Anat Cell Biol.  2022 Sep;55(3):320-329. 10.5115/acb.22.033.

Tamarindus indica ameliorates behavioral and cytoarchitectural changes in the cerebellar cortex following prenatal aluminum chloride exposure in Wistar rats

Affiliations
  • 1Department of Human Anatomy, Faculty of Biomedical Sciences, Kampala International University, Bushenyi, Uganda.
  • 2Department of Human Anatomy, College of Medicine and Health Science, Ahmadu Bello University, Zaria, Nigeria.
  • 3Department of Human Anatomy, Federal University Dutse, Jigawa, Nigeria.
  • 4Department of Human Anatomy, College of Medicine and Pharmacy, University of Rwanda, Kigali, Rwanda.
  • 5Infection Medicine, Deanery of Biomedical Sciences, College of Medicine and Veterinary Medicine, The University of Edinburgh, Edinburgh, United Kingdom.

Abstract

Aluminium exposure has been linked with developmental neurotoxicity in humans and experimental animals. The study aimed to evaluate the ameliorative effect of Tamarindus indica on the developing cerebellar cortex, neurobehavior, and immunohistochemistry of the cerebellar cortex following prenatal aluminum chloride (AlCl 3 ) exposure. Pregnant timed Wistar rats were divided into 5 groups (n=4). Group I (negative control) was given distilled water, group II was treated with 200 mg/kg of AlCl 3 , group III were given 200 mg/kg of AlCl 3 and 400 mg/kg of ethyl acetate leaf fraction of Tamarindus indica (EATI), group IV were given 200 mg/kg of AlCl 3 and 800 mg/kg of EATI, and group V were treated with 200 mg/kg of AlCl 3 s/c and 300 mg/kg of vitamin E for 14 days (prenatal day 7–21) via the oral route. Male pups (n=6) were randomly selected and taken for neurobehavioral studies, and humanely sacrificed via intraperitoneal injection of thiopental sodium. The cerebellum was removed, fixed and tissue processed for histological and immunohistochemical studies. The results revealed that prenatal AlCl 3 exposure impacted neurodevelopment and neurobehaviour among exposed pups. Prenatal AlCl 3 exposure was marked with delayed cytoarchitectural development of the cerebellar cortex and increased GFAP expression in the cerebellar cortex. On the other hand, treatment with EATI and vitamin E were marked with significant improvements. The present study therefore concluded treatment with EATI shows an ameliorative effect to prenatal AlCl 3 exposure.

Keyword

Tamarindus indica; Glial fibrillary protein; Motor cordination; Aluminum exposure

Figure

  • Fig. 1 Photmicrograph of the cerebellar cortex on post-natal day 7 from the treatment groups (H&E, ×400). Negative control (distilled water) (A), positive 2 control (200 mg/kg bw of AlCl3) (B), 200 mg/kg bw of AlCl3+400 mg/kg bw ethyl acetate leaf fraction of Tamarindus indica (EATI) (C), 200 mg/kg bw of AlCl3+800 mg/kg bw EATI (D), and 200 mg/kg bw of AlCl3+300 mg/kg bw of vitamin E (E). EGL, external granular layer; ML, molecular layer; PCL, Purkinje cell layer; IGL, internal granular layer; GC, granular cells.

  • Fig. 2 Photmicrograph of the cerebellar cortex on post-natal day 21 from the treatment groups (H&E, ×400). Negative control (distilled water) (A), positive 8 control (200 mg/kg bw of AlCl3) (B), 200 mg/kg bw of AlCl3+400 mg/kg bw ethyl acetate leaf fraction of Tamarindus indica (EATI) (C), 200 mg/kg bw of AlCl3+800 mg/kg bw EATI (D), and 200 mg/kg bw of AlCl3+300 mg/kg bw of vitamin E (E). Red arrow indicates degenerating cells. GL, granular layer; ML: molecular layer; PCL, Purkinje cell 10 layer; PC, Purkinje cell.

  • Fig. 3 Photmicrograph of the cerebellar cortex on post-natal day 21 from the treatment groups (Cluver 17 berrera; ×400). Negative control (distilled water) (A), positive 14 control (200 mg/kg bw of AlCl3) (B), 200 mg/kg bw of AlCl3+400 mg/kg bw ethyl acetate leaf fraction of Tamarindus indica (EATI) (C), 200 mg/kg bw of AlCl3+800 mg/kg bw EATI 15 (D), and 200 mg/kg bw of AlCl3+300 mg/kg bw of vitamin E (E). Black arrows indicate dendritic arborization. GL, granular layer; ML, molecular layer; PCL, Purkinje cell 16 layer; PC, Purkinje cell; RLD, region of reduced linear distribution of Purkinje cell.

