Abstract
The study investigates the role of Anogeissus leiocarpus methanol stem bark extract (ALSE) on seizure, oxidative stress and cognitive performance in pentylenetetrazole (PTZ)-induced epilepsy in rat model. Thirty Wistar rats were allocated into five groups (n = 6). Groups 1 and 2 received normal saline intra-peritoneal (i.p) every day and PTZ (i.p) at 35 mg/kg every other day respectively. Groups 3–5 were given ALSE orally at (250 mg/kg and 500 mg/kg) and Diazepam at 4 mg/kg (i.p) respectively. Groups 3–5 were given PTZ (i.p) at 35 mg/kg every other day for 30 days, 30 min after ALSE and Diazepam administration. The rats were observed for seizure activities and also evaluated for cognitive functions. The rats were euthanized thereafter and the brain histology and oxidative stress biomarkers were evaluated. PTZ induction resulted into increased seizure activities leading to the development of kindling, oxidative stress, cognitive impairment and histological aberration of the hippocampus. However, pretreatment with ALSE decreased seizure activities, reversed oxidative stress and cognitive impairment and preserved hippocampal histology relative to the PTZ alone treated rats. Conclusively, ALSE was found to increase seizure latency, prevented cognitive decline, and decreased seizure activities induced by PTZ-kindling in rats. Additionally, ALSE ameliorates PTZ-induced oxidative stress and histological aberrations of the hippocampus. Hence, this study proposed that ALSE might be a promising tool for ameliorating seizure in epilepsy.
Similar content being viewed by others
Data availability
Data are available from the corresponding author on reasonable request.
Abbreviations
- ALSE:
-
Anogeissus leiocarpus methanol stem bark extract
- PTZ:
-
Pentylenetetrazole
- CNS:
-
Central nervous system
- MDA:
-
Malondialdehyde
- GSH:
-
Reduced glutathione
- SOD:
-
Superoxide dismutase
- GAE:
-
Gallic acid equivalent
- QE:
-
Quercetin equivalent
- NVRI:
-
National Veterinary Research Institute
- mEPM:
-
Modified Elevated Plus Maze
- ITL:
-
Initial transfer latency
- FTL:
-
Final transfer latency
- H&E:
-
Hematoxylen and eosin
- ANOVA:
-
Analysis of variance
References
Adejoh IP, Mark-Maria AU, Ojochegbe AB, Mayowa OJ, Boniface MT (2019) Effect of aqueous leaf extract of Anogeissus leiocarpus against experimental models of pain and pyrexia. Int J Adv Res Biol Sci 6:181–188
Aebi H, Wyss SR, Scherz B, Skvaril F (1974) Heterogeneity of erythrocyte catalase II. Isolation and characterization of normal and variant erythrocyte catalase and their subunits. Eur J Biochem 48:137–145
Arbab AH (2014) Review on Anogeissus leiocarpus a potent African traditional drug. Int J Res Pharm Chem 4(3):496–500
Barku VY, Boye A, Ayaba S (2013) Phytochemical screening and assessment of wound healing activity of the leaves of Anogeissus leiocarpus. Eur J Exp Biol 3:18–25
Bello A, Wagini NH (2017) The leaves of Anogeissus leiocarpa (DC.) Guill. & Perr may substitute for its roots and stem bark in the treatment of microbial infections. Katsina J Nat Appl Sci 6:124–130
Campos DV, Lopim GM, da Silva DA, de Almeida AA, Amado D, Arida RM (2017) Epilepsy and exercise: an experimental study in female rats. Physiol Behav 171:120–126
Chiroma SM, Baharuldin MTH, Taib CNM, Amom Z, Jagadeesan S, Adenan MI, Moklas MAM (2019) Protective effect of Centella asiatica against D-galactose and aluminium chloride induced rats: Behavioral and ultrastructure approaches. Biomed Pharmacother 109:853–864
Chiroma SS, Nazifi AB, Ya’u J, Aliyu M, Bichi LA, Chiroma SM (2022) Anti-seizure properties of Ipomoea asarifolia (Desr.)(Convolvulaceae) ethanolic leaf extract in laboratory animals. Bull Natl Res Centre 46(1):1–7
Council NR (2011) Guide for the care and use of laboratory animals. Washington DC
Dhir A (2012) Pentylenetetrazole (PTZ) kindling model of epilepsy. Curr Protoc Neurosci 9:1–9
Dingledine R (2014) When and How Do Seizures kill neurons, and is cell death relevant to epileptogenesis? Adv Exp Med Biol 813:109–122
