Skip to main content

Advertisement

Log in

Evaluation of Cerebellar Function and Integrity of Adult Rats After Long-Term Exposure to Aluminum at Equivalent Urban Region Consumption Concentrations

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

High amounts of aluminum (Al) are found in soil and water. It is highly bioavailable, which makes it an important agent of environmental imbalance. Moreover, Al is considered a neurotoxic agent that is associated with several neurodegenerative diseases. Thus, this study investigated the effects of long-term Al chloride (AlCl3) exposure on motor behavior, oxidative biochemistry, and cerebellar tissue parameters. For this, adult Wistar rats were divided into three groups: Al-D1 (8.3 mg kg−1 day−1), Al-D2 (5.2 mg kg−1 day−1), and control (distilled water); all groups were orally exposed for 60 days by intragastric gavage. After the exposure period, animals performed the open field, elevated plus maze, rotarod, and beam walking tests. Then, the blood and cerebellum were collected to evaluate Al levels and biochemical and morphological analyses, respectively. Our results demonstrate that animals exposed to Al doses presented a higher Al level in the blood. In the spontaneous locomotor activity, Al exposure groups had traveled a lower total distance when compared with the control group. There was no statistically significant difference (p > 0.05) between exposed and control groups when anxiogenic profile, forced locomotion, fine motor coordination/balance, pro-oxidative parameter, and density Purkinje cells were compared. Thus, aluminum exposure in equivalent doses to human consumption in urban regions did not promote significant changes in the cerebellum or motor parameters.

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

Similar content being viewed by others

Availability of Data and Material

The quantitative and qualitative data used to support the findings of this study are included in the article.

References

  1. Gauthier E, Fortier I, Courchesne F, Pepin P, Mortimer J, Gauvreau D (2000) Aluminum forms in drinking water and risk of Alzheimer’s disease. Environ Res 84(3):234–246

    Article  CAS  PubMed  Google Scholar 

  2. Kozlowski H, Brown DR, Valensin G (2007) Metallochemistry of neurodegeneration: biological, chemical and genetic aspects. Royal Society of Chemistry, London

    Google Scholar 

  3. Exley C (2013) Human exposure to aluminium. Environ Sci Process Impacts 15(10):1807–1816

    Article  CAS  PubMed  Google Scholar 

  4. Walton J et al (1995) Uptake of trace amounts of aluminum into the brain from drinking water. Neurotoxicology 16(1):187–190

    CAS  PubMed  Google Scholar 

  5. Yokel RA, McNamara PJ (2001) Aluminium toxicokinetics: an updated minireview. Pharmacol Toxicol 88(4):159–167

    Article  CAS  PubMed  Google Scholar 

  6. Morris G, Puri BK, Frye RE (2017) The putative role of environmental aluminium in the development of chronic neuropathology in adults and children. How strong is the evidence and what could be the mechanisms involved? Metab Brain Dis 32(5):1335–1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Saba K et al (2017) Energetics of excitatory and inhibitory neurotransmission in aluminum chloride model of Alzheimer’s disease: reversal of behavioral and metabolic deficits by Rasa Sindoor. Front Mol Neurosci 10:323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Yokel RA et al (1996) Prevention and treatment of aluminum toxicity including chelation therapy: status and research needs. J Toxicol Environ Health 48(6):667–684

    Article  CAS  PubMed  Google Scholar 

  9. Fernandez-Lorenzo JR et al (1999) Aluminum contents of human milk, cow’s milk, and infant formula. J Pediatr Gastroenterol Nutr 28(3):270–275

    Article  CAS  PubMed  Google Scholar 

  10. Bondy SC (2016) Low levels of aluminum can lead to behavioral and morphological changes associated with Alzheimer’s disease and age-related neurodegeneration. Neurotoxicology 52:222–229

    Article  CAS  PubMed  Google Scholar 

  11. Bondy SC (2014) Prolonged exposure to low levels of aluminum leads to changes associated with brain aging and neurodegeneration. Toxicology 315:1–7

    Article  CAS  PubMed  Google Scholar 

  12. 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):1669–1703

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Julka D, Gill KD (1996) Effect of aluminum on regional brain antioxidant defense status in Wistar rats. Res Exp Med 196(1):187–194

    Article  CAS  Google Scholar 

  14. National Research Council (2011) Guide for the care and use of laboratory animals, vol 246, eighth edn. The National Academies Press, Washington, DC

