IDIOPATHIC FOCAL EPILEPSY WITH MOTOR SEIZURES IN 50 POODLES IN ARGENTINA: ELECTROCLINICAL CHARACTERIZATION AND RESPONSE TO THERAPY
Abstract
Focal motor seizures were described as a possible clinical manifestation of idiopathic epilepsy in Poodles. The objective of this work is to characterize the particular presentation of the Focal Idiopathic Epilepsy with Motor Seizures (FIEwMS) of this breed in Argentina.
Fifty Poodles (toy, miniature and moyen varieties) with Idiopathic Epilepsy with focal seizures, diagnosed according to the International Veterinary Task Force (IVETF) criteria were investigated. The statistical associations between the age of onset, weight, reproductive status, variety, generalization of the seizures, presence of cluster seizures, spontaneous evolution (need or not of medication), number of anti-seizure medications (ASMs) used, were investigated. The multivariate cluster analysis technique and principal component analysis were used. The dendogram was constructed using the averaging linked method. The partial association between variables was studied, according to their features, using Kruskall-Wallis and Mann-Whitney-Wilcoxon tests, independence test (χ2 Pearson), G2 test (maximum likelihood), or logistic regression. The significance level was 5% (p£0.05).
The motor seizures were classified as tonic/dystonic, asymmetric, with compromise of the epiaxial musculature and proximal appendicular region, with elevation of one limb, without alteration of consciousness. Six dogs presented generalized seizures. The electroencephalogram showed centroparietal epileptiform discharges. All dogs responded to therapy, with no therapeutic failures, most with monotherapy, indicating the benign nature of Focal Idiopathic Epilepsy with Motor Seizures (FIEwMS) in Poodles.
The analysis of the data obtained allows to identify 3 subpopulations with different severity of the clinical phenotype. They were differentiated by body weight, the evolution (or not) of the seizures to generalization, the age of onset, the spontaneous clinical evolution, and the number of ASMs used. Poodle varieties with a larger body size presented a more severe clinical phenotype, with an earlier age of onset.
The FIEwMS identified in a population of Poodles in Argentina is proposed as a potential epileptic syndrome, constituting a valuable spontaneous model for certain human focal motor epilepsies.
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Aiello, G., Santos, R.P., Beckmann, D.V., Andrades, A.O., Ripplinger, A., da Silva A.P., y Mazzanti, A. (2012). Epilepsia em cães: 66 casos (2005-2010), Pesq Vet Bras, 32(4), 347-351. doi: 10.1590/S0100-736X2012000400012.
Amrutkar, C. y Riel-Romero, R.M. (2022). Rolandic Epilepsy Seizure. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing;. Available from: https://www.ncbi.nlm.nih.gov/books/NBK534845/
Asadi-Pooya, A.A., Farazdaghi, M. & Shahpari, M. (2021). Clinical significance of bilateral epileptiform discharges in temporal lobe epilepsy, Acta Neurol Scand, 143, 608-613.
Belanger, J.M., Famula, L.C., Gershony, M,K., Palij, M.K. y Oberbauer, A.M. (2020). Genome-wide association analysis of idiopathic epilepsy in the Belgian shepherd, Canine Medicine and Genetics, -7-12. doi: 10.1186/s40575-020-00091-x.
Berendt, M., y Gram, L. (1999). Epilepsy and seizure classification in 63 dogs: a reappraisal of veterinary epilepsy terminology, J Vet Intern Med, 13, 14-20.
Berendt, M., Gredal, H., Pedersen, L.G., Alban, L. y Alving, J. (2002). A cross-sectional study of epilepsy in Danish Labrador Retrievers: prevalence and selected risk factors, J Vet Intern Med, 16(3), 262-268. doi: 10.1892/0891-6640(2002)016<0262:acsoei>2.3.co;2.
Berendt., M., Gredal, H., y Alving, J. (2004). Characteristics and phenomenology of epileptic partial seizures in dogs: similarities with human seizure semiology, Epilepsy Res, 61: 167-173. doi: 10.1016/j.eplepsyres.2004.07.009.
Berendt, M., Farquhar, R.G., Mandigers, P.J.J., Pakozdy, A., Bhatti, S.F.M., De Risio, L., Fischer, A., Long, S., Matiasek, K., Muñana, K., Patterson, E.E., Penderis, J., Platt, S., Podell, M., Potschka, H., Pumarola Batlle, M., Rusbridge, C., Stein, V.M., Tipold, A., y Volk, H.A. (2015). International veterinary epilepsy task force consensus report on epilepsy definition, classification and terminology in companion animals, BMC Vet Res, 11, 182, doi: 10.1186/s12917-015-0461-2.