Diniz TC, Silva JC, Lima-Saraiva SRGD, Ribeiro FPRDA, Pacheco AGM, de Freitas RM et al (2015) The role of flavonoids on oxidative stress in epilepsy.Med. Cell Longiv.71756
Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77
Fridovich I (1989) Superoxide dismutases: an adaptation to a paramagnetic gas. J Biol Chem 264:7761–7764
Geronzi U, Lotti F, Grosso S (2018) Oxidative stress in epilepsy. Expert Rev Neurother 18:427–434
Ho Y, Lin Y, Wu CJ, Chao Y, Alice YW, Chang AYW, Chan JYH (2015) Peripheral inflammation increases seizure susceptibility via the induction of neuroinflammation and oxidative stress in the hippocampus. J Biomed Sci 22:46
Hoeller AA, Ribeiro de Carvalho C, Franco PLC, Formolo DA, Imthon AK, Rodighero dos Santos H (2017) Behavioral and neurochemical consequences of pentylenetetrazol-induced kindling in young and middle-aged rats. Pharmaceuticals 10:75
Holmes GL (2015) Cognitive impairment in epilepsy: the role of network abnormalities. Epileptic Disord 17:101–116
Kola PK, Akula A, Nissankara-Rao LS, Danduga RCSR (2017) Protective effect of naringin on pentylenetetrazole (PTZ)-induced kindling; possible mechanisms of antikindling, memory improvement, and neuroprotection. Epilepsy Behav 75:114–126
Koshal P, Jamwal S, Akula KK, Bansal PK (2017) Animal models of epilepsy. Animal Models of neurological disorders. Springer, Singapore, pp 59–78
Lenck-Santini P, Scott RC (2015) Mechanisms responsible for cognitive impairment in epilepsy. Perspect Med 5:a022772
Maheshu V, Priyadarsini TD, Sasikumar JM (2013) Effects of processing conditions on the stability of polyphenolic contents and antioxidant capacity of Dolichos lablab L. J Food Sci Technol 50(4):731–738
Meenu M, Reeta KH, Dind AK, Kottarath SK, Gupta YK (2019) Evaluation of sodium valproate loaded nanoparticles in acute and chronic pentylenetetrazole induced seizure models. Epilepsy Res 158:106219
Menon B, Ramalingam K, Kumar RV (2012) Oxidative stress in patients with epilepsy is independent of antiepileptic drugs. Seizure 21:780–784
Mishra V, Shuai B, Kodali M, Shetty GA, Hattiangady B, Rao X, Shetty AK (2015) Resveratrol treatment after status epilepticus restrains neurodegeneration and abnormal neurogenesis with suppression of oxidative stress and inflammation. Sci Rep 5:17807
Mori T, Rezai-Zadeh K, Koyama N, Arendash GW, Yamaguchi H, Kakuda N (2012) Tannic acid is a natural-secretase inhibitor that prevents cognitive impairment and mitigates alzheimer-like pathology in transgenic mice. J Biol Chem 287:6912–6927
Mumtaz F, Raza S, Ahmad Z, Afitakhar A, Hussain M (2014) Qualitative phytochemical analysis of some selected medicinal plants occurring in local area of Faisalabad. Pakistan J Pharm Altern Med 3(3):17–21
Mutha RE, Tatiya AU, Surana SJ (2021) Flavonoids as natural phenolic compounds and their role in therapeutics: an overview. Future J Pharm Sci 7:25
Niehaus WG Jr, Samuelsson B (1968) Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 6:126–130
Num-Adom SM, Adamu S, Aluwong T, Ogbuagu NE, Umar IA, Esievo KAN (2022) Ethanolic extract of Anogeissus leiocarpus ameliorates hyperglycaemia, hepato-renal damage, deranged electrolytes and acid-base balance in alloxan-induced diabetes in dogs. Sci Afr 16:e01183
Obadoni BO, Ochuko PO (2001) Phytochemical Studies and comparative efficacy of the crude extracts of some homeostatic plants in Edo and Delta States of Nigeria. Global J Pure Appl Sci 8:203–208
Peng K, Lv X, Zhao H, Chen B, Chen X, Huang W (2022) Antioxidant and intestinal recovery function of condensed tannins in Lateolabrax maculatus responded to in vivo and in vitro oxidative stress. Aquaculture 547:737399
Puttachary S, Sharma S, Stark S, Thippeswamy T (2015) Seizure-Induced oxidative stress in temporal lobe epilepsy. BioMed Res. 745613
Salih EYA, Julkunen-Tiitto R, Luukkanen O, Sipi M, Mustafa KM, Fahmi MKM, Fyhrquist PJ (2020) Potential anti-tuberculosis activity of the extracts and their active components of Anogeissus leiocarpa (DC.) Guill. and Perr. with special emphasis on polyphenols. Antibiotics 9:364