    Google Scholar 

  15. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22(3):659–661

    Article  CAS  PubMed  Google Scholar 

  16. Martinez CS, Escobar AG, Uranga-Ocio JA, Peçanha FM, Vassallo DV, Exley C, Miguel M, Wiggers GA (2017) Aluminum exposure for 60days at human dietary levels impairs spermatogenesis and sperm quality in rats. Reprod Toxicol 73:128–141

    Article  CAS  PubMed  Google Scholar 

  17. Walton JR (2007) A longitudinal study of rats chronically exposed to aluminum at human dietary levels. Neurosci Lett 412(1):29–33

    Article  CAS  PubMed  Google Scholar 

  18. World Health Organization (2003) Aluminium in drinking-water: background document for development of WHO guidelines for drinking-water quality. Geneva, World Health Organization

    Google Scholar 

  19. Belém-Filho IJA, Ribera PC, Nascimento AL, Gomes ARQ, Lima RR, Crespo-Lopez ME, Monteiro MC, Fontes-Júnior EA, Lima MO, Maia CSF (2018) Low doses of methylmercury intoxication solely or associated to ethanol binge drinking induce psychiatric-like disorders in adolescent female rats. Environ Toxicol Pharmacol 60:184–194

    Article  PubMed  CAS  Google Scholar 

  20. Pellow S, File SE (1986) Evidence that the beta-carboline, ZK 91296, can reduce anxiety in animals at doses well below those causing sedation. Brain Res 363(1):174–177

    Article  CAS  PubMed  Google Scholar 

  21. Dunham N, Miya TS (1957) A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharm Assoc Am Pharm Assoc 46(3):208–209

    Article  CAS  PubMed  Google Scholar 

  22. Teixeira FB et al (2014) Evaluation of the effects of chronic intoxication with inorganic mercury on memory and motor control in rats. Int J Environ Res Public Health 11(9):9171–9185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Teixeira FB et al (2018) Exposure to inorganic mercury causes oxidative stress, cell death, and functional deficits in the motor cortex. Front Mol Neurosci 11:125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Amado LL et al (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407(6):2115–2123

    Article  CAS  PubMed  Google Scholar 

  25. Esterbauer H, Cheeseman KH(1990) [42] Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. in Methods Enzymol. Elsevier. 186:407–421

  26. Bittencourt LO, Dionizio A, Nascimento PC, Puty B, Leão LKR, Luz DA, Silva MCF, Amado LL, Leite A, Buzalaf MR, Crespo-Lopez ME, Maia CSF, Lima RR (2019) Proteomic approach underlying the hippocampal neurodegeneration caused by low doses of methylmercury after long-term exposure in adult rats. Metallomics 11(2):390–403

    Article  CAS  PubMed  Google Scholar 

  27. Santana L et al (2019) Low doses of methylmercury exposure during adulthood in rats display oxidative stress, neurodegeneration in the motor cortex and lead to impairment of motor skills. J Trace Elem Med Biol 51:19–27

    Article  CAS  PubMed  Google Scholar 

  28. Freire MAM, Santana LNS, Bittencourt LO, Nascimento PC, Fernandes RM, Leão LKR, Fernandes LMP, Silva MCF, Amado LL, Gomes-Leal W, Crespo-Lopez ME, Maia CSF, Lima RR (2019) Methylmercury intoxication and cortical ischemia: pre-clinical study of their comorbidity. Ecotoxicol Environ Saf 174:557–565

    Article  CAS  PubMed  Google Scholar 

  29. Teixeira FB, Leão LKR, Bittencourt LO, Aragão WAB, Nascimento PC, Luz DA, Braga DV, Silva MCF, Oliveira KRM, Herculano AM, Maia CSF, Lima RR (2019) Neurochemical dysfunction in motor cortex and hippocampus impairs the behavioral performance of rats chronically exposed to inorganic mercury. J Trace Elem Med Biol 52:143–150

    Article  CAS  PubMed  Google Scholar 

  30. Corrêa MG, Bittencourt LO, Nascimento PC, Ferreira RO, Aragão WAB, Silva MCF, Gomes-Leal W, Fernandes MS, Dionizio A, Buzalaf MR, Crespo-Lopez ME, Lima RR (2020) Spinal cord neurodegeneration after inorganic mercury long-term exposure in adult rats: ultrastructural, proteomic and biochemical damages associated with reduced neuronal density. Ecotoxicol Environ Saf 191:110159