Berendt, M., Gulløv, C.H., Christensen, S.L., Gudmundsdottir, H., Gredal, H., Fredholm, M., y Alban, L. (2008). Prevalence and characteristics of epilepsy in the Belgian shepherd variants Groenendael and Tervueren born in Denmark 1995–2004, Acta Vet Scand, 50, 51. doi: 10.1186/1751-0147-50-51.
Berendt, M. Gulløv, C.H. y Fredholm, M. (2009). Focal epilepsy in the Belgian shepherd: evidence for simple Mendelian inheritance, J Small Anim Pract, 50, 655-661.
Bhatti, S.F.M., De Risio, L., Muñana, K., Penderis, J., Stein, V.M., Tipold, A., Berendt, M., Farquhar, R.G., Fischer, A., Long, S., Löscher, W., Mandigers, P.J.J., Matiasek, K., Pakozdy, A., Patterson, E.E., Platt, S., Podell, M., Potschka, H., Rusbridge, C., y Volk, H.A. (2015). International Veterinary Epilepsy Task Force consensus proposal: medical treatment of canine epilepsy in Europe, BMC Vet Res, 11, 176. doi: 10.1186/s12917-015-0464-z.
Callaway, E. (2022). Big dog, Little dog: mutation explains range of canine sizes, Nature,602 (7895), 18. doi: 10.1038/d41586-022-00209-0.
Camfield, C.S., Camfield, P.R., Gordon, K., Wirrell, E. y Dooley, J.M. (1996). Incidence of epilepsy in childhood and adolescence: a population-based study in Nova Scotia from 1977 to 1985, Epilepsia, 37(1), 19-23.
Cappelletti, C. (1992). Estadística experimental (1era. ed.). Buenos Aires, Argentina, AgroVet.
Casal, M.L., Munuve, R.M., Janis, M.A., Werner, P., y Henthorn, P.S. (2006). Epilepsy in Irish Wolfhounds, J Vet Intern Med, 20(1), 131-135. doi: 10.1892/0891-6640(2006)20[131:eiiw]2.0.co;2.
Cerda-Gonzalez, S., Packer, R.A., Garosi, L., Lowrie, M., Mandigers, P.J.J., O´Brien, D.P, Volk, H.A. (2021). International veterinary canine dyskinesia task forcé ECVN consensus statement: Terminilogy and classification. J Vet Intern Med, 35(3), 1218-1230.
Chandler, K. (2006). Canine epilepsy: what can we learn from human seizure disorders? Vet J, 172, 207-217. doi: 10.1016/j.tvjl.2005.07.001.
Charalambous, M., Brodbelt, D., y Volk, H.A. (2016). The evidence behind the treatment of canine idiopathic epilepsy. Veterinary evidence on line, Vol1, Issue 1. doi: 10.18849/ve.v1i1.9.
Charalambous, M., Fischer, A., Potschka, H., Walker, M., Raedt, R., y Vonck, K., Boon, P., Lohi, H., Löscher, W., Worrel, G., Leeb, T., McEvoy, A., Strianoi, P., Kluger, G., Galanapoulou, A.S., Volk, H.A., y Bhatti, S.F.M. (2023). Translational veterinary epilepsy –a win-win situation between human and veterinary neurology? Vet J, doi: 10.1016/j.tvjl.2023.105956
Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for classification of epilepsies and epileptic syndromes. (1985), Epilepsia, 26, 268-278.
Commission on Classification and Terminology of the International League Against Epilepsy. Proposal for revised classification of epilepsies and epileptic syndromes (1989), Epilepsia, 30, 389-399. doi: 10.1111/j.1528-1157.1989.tb05316.x.
Conover, W.J. (1980). Practical Nonparametric Statistics (3rd ed.). New York, USA, John Wiley & Sons INc.
De Risio, L., Bhatti, S., Muñana, K., Penderis, J., Stein, V., Tipold, A., Berendt, M., Farqhuar, R., Fischer, A., Long, S., Mandigers, P.J.J., Matiasek, K., Packer, R.M.A., Pakozdy, A., Patterson, N., Platt, S., Podell, M., Potschka, H., Pumarola Batlle M.…..Volk, H.A. (2015). International veterinary epilepsy task force consensus proposal: diagnostic approach to epilepsy in dogs, BMC Vet Res, 11, 148. doi:10.1186/s12917-015-0462-1.