Shafaat HR, Hasanzadeha MM, Varmaziara O, Janda A, Palizvana MR (2019) The effect of co-administration of pentylenetetrazole with pilocarpine: new modified PTZ models of kindling and seizure. Pharmacol Biochem Behav 182:7–11
Shimada T, Yamagata K (2018) Pentylenetetrazole-induced kindling Mouse model. J Vis Exp 136:e56573
Singh N, Vijayanti S, Sahaa L, Bhatia A, Banerjee D, Chakrabarti A (2018) Neuroprotective effect of Nrf2 activator dimethyl fumarate, on the hippocampal neurons in chemical kindling model in rat. Epilepsy Res 143:98–104
Sun AY, Wang Q, Simonyi A, Sun GA (2008) Botanical phenolics and brain health. Neuromolecular Med 10:259–274
Szwajgier D, Borowiec K, Pustelniak K (2017) The Neuroprotective effects of phenolic acids: molecular mechanism of action. Nutrients 9:477
Vrinda M, Arun S, Srikumar BN, Kutty BM, Rao BS (2019) Temporal lobe epilepsy-induced neurodegeneration and cognitive deficits: Implications for aging. J Chem Neuroanat 95:146–153
Waterhouse AL (2002) Polyphenolics determination of total phenolics. In: Wrolstad REJ (ed) Current protocols in food analytical chemistry. Wiley, New York
Xie T, Wang WP, Mao ZF, Qu ZZ, Luan SQ, Jia LJ, Kan MC (2012) Effects of epigallocatechin-3-gallate on pentylenetetrazole-induced kindling, cognitive impairment and oxidative stress in rats. Neurosci Lett 516:237–241
Zamudio SR, Pichardo-Macías LA, Díaz-Villegas V, Flores-Navarrete IL, Guzmán-Velázquez S (2019) Subchronic cerebrolysin treatment alleviates cognitive impairments and dendritic arborization alterations of granular neurons in the hippocampal dentate gyrus of rats with temporal lobe epilepsy. Epilepsy & Behav 97:96–104
Zhang H, Tsao R (2016) Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects. Curr Opin Food Sci 8:33–42
Zhang R, Zeng Q, Deng Y, Zhang M, Wei Z, Zhang Y, Tang X (2013) Phenolic profiles and antioxidant activity of litchi pulp of different cultivars cultivated in Southern China. Food Chem 136:1169–1176
Zhu X, Dong J, Han B, Huang R, Zhang A, Xia Z, Chang H, Chao J, Yao H (2017) Neuronal nitric oxide synthase contributes to PTZ kindling-induced cognitive impairment and depressive-like behavior. Front Behav Neurosci 11:203
Acknowledgements
The authors acknowledge the contributions of Mr. Ephraim Ayuba and Mr. Sunday Joseph Manye for their technical support. Further, Pharm. S.S Chiroma of Pharmacist Council of Nigeria and Dr. A.B Nazifi of Faculty of Pharmaceutical Sciences, Bayero University Kano are also acknowledged for their scientific advises.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
Conceptualization: All authors; Experiment: HAA, AA, NID; Analysis: SMC, NID; Supervision: SMC, JVZ, NID; Writing draft: HAA, NID; Review: SMC, JVZ; Final write-up: Reviewed and approved by all authors.
Corresponding author
Ethics declarations
Ethical approval
This study was approved by the Postgraduate Board of Studies, Faculty of Basic Medical Sciences University of Maiduguri, and was conducted following the ARRIVE Guidelines and the National Institute of Health Guide for the Care and Use of laboratory Animals as reported in publication volume 25 No. 28 revised in 1996 (Council 2011).
Conflict of interest
Hauwa Adamu Audu has no conflict of interest. Amina Ahmed has no conflict of interest. Joseph Vandi Zirahei has no conflict of interest. Nathan Isaac Dibal has no conflict of interest. Samaila Musa Chiroma has no conflict of interest.
Consent for publication
Not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Audu, H.A., Ahmed, A., Zirahei, J.V. et al. Anogeissus leiocarpus (DC.) Guill and Perr ameliorates pentylenetetrazole-induced seizure/cognitive impairment in rats via inhibition of oxidative stress. ADV TRADIT MED (ADTM) 23, 1199–1208 (2023). https://doi.org/10.1007/s13596-022-00672-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13596-022-00672-0