Abstract
Pollution by heavy metals is a threat to public health because of the adverse effects on multiple organ systems including the brain. Here, we used the African giant rat (AGR) as a novel sentinel host to assess the effect of heavy metal accumulation and consequential neuropathology upon the brain. For this study, AGR were collected from distinct geographical regions of Nigeria: the rain forest region of south-west Nigeria (Ibadan), the central north of Nigeria (Abuja), and in oil-polluted areas of south Nigeria (Port-Harcourt). We found that zinc, copper, and iron were the major heavy metals that accumulated in the brain and serum of sentinel AGR, with the level of iron highest in animals from Port-Harcourt and least in animals from Abuja. Brain pathology, determined by immunohistochemistry markers of inflammation and oxidative stress, was most severe in animals from Port Harcourt followed by those from Abuja and those from Ibadan were the least affected. The brain pathologies were characterized by elevated brain advanced oxidation protein product (AOPP) levels, neuronal depletion in the prefrontal cortex, severe reactive astrogliosis in the hippocampus and cerebellar white matter, demyelination in the subcortical white matter and cerebellar white matter, and tauopathies. Selective vulnerabilities of different brain regions to heavy metal pollution in the AGR collected from the different regions of the country were evident. In conclusion, we propose that neuropathologies associated with redox dyshomeostasis because of environmental pollution may be localized and contextual, even in a heavily polluted environment. This novel study also highlights African giant rats as suitable epidemiological sentinels for use in ecotoxicological studies.
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References
Adamo AM, Zago MP, Mackenzie GG, Aimo L, Keen CL, Keenan A, Oteiza PI (2010) The role of zinc in the modulation of neuronal proliferation and apoptosis. Neurotox Res 17:1–14. https://doi.org/10.1007/s12640-009-9067-4
Agrawal S, Berggren KL, Marks E, Fox JH (2017) Impact of high iron intake on cognition and neurodegeneration in humans and in animal models: a systematic review. Nutr Rev 75(6):456–470. https://doi.org/10.1093/nutrit/nux015
Aizenman E, Mastroberardino PG (2015) Metals and neurodegeneration. Neurobiol Dis 81:1–3. https://doi.org/10.1016/j.nbd.2015.08.012
Ajayi SS (1977) Field observations on the African giant rat (Cricetomys gambianus Waterhouse) in southern Nigeria. Afr J Ecol 15(3):191–198. https://doi.org/10.1111/j.1365-2028.1977.tb00397.x
Akinrinde AS, Oyagbemi AA, Omobowale TO, Asenuga ER, Ajibade TO (2016) Alterations in blood pressure, antioxidant status and caspase 8 expression in cobalt chloride-induced cardio-renal dysfunction are reversed by Ocimum gratissimum and gallic acid in Wistar rats. J Trace Elem Med Biol 36:27–37. https://doi.org/10.1016/j.jtemb.2016.03.015
Anand KS, Dhikav V (2012) Hippocampus in health and disease: An overview. Ann Indian Acad Neur 15(4):239–246. https://doi.org/10.4103/0972-2327.104323
Andreini C, Bertini I (2012) A bioinformatics view of zinc enzymes. J Inorg Biochem 111:150–156. https://doi.org/10.1016/j.jinorgbio.2011.11.020
Anyanwu BO, Ezejiofor AN, Igweze ZN, Orisakwe OE (2018) Heavy Metal Mixture Exposure and Effects in Developing Nations: An Update. Toxics 6(4):65. https://doi.org/10.3390/toxics6040065
Azeez IA, Olopade F, Laperchia C, Andrioli A, Scambi I, Onwuka SK, Bentivoglio M, Olopade JO (2016) Regional myelin and axon damage and neuroinflammation in the adult mouse brain after long-term postnatal vanadium exposure. J Neuropathol Exp Neurol 75(9):843–854. https://doi.org/10.1093/jnen/nlw058
