Solid Calcium Carbonate formation detected by SEM-EDS within the epileptic focus of an in vivo epilepsy model of Wistar rats Formación de cristales de calcio dentro del foco epiléptico de un modelo de epilepsia in vivo
Conteúdo do artigo principal
Resumo
Epilepsy represents a significant health concern, affecting an estimated 2 million individuals in Mexico, with patients enduring more than 70 seizures daily. In the present study, refractory epilepsy was induced in Wistar rats by repeated stimulation with pentylenetetrazol (PTZ), ranging from one to one hundred stimulations. Hippocampal tissue was analyzed via scanning electron microscopy (SEM) and energy-dispersive X-ray fluorescence (EDS). The formation of solid calcium carbonate (CaCO3) crystals within the epileptic focus where observed. Notably, the concentration of CaCO3 exhibited a direct correlation with the number of stimulations, suggesting a progressive increase over the course of these events. This study puts forth a hypothesis elucidating the mechanism behind CaCO3 crystal formation in response to PTZ-induced seizures. Further research is needed to ascertain whether there exists a correlation between the dysregulation of calcium ions (Ca2+) in epilepsy and the formation of CaCO3. This inquiry opens avenues for deeper understanding and potential advancements in the diagnosis of epilepsy and related neurological disorders.
Downloads
Detalhes do artigo
Mundo Nano. Revista Interdisciplinaria en Nanociencias y Nanotecnología, editada por la Universidad Nacional Autónoma de México, se distribuye bajo una Licencia Creative Commons Atribución-NoComercial 4.0 Internacional.
Basada en una obra en http://www.mundonano.unam.mx.
Referências
Akita, Tenpei and Atsuo Fukuda. (2020). Intracellular Cl− Dysregulation causing and caused by pathogenic neuronal activity. Pflügers Archiv – European Journal of Physiology, 472(7): 977-87. https://doi.org/10.1007/s00424-020-02375-4.
Anzellotti, Francesca, Fedele Dono, Giacomo Evangelista, Martina Di Pietro, Claudia Carrarini, Mirella Russo, Camilla Ferrante, Stefano L. Sensi and Marco Onofrj. (2020). Psychogenic non-epileptic seizures and pseudo-refractory epilepsy, a management challenge. Frontiers in Neurology, 11(June). https://doi.org/10.3389/fneur.2020.00461.
Auer, Theresa, Philipp Schreppel, Thomas Erker and Christoph Schwarzer. (2020). Impaired chloride homeostasis in epilepsy: molecular basis, impact on treatment and current treatment approaches. Pharmacology & Therapeutics, 205(January): 107422. https://doi.org/10.1016/j.pharmthera.2019.107422.
Becker, Z. E. (1936). A comparison between the action of carbonic acid and other acids upon the living cell. Protoplasma 25(1): 161-75. https://doi.org/10.1007/BF01839067.
Beghi, Ettore. (2020). The epidemiology of epilepsy. Neuroepidemiology, 54(2): 185-91. https://doi.org/10.1159/000503831.
Begley, Charles, Ryan G. Wagner, Annette Abraham, Ettore Beghi, Charles Newton, Churl‐Su Kwon, David Labiner and Andrea S. Winkler. (2022). The global cost of epilepsy: a systematic review and extrapolation. Epilepsia, 63(4): 892-903. https://doi.org/10.1111/epi.17165.
Benaim, Gustavo, Alberto E. Paniz-Mondolfi, Emilia Mia Sordillo and Nathalia Martínez-Sotillo. (2020). Disruption of intracellular calcium homeostasis as a therapeutic target against trypanosoma cruzi. Frontiers in Cellular and Infection Microbiology, 10(February). https://doi.org/10.3389/fcimb.2020.00046.
Ben-Ari, Yehezkel. (2002). Excitatory actions of gaba during development: the nature of the nurture. Nature Reviews Neuroscience, 3 (9): 728-39. https://doi.org/10.1038/nrn920.
Bojarski, Lukasz, Jochen Herms and Jacek Kuznicki. (2008). Calcium dysregulation in Alzheimer’s disease. Neurochemistry International, 52(4-5): 621-33. https://doi.org/10.1016/j.neuint.2007.10.002.