    Article  PubMed  CAS  Google Scholar 

  31. Aragão WAB et al (2018) Hippocampal dysfunction provoked by mercury chloride exposure: evaluation of cognitive impairment, oxidative stress, tissue injury and nature of cell death. Oxid Med Cell Longev 2018:7878050

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. da Silva DRF, Bittencourt LO, Aragão WAB, Nascimento PC, Leão LKR, Oliveira ACA, Crespo-López ME, Lima RR (2020) Long-term exposure to lead reduces antioxidant capacity and triggers motor neurons degeneration and demyelination in spinal cord of adult rats. Ecotoxicol Environ Saf 194:110358

    Article  PubMed  CAS  Google Scholar 

  33. Leão LKR, Bittencourt LO, Oliveira AC, Nascimento PC, Miranda GHN, Ferreira RO, Nabiça M, Dantas K, Dionizio A, Cartágenes S, Buzalaf MAR, Crespo-Lopez ME, Maia CSF, Lima RR (2020) Long-term Lead exposure since adolescence causes proteomic and morphological alterations in the cerebellum associated with motor deficits in adult rats. Int J Mol Sci 21(10):3571

    Article  PubMed Central  CAS  Google Scholar 

  34. Silva AF et al (2013) Hippocampal neuronal loss, decreased GFAP immunoreactivity and cognitive impairment following experimental intoxication of rats with aluminum citrate. Brain Res 1491:23–33

    Article  CAS  PubMed  Google Scholar 

  35. Berniker M, Kording K (2009) Bayesian models of motor control. In: Encyclopedia of neuroscience, vol 2. Elsevier, Amsterdam, pp 127–133

    Chapter  Google Scholar 

  36. d'Avella A, Lacquaniti F (2013) Control of reaching movements by muscle synergy combinations. Front Comput Neurosci 7:42

    Article  PubMed  PubMed Central  Google Scholar 

  37. Schalow G, Zäch GA (2000) Reorganization of the human central nervous system. Gen Physiol Biophys 19(Suppl 1):11–240

    PubMed  Google Scholar 

  38. Clarac F, Brocard F, Vinay L (2004) The maturation of locomotor networks. Prog Brain Res 143:57–66

    Article  PubMed  Google Scholar 

  39. Goulding M (2009) Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 10(7):507–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kiehn O (2016) Decoding the organization of spinal circuits that control locomotion. Nat Rev Neurosci 17(4):224–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lacquaniti F, Ivanenko YP, Zago M (2012) Patterned control of human locomotion. J Physiol 590(10):2189–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lima LAO et al (2018) Methylmercury intoxication promotes metallothionein response and cell damage in salivary glands of rats. Biol Trace Elem Res 185(1):135–142

    Article  CAS  PubMed  Google Scholar 

  43. Elsby R, Maggs JL, Ashby J, Park BK (2001) Comparison of the modulatory effects of human and rat liver microsomal metabolism on the estrogenicity of bisphenol a: implications for extrapolation to humans. J Pharmacol Exp Ther 297(1):103–113

    CAS  PubMed  Google Scholar 

  44. Sharma V, McNeill JH (2009) To scale or not to scale: the principles of dose extrapolation. Br J Pharmacol 157(6):907–921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Van der Voet GB, De Wolff FA (1987) The effect of di- and trivalent iron on the intestinal absorption of aluminum in rats. Toxicol Appl Pharmacol 90(2):190–197

    Article  PubMed  Google Scholar 

  46. Sjögren B et al (1985) Exposure and urinary excretion of aluminum during welding. Scand J Work Environ Health 11(1):39–43

    Article  PubMed  Google Scholar 

  47. Provan SD, Yokel RA (1988) Influence of calcium on aluminum accumulation by the rat jejunal slice. Res Commun Chem Pathol Pharmacol 59(1):79–92

    CAS  PubMed  Google Scholar 

  48. Trapp GA (1983) Plasma aluminum is bound to transferrin. Life Sci 33(4):311–316

    Article  CAS  PubMed  Google Scholar 

  49. Akinrinade ID, Memudu AE, Ogundele OM (2015) Fluoride and aluminium disturb neuronal morphology, transport functions, cholinesterase, lysosomal and cell cycle activities. Pathophysiology 22(2):105–115