Bagheri S, Saboury AA, Haertlé T, Rongioletti M, Saso L (2022) Probable reasons for neuron copper deficiency in the brain of patients with Alzheimer’s disease: the complex role of amyloid. Inorganics 10(1):6. https://doi.org/10.3390/inorganics10010006
Bagheri S, Squitti R, Haertlé T, Siotto M, Saboury AA (2018) Role of copper in the onset of Alzheimer’s disease compared to other metals. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2017.00446
Barnham KJ, Bush AI (2008) Metals in Alzheimer’s and Parkinson’s diseases. Curr Opin Chem Biol 12:222–228. https://doi.org/10.1016/j.cbpa.2008.02.019
Bhutto M, Ahmed M, Parveen Z, Riazuddin M (2006) Determination of heavy and essential metals in different wheat varieties grown in three districts of Sindh (Pakistan). Int J Agric Biol 8(4):448–449
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. The World Allergy Organ J 5(1):9–19. https://doi.org/10.1097/WOX.0b013e3182439613
Briffa J, Sinagra E, Blundell R (2020) Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon. https://doi.org/10.1016/j.heliyon.2020.e04691
Brown GM (2013) Economic history and development of Port Harcourt, 1912-2003: an analysis. IOSR Journal of Business and Management (IOSR-JBM) 13(6):86–95
Bush AI (2013) The metal theory of Alzheimers disease. J Alzheimers Dis 33(Suppl 1):S277–S281. https://doi.org/10.3233/JAD-2012-129011
Bush AI, Tanzi RE (2008) Therapeutics for Alzheimers disease based on the metal hypothesis. Neurotherapeutics 5:421–432
Calderón-Garcidueñas L, Azzarelli B, Acuna H, Garcia R, Gambling TM, Osnaya N, Monroy S, DEL Tizapantzi MR, Carson JL, Villarreal-Calderon A, Rewcastle B (2002) Air pollution and brain damage. Toxicol Pathol. 30(3):373–389. https://doi.org/10.1080/01926230252929954
Chorin E, Vinograd O, Fleidervish I, Gilad D, Herrmann S, Sekler I, Aizenman E, Hershfinkel M (2011) Upregulation of KCC2 activity by zinc-mediated neurotransmission via the mZnR/GPR39 receptor. J Neurosci 31(36):12916–12926. https://doi.org/10.1523/JNEUROSCI.2205-11.2011
Evans J, Hastings L (1992) Accumulation of Cd(II) in the CNS depending on the route of administration: intraperitoneal, intratracheal, or intranasal. Fundam Appl Toxicol 19(2):275–278. https://doi.org/10.1016/0272-0590(92)90161-a
Farias S, Casa V, Vázquez C, Ferpozzi L, Pucci G, Cohen I (2003) Natural contamination with arsenic and other trace elements in ground waters of Argentine Pampean Plain. Sci Total Environ 309(1):187–199
Farombi EO, Tahnteng JG, Agboola AO, Nwanko JO, Emerole GO (2000) Chemoprevention of 2 acetylaminofluorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron a Garcina kola seed extract. Food Chem Toxicol 38:353–541. https://doi.org/10.1016/s0278-6915(00)00039-9
Femi-Akinlosotu OM, Olopade FE, Obiako J, Olopade JO, Shokunbi MT (2023) Vanadium improves memory and spatial learning and protects the pyramidal cells of the hippocampus in juvenile hydrocephalic mice. Front Neurol 14:1116727. https://doi.org/10.3389/fneur.2023.1116727
Fennell CW, Lindsey KL, McGaw LJ, Sparg SG, Stafford GI, Elgorashi EE et al (2004) Assessing African medicinal plants for efficacy and safety: Pharmacological screening and toxicology. J Ethnopharmacol 94:205–217. https://doi.org/10.1016/j.jep.2004.05.012
Folarin OR, Adaramoye OA, Akanni OO, Olopade JO (2018) Changes in the brain antioxidant profile after chronic vanadium administration in mice. Metab Brain Dis 33(2):377–385. https://doi.org/10.1007/s11011-017-0070-9
Folarin OR, Olopade FE, Olopade JO (2021) essential metals in the brain and the application of laser ablation-inductively coupled plasma-mass spectrometry for their detection. Niger J Physiol Sci 36(2):123–147. https://doi.org/10.54548/njps.v36i2.1