Dibbens, L.M., Mullen, S., Helbig, I., Mefford, H.C., Bayly, M.A., Bellows, S., Leu, C., Trucks, H., Obermeier, T., Wittig, M., Franke, A., Caglayan, H., Yapici, Z, EPICURE Consortium, Sander, T., Eichler, E.E., Scheffer, I.E., Mulley, J.C., y Berkovic, S.F. (2009). Familial and sporadic 15q13.3 microdeletions in idiopathic generalized epilepsy: precedent for disor-ders with complex inheritance. Hum Mol Genet, 18, 3626–363
Di Rienzo, J., Casanoves, F., Balzarini, M., Gonzalez, L., y Tablada, M. (2019). InfoStat versión 2019. F. U. Centro de Transferencia InfoStat, Editor. Recuperado de http://www.infostat.com.ar.
Driver, C.J., Chandler, K., Walmsley, G., Shihab, N., Volk, H.A. (2013). The association between Chiari-like malformation, ventriculomegaly and seizures in cavalier King Charles spaniels. Vet J, 195, 235-237.
Ekenstedt, K.J., Patterson, E.E., y Mickelson, J.R. (2012). Canine epilepsy genetics, Mamm Genome, 23(1-2), 28-39. doi: 10.1007/s00335-011-9362-2.
Ergene, E., Shih, J.J., Blum, D.E. y, So N.K. (2000). Frequency of Bitemporal independent interictal epileptiform discharges in temporal lobe epilepsy, Epilepsia, 41, 213-218.
Estey, C.M. (2016). Congenital hydrocephalus. Vet Clin North Am Small Anim Pract, 46, 217-229.
Farke, D., Kolecka, M., Czerwik, A., Wrzosek, M.A., Schaub, S., Kramer, M., Failing K., Schmidt, M.J. (2020). Prevalence of seizures in dogs and cats with idiopathic internal hydrocephalus and seizure prevalence after implantation of a ventriculo-peritoneal shunt. J Vet Intern Med, 34, 1986-1992.
Federación Cinológica Internacional. (2015). https://www.fci.be/Nomenclature/Standards/172g09-es.pdf.
Fisher, R.S., Cross, J.H., French, J.A., Higurashi, N., Hirsch, E., Jansen, F.E., Lagar, L., Moshe, S.L., Peltola, J., Roulet Perez, E., Scheffer, I.E., y Zuberi, S.M. (2017). Clasificación operacional de los tipos de crisis por la Liga Internacional contra la Epilepsia: Documento - Posición de la Comisión para Clasificación y Terminología de la ILAE, Epilepsia, 58(4), 220-530. doi: 10.1111/epi.13670.
Fischer, A. y Volk, H.A. (2023). Editorial: Epilepsy in veterinary science, Front. Vet. Sci. 10:1200311. doi: 10.3389/fvets.2023.1200311.
Fredsø, N., Toft, N., Sabers, A., y Berendt, M. (2016). A prospective study observational longitudinal study of new-onset seizures and newly diagnosed epilepsy in dogs, BMC Vet Res, 13, 54, https://doi.org/10.1186/s12917-017-0966-y.
Grayzel, S., y Lefebvre, S. (2014). Descriptive epidemiology of idiopathic seizures in dogs, Vet focus, 24, 25-27.
Gollwitzer, S., Scott, C.A., Farrell, F, Bell, G.S., de Tisi, J., Walker, M.C., Wehner, T., Sander, J.W., Hamer, H.M. y Diehl, B. (2017). The long-term course of temporal lobe epilepsy: from unilateral to bilateral interictal epileptiform discharges in repeated video-EEG monitorings, Epilepsy Behav, 68, 17-21.
Gulløv, C.H., Toft, N., Baadsager, M.M.N., y Berendt, M. (2011). Epilepsy in the Petit Basset Griffon Vendeen: prevalence, semiology, and clinical phenotype, Vet Intern Med, 25(6), 1372-1378. doi: 10.1111/j.1939-1676.2011.00791.x.
Guo, D., Zeng, L., Brody, D.L, y Wong, M. (2013). Rapamycin attenuates the development of posttraumatic epilepsy in a mouse model of traumatic brain injury, PloS One, 8(5), e64978. doi: 10.1371/journal.pone.0064078.
