Cardiovascular response to stress in patients with drug-resistant epilepsypreliminary data

  1. Alejandro Lozano García 1
  2. Judit Catalán 12
  3. Kevin Hampel 3
  4. Vicente Villanueva 3
  5. Esperanza González-Bono 1
  6. Irene Cano-López 1
  1. 1 Universitat de València
    info

    Universitat de València

    Valencia, España

    ROR https://ror.org/043nxc105

  2. 2 Universidad Internacional de Valencia
    info

    Universidad Internacional de Valencia

    Valencia, España

    ROR https://ror.org/00gjj5n39

  3. 3 Hospital Universitario La Fe
    info

    Hospital Universitario La Fe

    Valencia, España

    ROR https://ror.org/01ar2v535

Revista:
Anales de psicología

ISSN: 0212-9728 1695-2294

Año de publicación: 2021

Título del ejemplar: Cerebro y conducta: un enfoque neurocientífico/psicofisiológico

Volumen: 37

Número: 3

Páginas: 440-448

Tipo: Artículo

DOI: 10.6018/ANALESPS.483021 DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Anales de psicología

Resumen

El estrés es un factor de riesgo para las enfermedades cardiovasculares en la población general. La epilepsia se ha considerado un modelo adecuado de estrés crónico, con mayor incidencia de mortalidad cardiovascular que la población general. Este estudio proporciona datos preliminares sobre la respuesta cardiovascular ante un estresor cognitivo y una evaluación neuropsicológica en pacientes con epilepsia, explorando las relaciones entre la respuesta cardiovascular y el rendimiento cognitivo dependiendo del hemisferio responsable de la epilepsia. Treinta y cinco pacientes con epilepsia farmacorresistente, 17 con el área epileptógena(AE) en el hemisferio izquierdo (LH) y 18 con AE en el hemisferio derecho (RH), se sometieron a un estres cognitivo y una evaluación neuropsicológica. La respuesta cardiovascular se registró durante toda la sesión en ambas condiciones. Los resultados mostraron que una evaluación neuropsicológica de larga duración fue capaz de producir una respuesta cardiovascular modulada por el hemisferio, con disminuciones de la frecuencia cardíaca (y aumentos del intervalo RR) más pronunciadas en el período post-evaluación en pacientes con epilepsia del HI que en pacientes con epilepsia del HD (p = .05, p = .01, respectivamente). El hemisferio del AE moderó la relación entre la respuesta cardiovascular y el rendimiento cognitivo (para todos, p < .03). Nuestros hallazgos podrían tener implicaciones clínicas desde una perspectiva preventiva, ya que sugieren que el hemisferio del AE podría ser un factor relevante en el afrontamiento del estrés en personas con epilepsia farmacorresistente.

Información de financiación

Acknowledgments.- This work was supported by the Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund (MINECO/FEDER) [grant number PSI2015-66600-P, 2015]. The authors are grateful to John Rawlins for the revision of English style and grammar.