  • Fig. 4 Photomicrograph of Wistar rat cerebella cortex on post-natal day 21, showing immune-positive cells (black arrow head) (GFAP, ×400). (A) 2 ml/kg bw of distilled water, (B) 200 mg/kg bw of AlCl3, (C) 200 mg/kg bw of AlCl3 and 400 mg/kg bw ethyl acetate leaf fraction of Tamarindus indica (EATI), (D) 200 mg/kg bw of AlCl3 and 800 mg/kg bw EATI, (E) 200 mg/kg bw of AlCl3 and 300 mg/kg bw of vitamin E, and (F) the immuno-histochemical score (IHS) using Klein’s semiqualitative approach; with values presented as mean±SEM. a,b)Significance difference (P<0.05) compared to the negative control (group 1). GL, granular layer; ML, molecular layer. GFAP is the staining method in this case.


Reference

References

1. Tietz T, Lenzner A, Kolbaum AE, Zellmer S, Riebeling C, Gürtler R, Jung C, Kappenstein O, Tentschert J, Giulbudagian M, Merkel S, Pirow R, Lindtner O, Tralau T, Schäfer B, Laux P, Greiner M, Lampen A, Luch A, Wittkowski R, Hensel A. 2019; Aggregated aluminium exposure: risk assessment for the general population. Arch Toxicol. 93:3503–21. DOI: 10.1007/s00204-019-02599-z. PMID: 31659427.
Article
2. IAI. 2022. World aluminium - primary aluminium production [Internet]. International Aluminium Institute;London: Available from: https://international-aluminium.org/statistics/primary-aluminium-production/. cited 2021 Feb 16.
3. Igbokwe IO, Igwenagu E, Igbokwe NA. 2019; Aluminium toxicosis: a review of toxic actions and effects. Interdiscip Toxicol. 12:45–70. DOI: 10.2478/intox-2019-0007. PMID: 32206026. PMCID: PMC7071840.
Article
4. Shirley DG, Lote CJ. 2005; Renal handling of aluminium. Nephron Physiol. 101:p99–103. DOI: 10.1159/000088331. PMID: 16174991.
Article
5. Al-Hazmi MA, Rawi SM, Hamza RZ. 2021; Biochemical, histological, and neuro-physiological effects of long-term aluminum chloride exposure in rats. Metab Brain Dis. 36:429–36. DOI: 10.1007/s11011-020-00664-6. PMID: 33404936.
Article
6. Golub MS, Gershwin ME, Donald JM, Negri S, Keen CL. 1987; Maternal and developmental toxicity of chronic aluminum exposure in mice. Fundam Appl Toxicol. 8:346–57. DOI: 10.1016/0272-0590(87)90084-4. PMID: 3569705.
Article
7. Martinez CS, Vera G, Ocio JAU, Peçanha FM, Vassallo DV, Miguel M, Wiggers GA. 2018; Aluminum exposure for 60days at an equivalent human dietary level promotes peripheral dysfunction in rats. J Inorg Biochem. 181:169–76. DOI: 10.1016/j.jinorgbio.2017.08.011. PMID: 28865725.
8. Golub MS, Germann SL. 2001; Long-term consequences of developmental exposure to aluminum in a suboptimal diet for growth and behavior of Swiss Webster mice. Neurotoxicol Teratol. 23:365–72. DOI: 10.1016/S0892-0362(01)00144-1. PMID: 11485839.
Article
9. 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. 32:1335–55. DOI: 10.1007/s11011-017-0077-2. PMID: 28752219. PMCID: PMC5596046.
Article
10. Tugume P, Nyakoojo C. 2019; Ethno-pharmacological survey of herbal remedies used in the treatment of paediatric diseases in Buhunga parish, Rukungiri District, Uganda. BMC Complement Altern Med. 19:353. DOI: 10.1186/s12906-019-2763-6. PMID: 31806007. PMCID: PMC6896270. PMID: 800a0206b2244797b2f7290b2a82cbf9.
Article
11. Adekeye AO, Irawo GJ, Fafure AA. 2020; Ficus exasperata Vahl leaves extract attenuates motor deficit in vanadium-induced parkinsonism mice. Anat Cell Biol. 53:183–93. DOI: 10.5115/acb.19.205. PMID: 32647086. PMCID: PMC7343565.
Article
