Cardiac autonomic dynamics during sleep are lost in patients with TIA and stroke.
autonomic modulation
brain ischaemia
heart rate variability
insula
Journal
Journal of sleep research
ISSN: 1365-2869
Titre abrégé: J Sleep Res
Pays: England
ID NLM: 9214441
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
27
11
2018
revised:
26
04
2019
accepted:
27
04
2019
pubmed:
14
6
2019
medline:
8
1
2021
entrez:
14
6
2019
Statut:
ppublish
Résumé
Ischaemic stroke is accompanied by important alterations of cardiac autonomic control, which have an impact on stroke outcome. In sleep, cardiac autonomic control oscillates with a predominant sympathetic modulation during REM sleep. We aimed to assess cardiac autonomic control in different sleep stages in patients with ischaemic stroke. Forty-five patients enrolled in the prospective, multicentre SAS-CARE study but without significant sleep-disordered breathing (apnea-hypopnea index < 15/hr) and without atrial fibrillation were included in this analysis. The mean age was 56 years, 68% were male, 76% had a stroke (n = 34, mean National Institutes of Health Stroke Scale [NIHSS] score of 5, 11 involving the insula) and 24% (n = 11) had a transitory ischaemic attack. Cardiac autonomic control was evaluated using three different tools (spectral, symbolic and entropy analysis) according to sleep stages on short segments of 250 beats in all patients. Polysomnographic studies were performed within 7 days and 3 months after the ischaemic event. No significant differences in cardiac autonomic control between sleep stages were observed in the acute phase and after 3 months. Predominant vagal modulation and decreased sympathetic modulation were observed across all sleep stages in ischaemic stroke involving the insula. Patients with ischaemic stroke and transitory ischaemic attack present a loss of cardiac autonomic dynamics during sleep in the first 3 months after the ischaemic event. This change could represent an adaptive phenomenon, protecting the cardiovascular system from the instabilities of autonomic control, or a risk factor for stroke, which precedes the ischaemic event.
Types de publication
Journal Article
Multicenter Study
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12878Informations de copyright
© 2019 European Sleep Research Society.
Références
Abboud, H., Berroir, S., Labreuche, J., Orjuela, K., & Amarenco, P. (2006). Insular involvement in brain infarction increases risk for cardiac arrhythmia and death. Annals of Neurology, 59, 691-699. https://doi.org/10.1002/ana.20806
Beissner, F., Meissner, K., Bär, K.-J., & Napadow, V. (2013). The autonomic brain: An activation likelihood estimation meta-analysis for central processing of autonomic function. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 33, 10503-10511. https://doi.org/10.1523/jneurosci.1103-13.2013
Benarroch, E. E. (2018). Brainstem integration of arousal, sleep, cardiovascular, and respiratory control. Neurology, 91, 958-966. https://doi.org/10.1212/wnl.0000000000006537
Billman, G. E. (2013). The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance. Front Physiol4, 26.
Binici, Z., Mouridsen, M. R., Kober, L., & Sajadieh, A. (2011). Decreased nighttime heart rate variability is associated with increased stroke risk. Stroke, 42, 3196-3201. https://doi.org/10.1161/strokeaha.110.607697
Busek, P., Vanková, J., Opavský, J., Salinger, J., & Nevsímalová, S. (2005). Spectral analysis of the heart rate variability in sleep. Physiological Research, 54, 369-376.