Referencias bibliográficas

  • Ahern, G. L., Sollers, J. J., Lane, R. D., Labiner, D. M., Herring, A. M., Weinand, M. E., Thayer, J. F. (2001). Heart rate and heart rate variability changes in the intracarotid sodium amobarbital test. Epilepsia, 42(7), 912–921.
  • Allendorfer, J. B. & Szaflarski, J. P. (2014). Contributions of fMRI towards our understanding of the response to psychosocial stress in epilepsy and psychogenic nonepileptic seizures. Epilepsy & Behavior, 35, 19-25.
  • Allendorfer, J. B., Heyse, H., Mendoza, L., Nelson, E. B., Eliassen, J. C., Storrs, J. M. & Szaflarski, J. P. (2014). Physiologic and cortical response to acute psychosocial stress in left temporal lobe epilepsy—a pilot cross-sectional fMRI study. Epilepsy & Behavior, 36, 115-123.
  • Bali, A. & Jaggi, A. S. (2015). Clinical experimental stress studies: methods and assessment. Reviews in the Neurosciences, 26(5), 555-579.
  • Behbahani, S., Dabanloo, N. J., Nasrabadi, A. M. & Dourado, A. (2016). Classification of ictal and seizure-free HRV signals with focus on lateralization of epilepsy. Technology and Health Care, 24(1), 43-56.
  • Behbahani, S., Dabanloo, N. J., Nasrabadi, A. M. & Dourado, A. (2018). Gender-related differences in heart rate variability of epileptic patients. American Journal of Men's Health, 12(1), 117-125.
  • Błaszczyk, B. & Czuczwar, S. J. (2016). Epilepsy coexisting with depression. Pharmacological reports, 68(5), 1084-1092.
  • Camm, A. J., Malik, M., Bigger, J. T., Breithardt, G., Cerutti, S., Cohen, R. J., ... & Lombardi, F. (1996). Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology.
  • Cano-Lopez, I. & Gonzalez-Bono, E. (2019). Cortisol levels and seizures in adults with epilepsy: A systematic review. Neuroscience & Biobehavioral Reviews, 103, 216-229. https://doi.org/10.1016/j.neubiorev.2019.05.023
  • Constantinescu, V., Detante, O., Matei, D., Constantinescu, I., Arsenescu-Georgescu, C., Defaye, P., ... & Cuciureanu, D. (2017). Cortical lateralization and cardiac autonomic control. Insights from insular stroke and epilepsy. Archive of Clinical Cases, 4(3), 154-168.
  • Czéh, B., Perez-Cruz, C., Fuchs, E. & Flügge, G. (2008). Chronic stress-induced cellular changes in the medial prefrontal cortex and their potential clinical implications: does hemisphere location matter?. Behavioural brain research, 190(1), 1-13.
  • Delaney, J. P. A. & Brodie, D. A. (2000). Effects of short-term psychological stress on the time and frequency domains of heart-rate variability. Perceptual and motor skills, 91(2), 515-524.
  • Elger, C. E., Johnston, S. A. & Hoppe, C. (2017). Diagnosing and treating depression in epilepsy. Seizure, 44, 184-193.
  • Emery, C. F., Stoney, C. M., Thayer, J. F., Williams, D. & Bodine, A. (2018). Sex and family history of cardiovascular disease influence heart rate variability during stress among healthy adults. Journal of psychosomatic research, 110, 54-60.
  • Fialho, G. L., Pagani, A. G., Walz, R., Wolf, P. & Lin, K. (2017). Maximal/exhaustive treadmill test features in patients with temporal lobe epilepsy: Search for sudden unexpected death biomarkers. Epilepsy research, 133, 83-88.
  • Fisher, R. S., Acevedo, C., Arzimanoglou, A., Bogacz, A., Cross, J. H., Elger, C. E., ... & Hesdorffer, D. C. (2014). ILAE official report: a practical clinical definition of epilepsy. Epilepsia, 55(4), 475-482.
  • Ghchime, R., Benjelloun, H., Kiai, H., Belaidi, H., Lahjouji, F. & Ouazzani, R. (2016). Cerebral hemispheric lateralization associated with hippocampal sclerosis may affect interictal cardiovascular autonomic functions in temporal lobe epilepsy. Epilepsy research and treatment, Article ID 7417540, https://doi.org/10.1155/2016/7417540.
  • Giles, D., Draper, N. & Neil, W. (2016). Validity of the Polar V800 heart rate monitor to measure RR intervals at rest. European Journal of Applied Physiology, 116(3), 563–571.
