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Neuropathological lesions in the brains of goats in North-Western Nigeria: possible impact of artisanal mining

  • Afusat J. Jubril
  • Adedunsola A. Obasa
  • Shehu A. Mohammed
  • James O. OlopadeEmail author
  • Victor O. Taiwo
Research Article
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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.

Keywords

Brain pathology Goats Lead Cadmium Mining 

Notes

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 information

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).

References

  1. 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 4:397–400CrossRefGoogle Scholar
  2. Ahmed RG, Walaa GH, Asmaa FS (2018) Suppressive effects of neonatal bisphenol A on the neuroendocrine system. Toxicol Ind Health 34(6):397–407CrossRefGoogle Scholar
  3. Anetor JI (2012) Rising environmental cadmium levels in developing countries: threat to genome stability and health. Environ Anal Toxicol 2:140Google Scholar
  4. Argos M, Ahsan H, Raziano JH (2012) Arsenic and human health: epidemiologic progress and public health implications. Rev Environ Health 27(4):191–195CrossRefGoogle Scholar
  5. 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 617:94–100Google Scholar
  6. 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):51CrossRefGoogle Scholar
  7. 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 542:908–914CrossRefGoogle Scholar
  8. 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):323–332CrossRefGoogle Scholar
  9. 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):819–833CrossRefGoogle Scholar
  10. 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 184:5097–5104CrossRefGoogle Scholar
  11. 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 322–332Google Scholar
  12. 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 8:613Google Scholar
  13. 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, ChamGoogle Scholar
  14. 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 68:66–72CrossRefGoogle Scholar
  15. 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 ServiceGoogle Scholar
  16. 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 68:297–306CrossRefGoogle Scholar
  17. 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 256:2147–2163CrossRefGoogle Scholar
  18. Corkhill CL, Vaughan DJ (2009) Arsenopyrite oxidation – a review. Appl Geochem 24:2342–2361CrossRefGoogle Scholar
  19. 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)Google Scholar
  20. 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 RepCrossRefGoogle Scholar
  21. 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 160:237–243CrossRefGoogle Scholar
  22. 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):251–262CrossRefGoogle Scholar
  23. 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):e0179233CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 120:601–607CrossRefGoogle Scholar
  26. 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):1123–1132CrossRefGoogle Scholar
  27. 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):55–66CrossRefGoogle Scholar
  28. 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):87–92CrossRefGoogle Scholar
  29. 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):813–822CrossRefGoogle Scholar
  30. 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):2308–2320CrossRefGoogle Scholar
  31. 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 11:58Google Scholar
  32. 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):145–154CrossRefGoogle Scholar
  33. Goyer RA (1993) Lead toxicity: current concerns. Environ Health Perspect 100:177–187CrossRefGoogle Scholar
  34. 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):495–500CrossRefGoogle Scholar
  35. Hammond PB, Aronson AL (1964) Lead poisoning in cattle and horses in the vicinity of a smelter. Ann N Y Acad Sci 111:595–611CrossRefGoogle Scholar
  36. 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. 43-101Google Scholar
  37. Hernández JA, López-Sánchez RC, Rendón-Ramírez A (2016) Lipids and oxidative stress associated with ethanol-induced neurological damage. Oxidative Med Cell Longev 2016Google Scholar
  38. 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 56:94–106CrossRefGoogle Scholar
  39. 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):152CrossRefGoogle Scholar
  40. 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):75–84Google Scholar
  41. 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 11:305–309Google Scholar
  42. 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):159–164Google Scholar
  43. 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):2148–2150Google Scholar
  44. 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):107–113Google Scholar
  45. 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 59:109–116CrossRefGoogle Scholar
  46. Jorgensen SE, Fath B (2008) S2.pdf. In: Encyclopedia of ecology. Elsevier Science, London, pp 3486–3619Google Scholar
  47. 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):11–18Google Scholar
