Research Article
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Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy

Year 2024, Volume: 54 Issue: 3, 378 - 385, 30.12.2024

Batuhan Yağmur , Şura Akat Pişkin , Erkan Civelek , Deniz Kaleli Durman , Nihan Çarcak

https://doi.org/10.26650/IstanbulJPharm.2024.1467008

Abstract

Background and Aims: Anatolian propolis, which is rich in phenolic compounds, may offer neuroprotective benefits due to its anti-inflammatory and antioxidant properties. This study explored how Anatolian propolis affects the frequency of absence seizures and anxiety levels in rats with genetic absence epilepsy from Strasbourg (GAERS).
Methods: Adult male GAERS were orally administered Anatolian propolis samples at concentrations of 15% (120 mg/kg/day) and 30% (180 mg/kg/day), whereas the control group received an equivalent volume of tap water by oral gavage for 35 days. A 3-h EEG was recorded 9.00 and 12.00 a.m after 35 days of sub-chronic administration. The effects of Anatolian propolis on spike-and-wave discharge (SWD) duration, number, and mean duration of each SWDs were evaluated and compared with the control group. The elevated plus maze test was then performed to measure the anxiety level of GAERS rats. Finally, brains were isolated, and interleukin-1 beta (IL-1β) levels were measured in freshly frozen isolated brains using an ELISA method.
Results: Oral administration of Anatolian propolis (180 mg/kg/day) significantly reduced the number of SWDs and decreased IL-1β levels in the brain tissue of adult GAERS after 35 days of sub-chronic administration (p<0.05). Propolis treatment did not alter anxiety levels in terms of time spent in the closed and open arms.
Conclusion: This study represents an initial exploration of the effects of Anatolian propolis on absence seizures in GAERS. Our findings indicate that Anatolian propolis could offer therapeutic advantages by reducing the levels of the brain’s pro-inflammatory cytokine IL-1β in GAERS, potentially mitigating absence seizures. However, additional research is necessary to understand the potential mechanisms driving this benefit.

Keywords

Absence epilepsy Anatolian Propolis Anxiety GAERS IL-1β Neuroinflammation

Ethical Statement

All procedures were carried out in the Experimental Animal Care and Research Unit of Istanbul University Faculty of Pharmacy (EDEHAB), according to the approval by the Animal Ethics Committee of Istanbul University (2022/06) conforming with the EU Directive 2010/63/EU for animal experiments of the Istanbul University Local Ethics Committee of Animal Experiments (HADYEK).

Supporting Institution

This project was supported by TUBITAK-2209A University Students Research Projects Support Program. (Project number: 1919B012104927).

Project Number

1919B012104927

Thanks

Commercial Anatolian Propolis samples was provided by BEE’O Company’s as generous gift. This project is 5th grade thesis dissertation.