    Article  CAS  PubMed  Google Scholar 

  50. Yokel RA (2002) Brain uptake, retention, and efflux of aluminum and manganese. Environ Health Perspect 110(Suppl 5):699–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Cunat L, Lanhers MC, Joyeux M, Burnel D (2000) Bioavailability and intestinal absorption of aluminum in rats: effects of aluminum compounds and some dietary constituents. Biol Trace Elem Res 76(1):31–55

    Article  CAS  PubMed  Google Scholar 

  52. Roskams AJ, Connor JR (1990) Aluminum access to the brain: a role for transferrin and its receptor. Proc Natl Acad Sci U S A 87(22):9024–9027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Nagaoka MH, Maitani T (2005) Binding affinity of aluminium to human serum transferrin and effects of carbohydrate chain modification as studied by HPLC/high-resolution ICP-MS--speciation of aluminium in human serum. J Inorg Biochem 99(9):1887–1894

    Article  CAS  PubMed  Google Scholar 

  54. Greger JL, Sutherland JE (1997) Aluminum exposure and metabolism. Crit Rev Clin Lab Sci 34(5):439–474

    Article  CAS  PubMed  Google Scholar 

  55. Martin RB (1986) The chemistry of aluminum as related to biology and medicine. Clin Chem 32(10):1797–1806

    Article  CAS  PubMed  Google Scholar 

  56. Macdonald TL, Martin RB (1988) Aluminum ion in biological systems. Trends Biochem Sci 13(1):15–19

    Article  CAS  PubMed  Google Scholar 

  57. Birchall JD, Chappell JS (1988) The chemistry of aluminum and silicon in relation to Alzheimer’s disease. Clin Chem 34(2):265–267

    Article  CAS  PubMed  Google Scholar 

  58. Meiri H, Banin E, Roll M (1991) Aluminum ingestion—is it related to dementia? Rev Environ Health 9(4):191–205

    Article  CAS  PubMed  Google Scholar 

  59. Kawahara M, Kato M, Kuroda Y (2001) Effects of aluminum on the neurotoxicity of primary cultured neurons and on the aggregation of beta-amyloid protein. Brain Res Bull 55(2):211–217

    Article  CAS  PubMed  Google Scholar 

  60. Yokel RA (2000) The toxicology of aluminum in the brain: a review. Neurotoxicology 21(5):813–828

    CAS  PubMed  Google Scholar 

  61. Zatta P, ibn-Lkhayat-Idrissi M, Zambenedetti P, Kilyen M, Kiss T (2002) In vivo and in vitro effects of aluminum on the activity of mouse brain acetylcholinesterase. Brain Res Bull 59(1):41–45

    Article  CAS  PubMed  Google Scholar 

  62. Kihira T, Yoshida S, Komoto J, Wakayama I, Yase Y (1995) Aluminum-induced model of motor neuron degeneration: subperineurial injection of aluminum in rabbits. Neurotoxicology 16(3):413–424

    CAS  PubMed  Google Scholar 

  63. Martinez CS, Vera G, Ocio JAU, Peçanha FM, Vassallo DV, Miguel M, Wiggers GA (2018) Aluminum exposure for 60 days at an equivalent human dietary level promotes peripheral dysfunction in rats. J Inorg Biochem 181:169–176

    Article  CAS  PubMed  Google Scholar 

  64. Shaw CA, Petrik MS (2009) Aluminum hydroxide injections lead to motor deficits and motor neuron degeneration. J Inorg Biochem 103(11):1555–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lau AA, Crawley AC, Hopwood JJ, Hemsley KM (2008) Open field locomotor activity and anxiety-related behaviors in mucopolysaccharidosis type IIIA mice. Behav Brain Res 191(1):130–136

    Article  CAS  PubMed  Google Scholar 

  66. Tatem KS, Quinn JL, Phadke A, Yu Q, Gordish-Dressman H, Nagaraju K (2014) Behavioral and locomotor measurements using an open field activity monitoring system for skeletal muscle diseases. J Vis Exp (91):51785. https://doi.org/10.3791/51785

  67. Carola V, D’Olimpio F, Brunamonti E, Mangia F, Renzi P (2002) Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134(1–2):49–57

    Article  PubMed  Google Scholar 

  68. Lecorps B, Rödel HG, Féron C (2016) Assessment of anxiety in open field and elevated plus maze using infrared thermography. Physiol Behav 157:209–216