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 Neuroanat 11:58. https://doi.org/10.3389/fnana.2017.00058
Fourchard L (2003) Understanding slums: case studies for the global report on human settlements. In: Urban slums reports. Institut Francais de Recherche en Afrique (IFRA), University of Ibadan. pp 27 http://www.ucl.ac.uk/dpuprojects/Global_Report/pdfs/Ibadan.pdf. Accessed 5 Oct 2023
Garza-Lombó C, Posadas Y, Quintanar L, Gonsebatt ME, Franco R (2018) Neurotoxicity linked to dysfunctional metal ion homeostasis and xenobiotic metal exposure: redox signaling and oxidative stress. Antioxid Redox Signal 28(18):16069–11703. https://doi.org/10.1089/ars.2017.7272
Gebremedhin S, Enquselassie F, Umeta M (2011) Prevalence of prenatal zinc deficiency and its association with socio-demographic, dietary and health care related factors in rural Sidama, southern Ethiopia: a cross-sectional study. BMC Public Health 11:898. https://doi.org/10.1186/1471-2458-11-898
Gensel JC, Kigerl KA, Mandrekar-Colucci SS, Gaudet AD, Popovich PG (2012) Achieving CNS axon regeneration by manipulating convergent neuro-immune signaling. Cell Tissue Res 349:201–213. https://doi.org/10.1007/s00441-012-1425-5
Grabrucker AM, Knight MJ, Proepper C, Bockmann J, Joubert M, Rowan M, Nienhaus GU, Garner CC, Bowie JU, Kreutz MR, Gundelfinger ED, Boeckers TM (2011) Concerted action of zinc and ProSAP/Shank in synaptogenesis and synapse maturation. EMBO J 30(3):569–581. https://doi.org/10.1038/emboj.2010.336
Haywood S (2019) Brain–barrier regulation, metal (Cu, Fe) dyshomeostasis, and neurodegenerative disorders in man and animals. Inorganics 7(9):108. https://doi.org/10.3390/inorganics7090108
Henriksson J, Tallkvist J, Tjälve H (1999) Transport of manganese via olfactory pathway in rats: dosage dependency of the uptake and subcellular distribution of the metal in the olfactory epithelium and the brain. Toxicol Appl Pharmacol 156:119–128
Henriksson J, Tjälve H (2000) Manganese taken up into the CNS via the olfactory pathway in rats affects astrocytes. Toxicol Sci 55(2):392–398. https://doi.org/10.1093/toxsci/55.2.392
Hosseini NS, Sobhanardakani S, Cheraghi M, Lorestani B, Merrikhpour H (2020) Heavy metal concentrations in roadside plants (Achillea wilhelmsii and Cardaria draba) and soils along some highways in Hamedan, west of Iran. Environ Sci Pollut Res Int 27(12):13301–13314. https://doi.org/10.1007/s11356-020-07874-6
Hosseini SV, Sobhanardakani S, Kolangi Miandare H, Harsij M, Regenstein JM (2015) Determination of toxic (Pb, Cd) and essential (Zn, Mn) metals in canned tuna fish produced in Iran. J Environ Health Sci Eng 13:59
Igado OO, Olopade JO, Onwuka SK, Onwuka 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
Ikechukwu E (2015) The socio-economic impact of the greater Port Harcourt development project on the residents of the affected areas. Open J Soc Sci 3:82–93. https://doi.org/10.4236/jss.2015.31010
Jan AT, Azam M, Siddiqui K, Ali A, Choi I, Haq QM (2015) Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. Int J Mol Sci 16(12):29592–29630. https://doi.org/10.3390/ijms161226183
Jan HH, Chen IT, Tsai YY, Chang YC (2002) Structural role of zinc ions bound to postsynaptic densities. J Neurochem 83(3):525–534. https://doi.org/10.1046/j.1471-4159.2002.01093.x
Jomova K, Vondrakova D, Lawson M, Valko M (2010) Metals, oxidative stress and neurodegenerative disorders. Mol Cell Biochem 345(1-2):91–104. https://doi.org/10.1007/s11010-010-0563-x
Jubril AJ, Ayotunde ES, Adewole AA, Adekunle LA (2020) Tissue lead and cadmium levels and associated haematological changes in goats slaughtered at The Bodija Abattoir, Ibadan. Turk J Agric - Food Sci Tech 8(11):2277–2285