References

  • Akin, D., Ravizza, T., Maroso, M., Carcak, N., Eryigit, T., Vanzulli, I., ... Onat, F. Y. (2011). IL-ip is induced in reactive astro-cytes in the somatosensory cortex of rats with genetic absence epilepsy at the onset of spike-and-wave discharges, and contributes to their occurrence. Neurobiology of Disease, 44(3), 259-269. https://doi.org/10.1016/J.NBD.2011.05.015 google scholar
  • Altuntaş, Ü., Güzel, İ., & Özçelik, B. (2023). Phenolic con-stituents, antioxidant and antimicrobial activity and cluster-ing analysis of Propolis samples based on PCA from differ-ent regions of Anatolia. Molecules (Basel, Switzerland), 28(3). https://doi.org/10.3390/MOLECULES28031121 google scholar
  • Billiau, A. D., Witters, P., Ceulemans, B., Kasran, A., Wouters, C., & Lagae, L. (2007). Intravenous immunoglobulins in refractory childhood-onset epilepsy: effects on seizure frequency, EEG ac-tivity, and cerebrospinal fluid cytokine profile. Epilepsia, 48(9), 1739-1749. https://doi.org/10.1111/J.1528-1167.2007.01134.X google scholar
  • Braakhuis, A. (2019). Evidence on the health benefits of supplemental Propolis. Nutrients, 11(11). https://doi.org/10.3390/NU11112705 google scholar
  • Brigo, F., Igwe, S. C., & Lattanzi, S. (2019). Ethosuximide, sodium valproate or lamotrigine for absence seizures in children and ado-lescents. The Cochrane Database of Systematic Reviews, 2(2). https://doi.org/10.1002/14651858.CD003032.PUB4 google scholar
  • Crunelli, V., & Leresche, N. (2002). Childhood absence epilepsy: genes, channels, neurons and networks. Nature Reviews. Neuro-science, 3(5), 371-382. https://doi.org/10.1038/NRN811 google scholar
  • Da Silveira, C. C. S. D. M., Fernandes, L. M. P., Silva, M. L., Luz, D. A., Gomes, A. R. Q., Monteiro, M. C., Maia, C. S. F. (2016). Neu-robehavioral and Antioxidant Effects of Ethanolic Extract of Yel-low Propolis. Oxidative Medicine and Cellular Longevity, 2016. https://doi.org/10.1155/2016/2906953 google scholar
  • Danober, L., Deransart, C., Depaulis, A., Vergnes, M., & Marescaux, C. (1998). Pathophysiological mechanisms of genetic absence epilepsy in the rat. Progress in Neurobiology, 55(1), 27-57. https://doi.org/10.1016/S0301-0082(97)00091-9 google scholar
  • El Adaouia Taleb, R., Djebli, N., Chenini, H., Sahin, H., & Ko-layli, S. (2020). In vivo and in vitro anti-diabetic activity of ethanolic propolis extract. Journal of Food Biochemistry, 44(7). https://doi.org/10.1111/JFBC.13267 google scholar
  • Gocmez, S. S., Şahin, T. D., Yazir, Y., Duruksu, G., Eraldemir, F. C., Polat, S., & Utkan, T. (2019). Resveratrol prevents cognitive deficits by attenuating oxidative damage and in-flammation in rat model of streptozotocin diabetes induced vascular dementia. Physiology & Behavior, 201, 198-207. https://doi.org/10.1016/J.PHYSBEH.2018.12.012 google scholar
  • Guler, E., Bilir, O., Kocak, A. O., Atas, I., & Samanci, A. E. T. (2022). The prophylactic efficacy of Anatolian propo-lis in individuals at high risk of COVID-19. DOAJ (DOAJ: Directory of Open Access Journals), 26(2 Suppl), 53-60. https://doi.org/10.26355/eurrev_202212_30483 google scholar
  • Hirsch, E., French, J., Scheffer, I. E., Bogacz, A., Alsaadi, T., Sper-ling, M. R., . . . Zhou, D. (2022). ILAE definition of the Idio-pathic Generalized Epilepsy Syndromes: Position statement by the ILAE Task Force on Nosology and Definitions. Epilepsia, 63(6), 1475-1499. https://doi.org/10.1111/EPI.17236 google scholar
  • Hu, C., Luo, Y., Wang, H., Kuang, S., Liang, G., Yang, Y., . . . Yang, J. (2017). Re-evaluation of the interrelationships among the behav-ioral tests in rats exposed to chronic unpredictable mild stress. PloS One, 12(9). https://doi.org/10.1371/JOURNAL.PONE.0185129 google scholar
  • Jones, N. C., Salzberg, M. R., Kumar, G., Couper, A., Morris, M. J., & O’Brien, T. J. (2008). Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation. Experimental Neurology, 209(1), 254-260. https://doi.org/10.1016/J.EXPNEUROL.2007.09.026 google scholar
  • Kessler, S. K., & McGinnis, E. (2019). A Practical guide to treatment of childhood absence epilepsy. Paediatric Drugs, 21(1), 15-24. https://doi.org/10.1007/S40272-019-00325-X google scholar
  • Kulkarni, N. P., Vaidya, B., Narula, A. S., & Sharma, S. S. (2021). Neuroprotective Potential of Caffeic Acid Phenethyl Ester (CAPE) in CNS Disorders: Mechanistic and Therapeu-tic Insights. Current Neuropharmacology, 19(9), 1401-1415. https://doi.org/10.2174/1570159X19666210608165509 google scholar
  • Kwon, Y. S., Park, D. H., Shin, E. J., Kwon, M. S., Ko, K. H., Kim, W. K., . . . Kim, H. C. (2004). Antioxidant propolis at-tenuates kainate-induced neurotoxicity via adenosine A1 receptor modulation in the rat. Neuroscience Letters, 355(3), 231-235. https://doi.org/10.1016/j.neulet.2003.10.075 google scholar