Hamamoto, Y., Hasegawa, D., Mizoguchi, S., Yu, Y., Eada, M., Kuwabara, T., Fujiwara-Igarashi, A. y Fujita, M. (2016). Retrospective epidemiological study of canine epilepsy in Japan using the International Veterinary Epilepsy Task Force classification 2015 (2003–2013): etiological distribution, risk factors, survival time, and lifespan, BMC Vet Res,12, 248-262. doi: 10.1186/s12917-016-0877-3.
Harvey, S. (2010). Extrapituitary growth hormone, Endocrine, 38, 335-359. doi: 10.1007/s12020-010-9403-8.
Helbig, I., Mefford, H., Sharp, A, Guipponi, M., Fichera, M., Franke, A., Muhle, H., De Kovel, C., Baker, C., von Spiczak, S., Kron, K.L., Steinich, I., Kleefuss-Lie, A.A., Leu, C., Gaus, V., Schmitz, B., Klein, K.M., Reif, P.S., Rosenow, F…….Weber, Y. (2009). 15q13.3 microdeletions increase risk of idiopathic generalized epilepsy. Nat Genet, 41, 160–162.
Heske, L., Nodtvedt, A., Jaderlund, K.H., Berendt, M. y Egenvall, A. (2014). A cohort study of epilepsy among 665,000 insured dogs: incidence, mortality and survival after diagnosis, Vet J, 202(3), 471-476. Doi10.1016/J.TVJL.2014.09.023.
Hirsch, L.J., Fong, M.W.K., Leitinger, M., LaRoche, S.M., Beniczky, S., Abend, N.S., Lee, J.W., Wusthoff, C.J., Hahn, C.D., Westover, M.B., Gerard, E.E., Herman, S.T., Haider, H.A., Osman, G., Rodriguez-Ruiz, A., Maciel, C.B., Gilmore, E.J., Fernandez, A.,.…. Gaspard, N. (2021). American clinical neurophysiology society’s standardized critical care EEG terminology: 2021 version, J Clin Neurophysiol, 38(1), 1-29.
Horvon, S. (2014). The concept of symptomatic epilepsy and the complexities of assigning cause in epilepsy. Epilepsy Behav, 32, 1–8.
Hülsmeyer, V., Zimmermann, R., Brauer, C., Sauter-Louis, C., y Fischer, A. (2010). Epilepsy in Border Collies: clinical manifestation, outcome, and mode of inheritance. J Vet Intern Med, 24(1), 171-178.
Hülsmeyer, V.I., Fischer, A., Mandigers, P.J.J.J., De Risio, L., Berendt, M., Rusbridge, C., Bhatti, S.F.M., Oakozdy, A., Pattersona, E.E., Platt, S., Packer, R.M.A, y Volk, H.A. (2015). International Veterinary Epilepsy Task Force’s current understanding of idiopathic epilepsy of genetic or suspected genetic origin in purebred dogs, BMC Vet Res, 11, 175. doi: 10.1186/s12917-015-0463-0.
Jiang, G., Wang, W., Cao, Q., Gu, J., Mi, X., Wang, K., Chen, G, y Wang, X. (2015). Insulin growth factor-1 (IGF-1) enhances hippocampal excitatory and seizure activity through IGF-1 receptor-mediated mechanisms in the epileptic brain, Clin Sci (Lond.), 129(12), 1047-1060. doi: 10.1042/CS20150312.
Jokinen, T.S., Metsähonkala, L., Bergamasco, L., Viitmaa, R., Syrjä, P., Lohi, H., Snellman, M., Jeserev, J., y Cizinauskas, S. (2007). Benign familial juvenile epilepsy in lagotto romagnolo dogs, J Vet Intern Med, 21(3), 464-471. doi: q0.1892/0891-6640(2007)21[464:bfjeil]2.0.co;2.
Kearsley-Fleet, L., O'Neill, D.G., Volk, H.A., Church, D.B., y Brodbelt, D.C. (2013). Prevalence and risk factors for canine epilepsy of unknown origin the UK, Vet Rec, 172(13), 338. doi: 10.1136/vr.101133.
Koskinen, L.L.E., Seppälä, E.H., Belanger, J.M., Arumilli, M., Hakosalo, O., Jokinen, P., Nevalainen, E.M., Viitmaa, R., Jokinen, T.S., Oberbauer, A.M., y Lohi, H. (2015). Identification of a common risk haplotype for canine idiopathic epilepsy in the ADAM23 gene, BMC Genomics,16, 465.