12. El-Bassouny DR, Omar NM, Khalaf HA, Al-Salam RAA. 2021; Role of nuclear factor-kappa B in bleomycin induced pulmonary fibrosis and the probable alleviating role of ginsenoside: histological, immunohistochemical, and biochemical study. Anat Cell Biol. 54:448–64. DOI: 10.5115/acb.21.068. PMID: 34936986. PMCID: PMC8693141.
Article
13. Abdelrahman GH, Mariod AA. Mariod A, editor. 2019. Tamarindus indica: phytochemical constituents, bioactive compounds and traditional and medicinal uses. Wild Fruits: Composition, Nutritional Value and Products. Springer;Cham: p. 229–38. DOI: 10.1007/978-3-030-31885-7_19.
14. Panara K, Harisha CR, Shukla VJ. 2014; Pharmacognostic and phytochemical evaluation of fruit pulp of Tamarindus Indica linn. Int J Ayurvedic Med. 5:37–42.
15. Chong UR, Abdul-Rahman PS, Abdul-Aziz A, Hashim OH, Junit SM. 2012; Tamarindus indica extract alters release of alpha enolase, apolipoprotein A-I, transthyretin and Rab GDP dissociation inhibitor beta from HepG2 cells. PLoS One. 7:e39476. DOI: 10.1371/journal.pone.0039476. PMID: 22724021. PMCID: PMC3378544. PMID: da9c3f5c3855468ebd14f59c4fa851b3.
Article
16. Ajiboye BO, Ojo OA, Okesola MA, Oyinloye BE, Kappo AP. 2018; Ethyl acetate leaf fraction of Cnidoscolus aconitifolius (Mill.) I. M. Johnst: antioxidant potential, inhibitory activities of key enzymes on carbohydrate metabolism, cholinergic, monoaminergic, purinergic, and chemical fingerprinting. Int J Food Prop. 21:1697–715. DOI: 10.1080/10942912.2018.1504787.
17. Paccola CC, Resende CG, Stumpp T, Miraglia SM, Cipriano I. 2013; The rat estrous cycle revisited: a quantitative and qualitative analysis. Anim Reprod. 10:677–83.
18. Marcondes FK, Bianchi FJ, Tanno AP. 2002; Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol. 62:609–14. DOI: 10.1590/S1519-69842002000400008. PMID: 12659010.
Article
19. Yener T, Turkkani Tunc A, Aslan H, Aytan H, Cantug Caliskan A. 2007; Determination of oestrous cycle of the rats by direct examination: how reliable? Anat Histol Embryol. 36:75–7. DOI: 10.1111/j.1439-0264.2006.00743.x. PMID: 17266672.
Article
20. Chinoy NJ, Sorathia HP, Jhala DD. 2005; Fluoride+aluminium induced toxicity in mice testis with giant cells and its reversal by vitamin C. Fluoride. 38:109–14.
21. Elizabeth MA, Samson P, Itohan OR. 2020; Histomorphological evaluations on the frontal cortex extrapyramidal cell layer following administration of N-Acetyl cysteine in aluminum induced neurodegeneration rat model. Metab Brain Dis. 35:829–39. DOI: 10.1007/s11011-020-00556-9. PMID: 32212044. PMCID: PMC7220982.
Article
22. Stanley JL, Lincoln RJ, Brown TA, McDonald LM, Dawson GR, Reynolds DS. 2005; The mouse beam walking assay offers improved sensitivity over the mouse rotarod in determining motor coordination deficits induced by benzodiazepines. J Psychopharmacol. 19:221–7. DOI: 10.1177/0269881105051524. PMID: 15888506.
Article
23. Kasozi KI, Namubiru S, Safiriyu AA, Ninsiima HI, Nakimbugwe D, Namayanja M, Valladares MB. 2018; Grain amaranth is associated with improved hepatic and renal calcium metabolism in type 2 diabetes mellitus of male wistar rats. Evid Based Complement Alternat Med. 2018:4098942. DOI: 10.1155/2018/4098942. PMID: 30420893. PMCID: PMC6211157.
Article
24. Usman IM, Iliya IA, Ivang AE, Ssempijja F, Ojewale AO, Yusuf HR. 2019; Microanatomical and biochemical changes of the cerebellum following ethanol gavage in adult Wistar rats. Anat J Afr. 8:1662–9. DOI: 10.4314/aja.v8i2.189708.
Article
25. Feldman AT, Wolfe D. 2014; Tissue processing and hematoxylin and eosin staining. Methods Mol Biol. 1180:31–43. DOI: 10.1007/978-1-4939-1050-2_3. PMID: 25015141.
Article