  • Kuru, P., Torun, M., Halac, H. M., Temiz, G., Iskender, E., Karamahmutoglu, T., . . . Onat, F. Y. (2014). Electroencephalo-graphic and behavioral effects of intracerebroventricular or in-traperitoneal injections of toxic honey extract in adult Wistar rats and GAERS. Neurological Sciences, 35(12), 1903-1908. https://doi.org/10.1007/s10072-014-1858-6 google scholar
  • Leo, A., Nesci, V., Tallarico, M., Amodio, N., Gallo Cantafio, E. M., De Sarro, G., . . . Citraro, R. (2020). IL-6 receptor blockade by Tocilizumab has anti-absence and anti-epileptogenic effects in the WAG/Rij rat model of absence epilepsy. Neurotherapeutics: The Journal of the American Society for Experimental NeuroThera-peutics, 17(4), 2004-2014. https://doi.org/10.1007/S13311-020-00893-8 google scholar
  • Löscher, W., & Schmidt, D. (2011). Modern antiepileptic drug devel-opment has failed to deliver: ways out of the current dilemma. Epilepsia, 52(4), 657-678. https://doi.org/10.1111/J.1528-1167.2011.03024.X google scholar
  • Mannaa, F., El-Shamy, K. A., El-Shaikh, K. A., & El-Kassaby, M. (2011). Efficacy of fish liver oil and propolis as neu-roprotective agents in pilocarpine epileptic rats treated with valproate. Pathophysiology: The Official Journal of the In-ternational Society for Pathophysiology, 18(4), 287-294. https://doi.org/10.1016/J.PATHOPHYS.2011.04.002 google scholar
  • Masur, D., Shinnar, S., Cnaan, A., Shinnar, R. C., Clark, P., Wang, J., . . . Glauser, T. A. (2013). Pretreatment cognitive deficits and treatment effects on attention in childhood absence epilepsy. Neurology, 81(18), 1572-1580. https://doi.org/10.1212/WNL.0B013E3182A9F3CA google scholar
  • Mehta, V., Parashar, A., & Udayabanu, M. (2017). Quercetin prevents chronic unpredictable stress induced behavioral dys-function in mice by alleviating hippocampal oxidative and inflammatory stress. Physiology & Behavior, 171, 69-78. https://doi.org/10.1016/J.PHYSBEH.2017.01.006 google scholar
  • Orsolic, N., & Basic, I. (2003). Immunomodulation by water-soluble derivative of propolis: A factor of antitumor re-activity. Journal of Ethnopharmacology, 84(2-3), 265-273. https://doi.org/10.1016/S0378-8741(02)00329-X google scholar
  • Ott, D., Siddarth, P., Gurbani, S., Koh, S., Tournay, A., Shields, W. D., & Caplan, R. (2003). Behavioral disorders in pediatric epilepsy: unmet psychiatric need. Epilepsia, 44(4), 591-597. https://doi.org/10.1046/J.1528-1157.2003.25002.X google scholar
  • Reis, J. S. S., Oliveira, G. B., Monteiro, M. C., Machado, C. S., Torres, Y. R., Prediger, R. D., & Maia, C. S. F. (2014). Antidepressant- and anxiolytic-like activities of an oil ex-tract of propolis in rats. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 21(11), 1466-1472. https://doi.org/10.1016/J.PHYMED.2014.06.001 google scholar
  • Shorvon, S. (2011). Handbook of Epilepsy Treatment, Third Edition. Handbook of Epilepsy Treatment, Third Edition. https://doi.org/10.1002/9781444325201 google scholar
  • Slupski, W., Trocha, M., & Rutkowska, M. (2017). Pharmacodynamic and pharmacokinetic interactions between simvastatin and di-azepam in rats. Pharmacological Reports: PR, 69(5), 943-952. https://doi.org/10.1016/J.PHAREP.2017.03.012 google scholar
  • Steinborn, B., Zarowski, M., Winczewska-Wiktor, A., Wojcicka, M., Mlodzikowska-Albrecht, J., & Losy, J. (2014). Concentration of Il-10, Il-2, Il-6, TNFa in the blood serum in children with general-ized epilepsy treated by valproate. Pharmacological Reports: PR, 66(6), 972-975. https://doi.org/10.1016/J.PHAREP.2014.06.005 google scholar
  • Swamy, M., Suhaili, D., Sirajudeen, K. N. S., Mustapha, Z., & Govin-dasamy, C. (2014). Propolis ameliorates tumor nerosis factor-a, nitric oxide levels, caspase-3 and nitric oxide synthase activities in kainic acid mediated excitotoxicity in rat brain. African Journal of Traditional, Complementary, and Alternative Medicines: AJT-CAM, 11(5), 48-53. https://doi.org/10.4314/AJTCAM.V11I5.8 google scholar
  • Vrielynck, P. (2013). Current and emerging treatments for absence seizures in young patients. Neuropsychiatric Disease and Treat-ment, 9, 963-975. https://doi.org/10.2147/NDT.S30991 google scholar
  • Zimmerman, F. T., & Burgemeister, B. B. (1958). A new drug for petit mal epilepsy. Neurology, 8(10), 769-775. https://doi.org/10.1212/WNL.8.10.769 google scholar
  • Zingue, S., Nde, C. B. M., Michel, T., Ndinteh, D. T., Tchatchou, J., Adamou, M., . . . Njamen, D. (2017). Ethanol-extracted Cameroo-nian propolis exerts estrogenic effects and alleviates hot flushes in ovariectomized Wistar rats. BMC Complementary and Alternative Medicine, 17(1). https://doi.org/10.1186/S12906-017-1568-8 google scholar
  • Zulhendri, F., Perera, C. O., & Tandean, S. (2021). Can propolis be a useful adjuvant in brain and neurologi-cal disorders and injuries? A systematic scoping review of the latest experimental evidence. Biomedicines, 9(9). https://doi.org/10.3390/BIOMEDICINES9091227 google scholar
  • Zullkiflee, N., Taha, H., & Usman, A. (2022). Propolis: Its role and efficacy in human health and diseases. Molecules (Basel, Switzer-land), 27(18). https://doi.org/10.3390/MOLECULES27186120 google scholar