Koskinen L.L.E., Seppälä E.H., Weissl J, Jokinen, T.S., Viitmaa, R., Hänninen, R.L., Quignon, P., Fischer, A., André, C., y Lohi, H. (2017). ADAM23 is a common risk gene for canine idiopathic epilepsy. BMC Genetics, 18:8. doi: 10.1186/s12863-017-0478-6.
Laubner, S., Ondreka, N., Failing, K., Kramer, M., y Schmidt, M.J. (2015). Magnetic resonance imaging signs of high intraventricular pressure – comparison of findings in dogs with clinically relevant internal hydrocephalus and asymptomatic dogs with ventriculomegaly. BMC Vet Res,11, 181-192.
Lee, Y.J., Hwang, S.K. y Kwon, S. (2017). The Clinical Spectrum of Benign Epilepsy with Centro-Temporal Spikes: a Challenge in Categorization and Predictability, J Epilepsy Res, 7(1), 1-6. doi: 10.14581/jer.17001. PMID: 28775948.
Lequarré AS, Andersson L, André C, Fredholm, M., Hitte, C., Leeb, T., Lohi, H., Linblad-Toh, K., y Georges, M. (2011). LUPA: a European initiative taking advantage of the canine genome architecture for unravelling complex disorders in both human and dogs. Vet J,, 189,155-159.
Licht, B.G., Licht, M.H., Harper, K.M., Lin, S., Curtin, J.J., Hyson, L.L., y Willard, K. (2002). Clinical presentations of naturally occurring canine seizures: similarities to human seizures, Epilepsy Behav, 3(5), 460-470. doi: 10.1016/s1525-5050(02)00523-1.
Licht, B.G., Lin, S., Luo, Y., Hyson, L.L., Licht, M.H., Harper, K.M., Sullivan, S.A., Fernandez, S.A., y Johnston, E.V. (2007). Clinical characteristics and mode of inheritance of familial focal seizures in Standard Poodles, J Am Vet Med Assoc, 231(10), 1520-1528. doi: 10.2460/javma.231.10.1520.
Löscher, W. (2022). Dogs as a natural animal model of epilepsy, Front Vet Sci, 9, 928009. doi: 10.3389/fvets.2022.928009.
Lowrie, M., y Garosi, L. (2017). Classification of involuntary movements in dogs: paroxysmal dyskinesias, Vet J, 220, 65-71. doi: 10.1016/j.tvjl.2016.12.017.
Ostermann, T.E., Nessler, J.N., Urankar, H., Bachmann, N., Fechler, C., Bathen-Nöthen, A., y Tipold, A. (2022). Phenotype of Idiopathic Epilepsy in Great Swiss Mountain Dogs in Germany—A Retrospective Study. Front. Vet. Sci. 9:921134. doi: 10.3389/fvets.2022.921134.
Ostrander, E.A. (2008). Base genética de la morfología canina, Investigación y Ciencia (US), 376, 26-34.
Packer, R.M., Shihab, N.K., Torres, B.B., Volk, H.A. (2014). Clinical risk factors associated with anti-epileptic drug responsiveness in canine epilepsy, PLoS ONE, 9(8):e106026.
Pakozdy, A., Leschnik, M., Tichy, A.G. y Thalhammer J.G. (2008). Retrospective clinical comparison of idiopathic versus symptomatic epilepsy in 240 dogs with seizures. Acta Vet Hung, 56, 471-483.
Patterson, E.E., Mickelson, J.R., Da, Y., Roberts, M.C., McVey A.S., O´Brien, D.P., Johnson, G.S., y Armstrong, P.J. (2003). Clinical characteristics and inheritance of idiopathic epilepsy in Vizslas, J Vet Intern Med, 17, 319-325. doi: 10.1111/j.1939-1676.2003.tb02455.x.
Patterson, E.E. (2014). Canine epilepsy: an underutilized model, ILAR J, 55, 182-186. doi: 10.1093/ilar/ilu021.
Pellegrino, F. (2000a). Estandarización de los patrones electroencefalográficos de los caninos. Tesis Doctoral. Universidad de Buenos Aires, Argentina.
Pellegrino, F.C., Sica, R. (2004). Canine electroencephalographic recording technique: findings in normal and 546 epileptic dogs. Clin Neurophysiol, 115, 477- 487.
Pellegrino, F., Pacheco, E., y Vazzoler, M.L. (2011a). Caracterización de los trastornos neurológicos en los perros: 1652 casos (marzo 2008-junio 2010). Parte I, Revista Argentina de Neurología Veterinaria, 1(2), 78-96.