    Article  CAS  PubMed  Google Scholar 

  69. Biedermann SV, Biedermann DG, Wenzlaff F, Kurjak T, Nouri S, Auer MK, Wiedemann K, Briken P, Haaker J, Lonsdorf TB, Fuss J (2017) An elevated plus-maze in mixed reality for studying human anxiety-related behavior. BMC Biol 15(1):125

    Article  PubMed  PubMed Central  Google Scholar 

  70. Deacon RM (2013) The successive alleys test of anxiety in mice and rats. J Vis Exp (76):2705. https://doi.org/10.3791/2705

  71. Komada M, Takao K, Miyakawa T (2008) Elevated plus maze for mice. J Vis Exp (22):1088. https://doi.org/10.3791/1088

  72. Morato S, Brandão ML (1997) Paradoxical increase of exploratory behavior in the elevated plus-maze by rats exposed to two kinds of aversive stimuli. Braz J Med Biol Res 30(9):1113–1120

    Article  CAS  PubMed  Google Scholar 

  73. Galante M et al (2009) Impairments in motor coordination without major changes in cerebellar plasticity in the Tc1 mouse model of Down syndrome. Hum Mol Genet 18(8):1449–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Hamm RJ et al (1994) The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J Neurotrauma 11(2):187–196

    Article  CAS  PubMed  Google Scholar 

  75. Deacon RM (2013) Measuring motor coordination in mice. J Vis Exp (75):e2609. https://doi.org/10.3791/2609

  76. Goldstein LB, Davis JN (1990) Beam-walking in rats: studies towards developing an animal model of functional recovery after brain injury. J Neurosci Methods 31(2):101–107

    Article  CAS  PubMed  Google Scholar 

  77. Luong TN, Carlisle HJ, Southwell A, Patterson PH (2011) Assessment of motor balance and coordination in mice using the balance beam. J Vis Exp (49):2376. https://doi.org/10.3791/2376

  78. Stanley JL et al (2005) The mouse beam walking assay offers improved sensitivity over the mouse rotarod in determining motor coordination deficits induced by benzodiazepines. J Psychopharmacol 19(3):221–227

    Article  CAS  PubMed  Google Scholar 

  79. Christe B, Burkhard PR, Pegna AJ, Mayer E, Hauert CA (2007) Clinical assessment of motor function: a processes oriented instrument based on a speed-accuracy trade-off paradigm. Behav Neurol 18(1):19–29

    Article  PubMed  PubMed Central  Google Scholar 

  80. Harrison TC, Murphy TH (2012) Towards a circuit mechanism for movement tuning in motor cortex. Front Neural Circuits 6:127

    PubMed  Google Scholar 

  81. Rothwell JC, MacKinnon CD, Valls-Solé J (2002) Role of brainstem-spinal projections in voluntary movement. Mov Disord 17(Suppl 2):S27–S29

    Article  PubMed  Google Scholar 

  82. Kawaguchi Y (2017) Pyramidal cell subtypes and their synaptic connections in layer 5 of rat frontal cortex. Cereb Cortex 27(12):5755–5771

    Article  PubMed  Google Scholar 

  83. Vitrac C et al (2014) Dopamine control of pyramidal neuron activity in the primary motor cortex via D2 receptors. Front Neural Circuits 8:13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Oliveira GB, Fontes EA Jr, de Carvalho S, da Silva JB, Fernandes LMP, Oliveira MCSP, Prediger RD, Gomes-Leal W, Rodrigues Lima R, Maia CSF (2014) Minocycline mitigates motor impairments and cortical neuronal loss induced by focal ischemia in rats chronically exposed to ethanol during adolescence. Brain Res 1561:23–34

    Article  CAS  PubMed  Google Scholar 

  85. Misra G, Coombes SA (2015) Neuroimaging evidence of motor control and pain processing in the human Midcingulate cortex. Cereb Cortex 25(7):1906–1919

    Article  PubMed  Google Scholar 

  86. Sheets PL, Shepherd GM (2011) Cortical circuits for motor control. Neuropsychopharmacology 36(1):365–366

    Article  PubMed  Google Scholar 

  87. Coco M, Perciavalle V (2015) Where did the motor function of the cerebellum come from? Cerebellum Ataxias 2:10

    Article  PubMed  PubMed Central  Google Scholar 

  88. Prevosto V, Sommer MA (2013) Cognitive control of movement via the cerebellar-recipient thalamus. Front Syst Neurosci 7:56