26. National Diagnostics. c2011. Staining procedures: national diagnostics [Internet]. National Diagnostics;Atlanta: Available from: https://www.nationaldiagnostics.com/histology/article/staining-procedures. cited 2022 Feb 14.
27. Gomes-Leal W, Corkill DJ, Freire MA, Picanço-Diniz CW, Perry VH. 2004; Astrocytosis, microglia activation, oligodendrocyte degeneration, and pyknosis following acute spinal cord injury. Exp Neurol. 190:456–67. DOI: 10.1016/j.expneurol.2004.06.028. PMID: 15530884.
Article
28. Fedchenko N, Reifenrath J. 2014; Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue - a review. Diagn Pathol. 9:221. DOI: 10.1186/s13000-014-0221-9. PMID: 25432701. PMCID: PMC4260254.
Article
29. Archibong VB, Ekanem TB, Igiri AO, Lemuel AM, Usman IM, Okesina AA, Obosi NJ. 2020; Immunohistochemical studies of codeine medication on the prefrontal cortex and cerebellum of adult Wistar rats. Cogent Med. 7:1824390. DOI: 10.1080/2331205X.2020.1824390.
Article
30. Gonda Z, Lehotzky K. 1996; Effect of prenatal aluminium lactate exposure on conditioned taste aversion and passive avoidance task in the rat. J Appl Toxicol. 16:529–32. DOI: 10.1002/(SICI)1099-1263(199611)16:6<529::AID-JAT392>3.0.CO;2-S. PMID: 8956099.
Article
31. Rankin J, Manning A. 1993; Alterations to the pattern of ultrasonic calling after prenatal exposure to aluminium sulfate. Behav Neural Biol. 59:136–42. DOI: 10.1016/0163-1047(93)90860-K. PMID: 8476381.
Article
32. Muller G, Bernuzzi V, Desor D, Hutin MF, Burnel D, Lehr PR. 1990; Developmental alterations in offspring of female rats orally intoxicated by aluminum lactate at different gestation periods. Teratology. 42:253–61. DOI: 10.1002/tera.1420420309. PMID: 2274891.
Article
33. Röllin HB, Nogueira C, Olutola B, Channa K, Odland JØ. 2018; Prenatal exposure to aluminum and status of selected essential trace elements in rural South African women at delivery. Int J Environ Res Public Health. 15:1494. DOI: 10.3390/ijerph15071494. PMID: 30011954. PMCID: PMC6068832.
Article
34. Fernandes RM, Nascimento PC, Martins MK, Aragão WAB, Rivera LFS, Bittencourt LO, Cartágenes SC, Crespo-Lopez ME, do Socorro Ferraz Maia C, Lima RR. 2021; 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. 199:1425–36. DOI: 10.1007/s12011-020-02244-2. PMID: 32564201.
Article
35. Reichert KP, Schetinger MRC, Pillat MM, Bottari NB, Palma TV, Gutierres JM, Ulrich H, Andrade CM, Exley C, Morsch VMM. 2019; Aluminum affects neural phenotype determination of embryonic neural progenitor cells. Arch Toxicol. 93:2515–24. DOI: 10.1007/s00204-019-02522-6. PMID: 31363819.
Article
36. Butts T, Green MJ, Wingate RJ. 2014; Development of the cerebellum: simple steps to make a 'little brain'. Development. 141:4031–41. DOI: 10.1242/dev.106559. PMID: 25336734.
Article
37. Allam A, Abdul-Hamid M, Allam G, Al-hroob A, Ibraheem G, Alsubaie M. 2013; Perinatal ethyl alcohol effects on the development of cerebellar cortex in albino rat. Afr J Pharm Pharmacol. 7:1293–301. DOI: 10.5897/AJPP12.1191.
Article
38. Ulfanov O, Cil N, Adiguzel E. 2020; Protective effects of vitamin E on aluminium sulphate-induced testicular damage. Toxicol Ind Health. 36:215–27. DOI: 10.1177/0748233720919663. PMID: 32330100.
Article
39. Wang M, Ruan DY, Chen JT, Xu YZ. 2002; Lack of effects of vitamin E on aluminium-induced deficit of synaptic plasticity in rat dentate gyrus in vivo. Food Chem Toxicol. 40:471–8. DOI: 10.1016/S0278-6915(01)00094-1. PMID: 11893406.
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