Brenner, Robert, Karen S. Wilcox, Jeffrey L. Noebels, Massimo Avoli, Michael A. Rogawski, Richard W. Olsen, Antonio V. Delgado-Escueta (eds.). (2012). Potassium channelopathies of epilepsy. En Jasper’s basic mechanisms of the epilepsies. 4a ed. Bethesda (MD): National Center for Biotechnology Information (US).
Bushinsky, D. A. and R. J. Lechleider. (1987). Mechanism of proton-induced bone calcium release: calcium carbonate-dissolution. American Journal of Physiology-Renal Physiology, 253(5): F998-1005. https://doi.org/10.1152/ajprenal.1987.253.5.F998.
Calì, Tito, Denis Ottolini and Marisa Brini. (2014). Calcium signaling in Parkinson’s disease. Cell and Tissue Research, 357(2): 439-54. https://doi.org/10.1007/s00441-014-1866-0.
Calvo-Rodríguez, María, Elizabeth K. Kharitonova and Brian J. Bacskai. (2020). Therapeutic strategies to target calcium dysregulation in Alzheimer’s disease. Cells, 9(11): 2513. https://doi.org/10.3390/cells9112513.
Campbell, Iain L., Thomas Krucker, Scott Steffensen, Yvette Akwa, Henry C. Powell, Thomas Lane, Daniel J. Carr, Lisa H. Gold, Steven J. Henriksen and George R. Siggins. (1999). Structural and functional neuropathology in transgenic mice with CNS expression of IFN-Α1 published on the World Wide Web on 17 March, 1999.1. Brain Research, 835(1): 46-61. https://doi.org/10.1016/S0006-8993(99)01328-1.
Catterall, William A. (2014). Sodium channels, inherited epilepsy y antiepileptic drugs. Annual Review of Pharmacology and Toxicology, 54(1): 317-38. https://doi.org/10.1146/annurev-pharmtox-011112-140232.
Chen, Tsang-Shan, Tzu-Hsin Huang, Ming-Chi Lai and Chin-Wei Huang. (2023). The role of glutamate receptors in epilepsy. Biomedicines, 11(3): 783. https://doi.org/10.3390/biomedicines11030783.
Cheville, N. F. and J. Stasko. (2014). Techniques in electron microscopy of animal tissue. Veterinary Pathology, 51(1): 28-41. https://doi.org/10.1177/0300985813505114.
Clapham, David E. (1995). Calcium signaling. Cell, 80(2): 259-68. https://doi.org/10.1016/0092-8674(95)90408-5.
Dhir, Ashish. (2012). Pentylenetetrazol (PTZ) kindling model of epilepsy. Current Protocols in Neuroscience, 58(1). https://doi.org/10.1002/0471142301.ns0937s58.
Ding, Fengfei, Qian Sun, Carter Long, Rune Nguyen Rasmussen, Sisi Peng, Qiwu Xu, Ning Kang et al. (2024). Dysregulation of extracellular potassium distinguishes healthy ageing from neurodegeneration. Brain, 147(5): 1726-39. https://doi.org/10.1093/brain/awae075.
Dodd, Antony N., Jörg Kudla and Dale Sanders. (2010). The language of calcium signaling. Annual Review of Plant Biology, 61(1): 593-620. https://doi.org/10.1146/annurev-arplant-070109-104628.
Dreier, J. P. and U. Heinemann. (1991). Regional and time dependent variations of low Mg2+ induced epileptiform activity in rat temporal cortex slices. Experimental Brain Research, 87(3). https://doi.org/10.1007/BF00227083.
Elger, Christian E., Christoph Helmstaedter and Martin Kurthen. (2004). Chronic epilepsy and cognition. The Lancet Neurology, 3(11): 663-72. https://doi.org/10.1016/S1474-4422(04)00906-8.
Engel, Jerome, Asla Pitkänen, Jeffrey A. Loeb, F. Edward Dudek, Edward H. Bertram, Andrew J. Cole, Solomon L. Moshé et al. (2013). Epilepsy biomarkers. Epilepsia, 54(s4): 61-69. https://doi.org/10.1111/epi.12299.
Falco-Walter, Jessica. (2020). Epilepsy – Definition, classification, pathophysiology and epidemiology. Seminars in Neurology, 40(06): 617-23. https://doi.org/10.1055/s-0040-1718719.