  48. Kaplan O, Yildirim NC, Yildirim N, Cimen M (2011) Toxic elements in animal products and environmental health. Asian J Anim Vet Adv 6:228–232CrossRefGoogle Scholar
  49. 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 48:203–213CrossRefGoogle Scholar
  50. 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):1544–1552CrossRefGoogle Scholar
  51. 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):327–332Google Scholar
  52. 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):789–828CrossRefGoogle Scholar
  53. 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):357–363CrossRefGoogle Scholar
  54. Liu J, Lewis G (2014) Environmental toxicity and poor cognitive outcomes in children and adults. J Environ Health 76(6):130–138Google Scholar
  55. Lucchini RG, Dorman DC, Elder A, Veronesi B (2012) Neurological impacts from inhalation of pollutants and the nose-brain connection. Neurotoxicology 33(4):838–841CrossRefGoogle Scholar
  56. Mahaffey KR (1990) Environmental lead toxicity: nutrition as a component of intervention. Environ Health Perspect 89:75–78CrossRefGoogle Scholar
  57. Manton WI, Cook JD (1984) High accuracy (stable isotope dilution) measurements of lead in serum and cerebrospinal fluid. Br J Ind Med 41(3):313–319Google Scholar
  58. Marçal WS, Gaste L, Ascimento MRL (2005) Identificação e quantificação de chumboemmisturasmineraiscomercializadas no estado de São Paulo. CiencAnim Bras 6:249–253Google Scholar
  59. Médecins sans Frontières MSF-Holland MSF (2010) Lead poisoning crisis in Zamfara state, northern Nigeria. www.msf.org.Reports
  60. 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 37:248–257CrossRefGoogle Scholar
  61. Mombaerts P (2006) Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22:713–737CrossRefGoogle Scholar
  62. 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):183–188Google Scholar
  63. 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):201–211CrossRefGoogle Scholar
  64. 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 26:055–060Google Scholar
  65. 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):1200–1206CrossRefGoogle Scholar
  66. 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)Google Scholar
  67. 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):19–27CrossRefGoogle Scholar
  68. 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 610:831–844CrossRefGoogle Scholar
  69. 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 4:965–974Google Scholar
  70. Reid IS (2011) Animal sentinels for environmental and public health. Pub Health Rep Supp 126(1):50–57Google Scholar
  71. 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 83:3–13CrossRefGoogle Scholar
  72. Sergaki MC, Ibáñez CF (2017) GFRα1 regulates Purkinje cell migration by counteracting NCAM functions. Cell Rep 18:367–379CrossRefGoogle Scholar
  73. Stephen C, Duncan C (2017) Can wildlife surveillance contribute to public health preparedness for climate change? A Canadian perspective. Clim Chang 141(2):259–271CrossRefGoogle Scholar
  74. 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 77:663–678CrossRefGoogle Scholar
  75. Talha KB (2012) Nigeria’s lead poisoning crisis could leave a long legacy. Lancet 379(9818):792CrossRefGoogle Scholar
  76. 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 9–71Google Scholar
  77. Thompson J, Bannigan J (2008) Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 25:304–315CrossRefGoogle Scholar
  78. 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 67:260–272CrossRefGoogle Scholar
  79. Tjalve H, Henriksson J (1999) Uptake of metals in the brain via olfactory pathways. Neurotoxicology 20:181–195Google Scholar
  80. Toscano C, Guilarte TR (2005) Lead neurotoxicity: from exposure to molecular effects. Brain Res Rev 49:529–554CrossRefGoogle Scholar
  81. Tsuchiya K (1992) The discovery of the causal agent of Minamata disease. Am J Ind Med 21:275–280CrossRefGoogle Scholar
  82. United State Environmental Protection Agency EPA (2010) An introduction to indoor air quality. U.S. Environmental Protection Agency. www.epa.gov/iaq/lead.html
  83. 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):1–37CrossRefGoogle Scholar
  84. 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 8:1209–1217Google Scholar
  85. World Health Organization (WHO) (2010) Environmental Health Criteria 165: inorganic lead, Geneva. International Programme on Chemical Safety; World Health Organization: GenevaGoogle Scholar
  86. 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):318–326Google Scholar
  87. 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 3:107–122Google Scholar
  88. 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):1098–1104CrossRefGoogle Scholar

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

Authors and Affiliations

  1. 1.Department of Veterinary PathologyUniversity of IbadanIbadanNigeria
  2. 2.Department of Veterinary AnatomyUniversity of IbadanIbadanNigeria
  3. 3.Department of EnvironmentState Ministry of EnvironmentGusauNigeria

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