    Article  PubMed  PubMed Central  Google Scholar 

  89. Robinson FR, Fuchs AF (2001) The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci 24:981–1004

    Article  CAS  PubMed  Google Scholar 

  90. Sokolov AA, Miall RC, Ivry RB (2017) The cerebellum: adaptive prediction for movement and cognition. Trends Cogn Sci 21(5):313–332

    Article  PubMed  PubMed Central  Google Scholar 

  91. Louis ED, Lee M, Babij R, Ma K, Cortés E, Vonsattel JPG, Faust PL (2014) Reduced Purkinje cell dendritic arborization and loss of dendritic spines in essential tremor. Brain 137(Pt 12):3142–3148

    Article  PubMed  PubMed Central  Google Scholar 

  92. Pascual R, Hervias MC, Tohá ME, Valero A, Figueroa HR (1998) Purkinje cell impairment induced by early movement restriction. Biol Neonate 73(1):47–51

    Article  CAS  PubMed  Google Scholar 

  93. Kumar V, Gill KD (2014) Oxidative stress and mitochondrial dysfunction in aluminium neurotoxicity and its amelioration: a review. Neurotoxicology 41:154–166

    Article  CAS  PubMed  Google Scholar 

  94. Ghorbel I, Amara IB, Ktari N, Elwej A, Boudawara O, Boudawara T, Zeghal N (2016) Aluminium and acrylamide disrupt cerebellum redox states, cholinergic function and membrane-bound ATPase in adult rats and their offspring. Biol Trace Elem Res 174(2):335–346

    Article  CAS  PubMed  Google Scholar 

  95. Nehru B, Anand P (2005) Oxidative damage following chronic aluminium exposure in adult and pup rat brains. J Trace Elem Med Biol 19(2–3):203–208

    Article  CAS  PubMed  Google Scholar 

  96. Singla N, Dhawan DK (2014) Influence of zinc on calcium-dependent signal transduction pathways during aluminium-induced neurodegeneration. Mol Neurobiol 50(2):613–625

    Article  CAS  PubMed  Google Scholar 

  97. Tripathi S et al (2011) Protective potential of Bacopa monniera (Brahmi) extract on aluminum induced cerebellar toxicity and associated neuromuscular status in aged rats. Cell Mol Biol (Noisy-le-grand) 57(1):3–15

    CAS  Google Scholar 

  98. Esparza JL, Gómez M, Rosa Nogués M, Paternain JL, Mallol J, Domingo JL (2005) Melatonin reduces oxidative stress and increases gene expression in the cerebral cortex and cerebellum of aluminum-exposed rats. J Pineal Res 39(2):129–136

    Article  CAS  PubMed  Google Scholar 

  99. Flora SJ et al (2003) Aluminum-induced oxidative stress in rat brain: response to combined administration of citric acid and HEDTA. Comp Biochem Physiol C Toxicol Pharmacol 134(3):319–328

    Article  PubMed  CAS  Google Scholar 

  100. Tirumanyam M, Nadella R, Kondammagari S, Borelli DPR, Nannepaga JS (2019) Bacopa phospholipid complex retrieves aluminum maltolate complex-induced oxidative stress and apoptotic alterations in the brain regions of albino rat. Environ Sci Pollut Res Int 26(12):12071–12079

    Article  CAS  PubMed  Google Scholar 

  101. Bhalla P, Dhawan DK (2009) Protective role of lithium in ameliorating the aluminium-induced oxidative stress and histological changes in rat brain. Cell Mol Neurobiol 29(4):513–521

    Article  CAS  PubMed  Google Scholar 

  102. Chaudhary M, Joshi DK, Tripathi S, Kulshrestha S, Mahdi AA (2014) Docosahexaenoic acid ameliorates aluminum induced biochemical and morphological alteration in rat cerebellum. Ann Neurosci 21(1):5–9

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Federal University of Pará for technical and scientific support.

Funding

This study was supported by the Brazilian National Council for Scientific and Technological Development (CNPq). It was also partially financed by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES)—Finance Code 001.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafael Rodrigues Lima.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernandes, R.M., Nascimento, P.C., Martins, M.K. et al. Evaluation of Cerebellar Function and Integrity of Adult Rats After Long-Term Exposure to Aluminum at Equivalent Urban Region Consumption Concentrations. Biol Trace Elem Res 199, 1425–1436 (2021). https://doi.org/10.1007/s12011-020-02244-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-020-02244-2

Keywords

Navigation