Pellegrino, F., Pacheco, E., y Vazzoler, M.L. (2011b). Características clínicas y respuesta al tratamiento de perros con epilepsia idiopática: 326 casos, Revista Argentina de Neurología Veterinaria, 1(2), 129-144.
Pellegrino, F. (2021). Algunas consideraciones complementarias a las declaraciones de consenso IVETF 2015. Parte 1: Clasificación de las crisis epilépticas y de las epilepsias, Revista Argentina de neurología Veterinaria, 9(2), 1-13.
Pellegrino; F, Alarcón, F., Castro Borda, S., Diblasi, A., Espina, C., Garibaldi, L., Pacheco, E.L., Patricelli, A., Rigazzi, A., Stangaferro, R., y Toledo, V. (2022a). Propuesta de consenso del Grupo de Trabajo de la Reunión Argentina de consenso en epilepsia veterinaria en definiciones, clasificación etiológica de las crisis cerebrales y clasificación semiológica de las crisis epilépticas en animales de compañía, Revista Argentina de Neurología Veterinaria, 10(1), 3-15.
Pellegrino, F, Alarcón, F., Castro Borda, S., Diblasi, A., Espina, C., Garibaldi, L., Pacheco, E.L., Patricelli, A., Rigazzi, A., Stangaferro, R., y Toledo, V. (2022b). Propuesta de consenso del Grupo de Trabajo de la Reunión Argentina de consenso en epilepsia veterinaria en clasificación semiológica de las epilepsias en animales de compañía, Revista Argentina de Neurología Veterinaria, 10(1), 16-23.
Pellegrino, F, Blanco, C. (2023). Caracterización clínica y epidemiológica de los tipos de epilepsia idiopática canina: estudio retrospectivo en 258 perros. AN. VET (MURCIA), 37, 1-29.
Plassais, J., vonHoldt, B.M., Parker, H.G., Carmagnini, A., Dubos, N., Papa, I., Bevant, K., Derrien, T., Hennelly, L.M., Whitaker, D.T., Harris, A.C., Hogan, A.N., Huson, H.J., Zaibert, V.F., Linderholm, A., Haile, J., Fest, T., Habib, B., Sacks, B.N,…. Ostrander, E.A. (2022). Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids, Curr Biol, 32, 889-897. doi: 10.1016/j.cub.2021.12.036.
Potschka, H., Fischer, A., Löscher, W., Patterson, N., Bhatti, S., Berendt, M., De Risio, L., Farquhar, R., Long, S., Mandigers, P., Matiasek, K., Muñana, K., Pakozdy, A., Penderis, J., Platt, S., Podell, M., Rusbridge, C., Stein, V., Tipold, A., y Volk, H.A. (2015). International veterinary epilepsy task force consensus proposal: outcome of therapeutic interventions in canine and feline epilepsy, BMC Vet Res, 11, 177. doi: 10.1186/s12917-015-0465-y.
Provini, F., Plazzi, G., Tinuper, P., Vandi, S., Lugaresi, E., y Montagna, P. (1999). Nocturnal frontal lobe epilepsy.A clinical and polygraphic overview of 100 consecutive cases, Brain, 122, 1017-1031.
Ramírez-Anormaliza, R., Guevara-Viejo, F., D´Armas Regnault, M., Pena-Holguin, R., Farías-Lema, R., Bravo-Duarte, F., Díaz-Montenegro, J., Calderón-Cisneros, J., Franco-Arias, O., Ramírez-Granda, F., Carrasquero Rodríguez, E., Vargas-Decimavilla, D., Basurto-Quilligana, R., Vargas-Ortiz, O., Bermeo-Paucar, J., y Castelo-Gonzalez, J. (2017). Análisis Multivariante: Teoría y práctica de las principales técnicas. Milagro, Ecuador, Universidad estatal del Milagro-UNEMI, http://repositorio.unemi.edu.ec/xmlui/handle/123456789/3855.