Froberg, K., R. P. Dorion and K. E. McMartin. (2006). The role of calcium oxalate crystal deposition in cerebral vessels during ethylene glycol poisoning. Clinical Toxicology, 44(3): 315-18. https://doi.org/10.1080/15563650600588460.
Ghosh, Shampa, Jitendra Kumar Sinha, Tarab Khan, Kuramkote Shivanna Devaraju, Prabhakar Singh, Kumar Vaibhav and Pankaj Gaur. (2021). Pharmacological and therapeutic approaches in the treatment of epilepsy. Biomedicines, 9(5): 470. https://doi.org/10.3390/biomedicines9050470.
Girardi‐Schappo, Mauricio, Fatemeh Fadaie, Hyo Min Lee, Benoit Caldairou, Viviane Sziklas, Joelle Crane, Boris C. Bernhardt, Andrea Bernasconi and Neda Bernasconi. (2021). Altered communication dynamics reflect cognitive deficits in temporal lobe epilepsy. Epilepsia, 62(4): 1022-33. https://doi.org/10.1111/epi.16864.
Gleichmann, Marc and Mark P. Mattson. (2011). Neuronal calcium homeostasis and dysregulation. Antioxidants & Redox Signaling, 14(7): 1261-73. https://doi.org/10.1089/ars.2010.3386.
Goldstein, Joseph I., Dale E. Newbury, Joseph R. Michael, Nicholas W. M. Ritchie, John Henry J. Scott and David C. Joy. (2018). Scanning Electron Microscopy and X-Ray Microanalysis. Nueva York, NY: Springer New York. https://doi.org/10.1007/978-1-4939-6676-9.
Grisar, Thierry. (1984). Glial and neuronal Na+–K+ pump in epilepsy. Annals of Neurology, 16(S1): S128-34. https://doi.org/10.1002/ana.410160719.
Grosskreutz, Julian, Ludo van den Bosch and Bernhard U. Keller. (2010). Calcium dysregulation in amyotrophic lateral sclerosis. Cell Calcium, 47(2): 165-74. https://doi.org/10.1016/j.ceca.2009.12.002.
Guery, Deborah and Sylvain Rheims. (2021). Clinical management of drug resistant epilepsy: a review on current strategies. Neuropsychiatric Disease and Treatment, 17(July): 2229-42. https://doi.org/10.2147/NDT.S256699.
Guzmán-Jiménez, Diana Elena, Jaime Berumen Campos, Carlos Alberto Venegas-Vega, Mariana Alejandre Sánchez and Ana Luisa Velasco. (2020). Familial mesial temporal lobe epilepsy in Mexico: inheritance pattern and clinical features. Epilepsy Research, 167(November): 106450. https://doi.org/10.1016/j.eplepsyres.2020.106450.
Harvey, Jean A., Margaret M. Zobitz and Charles Y. C. Pak. (1988). Dose dependency of calcium absorption: a comparison of calcium carbonate and calcium citrate. Journal of Bone and Mineral Research, 3(3): 253-58. https://doi.org/10.1002/jbmr.5650030303.
Heinemann, U., A. Konnerth, R. Pumain y W. J. Wadman. (1986). Extracellular calcium and potassium concentration changes in chronic epileptic brain tissue. Advances in Neurology, 44: 641-61.
Helmstaedter, Christoph, Martin Kurthen, Silke Lux, Markus Reuber and Christian Erich Elger. (2003). Chronic epilepsy and cognition: a longitudinal study in temporal lobe epilepsy. Annals of Neurology, 54(4): 425-32. https://doi.org/10.1002/ana.10692.
Hotka, Matej and Helmut Kubista. (2019). The paroxysmal depolarization shift in epilepsy research. The International Journal of Biochemistry & Cell Biology, 107(February): 77-81. https://doi.org/10.1016/j.biocel.2018.12.006.
Ives-Deliperi, Victoria and James T. Butler. (2021). Mechanisms of cognitive impairment in temporal lobe epilepsy: a systematic review of resting-state functional connectivity studies. Epilepsy & Behavior, 115(February): 107686. https://doi.org/10.1016/j.yebeh.2020.107686.
Janson, Marnie T. and Jacquelyn L. Bainbridge. (2021). Continuing burden of refractory epilepsy. Annals of Pharmacotherapy, 55(3): 406-8. https://doi.org/10.1177/1060028020948056.