  • Ginty, A. T., Kraynak, T. E., Fisher, J. P. & Gianaros, P. J. (2017). Cardiovascular and autonomic reactivity to psychological stress: neurophysiological substrates and links to cardiovascular disease. Autonomic Neuroscience, 207, 2-9.
  • Helmstaedter, C. (2013). Cognitive outcomes of different surgical approaches in temporal lobe epilepsy. Epileptic Disorders, 15(3), 221-239.
  • Helmstaedter, C., Schoof, K., Rossmann, T., Reuner, G., Karlmeier, A. & Kurlemann, G. (2010). Introduction and first validation of EpiTrack Junior, a screening tool for the assessment of cognitive side effects of antiepileptic medication on attention and executive functions in children and adolescents with epilepsy. Epilepsy & Behavior, 19(1), 55-64.
  • Kadish, N. E., Baumann, M., Pietz, J., Schubert-Bast, S. & Reuner, G. (2013). Validation of a screening tool for attention and executive functions (EpiTrack Junior®) in children and adolescents with absence epilepsy. Epilepsy & Behavior, 29(1), 96-102.
  • Kirchner, A., Pauli, E., Hilz, M. J., Neundörfer, B. & Stefan, H. (2002). Sex differences and lateral asymmetry in heart rate modulation in patients with temporal lobe epilepsy. Journal of Neurology, Neurosurgery & Psychiatry, 73(1), 73-75.
  • Kwan, P., Schachter, S. C. & Brodie, M. J. (2011). Drug-resistant epilepsy. New England Journal of Medicine, 365(10), 919-926.
  • Levira, F., Thurman, D. J., Sander, J. W., Hauser, W. A., Hesdorffer, D. C., Masanja, H., ... & Epidemiology Commission of the International League Against Epilepsy. (2017). Premature mortality of epilepsy in low‐and middle‐income countries: a systematic review from the Mortality Task Force of the International League Against Epilepsy. Epilepsia, 58(1), 6-16.
  • Lotufo, P. A., Valiengo, L., Benseñor, I. M. & Brunoni, A. R. (2012). A systematic review and meta‐analysis of heart rate variability in epilepsy and antiepileptic drugs. Epilepsia, 53(2), 272-282.
  • Lutz, M. T. & Helmstaedter, C. (2005). EpiTrack: tracking cognitive side effects of medication on attention and executive functions in patients with epilepsy. Epilepsy & Behavior, 7(4), 708-714.
  • MacLeod, C. M. (1991). Half a century of research on the Stroop effect: an integrative review. Psychological bulletin, 109(2), 163.
  • McKee, H. R. & Privitera, M. D. (2017). Stress as a seizure precipitant: identification, associated factors, and treatment options. Seizure, 44, 21-26.
  • McKlveen, J. M., Myers, B. & Herman, J. P. (2015). The medial prefrontal cortex: coordinator of autonomic, neuroendocrine and behavioural responses to stress. Journal of neuroendocrinology, 27(6), 446-456.
  • Mueller, S. T. (2012). The Psychology Experiment Building Language, Version 0.13. In https://pebl.sourceforge.net
  • Nair, S. S., Harikrishnan, S., Sarma, P. S. & Thomas, S. V. (2016). Metabolic syndrome in young adults with epilepsy. Seizure, 37, 61-64.
  • Nass, R. D., Hampel, K. G., Elger, C. E. & Surges, R. (2019). Blood pressure in seizures and epilepsy. Frontiers in Neurology, 10, 501.
  • Novakova, B., Harris, P. R. & Reuber, M. (2017). Diurnal patterns and relationships between physiological and self-reported stress in patients with epilepsy and psychogenic non-epileptic seizures. Epilepsy & Behavior, 70, 204-211.
  • Novakova, B., Harris, P. R., Ponnusamy, A. & Reuber, M. (2013). The role of stress as a trigger for epileptic seizures: a narrative review of evidence from human and animal studies. Epilepsia, 54(11), 1866-1876.
  • Oppenheimer, S. (2006). Cerebrogenic cardiac arrhythmias: Cortical lateralization and clinical significance. Clinical Autonomic Research, 16(1), 6.
  • Porcelli, A. J., Cruz, D., Wenberg, K., Patterson, M. D., Biswal, B. B. & Rypma, B. (2008). The effects of acute stress on human prefrontal working memory systems. Physiology & behavior, 95(3), 282-289.