Riney, K., Bogacz, A., Somerville, E., Hirsch, E., Nabbout, R., Scheffer, I. E., Zuberi, S.M., Alsaadi, T., Jain, S., French, J., Specchio, N., Trinka, E., Wiebe, S., Auvin, S., Cabral-Lim, L., Naidoo, A., Peurcca, E., Moshé, S., Wirrell, E.C. y Tinuper, P. (2022). International League Against Epilepsy classification and definition of epilepsy syndromes with onset at a variable age: position statement by the ILAE Task Force on Nosology and Definitions, Epilepsia, 63, 1443-1474. https://doi.org/10.1111/epi.17240
Rusbridge, C., Long, S., Jovanovik, J., Milne, M., Berendt, M., Bhatti, S., De Risio, L., Farqhuar, R., Fischer, A., Matiasek, K., Muñana, K., Patterson, N., Pakozdy, A., Penderis, J., Platt, S., Podell, M., Potschka, H., Stein, V., Tipold, A., y Volk, H.A. (2015). International Veterinary Epilepsy Task Force recommendations for a veterinary epilepsy-specific MRI protocol, BMC Vet Res, 11, 194. doi: 10.1186/s12917-015-0466-x.
Salanova, V., Morris, H.H., Van Ness, P., Kotagal, P., Wyllie, E., y Lüders H. (1995). Frontal lobe seizures: electroclinical syndromes, Epilepsia, 36(1), 16-24. doi: 10.1111/j.1528-1157.1995.tb01659.x.
Santifort, K.M., Bertijn, E., Bhatti, S.F.M., Leegwater, P., Fischer, A. y Mandigers, P.J.J. (2022) Phenotypic Characterization of Idiopathic Epilepsy in Border Collies. Front. Vet. Sci. 9:880318. doi: 10.3389/fvets.2022.880318.
Scheepens, A., Sirimanne, E.S., Breier, B.H., Clark, R.G., Gluckman, P.D., y Williams, C.E. (2001). Growth hormone as a neuronal rescue factor during recovery from CNS injury, Neuroscience, 104, 677-687. doi: 10.1016/s0306-4522(01)00109-9.
Scheffer, I.E., Bhatia, K.P., Lopes-Cendes, I., Fish, D.R., Marsden, C.D., Andermann, E., Andermann, F., Desbiens, R., Keene, D., Cendes, F., Manson, J.I., Constantinou, J.E,C., McIntosh, A., y Berkovic, S.F. (1995). Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder, Brain, 118(Pt 1), 61-73.
Scheffer, I.E., Berkovic, S., Capovilla, G., Connolly, M.B., French, J., Guilhoto, L., Hirsch, E., Jain, S., Mathern, G.W., Moshe, S.L., Nordli, D.R., Perucca, E., Tomson, T., Wiebe, S., Zhang, Y-H., y Zuberi, S.M. (2017). Clasificación de las epilepsias de la ILAE: Documento de posición de la Comisión de Clasificación y Terminología de la ILAE, Epilepsia, 58(4), 512-521. doi: 10.1111/epi.13709.
Seppälä, E.H., Jokinen, T.S., Fukata, M., Fukata, Y., Webster, M.T., Karlsson, E.K., Kilpinen, S.K., Steffen, F., Dietschi, E., Leeb, T., Eklund, R., Zhao, X., Rilstone J.J., Lindblad-Toh, K., Minassian, B.A., y Lohi, H. (2011). LGI2 truncation causes a remitting focal epilepsy in dogs, PLoS Genet, 7(7), e1002194. doi: 10.1371/journal.pgen.1002194.
Seppälä, E.H., Lotta, L., Koskinen, E. Gulløv, C.H., Jokinen, P., Karslov-Mortensen, P., Bergamasco, L., Baranowska Körberg, I., Cizinauskas, S., Oberbauer, A.M., Berendt, M., Fredholm, M. y Lohi, H. (2012). Identification of a Novel Idiopathic Epilepsy Locus in Belgian Shepherd Dogs, PLoS ONE 7(3), e33549. doi:10.1371/journal.pone.0033549.
Short, A.D., Dunne, A., Lohi, H., Boulton, S., Carter, S.D., Timofte, D. y Ollier, W.E. (2011). Characteristics of epileptic episodes in UK dog breeds: an epidemiological approach. Vet Rec, 169(2), 48. doi: 10.1136/vr.d1901.
Song, Y., Pimentel, C., y Walters, K. (2016). Neuroprotective levels of IGF-1 exacerbate epileptogenesis after brain injury, Scientific Reports, 6, 32095. doi:10.1038/srep32095.
Specchio, N., Wirrell, E.C., Scheffer, I.E., Nabbout, R., Riney, K., Samia, P., Guerreiro, M., Gwer, S., Zuberi, S.M., Wilmshurst, J.M., Yozawitz, E., Pressler, R., Hirsch, E., Wiebe, S., Cross, H.J., Perucca, ED., Moshé, S.L., Tinuoer, P., y Auvin, S. (2022). International League Against Epilepsy classification and definition of epilepsy syndromes with onset in childhood: Position paper by the ILAE Task Force on Nosology and Definitions, Epilepsia, 63, 1398-1442.
