternal exposure to arsenic and cadmium and the risk of congenital heart defects in offspring. Reprod Toxicol 59:109–116
Jorgensen SE, Fath B (2008) S2.pdf. In: Encyclopedia of ecology. Elsevier Science, London, pp 3486–3619
Jubril AJ, Kabiru M, Olopade JO, Taiwo VO (2017) Biological monitoring of heavy metals in goats exposed to environmental contamination in Bagega, Zamfara State, Nigeria. Adv Environ Biol 11(6):11–18
Kaplan O, Yildirim NC, Yildirim N, Cimen M (2011) Toxic elements in animal products and environmental health. Asian J Anim Vet Adv 6:228–232
Karri V, Schuhmacher M, Kumar V (2016) Heavy metals (Pb, Cd, As and MeHg) as risk factors for cognitive dysfunction: a general review of metal mixture mechanism in brain. Environ Toxicol Pharmacol 48:203–213
Kumar VM, Henley AK, Nelson CJ, Indumati O, Rao YP, Rajanna S, Rajanna B (2017) Protective effect of Allium sativum (garlic) aqueous extract against lead-induced oxidative stress in the rat brain, liver, and kidney. Environ Sci Pollut Res Int 24(2):1544–1552
Laure-Kamionowska M, Taraszewska A, Maślińska D, Raczkowska B (2006) Faulty position of cerebellar cortical neurons as a sequel of disturbed neuronal migration. Folia Neuropathol 44(4):327–332
Leto K, Arancillo M, Becker EB, Buffo A, Chiang C, Ding B, Dobyns WB, Dusart I, Haldipur P, Hatten ME, Hoshino M (2016) Consensus paper: cerebellar development. Cerebellum 15(6):789–828
Li N, Liu X, Zhang P, Qiao M, Li H, Li H, Zhang H, Yu Z (2015) The effects of early life lead exposure on the expression of interleukin (IL) 1, IL-6, and glial fibrillary acidic proteinin the hippocampus of mouse pups. Hum Exp Toxicol 34(4):357–363
Liu J, Lewis G (2014) Environmental toxicity and poor cognitive outcomes in children and adults. J Environ Health 76(6):130–138
Lucchini RG, Dorman DC, Elder A, Veronesi B (2012) Neurological impacts from inhalation of pollutants and the nose-brain connection. Neurotoxicology 33(4):838–841
Mahaffey KR (1990) Environmental lead toxicity: nutrition as a component of intervention. Environ Health Perspect 89:75–78
Manton WI, Cook JD (1984) High accuracy (stable isotope dilution) measurements of lead in serum and cerebrospinal fluid. Br J Ind Med 41(3):313–319
Marçal WS, Gaste L, Ascimento MRL (2005) Identificação e quantificação de chumboemmisturasmineraiscomercializadas no estado de São Paulo. CiencAnim Bras 6:249–253
Médecins sans Frontières MSF-Holland MSF (2010) Lead poisoning crisis in Zamfara state, northern Nigeria. www.msf.org.Reports
Mielke HW, Laidlaw MAS, Gonzales CR (2011) Estimation of leaded (Pb) gasoline’s continuing material and health impacts on 90 US urbanized areas. Environ Int 37:248–257
Mombaerts P (2006) Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22:713–737
Ogabiela EE, Okwonkwo EM, Agbaji AS, Udiba UU, Hammuel C, Ade-Ajayi AF, Nwobi B (2011) Trace metal level of human blood from Dareta Village, Anka, Nigeria. Global J Pure Appl Sci 17(2):183–188
Olanreaju CA, Adeniyi PA (2017) Health risk ranking of lead contaminated sites in Bagega Community, Zamfara State, Nigeria. J Hum Environ Health Promot 2(4):201–211
Olopade JO, Fatola IO, Olopade FE (2011) Vertical administration of vanadium through lactation induces behavioural and neuro-morphological changes: protective role of Vitamin E. Nig J Physiol Sci 26:055–060
Pan L, Wang Z, Peng Z, Liu G, Zhang H, Zhang J, Jiang J, Pathiraja N, Xiao Y, Jiao R, Huang W (2016) Dietary exposure to lead of adults in Shenzhen city, China. Food Addit Contamin Part A 33(7):1200–1206
Pančevski Z, Stafilov T, Bačeva K (2017) Distribution of heavy metals in some vegetables grown in the vicinity of lead and zinc smelter plant. Contrib, Sec Nat, Math Biotech Sci 35(1)
Persson E, Henriksson J, Tjälve H (2003) Uptake of cobalt from the nasal mucosa into the brain via olfactory pathways in rats. Toxicol Lett 145(1):19–27
Rakotondrabe F, Ngoupayou JRN, Mfonka Z, Rasolomanana EH, Abolo AJN, Ako AA (2018) Water quality assessment in the Betare-Oya gold mining area (East-Cameroon): multivariate statistical analysis approach. Sci Total Environ 610:831–844