Jiang, C. and G. G. Haddad. (1991). Effect of anoxia on intracellular and extracellular potassium activity in hypoglossal neurons in vitro. Journal of Neurophysiology, 66(1): 103-11. https://doi.org/10.1152/jn.1991.66.1.103.
Kawamata, Hibiki and Giovanni Manfredi. (2010). Mitochondrial dysfunction and intracellular calcium dysregulation in ALS. Mechanisms of Ageing and Development, 131(7-8): 517-26. https://doi.org/10.1016/j.mad.2010.05.003.
Kempen, Paul J., Moritz F. Kircher, Adam de la Zerda, Cristina L. Zavaleta, Jesse V. Jokerst, Ingo K. Mellinghoff, Sanjiv S. Gambhir and Robert Sinclair. (2015). A correlative optical microscopy and scanning electron microscopy approach to locating nanoparticles in brain tumors. Micron, 68(January): 70-76. https://doi.org/10.1016/j.micron.2014.09.004.
Knott, Graham, Herschel Marchman, David Wall and Ben Lich. (2008). Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. The Journal of Neuroscience, 28(12): 2959-64. https://doi.org/10.1523/JNEUROSCI.3189-07.2008.
Knott, Graham, Stéphanie Rosset and Marco Cantoni. (2011). Focussed ion beam milling and scanning electron microscopy of brain tissue. Journal of Visualized Experiments, 53(July). https://doi.org/10.3791/2588.
Kovac, Stjepana, Albena Dinkova Kostova, Alexander Herrmann, Nico Melzer, Sven Meuth and Ali Gorji. (2017). Metabolic and homeostatic changes in seizures and acquired epilepsy – Mitochondria, calcium dynamics and reactive oxygen species. International Journal of Molecular Sciences, 18(9): 1935. https://doi.org/10.3390/ijms18091935.
Kraus-Friedmann, N. (1990). Calcium sequestration in the liver. Cell Calcium, 11(10): 625-40. https://doi.org/10.1016/0143-4160(90)90017-O.
Kubista, Helmut, Stefan Boehm and Matej Hotka. (2019). The paroxysmal depolarization shift: reconsidering its role in epilepsy, epileptogenesis and beyond. International Journal of Molecular Sciences, 20(3): 577. https://doi.org/10.3390/ijms20030577.
Kwan, Patrick, Alexis Arzimanoglou, Anne T. Berg, Martin J. Brodie, W. Allen Hauser, Gary Mathern, Solomon L. Moshé, Emilio Perucca, Samuel Wiebe and Jacqueline French. (2010). Definition of drug resistant epilepsy: consensus proposal by the ad hoc task force of the ILAE Commission on Therapeutic Strategies. Epilepsia, 51(6): 1069-77. https://doi.org/10.1111/j.1528-1167.2009.02397.x.
Leal, Sonia S. and Claudio M. Gomes. (2015). Calcium dysregulation links ALS defective proteins and motor neuron selective vulnerability. Frontiers in Cellular Neuroscience, 9(June). https://doi.org/10.3389/fncel.2015.00225.
Lenton, Samuel, Tommy Nylander, Susana C. M. Teixeira and Carl Holt. (2015). A review of the biology of calcium phosphate sequestration with special reference to milk. Dairy Science & Technology, 95(1): 3-14. https://doi.org/10.1007/s13594-014-0177-2.
Lerche, Holger. (2020). Drug-resistant epilepsy – Time to target mechanisms. Nature Reviews Neurology, 16(11): 595-96. https://doi.org/10.1038/s41582-020-00419-y.
Lévesque, Maxime, David Ragsdale and Massimo Avoli. (2019). Evolving mechanistic concepts of epileptiform synchronization and their relevance in curing focal epileptic disorders. Current Neuropharmacology, 17(9): 830-42. https://doi.org/10.2174/1570159X17666181127124803.
Lewis, Amanda J., Christel Genoud, Mélissa Pont, Wilma D. J. van de Berg, Stephan Frank, Henning Stahlberg, Sarah H. Shahmoradian and Ashraf Al-Amoudi. (2019). Imaging of post-mortem human brain tissue using electron and X-ray microscopy. Current Opinion in Structural Biology, 58(October):138-48. https://doi.org/10.1016/j.sbi.2019.06.003.