Jubril AJ, Obasa AA, Mohammed SA, Olopade JO, Taiwo VO (2019) Neuropathological lesions in the brains of goats in North-Western Nigeria: possible impact of artisanal mining. Environ Sci Pollut Res Int 26(36):36589–36597. https://doi.org/10.1007/s11356-019-06611-y
Katerji M, Filippova M, Duerksen-Hughes P (2019) Approaches and methods to measure oxidative stress in clinical samples: research applications in the cancer field. Oxid Med Cell Longev 2019:1279250. https://doi.org/10.1155/2019/1279250
Kayali R, Cakatay U, Akcay T, Altug T (2006) Effect of alpha-lipoic acid supplementation on markers of protein oxidation in post-mitotic tissues of ageing rat. Cell Biochem Funct 24:79–85. https://doi.org/10.1002/cbf.1190
Kim YS, Kim SS, Cho JJ, Choi DH, Hwang O, Shin DH et al (2005) Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J Neurosci 25:3701–3711. https://doi.org/10.1523/JNeurosci.4346-04.2005
Kozlowski H, Janicka-Klos A, Brasun J, Gaggelli E, Valensin D, Valensin G (2009) Copper, iron, and zinc ions homeostasis and their role in neurodegenerative disorders (metal uptake, transport, distribution and regulation). Coord Chem Rev 253(21–22):2665–2685. https://doi.org/10.1016/j.ccr.2009.05.011
Kozlowski H, Luczkowski M, Remelli M, Valensin D, Valensin D (2012) Copper, zinc and iron in neurodegenerative diseases (Alzheimer’s, Parkinson’s and prion diseases). Coord Chem Rev 256(19-20):2129–2141. https://doi.org/10.1016/j.ccr.2012.03.013
Krall RF, Tzounopoulos T, Aizenman E (2021) The function and regulation of zinc in the brain. Neuroscience 457:235–258. https://doi.org/10.1016/j.neuroscience.2021.01.010
Li Y, Jiao Q, Xu H, Du X, Shi L, Jia F, Jiang H (2017) Biometal dyshomeostasis and toxic metal accumulations in the development of Alzheimer's disease. Front Mol Neurosci 10:339. https://doi.org/10.3389/fnmol.2017.00339
Liuzzi JP, Cousins RJ (2004) Mammalian zinc transporters. Annu Rev Nutr 24:151–172. https://doi.org/10.1146/annurev.nutr.24.012003.132402
Lutsenko S, Washington-Hughes C, Ralle M, Schmidt K (2019) Copper and the brain noradrenergic system. J Biol Inorg Chem 24(8):1179–1188. https://doi.org/10.1007/s00775-019-01737-3
Mahoney A, Weetjens B, Cox C, Beyene N, Reither K, Makingi G, Jubitana M, Kazwala R, Mfinanga GS, Kahwa A, Durgin A, Poling A (2012) Pouched rats detection of tuberculosis in human sputum: Comparison to culturing and polymerase chain reaction. Tuberc Res Treat. https://doi.org/10.1155/2012/716989
Maina MB, Al-Hilaly YK, Serpell LC (2016) Nuclear Tau and its potential role in Alzheimer's disease. Biomolecules 6(1):9. https://doi.org/10.3390/biom6010009
Marrocco I, Altieri F, Peluso I (2017) Measurement and clinical significance of biomarkers of oxidative stress in humans. Oxid Med Cell Longev 2017:6501046. https://doi.org/10.1155/2017/6501046
McCord JM (2000) The evolution of free radicals and oxidative stress. Am J Med 108(8):652–659
Mocchegiani E, Giacconi R, Cipriano C, Muzzioli M, Fattoretti P, Bertoni-Freddari C, Isani G, Zambenedetti P, Zatta P (2001) Zinc-bound metallothioneins as potential biological markers of ageing. Brain Res Bull 55:147–153. https://doi.org/10.1016/S0361-9230(01)00468-3
Mohammadi MJ, Yari AR, Saghazadeh M, Sobhanardakani S, Geravandi S, Afkar A, Salehi SZ, Valipour A, Biglari H, Hosseini SA, Rastegarimehr B, Vosoughi M, Omidi Khaniabadi Y (2018) A health risk assessment of heavy metals in people consuming Sohan in Qom. Iran. Toxin Rev 37(4):278–286
Moon MY, Kim HJ, Choi BY, Sohn M, Chung TN, Suh SW (2018) Zinc promotes adipose-derived mesenchymal stem cell proliferation and differentiation towards a neuronal fate. Stem Cells Int. https://doi.org/10.1155/2018/5736535