Year 2024, Volume: 54 Issue: 3, 378 - 385, 30.12.2024

Batuhan Yağmur , Şura Akat Pişkin , Erkan Civelek , Deniz Kaleli Durman , Nihan Çarcak

https://doi.org/10.26650/IstanbulJPharm.2024.1467008

Abstract

Project Number

1919B012104927

References

  • Akin, D., Ravizza, T., Maroso, M., Carcak, N., Eryigit, T., Vanzulli, I., ... Onat, F. Y. (2011). IL-ip is induced in reactive astro-cytes in the somatosensory cortex of rats with genetic absence epilepsy at the onset of spike-and-wave discharges, and contributes to their occurrence. Neurobiology of Disease, 44(3), 259-269. https://doi.org/10.1016/J.NBD.2011.05.015 google scholar
  • Altuntaş, Ü., Güzel, İ., & Özçelik, B. (2023). Phenolic con-stituents, antioxidant and antimicrobial activity and cluster-ing analysis of Propolis samples based on PCA from differ-ent regions of Anatolia. Molecules (Basel, Switzerland), 28(3). https://doi.org/10.3390/MOLECULES28031121 google scholar
  • Billiau, A. D., Witters, P., Ceulemans, B., Kasran, A., Wouters, C., & Lagae, L. (2007). Intravenous immunoglobulins in refractory childhood-onset epilepsy: effects on seizure frequency, EEG ac-tivity, and cerebrospinal fluid cytokine profile. Epilepsia, 48(9), 1739-1749. https://doi.org/10.1111/J.1528-1167.2007.01134.X google scholar
  • Braakhuis, A. (2019). Evidence on the health benefits of supplemental Propolis. Nutrients, 11(11). https://doi.org/10.3390/NU11112705 google scholar
  • Brigo, F., Igwe, S. C., & Lattanzi, S. (2019). Ethosuximide, sodium valproate or lamotrigine for absence seizures in children and ado-lescents. The Cochrane Database of Systematic Reviews, 2(2). https://doi.org/10.1002/14651858.CD003032.PUB4 google scholar
  • Crunelli, V., & Leresche, N. (2002). Childhood absence epilepsy: genes, channels, neurons and networks. Nature Reviews. Neuro-science, 3(5), 371-382. https://doi.org/10.1038/NRN811 google scholar
  • Da Silveira, C. C. S. D. M., Fernandes, L. M. P., Silva, M. L., Luz, D. A., Gomes, A. R. Q., Monteiro, M. C., Maia, C. S. F. (2016). Neu-robehavioral and Antioxidant Effects of Ethanolic Extract of Yel-low Propolis. Oxidative Medicine and Cellular Longevity, 2016. https://doi.org/10.1155/2016/2906953 google scholar
  • Danober, L., Deransart, C., Depaulis, A., Vergnes, M., & Marescaux, C. (1998). Pathophysiological mechanisms of genetic absence epilepsy in the rat. Progress in Neurobiology, 55(1), 27-57. https://doi.org/10.1016/S0301-0082(97)00091-9 google scholar
  • El Adaouia Taleb, R., Djebli, N., Chenini, H., Sahin, H., & Ko-layli, S. (2020). In vivo and in vitro anti-diabetic activity of ethanolic propolis extract. Journal of Food Biochemistry, 44(7). https://doi.org/10.1111/JFBC.13267 google scholar
  • Gocmez, S. S., Şahin, T. D., Yazir, Y., Duruksu, G., Eraldemir, F. C., Polat, S., & Utkan, T. (2019). Resveratrol prevents cognitive deficits by attenuating oxidative damage and in-flammation in rat model of streptozotocin diabetes induced vascular dementia. Physiology & Behavior, 201, 198-207. https://doi.org/10.1016/J.PHYSBEH.2018.12.012 google scholar
  • Guler, E., Bilir, O., Kocak, A. O., Atas, I., & Samanci, A. E. T. (2022). The prophylactic efficacy of Anatolian propo-lis in individuals at high risk of COVID-19. DOAJ (DOAJ: Directory of Open Access Journals), 26(2 Suppl), 53-60. https://doi.org/10.26355/eurrev_202212_30483 google scholar