Löscher, Wolfgang. (2017). Animal models of seizures and epilepsy: past, present and future role for the discovery of antiseizure drugs. Neurochemical Research, 42(7): 1873-88. https://doi.org/10.1007/s11064-017-2222-z.
Ludtmann, Marthe H. R. and Andrey Y. Abramov. (2018). Mitochondrial calcium imbalance in Parkinson’s disease. Neuroscience Letters, 663(January):86-90. https://doi.org/10.1016/j.neulet.2017.08.044.
Moore, L., T. Chen, H. R. Knapp and E. J. Landon. (1975). Energy-dependent cal- cium sequestration activity in rat liver microsomes. Journal of Biological Chemistry, 250(12): 4562-68. https://doi.org/10.1016/S0021-9258(19)41338-0.
Movsesian, M. (1998). Calcium sequestration by the sarcoplasmic reticulum in heart failure. Cardiovascular Research, 37(2): 352-59. https://doi.org/10.1016/S0008-6363(97)00259-9.
Newbury, Dale E. (2005). Misidentification of major constituents by automatic qualitative energy dispersive X-ray microanalysis: a problem that threatens the credibility of the analytical community. Microscopy and Microanalysis, 11(6): 545-61. https://doi.org/10.1017/S1431927605050531.
Novak, Ajda, Karmen Vizjak and Martin Rakusa. (2022). Cognitive impairment in people with epilepsy. Journal of Clinical Medicine, 11(1): 267. https://doi.org/10.3390/jcm11010267.
Ohgushi, Hajime, Motoaki Okumura, Takafumi Yoshikawa, Keisuke Inboue, Norio Senpuku, Susumu Tamai and Edwin C. Shors. (1992). Bone formation pro- cessin porous calcium carbonate and hydroxyapatite. Journal of Biomedical Materials Research, 26(7): 885-95. https://doi.org/10.1002/jbm.820260705.
Oyrer, Julia, Snezana Maljevic, Ingrid E. Scheffer, Samuel F. Berkovic, Steven Petrou and Christopher A. Reid. (2018). Ion channels in genetic epilepsy: from genes and mechanisms to disease-targeted therapies. Pharmacological Reviews, 70(1): 142-73. https://doi.org/10.1124/pr.117.014456.
Perucca, Emilio. (2021). The pharmacological treatment of epilepsy: recent advances and future perspectives. Acta Epileptologica, 3(1): 22. https://doi.org/10.1186/s42494-021-00055-z.
Perucca, Piero, Melanie Bahlo and Samuel F. Berkovic. (2020). The genetics of epilepsy. Annual Review of Genomics and Human Genetics, 21(1): 205-30. https://doi.org/10.1146/annurev-genom-120219-074937.
Pesqueira, Gerardo Quiñones, Daniel San-Juan, Rosana Huerta Albarrán, Máximo León Vázquez, Gerardo Quiñones Canales and Jorge González Pesqueira. (2023). A systematic review of the epidemiology of epilepsy in Mexico during 1970 to 2020. Arquivos de Neuro-Psiquiatria, 81(01): 074-080. https://doi.org/10.1055/s-0042-1758647.
Pires, Geoffrey, Dominique Leitner, Eleanor Drummond, Evgeny Kanshin, Shruti Nayak, Manor Askenazi, Arline Faustin et al. (2021). Proteomic differences in the hippocampus and cortex of epilepsy brain tissue. Brain Communications, 3(2). https://doi.org/10.1093/braincomms/fcab021.
Pumain, R., C. Menini, U. Heinemann, J. Louvel and C. Silva-Barrat. (1985). Chemical synaptic transmission is not necessary for epileptic seizures to persist in the baboon Papio papio. Experimental Neurology, 89(1): 250-58. https://doi.org/10.1016/0014-4886(85)90280-8.
Raimondo, Joseph V., Richard J. Burman, Arieh A. Katz and Colin J. Akerman. (2015). Ion dynamics during seizures. Frontiers in Cellular Neuroscience, 9(October). https://doi.org/10.3389/fncel.2015.00419.
Rho, Jong M. and Detlev Boison. (2022). The metabolic basis of epilepsy. Nature Reviews Neurology 18(6): 333-47. https://doi.org/10.1038/s41582-022-00651-8.