  • Qin, S., Hermans, E. J., van Marle, H. J., Luo, J. & Fernández, G. (2009). Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological psychiatry, 66(1), 25-32.
  • Ramaekers, D., Ector, H., Aubert, A. E., Rubens, A. & Van de Werf, F. (1998). Heart rate variability and heart rate in healthy volunteers. Is the female autonomic nervous system cardioprotective?. European Heart Journal, 19(9), 1334-1341.
  • Remue, J., Vanderhasselt, M. A., Baeken, C., Rossi, V., Tullo, J. & De Raedt, R. (2016). The effect of a single HF-rTMS session over the left DLPFC on the physiological stress response as measured by heart rate variability. Neuropsychology, 30(6), 756.
  • Renaud, P. & Blondin, J. P. (1997). The stress of Stroop performance: Physiological and emotional responses to color–word interference, task pacing, and pacing speed. International Journal of Psychophysiology, 27(2), 87-97.
  • Ryan, S. M., Goldberger, A. L., Pincus, S. M., Mietus, J. & Lipsitz, L. A. (1994). Gender-and age-related differences in heart rate dynamics: are women more complex than men?. Journal of the American College of Cardiology, 24(7), 1700-1707.
  • Saleh, Y., Kirchner, A., Pauli, E., Hilz, M. J., Neundörfer, B. & Stefan, H. (2000). Temporallappenepilepsien Einfluss der Fokusseite auf die autonome Regulation der Herzfrequenz?. [Temporal lobe epilepsies Influence of the focus side on the autonomic regulation of the heart rate ?.], Der Nervenarzt, 71(6), 477-480.
  • Spielberger, C. D., Gorsuch, R. L., Lushene, R. E., Vagg, P. R. & Jacobs, G. A. (1970). Manual for the state-trait inventory. Consulting Psychologists.
  • Sullivan, R. M. & Gratton, A. (1999). Lateralized effects of medial prefrontal cortex lesions on neuroendocrine and autonomic stress responses in rats. Journal of Neuroscience, 19(7), 2834-2840.
  • Tegeler, C. H., Shaltout, H. A., Tegeler, C. L., Gerdes, L. & Lee, S. W. (2015). Rightward dominance in temporal high‐frequency electrical asymmetry corresponds to higher resting heart rate and lower baroreflex sensitivity in a heterogeneous population. Brain and behavior, 5(6), e00343.
  • Thayer, J. F. & Lane, R. D. (2009). Claude Bernard and the heart–brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 33(2), 81-88.
  • Thayer, J. F., Åhs, F., Fredrikson, M., Sollers III, J. J. & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neuroscience & Biobehavioral Reviews, 36(2), 747-756.
  • Thijs, R. D., Surges, R., O'Brien, T. J. & Sander, J. W. (2019). Epilepsy in adults. The Lancet, 16, 689-701. https://doi.org/10.1016/S0140-6736(18)32596-0
  • van Campen, J. S., Jansen, F. E., de Graan, P. N., Braun, K. P. & Joels, M. (2014). Early life stress in epilepsy: a seizure precipitant and risk factor for epileptogenesis. Epilepsy & Behavior, 38, 160-171.
  • Vivanco‐Hidalgo, R. M., Gomez, A., Moreira, A., Díez, L., Elosua, R. & Roquer, J. (2017). Prevalence of cardiovascular risk factors in people with epilepsy. Brain and behavior, 7(2), e00618.
  • Vlcek, M., Penesova, A., Imrich, R., Meskova, M., Mravcova, M., Grunnerova, L., ... & Jezova, D. (2018). Autonomic nervous system response to stressors in newly diagnosed patients with multiple sclerosis. Cellular and molecular neurobiology, 38(1), 363-370.
  • Watson, D., Clark, L. A. & Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology, 54(6), 1063.
  • Xavier, C. H., Nalivaiko, E., Beig, M. I., Menezes, G. B., Cara, D. C., Campagnole-Santos, M. J. & Fontes, M. A. P. (2009). Functional asymmetry in the descending cardiovascular pathways from dorsomedial hypothalamic nucleus. Neuroscience, 164(3), 1360-1368.
  • Yuen, A. W., Keezer, M. R. & Sander, J. W. (2018). Epilepsy is a neurological and a systemic disorder. Epilepsy & Behavior, 78, 57-61.
  • Zhang, X., Bachmann, P., Schilling, T. M., Naumann, E., Schaechinger, H. & Larra, M. F. (2018). Emotional stress regulation: The role of relative frontal alpha asymmetry in shaping the stress response. Biological psychology, 138, 231-239.