Musilova J, Bystricka J, Lachman J, Harangozo L, Trebichalsky P, Volnova B (2016) Potatoes - A crop resistant against input of heavy metals from the metallicaly contaminated soil. Int J Phytoremediation 18(6):547–552. https://doi.org/10.1080/15226514.2015.1086303
Mustapha OA, Awala-Ajakaiye M, Agbalu B, Bello ST, Olude MA, Olopade JO (2023) Vanadium impairs neuronal cytoarchitecture of the hippocampal trisynaptic loop in the African giant rat (cricetomys gambianus, waterhouse). Nig J Neurosci 14(1):1–9
Mustapha OA, Oke B, Offen N, Siren AL, Olopade JO (2014) Neurobehavioral and cytotoxic effects of vanadium during oligodendrocyte maturation: a protective role for erythropoietin. Environ Toxicol Pharmacol 38(1):98–111. https://doi.org/10.1016/j.etap.2014.05.001
Mustapha OA, Olude MA, Taiwo B, Olopade JO (2019) Cytoarchitecture of the Hippocampal Formation in the African Giant Rat (Cricetomys gambianus, Waterhouse). Nig J Physiol Sci 34:55–62
Myhre O, Utkilen H, Duale N, Brunborg G, Hofer T (2013) Metal dyshomeostasis and inflammation in Alzheimer's and Parkinson's diseases: possible impact of environmental exposures. Oxid Med Cell Longev. https://doi.org/10.1155/2013/726954
Nuttall JR, Oteiza PI (2014) Zinc and the aging brain. Genes Nutr 9(1):379. https://doi.org/10.1007/s12263-013-0379-x
Olaleye SB, Adaramoye OA, Erigbali PP, Adeniyi OS (2007) Lead exposure increases oxidative stress in the gastric mucosa of HCl/ethanol-exposed rats. World J Gastroenterol 13(38):5121–5126. https://doi.org/10.3748/wjg.v13.i38.5121
Olaolorun FA, Olopade FE, Usende IL, Lijoka AD, Ladagu AD, Olopade JO (2021) Neurotoxicity of vanadium. Advances in Neurotoxicology 5:299–327. https://doi.org/10.1016/bs.ant.2021.01.002
Olopade JO, Adejumo DO, Ladokun AO, Okandeji ME, Adeshina AA, Onwuka SK (2006) Cortical concentrations of metals and protein in the brain of two breeds of goats in Nigeria. Afr J Biomed Res 8(3):191–196
Olude MA, Mouihate A, Mustapha OA, Farina C, Quintana FJ, Olopade JO (2022) Astrocytes and microglia in stress-induced neuroinflammation: the African perspective. Front Immunol 13:795089. https://doi.org/10.3389/fimmu.2022.795089
Olude MA, Ogunbunmi TK, Olopade JO, Ihunwo AO (2014a) The olfactory bulb structure of African giant rat (Cricetomys gambianus, waterhouse 1840) I: cytoarchitecture. Anat Sci Int 89(4):224–231. https://doi.org/10.1007/s12565-014-0227-0
Olude MA, Olopade JO, Ihunwo AO (2014b) Adult neurogenesis in the African giant rat (Cricetomys gambianus, Waterhouse). Metab Brain Dis 29(3):857–866. https://doi.org/10.1007/s11011-014-9512-9
Osibanjo O, Daso AP, Gbadebo AM (2011) The impact of industries on surface water quality of River Ona and River Alaro in Oluyole Industrial Estate, Ibadan, Nigeria. Afr J Biotech 10:696–702
Oteiza PI (2012) Zinc and the modulation of redox homeostasis. Free Radic Biol Med 53(9):1748–1759. https://doi.org/10.1016/j.freeradbiomed.2012.08.568
Owonikoko M, Emikpe B, Olaleye S (2021) Standardized experimental model for cement dust exposure; tissue heavy metal bioaccumulation and pulmonary pathological changes in rats. Toxicol Rep 8:1169–1178
Oyagbemi AA, Omobowale TO, Asenuga ER, Adejumobi AO, Ajibade TO, Ige TM et al (2016) Sodium fluoride induces hypertension and cardiac complications through generation of reactive oxygen species and activation of nuclear factor Kappa Beta. Environ Toxicol 32:1089–1101. https://doi.org/10.1002/tox.22306
Pal A, Prasad R (2016) Regional distribution of copper, zinc and iron in brain of wistar rat model for non-Wilsonian brain copper toxicosis. Indian J Clin Biochem 31(1):93–98. https://doi.org/10.1007/s12291-015-0503-3
Pfeiffer CC, Braverman ER (1982) Zinc, the brain and behavior. Biol Psychiatry 17(4):513–532