Riva, Antonella, Alice Golda, Ganna Balagura, Elisabetta Amadori, Maria Stella Vari, Gianluca Piccolo, Michele Iacomino et al. (2021). New trends and most promising therapeutic strategies for epilepsy treatment. Frontiers in Neurology, 12(December). https://doi.org/10.3389/fneur.2021.753753.
Rozensztrauch, Anna and Aleksandra Kołtuniuk. (2022). The quality of life of children with epilepsy and the impact of the disease on the family functioning. International Journal of Environmental Research and Public Health, 19(4): 2277. https://doi.org/10.3390/ijerph19042277.
Rubio, Carmen, Rudy Luna, Monserrat Ibarra-Velasco and Ángel Lee. (2021). Epilepsy: a bibliometric analysis (1968-2020) of the Instituto Nacional de Neurología y Neurocirugía ‘Manuel Velasco Suárez’ in Mexico. Epilepsy & Behavior, 115(February): 107676. https://doi.org/10.1016/j.yebeh.2020.107676.
Samokhina, E. and Alexander Samokhin. (2018). Neuropathological profile of the pentylenetetrazol (PTZ) kindling model. International Journal of Neuroscience, 128(11): 1086-96. https://doi.org/10.1080/00207454.2018.1481064.
Sarlo, Gabrielle L. and Kathleen F. Holton. (2021). Brain concentrations of glutamate and GABA in human epilepsy: a review. Seizure, 91(October): 213-27. https://doi.org/10.1016/j.seizure.2021.06.028.
Schapira, Anthony H. V. (2013). Calcium dysregulation in Parkinson’s disease. Brain, 136(7): 2015-16. https://doi.org/10.1093/brain/awt180.
Scharfman, Helen E. (2007). The neurobiology of epilepsy. Current Neurology and Neuroscience Reports, 7(4): 348-54. https://doi.org/10.1007/s11910-007-0053-z.
Schneider, Gerd, Peter Guttmann, Stefan Heim, Stefan Rehbein, Florian Mueller, Kunio Nagashima, J. Bernard Heymann, Waltraud G. Müller and James G. McNally. (2010). Three-dimensional cellular ultrastructure resolved by X-ray microscopy. Nature Methods, 7(12): 985-87. https://doi.org/10.1038/nmeth.1533.
Siesjö, Bo K. (1986). Cellular calcium metabolism, seizures y ischemia. Mayo Clinic Proceedings, 61(4): 299-302. https://doi.org/10.1016/S0025-6196(12)61935-1.
Singh, Tanveer, Awanish Mishra and Rajesh Kumar Goel. (2021). PTZ kindling model for epileptogenesis, refractory epilepsy, and associated comorbidities: relevance and reliability. Metabolic Brain Disease, 36(7): 1573-90. https://doi.org/10.1007/s11011-021-00823-3.
Spampanato, Jay, Ildiko Aradi, Ivan Soltesz and Alan L. Goldin. (2004). Increased neuronal firing in computer simulations of sodium channel mutations that cause generalized epilepsy with febrile seizures plus. Journal of Neurophysiology, 91(5): 2040-50. https://doi.org/10.1152/jn.00982.2003.
Spiller, Allison E. y Ronald J. Racine. (1994). The effect of kindling beyond the ‘Stage 5’ criterion on paired-pulse depression and hilar cell counts in the dentate gyrus. Brain Research, 635(1-2): 139-47. https://doi.org/10.1016/0006-8993(94)91433-8.
Steinlein, Ortrud K. (2014). Calcium signaling and epilepsy. Cell and Tissue Research, 357(2): 385-93. https://doi.org/10.1007/s00441-014-1849-1.
Strzelczyk, Adam, Angel Aledo-Serrano, Antonietta Coppola, Adrien Didelot, Elizabeth Bates, Ricardo Sainz-Fuertes and Charlotte Lawthom. (2023). The impact of epilepsy on quality of life: findings from a European survey. Epilepsy & Behavior, 142(May): 109179. https://doi.org/10.1016/j.yebeh.2023.109179.
Sultana, Bushra, Marie-Andrée Panzini, Ariane Veilleux Carpentier, Jacynthe Comtois, Bastien Rioux, Geneviève Gore, Prisca R. Bauer et al. (2021). Incidence and prevalence of drug-resistant epilepsy. Neurology, 96(17): 805-17. https://doi.org/10.1212/WNL.0000000000011839.
