Cardiovascular response to stress in patients with drug-resistant epilepsy: preliminary data
Abstract
Stress is a risk factor for cardiovascular diseases in the general population. Epilepsy has been considered a suitable model of chronic stress with a higher incidence of cardiovascular mortality than the general population. This study provides preliminary data about cardiovascular response to a cognitive stressor and a neuropsychological assessment in patients with epilepsy. It also explores the relationship between cardiovascular response and cognitive performance, depending on the side of seizure focus. Thirty-five patients with drug-resistant epilepsy, 17 with epileptogenic area (EA) in the left hemisphere (LH) and 18 with EA in the right hemisphere (RH), underwent a cognitive stressor and a neuropsychological assessment. The cardiovascular response was recorded throughout both conditions. Results showed that a long-lasting neuropsychological assessment was capable of producing a hemisphere-modulated cardiovascular response with heart rate (HR) decreases (and R-R interval increases) more pronounced in the LH patients than in the RH patients at the post-assessment period (p = .05 and p = .01, respectively). The hemisphere of EA moderated the relationship between cardiovascular response and cognitive performance (for all, p < .03). Our findings may have clinical implications from a preventive perspective since the EA hemisphere may be a relevant factor for coping with stress in people with drug-resistant epilepsy.
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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.
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