  • Hirsch, E., French, J., Scheffer, I. E., Bogacz, A., Alsaadi, T., Sper-ling, M. R., . . . Zhou, D. (2022). ILAE definition of the Idio-pathic Generalized Epilepsy Syndromes: Position statement by the ILAE Task Force on Nosology and Definitions. Epilepsia, 63(6), 1475-1499. https://doi.org/10.1111/EPI.17236 google scholar
  • Hu, C., Luo, Y., Wang, H., Kuang, S., Liang, G., Yang, Y., . . . Yang, J. (2017). Re-evaluation of the interrelationships among the behav-ioral tests in rats exposed to chronic unpredictable mild stress. PloS One, 12(9). https://doi.org/10.1371/JOURNAL.PONE.0185129 google scholar
  • Jones, N. C., Salzberg, M. R., Kumar, G., Couper, A., Morris, M. J., & O’Brien, T. J. (2008). Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation. Experimental Neurology, 209(1), 254-260. https://doi.org/10.1016/J.EXPNEUROL.2007.09.026 google scholar
  • Kessler, S. K., & McGinnis, E. (2019). A Practical guide to treatment of childhood absence epilepsy. Paediatric Drugs, 21(1), 15-24. https://doi.org/10.1007/S40272-019-00325-X google scholar
  • Kulkarni, N. P., Vaidya, B., Narula, A. S., & Sharma, S. S. (2021). Neuroprotective Potential of Caffeic Acid Phenethyl Ester (CAPE) in CNS Disorders: Mechanistic and Therapeu-tic Insights. Current Neuropharmacology, 19(9), 1401-1415. https://doi.org/10.2174/1570159X19666210608165509 google scholar
  • Kwon, Y. S., Park, D. H., Shin, E. J., Kwon, M. S., Ko, K. H., Kim, W. K., . . . Kim, H. C. (2004). Antioxidant propolis at-tenuates kainate-induced neurotoxicity via adenosine A1 receptor modulation in the rat. Neuroscience Letters, 355(3), 231-235. https://doi.org/10.1016/j.neulet.2003.10.075 google scholar
  • Kuru, P., Torun, M., Halac, H. M., Temiz, G., Iskender, E., Karamahmutoglu, T., . . . Onat, F. Y. (2014). Electroencephalo-graphic and behavioral effects of intracerebroventricular or in-traperitoneal injections of toxic honey extract in adult Wistar rats and GAERS. Neurological Sciences, 35(12), 1903-1908. https://doi.org/10.1007/s10072-014-1858-6 google scholar
  • Leo, A., Nesci, V., Tallarico, M., Amodio, N., Gallo Cantafio, E. M., De Sarro, G., . . . Citraro, R. (2020). IL-6 receptor blockade by Tocilizumab has anti-absence and anti-epileptogenic effects in the WAG/Rij rat model of absence epilepsy. Neurotherapeutics: The Journal of the American Society for Experimental NeuroThera-peutics, 17(4), 2004-2014. https://doi.org/10.1007/S13311-020-00893-8 google scholar
  • Löscher, W., & Schmidt, D. (2011). Modern antiepileptic drug devel-opment has failed to deliver: ways out of the current dilemma. Epilepsia, 52(4), 657-678. https://doi.org/10.1111/J.1528-1167.2011.03024.X google scholar
  • Mannaa, F., El-Shamy, K. A., El-Shaikh, K. A., & El-Kassaby, M. (2011). Efficacy of fish liver oil and propolis as neu-roprotective agents in pilocarpine epileptic rats treated with valproate. Pathophysiology: The Official Journal of the In-ternational Society for Pathophysiology, 18(4), 287-294. https://doi.org/10.1016/J.PATHOPHYS.2011.04.002 google scholar
  • Masur, D., Shinnar, S., Cnaan, A., Shinnar, R. C., Clark, P., Wang, J., . . . Glauser, T. A. (2013). Pretreatment cognitive deficits and treatment effects on attention in childhood absence epilepsy. Neurology, 81(18), 1572-1580. https://doi.org/10.1212/WNL.0B013E3182A9F3CA google scholar