Poling A, Amanda M, Negussie B, Georgies M, Weetjens B, Cox C, Durgin A (2015) Using giant African pouched rats to detect human tuberculosis: a review. Pan Afr Med J 21:333. https://doi.org/10.11604/pamj.2015.21.333.2977
Portbury SD, Adlard PA (2017) Zinc Signal in Brain Diseases. Int J Mol Sci 18(12):2506. https://doi.org/10.3390/ijms18122506
Public Health Service (PHS) (1996) Public health service policy on humane care and the use of laboratory animals. US Department of Health and Humane Services, Washington, DC, pp 99–158
Rink C, Khanna S (2011) Significance of brain tissue oxygenation and the arachidonic acid cascade in stroke. Antioxid Redox Signal 14(10):1889–1903. https://doi.org/10.1089/ars.2010.3474
Rojas-Lemus M, Bizarro-Nevares P, López-Valdez N, González-Villalva A, Guerrero-Palomo G, Cervantes-Valencia ME, Tavera-Cabrera O, Rivera-Fernández N, Casarrubias-Tabarez B, Ustarroz-Cano M, Rodríguez-Zepeda A, Pasos-Nájera F, Goes TFD (2020) Oxidative stress and vanadium. In: Soloneski S, Larramendy ML (eds) Genotoxicity and mutagenicity - mechanisms and test methods. IntechOpen. https://doi.org/10.5772/intechopen.90861
Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590
Sharif R, Thomas P, Zalewski P, Fenech M (2012) The role of zinc in genomic stability. Mutat Res 733(1–2):111–121. https://doi.org/10.1016/j.mrfmmm.2011.08.009
Sobhanardakani S (2017) Potential health risk assessment of heavy metals via consumption of caviar of Persian sturgeon. Mar Pollut Bull 123(1-2):34–38. https://doi.org/10.1016/j.marpolbul.2017.09.033
Sobhanardakani S (2018) Human health risk assessment of potentially toxic heavy metals in the atmospheric dust of city of Hamedan, west of Iran. Environ Sci Pollut Res 25(28):28086–28093
Szewczyk B (2013) Zinc homeostasis and neurodegenerative disorders. Front Aging Neurosci 5:33. https://doi.org/10.3389/fnagi.2013.00033
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. In: Luch A (ed) Molecular, clinical and environmental toxicology. Experientia supplementum 101. Springer, Basel. https://doi.org/10.1007/978-3-7643-8340-4_6
Therond P (2006) Oxidative stress and damages to biomolecules (lipids, proteins, DNA). Annales Pharmaceutiques Françaises 64(6):383–389. https://doi.org/10.1016/s0003-4509(06)75333-0
Tjälve H, Mejàre C, Borg-Neczak K (1995) Uptake and transport of manganese in primary and secondary olfactory neurones in pike. Pharmacol Toxicol 77:23–31. https://doi.org/10.1111/j.1600-0773.1995.tb01909.x
Tjälve H, Henriksson J, Tallkvist J, Larsson BS, Lindquist NG (1996) Uptake of manganese and cadmium from the nasal mucosa into the central nervous system via olfactory pathways in rats. Pharm Toxicol 79(6):347–356. https://doi.org/10.1111/j.1600-0773.1996.tb00021.x
Usende IL, Alimba CG, Emikpe BO, Bakare AA, Olopade JO (2018) Intraperitoneal sodium metavanadate exposure induced severe clinicopathological alterations, hepato-renal toxicity and cytogenotoxicity in African giant rats (Cricetomys gambianus, Waterhouse, 1840). Environ Sci Pollut Res Int 25(26):26383–26393. https://doi.org/10.1007/s11356-018-2588-8
Usende IL, Emikpe BO, Olopade JO (2017) Heavy metal pollutants in selected organs of African giant rats from three agro-ecological zones of Nigeria: evidence for their role as an environmental specimen bank. Environ Sci Pollut Res Int 24(28):22570–22578. https://doi.org/10.1007/s11356-017-9904-6
Usende IL, Leitner DF, Neely E, Connor JR, Olopade JO (2016) The deterioration seen in myelin related morphophysiology in vanadium exposed rats is partially protected by concurrent iron deficiency. Nig J Physiol Sci 31(1):11–22