Cereda, C. W., Petrini, L., Azzola, A., Ciccone, A., Fischer, U., Gallino, A., … Limoni, C. (2012). Sleep-disordered breathing in acute ischemic stroke and transient ischemic attack: Effects on short- and long-term outcome and efficacy of treatment with continuous positive airways pressure-rationale and design of the SAS CARE study. International Journal of Stroke: Official Journal of the International Stroke Society, 7, 597-603. https://doi.org/10.1111/j.1747-4949.2012.00836.x
Chen, Z., Venkat, P., Seyfried, D., Chopp, M., Yan, T., & Chen, J. (2017). Brain-Heart interaction: Cardiac complications after stroke. Circulation Research, 121, 451-468. https://doi.org/10.1161/circresaha.117.311170
Christensen, H. (2005). Insular lesions, ECG abnormalities, and outcome in acute stroke. Journal of Neurology, Neurosurgery and Psychiatry, 76, 269-271. https://doi.org/10.1136/jnnp.2004.037531
Colivicchi, F., Bassi, A., Santini, M., & Caltagirone, C. (2004). Cardiac autonomic derangement and arrhythmias in right-sided stroke with insular involvement. Stroke, 35, 2094-2098. https://doi.org/10.1161/01.str.0000138452.81003.4c
De Raedt, S., De Vos, A., & De Keyser, J. (2015). Autonomic dysfunction in acute ischemic stroke: An underexplored therapeutic area? Journal of the Neurological Sciences, 348, 24-34. https://doi.org/10.1016/j.jns.2014.12.007
Eckardt, M., Gerlach, L., & Welter, F. L. (1999). Prolongation of the frequency-corrected QT dispersion following cerebral strokes with involvement of the insula of Reil. European Neurology, 42, 190-193. https://doi.org/10.1159/000008105
Eckberg, D. L. (1997). Sympathovagal balance: A critical appraisal. Circulation, 96, 3224-3232. https://doi.org/10.1161/01.cir.96.9.3224
Ferri, R., Parrino, L., Smerieri, A., Terzano, M. G., Elia, M., Musumeci, S. A., & Pettinato, S. (2000). Cyclic alternating pattern and spectral analysis of heart rate variability during normal sleep. Journal of Sleep Research, 9, 13-18. https://doi.org/10.1046/j.1365-2869.2000.00190.x
Gasanov, R. L., Gitlevich, T. R., Lesnyak, V. N., & YaI, L. (1998). Structure of nocturnal sleep in patients with cerebral insult. Neuroscience and Behavioral Physiology, 28, 325-329. https://doi.org/10.1007/bf02462964
Giubilei, F., Strano, S., Lino, S., Calcagnini, G., Tisei, P., Fiorelli, M., … Fieschi, C. (1998). Autonomic nervous activity during sleep in middle cerebral artery infarction. Cerebrovascular Disease, 8, 118-123. https://doi.org/10.1159/000015829
Goldstein, D. S., Bentho, O., Park, M., & Sharabi, Y. (2011). Low-frequency power of heart rate variability is not a measure of cardiac sympathetic tone but may be a measure of modulation of cardiac autonomic outflows by baroreflexes. Experimental Physiology, 1255-1261.
Graff, B., Gasecki, D., Rojek, A., Boutouyrie, P., Nyka, W., Laurent, S., & Narkiewicz, K. (2013). Heart rate variability and functional outcome in ischemic stroke: A multiparameter approach. Journal of Hypertension, 31, 1629-1636. https://doi.org/10.1097/hjh.0b013e328361e48b
Hermann, D. M., & Bassetti, C. L. (2016). Role of sleep-disordered breathing and sleep-wake disturbances for stroke and stroke recovery. Neurology, 87, 1407-1416. https://doi.org/10.1212/wnl.0000000000003037