Ramezani A, Goudarzi I, Lashkarboluki T, Ghorbanian MT, Abrari K, Salmani ME (2012) Role of oxidative stress in ethanol-induced neurotoxicity in the developing cerebellum. Iran J Bas Med Sci 4:965–974
Reid IS (2011) Animal sentinels for environmental and public health. Pub Health Rep Supp 126(1):50–57
Sarnat HB (2018) Bernard Sachs Lecture of 2016: timing in morphogenesis and genetic gradients during normal development and in malformations of the nervous system. Pediatr Neurol 83:3–13
Sergaki MC, Ibáñez CF (2017) GFRα1 regulates Purkinje cell migration by counteracting NCAM functions. Cell Rep 18:367–379
Stephen C, Duncan C (2017) Can wildlife surveillance contribute to public health preparedness for climate change? A Canadian perspective. Clim Chang 141(2):259–271
Steuerwald AJ, Blaisdell FS, Geraghty CM, Parsons PJ (2014) Regional distribution and accumulation of lead in caprine brain tissues following a long-term oral dosing regimen. J Toxicol Environ Health 77:663–678
Talha KB (2012) Nigeria’s lead poisoning crisis could leave a long legacy. Lancet 379(9818):792
Tan LC, Nancharaiah YV, van Hullebusch ED, Lens PN (2018) Selenium: environmental significance, pollution, and biological treatment technologies. In Anaerobic treatment of mine wastewater for the removal of selenate and its co-contaminants. CRC Press, pp 9–71
Thompson J, Bannigan J (2008) Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 25:304–315
Tirima S, Bartrem C, von Lindern I, von Braun M, Lind D, Anka SM, Abdullahi A (2018) Food contamination as a pathway for lead exposure in children during the 2010–2013 lead poisoning epidemics in Zamfara, Nigeria. J Environ Sci 67:260–272
Tjalve H, Henriksson J (1999) Uptake of metals in the brain via olfactory pathways. Neurotoxicology 20:181–195
Toscano C, Guilarte TR (2005) Lead neurotoxicity: from exposure to molecular effects. Brain Res Rev 49:529–554
Tsuchiya K (1992) The discovery of the causal agent of Minamata disease. Am J Ind Med 21:275–280
United State Environmental Protection Agency EPA (2010) An introduction to indoor air quality. U.S. Environmental Protection Agency. www.epa.gov/iaq/lead.html
Valko M, Jomova K, Rhodes CJ, Kuča K, Musílek K (2016) Redox-and non-redox-metal-induced formation of free radicals and their role in human disease. Arch Toxicol 90(1):1–37
Weglarzy K (2010) Effect of lead, cadmium, copper and zinc content in soil on their deposition in pastures as well as in products and tissues of the cows grazed on pasture. J Food Agric Environ 8:1209–1217
World Health Organization (WHO) (2010) Environmental Health Criteria 165: inorganic lead, Geneva. International Programme on Chemical Safety; World Health Organization: Geneva
Yanping S, Jinfa H, Xiongwei N, Jianping X, Jiajia R (2016) Sources and accumulation risk of heavy metal in major animal manure. Anim Husb Feed Sci 8(6):318–326
Zahran MA, El Amier YA, Elnaggar AA, Abd El Azim H, ElAlfy MA (2015) Assessment and distribution of heavy metals pollutants in Manzala Lake, Egypt. J Geosci Environ Prot 3:107–122
Zhang Q, Zhang L, Xiao X, Su Z, Zou P, Hu H, Huang Y, He QY (2010) Heavy metals chromium and neodymium reduced phosphorylation level of heat shock protein 27 in human keratinocytes. Toxicol In Vitro 24(4):1098–1104
Acknowledgements
We wish to acknowledge the assistance of the Ministry of Agriculture and Natural resources of Zamfara State and the Anka Emirate Council for the logistics support for sample collection.
Funding
This study received funding from the Centre of Control and Prevention of Zoonosis of the University of Ibadan and the International Society for Neurochemistry (ISN).
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Jubril, A.J., Obasa, A.A., Mohammed, S.A. et al. Neuropathological lesions in the brains of goats in North-Western Nigeria: possible impact of artisanal mining. Environ Sci Pollut Res 26, 36589–36597 (2019). https://doi.org/10.1007/s11356-019-06611-y
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DOI: https://doi.org/10.1007/s11356-019-06611-y