  • Mehta, V., Parashar, A., & Udayabanu, M. (2017). Quercetin prevents chronic unpredictable stress induced behavioral dys-function in mice by alleviating hippocampal oxidative and inflammatory stress. Physiology & Behavior, 171, 69-78. https://doi.org/10.1016/J.PHYSBEH.2017.01.006 google scholar
  • Orsolic, N., & Basic, I. (2003). Immunomodulation by water-soluble derivative of propolis: A factor of antitumor re-activity. Journal of Ethnopharmacology, 84(2-3), 265-273. https://doi.org/10.1016/S0378-8741(02)00329-X google scholar
  • Ott, D., Siddarth, P., Gurbani, S., Koh, S., Tournay, A., Shields, W. D., & Caplan, R. (2003). Behavioral disorders in pediatric epilepsy: unmet psychiatric need. Epilepsia, 44(4), 591-597. https://doi.org/10.1046/J.1528-1157.2003.25002.X google scholar
  • Reis, J. S. S., Oliveira, G. B., Monteiro, M. C., Machado, C. S., Torres, Y. R., Prediger, R. D., & Maia, C. S. F. (2014). Antidepressant- and anxiolytic-like activities of an oil ex-tract of propolis in rats. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 21(11), 1466-1472. https://doi.org/10.1016/J.PHYMED.2014.06.001 google scholar
  • Shorvon, S. (2011). Handbook of Epilepsy Treatment, Third Edition. Handbook of Epilepsy Treatment, Third Edition. https://doi.org/10.1002/9781444325201 google scholar
  • Slupski, W., Trocha, M., & Rutkowska, M. (2017). Pharmacodynamic and pharmacokinetic interactions between simvastatin and di-azepam in rats. Pharmacological Reports: PR, 69(5), 943-952. https://doi.org/10.1016/J.PHAREP.2017.03.012 google scholar
  • Steinborn, B., Zarowski, M., Winczewska-Wiktor, A., Wojcicka, M., Mlodzikowska-Albrecht, J., & Losy, J. (2014). Concentration of Il-10, Il-2, Il-6, TNFa in the blood serum in children with general-ized epilepsy treated by valproate. Pharmacological Reports: PR, 66(6), 972-975. https://doi.org/10.1016/J.PHAREP.2014.06.005 google scholar
  • Swamy, M., Suhaili, D., Sirajudeen, K. N. S., Mustapha, Z., & Govin-dasamy, C. (2014). Propolis ameliorates tumor nerosis factor-a, nitric oxide levels, caspase-3 and nitric oxide synthase activities in kainic acid mediated excitotoxicity in rat brain. African Journal of Traditional, Complementary, and Alternative Medicines: AJT-CAM, 11(5), 48-53. https://doi.org/10.4314/AJTCAM.V11I5.8 google scholar
  • Vrielynck, P. (2013). Current and emerging treatments for absence seizures in young patients. Neuropsychiatric Disease and Treat-ment, 9, 963-975. https://doi.org/10.2147/NDT.S30991 google scholar
  • Zimmerman, F. T., & Burgemeister, B. B. (1958). A new drug for petit mal epilepsy. Neurology, 8(10), 769-775. https://doi.org/10.1212/WNL.8.10.769 google scholar
  • Zingue, S., Nde, C. B. M., Michel, T., Ndinteh, D. T., Tchatchou, J., Adamou, M., . . . Njamen, D. (2017). Ethanol-extracted Cameroo-nian propolis exerts estrogenic effects and alleviates hot flushes in ovariectomized Wistar rats. BMC Complementary and Alternative Medicine, 17(1). https://doi.org/10.1186/S12906-017-1568-8 google scholar
  • Zulhendri, F., Perera, C. O., & Tandean, S. (2021). Can propolis be a useful adjuvant in brain and neurologi-cal disorders and injuries? A systematic scoping review of the latest experimental evidence. Biomedicines, 9(9). https://doi.org/10.3390/BIOMEDICINES9091227 google scholar
  • Zullkiflee, N., Taha, H., & Usman, A. (2022). Propolis: Its role and efficacy in human health and diseases. Molecules (Basel, Switzer-land), 27(18). https://doi.org/10.3390/MOLECULES27186120 google scholar
There are 35 citations in total.