Stassen, Q.E.M., Grinwis, G.C.M., van Rhijn, N.C., Beukers, M., Verhoeven-Duif, N.M., y Leegwater, P.A.J. (2019). Focal epilepsy with fear-related behavior as primary presentation in Boerboel dogs. J Vet Intern Med, 33, 694-700.
Sutter, N.B., Bustamante, C.D., Chase, K., Gray, M.M., Zhao, K., Zhu, L., Padhukasahasram, B., Karlins, E., Davis, S., Jones, P.G., Quignon, P., Johnson, G.S., Parker, H.G., Fretwell, N., Mosher, D.S., Lawler, D.F., Satyaraj, E., Nordborg, M., Lark, K.G.,…Ostrander, E.A. (2007). A single IGF1 allele is a major determinant of small size in dogs, Science, 316(5289), 112-5. doi: 10.1126/science.1137045.
Togawa, G. (2019). A Retrospective study of canine idiopathic epilepsy in referral centers in Japan. Tesis doctoral. Universidad Azabu, Japón.
Urkasemsin, G., y Olby, N.J. (2014). Canine paroxysmal movement disorders, Vet Clin North Am Small Anim Pract, 44, 1091-102. doi: 10.1016/j.cvsm.2014.07.006.
Watson, F., Coppi, A.A., Volk, H.A., Packer, R.M.A., Tauro, A., y Rusbridge, C. (2021). Comparison of volume of the forebrain, subarachnoid space and lateral ventricles between dogs with idiopathic epilepsy and controls using a stereological approach: Cavalieri's principle. Canine Med Genet, 8, 3-15.
Weissl, J., Hülsmeyer, V., Brauer, C., Tipold, A., Koskinen, L.L., Kyöstila, K, Lohi, H., Sauter-Louis, C., Wolf, M., y Fischer, A. (2012). Disease progression and treatment response of idiopathic epilepsy in Australian Shepherd dogs. J Vet Intern Med, 26(1), 116-25.
Wielaender, F., Sarviaho, R., James, F., Hytönen, M.K., Cortez, M.A., Kluger, G., Koskinen, L.L.E., Arumilli, M., Kornberg, M., Bathen-Noethen, A., Tipold, A., Rentmeister, K., Bhatti, S.F.M., Hülsmeyer, V., Boettcher, I.C., Tänsten, C., Flegel, T., Dierschi, E., Leeb, T.,….Lohi, H. (2017). Generalized myoclonic epilepsy with photosensivity in juvenil dogs caused by a defective DIRAS familiy GTPase 1, PNAS, 114(10), 2669-2674. doi: 10.1073/pnas.1614478114.
Wielaender F. (2018). Clinical and electroencephalographic characterization of juvenile myoclonic epilepsy in Rhodesian Ridgebacks. Tesis doctoral. Universidad Ludwig-Maximilians, Munich.
Wirrell, E.C., Camfield, P.R., Gordon, K.E., Dooley, J.M., y Camfield, C.S. (1995). Benign Rolandic epilepsy: atypical features are very common, J Child Neurol, 10(6), 455-458.
Wirrell, E.C., Grossardt. B.R., Wong-Kisiel, L.C.L. y Nickels, K.C. (2011). Incidence and classification of new-onset epilepsy and epilepsy syndromes in children in Olmsted County, Minnesota from 1980 to 2004: a population-based study, Epilepsy Res, 95(1-2), 110-118.
Wirrell, E.C., Nabbout, R., Scheffer, I.E., Alsaadi, T., Bocacz, A., French, J.A., Hirsch, E., Jain, S., Kaneko, S., Riney. K., Samia, P., Carter Snead, O., Somerville, E., Specchio, N., Trinka, E., Zuberi, S.M., Balestrini, S., Wiebe, S., Cross, J.H,….Tinuoer, P. (2022). Methodology for classification and definition of epilepsy syndromes with list of syndromes: report of the ILAE Task Force on Nosology and Definitions, Epilepsia, 2022:epi.17237. doi: 10.1111/epi.17237.
Yu, Y., Hasegawa, D., Kanazono, S, y Saito, M. (2022). Clinical characterization of epileptic seizures in Pomeranians with idiopathic epilepsy or epilepsy of unknown cause. J Vet Intern Med, 1-10. DOI: 10.1111/jvim.16578
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