Hilz, M. J., Dütsch, M., Perrine, K., Nelson, P. K., Rauhut, U., & Devinsky, O. (2001). Hemispheric influence on autonomic modulation and baroreflex sensitivity. Annals of Neurology, 49, 575-584. https://doi.org/10.1002/ana.1006
Huang, S. S., Su, H. H., Kuo, T. B., Chen, C. Y., Lan, Y. Y., Liu, B. Y., … Yang, C. C. (2012). Suppressing cardiac vagal modulation and changing sleep patterns in rats after chronic ischemic stroke injury. Autonomic Neuroscience, 169, 116-123. https://doi.org/10.1016/j.autneu.2012.05.006
Iber, C., Ancoli-Israel, S., Chesson, A., & Quan, S. (2007). The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. 1st ed., american academy of sleep medicine
Kallmünzer, B., Breuer, L., Kahl, N., Bobinger, T., Raaz-Schrauder, D., Huttner, H. B., … Köhrmann, M. (2012). Serious cardiac arrhythmias after stroke: Incidence, time course, and predictors-a systematic, prospective analysis. Stroke, 43, 2892-2897. https://doi.org/10.1161/strokeaha.112.664318
Korpelainen, J. T., Sotaniemi, K. A., Huikuri, H. V., & Myllyä, V. V. (1996). Abnormal heart rate variability as a manifestation of autonomic dysfunction in hemispheric brain infarction. Stroke, 27, 2059-2063. https://doi.org/10.1161/01.str.27.11.2059
Korpelainen, J. T., Sotaniemi, K. A., Huikuri, H. V., & Myllylä, V. V. (1997). Circadian rhythm of heart rate variability is reversibly abolished in ischemic stroke. Stroke, 28, 2150-2154. https://doi.org/10.1161/01.str.28.11.2150
Korpelainen, J. T., Sotaniemi, K. A., Mäkikallio, A., Huikuri, H. V., & Myllylä, V. V. (1999). Dynamic behavior of heart rate in ischemic stroke. Stroke, 30, 1008-1013. https://doi.org/10.1161/01.str.30.5.1008
Kuriyama, N., Mizuno, T., Niwa, F., Watanabe, Y., & Nakagawa, M. (2010). Autonomic nervous dysfunction during acute cerebral infarction. Neurological Research, 32, 821-827. https://doi.org/10.1179/016164109x12464612122696
Laowattana, S., Zeger, S. L., Lima, J. A. C., Goodman, S. N., Wittstein, I. S., & Oppenheimer, S. M. (2006). Left insular stroke is associated with adverse cardiac outcome. Neurology, 66, 477-483; discussion 463. https://doi.org/10.1212/01.wnl.0000202684.29640.60
Li, D., Hodge, J., Wei, X.-C., & Kirton, A. (2012). Reduced ipsilesional cortical volumes in fetal periventricular venous infarction. Stroke, 43, 1404-1407. https://doi.org/10.1161/strokeaha.111.645077
Martelli, D., Silvani, A., McAllen, R. M., May, C. N., & Ramchandra, R. (2014). The low frequency power of heart rate variability is neither a measure of cardiac sympathetic tone nor of baroreflex sensitivity. American Journal of Physiology. Heart and Circulatory Physiology, 307, H1005-H1012. https://doi.org/10.1152/ajpheart.00361.2014
Meglic, B., Kobal, J., Osredkar, J., & Pogacnik, T. (2001). Autonomic nervous system function in patients with acute brainstem stroke. Cerebrovascular Disease, 11, 2-8. https://doi.org/10.1159/000047605
Montano, N., Porta, A., Cogliati, C., Costantino, G., Tobaldini, E., Casali, K. R., & Iellamo, F. (2009). Heart rate variability explored in the frequency domain: A tool to investigate the link between heart and behavior. Neuroscience and Biobehavioral Reviews, 33, 71-80. https://doi.org/10.1016/j.neubiorev.2008.07.006
Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., … Howard, V. J. (2016). Heart Disease and Stroke Statistics-2016 update: A report from the American Heart Association. Circulation, 133, e38-e360.