Details

Primary Language English
Subjects Pharmacology and Pharmaceutical Sciences (Other)
Journal Section Original Article
Authors

Batuhan Yağmur 0009-0006-2560-5008

Şura Akat Pişkin 0000-0002-0437-3379

Erkan Civelek 0000-0002-6503-5226

Deniz Kaleli Durman 0000-0002-8669-7480

Nihan Çarcak 0000-0001-6254-4319

Project Number 1919B012104927
Publication Date December 30, 2024
Submission Date April 9, 2024
Acceptance Date June 29, 2024
Published in Issue Year 2024 Volume: 54 Issue: 3

Cite

APA Yağmur, B., Akat Pişkin, Ş., Civelek, E., Kaleli Durman, D., et al. (2024). Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy. İstanbul Journal of Pharmacy, 54(3), 378-385. https://doi.org/10.26650/IstanbulJPharm.2024.1467008
AMA Yağmur B, Akat Pişkin Ş, Civelek E, Kaleli Durman D, Çarcak N. Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy. iujp. December 2024;54(3):378-385. doi:10.26650/IstanbulJPharm.2024.1467008
Chicago Yağmur, Batuhan, Şura Akat Pişkin, Erkan Civelek, Deniz Kaleli Durman, and Nihan Çarcak. “Effects of Anatolian Propolis on Absence Seizures and Anxiety in Rats With Genetic Absence Epilepsy”. İstanbul Journal of Pharmacy 54, no. 3 (December 2024): 378-85. https://doi.org/10.26650/IstanbulJPharm.2024.1467008.
EndNote Yağmur B, Akat Pişkin Ş, Civelek E, Kaleli Durman D, Çarcak N (December 1, 2024) Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy. İstanbul Journal of Pharmacy 54 3 378–385.
IEEE B. Yağmur, Ş. Akat Pişkin, E. Civelek, D. Kaleli Durman, and N. Çarcak, “Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy”, iujp, vol. 54, no. 3, pp. 378–385, 2024, doi: 10.26650/IstanbulJPharm.2024.1467008.
ISNAD Yağmur, Batuhan et al. “Effects of Anatolian Propolis on Absence Seizures and Anxiety in Rats With Genetic Absence Epilepsy”. İstanbul Journal of Pharmacy 54/3 (December 2024), 378-385. https://doi.org/10.26650/IstanbulJPharm.2024.1467008.
JAMA Yağmur B, Akat Pişkin Ş, Civelek E, Kaleli Durman D, Çarcak N. Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy. iujp. 2024;54:378–385.
MLA Yağmur, Batuhan et al. “Effects of Anatolian Propolis on Absence Seizures and Anxiety in Rats With Genetic Absence Epilepsy”. İstanbul Journal of Pharmacy, vol. 54, no. 3, 2024, pp. 378-85, doi:10.26650/IstanbulJPharm.2024.1467008.
Vancouver Yağmur B, Akat Pişkin Ş, Civelek E, Kaleli Durman D, Çarcak N. Effects of Anatolian propolis on absence seizures and anxiety in rats with genetic absence epilepsy. iujp. 2024;54(3):378-85.
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