Vassalle C (2008) An easy and reliable automated method to estimate oxidative stress in the clinical setting. Methods Mol Biol 477:31–39. https://doi.org/10.1007/978-1-60327-517-0_3
Veglia F, Cavalca V, Tremoli E (2010) OXY-SCORE: a global index to improve evaluation of oxidative stress by combining pro- and antioxidant markers. Methods Mol Biol 594:197–213. https://doi.org/10.1007/978-1-60761-411-1_14
Walsh TJ, Emerich DF (1988) The hippocampus as a common target of neurotoxic agents. Toxicology 49(1):137–140. https://doi.org/10.1016/0300-483x(88)90185-0
Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) The role of iron in brain ageing and neurodegenerative disorders. The Lancet Neurol 13(10):1045–1060. https://doi.org/10.1016/S1474-4422(14)70117-6
Wolfe MS (2012) The role of tau in neurodegenerative diseases and its potential as a therapeutic target. Scientifica. https://doi.org/10.6064/2012/796024
Wolff SP (1994) Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods Enzymol 233:182–189
Xia Y, Zweier JL (1997) Measurement of myeloperoxidase in leukocyte-containing tissues. Anal Biochem 245:93–96. https://doi.org/10.1006/abio.1996.9940
Xiong DW, Fang T, Chen XD, Sima XF, Zhu WT (2010) Oxidative stress effects and damage of nanoscale TiO2 and ZnO on zebrafish. Huan Jing Ke Xue 31(5):1320–1327
Xu J, Church SJ, Patassini S, Begley P, Waldvogel HJ, Curtis MA, Faull RLM, Unwin RD, Cooper GJS (2017) Evidence for widespread, severe brain copper deficiency in Alzheimer's dementia. Metallomics 9(8):1106–1119. https://doi.org/10.1039/c7mt00074j
Yassine HN, Self W, Kerman BE, Santoni G, Navalpur Shanmugam N, Abdullah L, Golden LR, Fonteh AN, Harrington MG, Gräff J, Gibson GE, Kalaria R, Luchsinger JA, Feldman HH, Swerdlow RH, Johnson LA, Albensi BC, Zlokovic BV, Tanzi R et al (2022) Nutritional metabolism and cerebral bioenergetics in Alzheimer's disease and related dementias. Alzheimers Dement. https://doi.org/10.1002/alz.12845.10.1002/alz.12845
Zheng W, Monnot AD (2012) Regulation of brain iron and copper homeostasis by brain barrier systems: implication in neurodegenerative diseases. Pharmacol Ther 133(2):177–188. https://doi.org/10.1016/j.pharmthera.2011.10.006
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We acknowledge funding from the Cambridge-Africa Alborada Research Fund (Grant Number G109329).
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Conceptualization: James Olukayode Olopade, Raymond Bujdoso; methodology: Olanrewaju Ifeoluwa Fatola, Ighorodje Ejiro, Olubusayo Rachael Folarin, Funmilayo Eniola Olopade, Adedunsola Ajike Obasa, Ademola Adetokunbo Oyagbemi, Irene Chizubelu Omile, Alana Thackray; formal analysis and investigation: James Olukayode Olopade, Oluwaseun Ahmed Mustapha; writing—original draft preparation: Alana Thackray, Oluwaseun Ahmed Mustapha, James Olukayode Olopade, Raymond Bujdoso; writing—review and editing: James Olukayode Olopade, Matthew Ayokunle Olude, Raymond Bujdoso; funding acquisition: James Olukayode Olopade, Raymond Bujdoso; supervision: James Olukayode Olopade, Matthew Ayokunle Olude, Funmilayo Eniola Olopade
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Ethical approval was obtained from University of Ibadan Animal Care and Use in Research Committee with an approval number of UI-ACUREC/18/0059.
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Olopade, J.O., Mustapha, O.A., Fatola, O.I. et al. Neuropathological profile of the African Giant Rat brain (Cricetomys gambianus) after natural exposure to heavy metal environmental pollution in the Nigerian Niger Delta. Environ Sci Pollut Res 30, 120496–120514 (2023). https://doi.org/10.1007/s11356-023-30619-0
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DOI: https://doi.org/10.1007/s11356-023-30619-0