Narkiewicz, K., Montano, N., Cogliati, C., van de Borne, P. J., Dyken, M. E., & Somers, V. K. (1998). Altered cardiovascular variability in obstructive sleep apnea. Circulation, 98, 1071-1077. https://doi.org/10.1161/01.cir.98.11.1071
Oluigbo, C. O., Wang, J., Whitehead, M. T., Magge, S., Myseros, J. S., Yaun, A., … Keating, R. (2015). The influence of lesion volume, perilesion resection volume, and completeness of resection on seizure outcome after resective epilepsy surgery for cortical dysplasia in children. Journal of Neurosurgery Pediatrics, 15, 644-650. https://doi.org/10.3171/2014.10.peds14282
Oppenheimer, S. M., Gelb, A., Girvin, J. P., & Hachinski, V. C. (1992). Cardiovascular effects of human insular cortex stimulation. Neurology, 42, 1727-1727. https://doi.org/10.1212/wnl.42.9.1727
Ozdemir, O., & Hachinski, V. (2008). Brain lateralization and sudden death: Its role in the neurogenic heart syndrome. Journal of the Neurological Sciences, 268, 6-11. https://doi.org/10.1016/j.jns.2007.11.009
Porta, A., Gnecchi-Ruscone, T., Tobaldini, E., Guzzetti, S., Furlan, R., & Montano, N. (2007). Progressive decrease of heart period variability entropy-based complexity during graded head-up tilt. Journal of Applied Physiology, 103, 1143-1149.
Porta, A., Tobaldini, E., Guzzetti, S., Furlan, R., Montano, N., & Gnecchi-Ruscone, T. (2007). Assessment of cardiac autonomic modulation during graded head-up tilt by symbolic analysis of heart rate variability. American Journal of Physiology: Heart and Circulatory Physiology, 293, H702-H708. https://doi.org/10.1152/ajpheart.00006.2007
Rossi, S., Santarnecchi, E., Valenza, G., Ulivelli, M., & Rossi, S. (2016). The heart side of brain neuromodulation. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 374, 20150187.
Sander, D., Winbeck, K., Klingelhöfer, J., Etgen, T., & Conrad, B. (2001). Prognostic relevance of pathological sympathetic activation after acute thromboembolic stroke. Neurology, 57, 833-838. https://doi.org/10.1212/wnl.57.5.833
Sörös, P., & Hachinski, V. (2012). Cardiovascular and neurological causes of sudden death after ischaemic stroke. lancet. The Lancet. Neurology, 11, 179-188.
Tahsili-Fahadan, P., & Geocadin, R. G. (2017). Heart-Brain axis. Circulation Research, 120, 559-572. https://doi.org/10.1161/circresaha.116.308446
Tobaldini, E., Brugada, J., Benito, B., Molina, I., Montserrat, J., Kara, T., … Somers, V. K. (2013). Cardiac autonomic control in Brugada syndrome patients during sleep: The effects of sleep disordered breathing. International Journal of Cardiology, 168, 3267-3272. https://doi.org/10.1016/j.ijcard.2013.04.137
Tobaldini, E., Nobili, L., Strada, S., Casali, K. R., Braghiroli, A., & Montano, N. (2013). Heart rate variability in normal and pathological sleep. Frontiers in Physiology, 4, 294.
Tobaldini, E., Proserpio, P., Sambusida, K., Lanza, A., Redaelli, T., Frigerio, P., … Nobili, L. (2015). Preserved cardiac autonomic dynamics during sleep in subjects with spinal cord injuries. Sleep Medicine, 16, 779-784. https://doi.org/10.1016/j.sleep.2014.12.023
Tokgözoglu, S. L., Batur, M. K., Topçuoglu, M. A., Saribas, O., Kes, S., & Oto, A. (1999). Effects of stroke localization on cardiac autonomic balance and sudden death. Stroke, 30, 1307-1311. https://doi.org/10.1161/01.str.30.7.1307
Verberne, A. J., & Owens, N. C. (1998). Cortical modulation of the cardiovascular system. Progress in Neurobiology, 54, 149-168. https://doi.org/10.1016/s0301-0082(97)00056-7
de Zambotti, M., Trinder, J., Silvani, A., Colrain, I. M., & Baker, F. C. (2018). Dynamic coupling between the central and autonomic nervous systems during sleep: A review. Neuroscience and Biobehavioral Reviews, 90, 84-103. https://doi.org/10.1016/j.neubiorev.2018.03.027