Sun, Jinyi, Yang Zheng, Zhong Chen and Yi Wang. (2022). The role of Na+ – K+ – ATPase in the epileptic brain. CNS Neuroscience & Therapeutics, 28(9): 1294-1302. https://doi.org/10.1111/cns.13893.
Symonds, Joseph D. and Amy McTague. (2020). Epilepsy and developmental disorders: next generation sequencing in the clinic. European Journal of Paediatric Neurology, 24(January):15-23. https://doi.org/10.1016/j.ejpn.2019.12.008.
Tian, Guo-Feng, Hooman Azmi, Takahiro Takano, Qiwu Xu, Weiguo Peng, Jane Lin, NancyAnn Oberheim et al. (2005). An astrocytic basis of epilepsy. Nature Medicine, 11(9): 973-81. https://doi.org/10.1038/nm1277.
Toro Pérez, Juan Enrique, Ana Suller Martí, Manuel Herrera Aramburu, Juan Bottan and Jorge G. Burneo. (2020). Epilepsia del lóbulo temporal plus: revisión. Revista de Neurología, 71(06): 225. https://doi.org/10.33588/rn.7106.2020339.
Tryba, Andrew K., Edward M. Merricks, Somin Lee, Tuan Pham, SungJun Cho, Douglas R. Nordli, Tahra L. Eissa et al. (2019). Role of paroxysmal depolarization in focal seizure activity. Journal of Neurophysiology, 122(5): 1861-73. https://doi.org/10.1152/jn.00392.2019.
Tsolaki, Elena and Sergio Bertazzo. (2019). Pathological mineralization: the potential of mineralomics. Materials, 12(19): 3126. https://doi.org/10.3390/ma12193126.
Vonck, Kristl, Arnaud Biraben, Magdalena Bosak, Poul Jørgen Jennum, Vasilios K. Kimiskidis, Petr Marusic, James W. Mitchell et al. (2023). Usage and impact of patient‐reported outcomes in epilepsy. Brain and Behavior, 13(12). https://doi.org/10.1002/brb3.3342.
Wang, Yong, Yun Shi and Huafeng Wei. (2017). Calcium dysregulation in Alzheimer’s disease: a target for new drug development. Journal of Alzheimer’s Disease & Parkinsonism, 7(5). https://doi.org/10.4172/2161-0460.1000374.
WHO. (2024). Epilepsy. World Health Organization. February 7, 2024.
Wiechers, H. N. S, P Sturrock and G. V. R. Marais. (1975). Calcium carbonate crystallization kinetics. Water Research, 9(9): 835-45. https://doi.org/10.1016/0043-1354(75)90143-8.
Wojda, Urszula, Elzbieta Salinska and Jacek Kuznicki. (2008). Calcium ions in neuronal degeneration. IUBMB Life, 60(9): 575-90. https://doi.org/10.1002/iub.91.
Wu, Dongyan, Feiyan Chang, Dantao Peng, Sheng Xie, Xiaoxuan Li and Wenjing Zheng. (2020). The morphological characteristics of hippocampus and thalamus in mesial temporal lobe epilepsy. BMC Neurology, 20(1): 235. https://doi.org/10.1186/s12883-020-01817-x.
Wyroba, Elżbieta, Szymon Suski, Karolina Miller and Rafał Bartosiewicz. (2015). Biomedical and agricultural applications of energy dispersive X-ray spectroscopy in electron microscopy. Cellular and Molecular Biology Letters, 20(3). https://doi.org/10.1515/cmble-2015-0028.
Yu, Jin-Tai, Raymond Chuen-Chung Chang and Lan Tan. (2009). Calcium dysregulation in Alzheimer’s disease: from mechanisms to therapeutic opportunities. Progress in Neurobiology, 89(3): 240-55. https://doi.org/10.1016/j.pneurobio.2009.07.009.
Zündorf, Gregor and Georg Reiser. (2011). Calcium dysregulation and homeostasis of neural calcium in the molecular mechanisms of neurodegenerative diseases provide multiple targets for neuroprotection. Antioxidants & Redox Signaling, 14(7): 1275-88. https://doi.org/10.1089/ars.2010.3359.