Association of Seizure Control with Mortality, Cognition, and Function in People With Dementia.
Journal
Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
revised:
21
09
2024
received:
17
07
2024
accepted:
17
10
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
aheadofprint
Résumé
The effects of seizure control on outcomes in persons with dementia (PWD) remain unclear. Our study aimed to investigate the impact of seizure control on mortality, function, cognition, and mood among PWD. This longitudinal, multicenter study is based on 39 Alzheimer's disease centers (ADCs) in the United States from September 2005 to December 2021. PWD were grouped by seizure status into recurrent (seizures in the past year), remote (prior seizures but none in the past year), and no seizures (controls). The primary outcome was all-cause mortality among seizure groups. We used Weibull survival analysis to assess the mortality risks by seizure status after adjusting for age, sex, education, race, ethnicity, hypertension, diabetes, hyperlipidemia, degree of cognitive impairment, dominant Alzheimer's disease (AD) mutation, brain trauma, stroke, Parkinson's disease, alcohol abuse, and depression. Cognition (Clinical Dementia Rating), function (physical dependence and nursing home residence), day-to-day activities (Functional Assessment Scores), and mood (Geriatric Depression Scale) were compared among seizure groups after adjusting for dementia duration and age. Among 26,501 participants, 374 (1.4%) had recurrent seizures and 510 (1.9%) had remote seizures. In multivariable survival analysis, recurrent seizures were associated with a higher mortality risk than remote and no seizures (adjusted hazard ratio [aHR], 95% confidence interval [95% CI]; recurrent aHR = 1.79, 95% CI = 1.51 to 2.12; remote aHR = 1.17, 95% CI = 0.98 to 1.38). Median time-to-death for recurrent, remote, and no seizures was 2.4, 4.0, and 4.7 years, respectively. People with recurrent seizures had worse cognition, day-to-day function, and physical dependence than those with remote seizures and controls. PWD with poorly controlled recurrent seizures have worse mortality, functional, and cognitive outcomes than PWD with remote and no seizures. These findings underscore the need for timely identification and management of ongoing seizures in PWD. ANN NEUROL 2024.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIH HHS
ID : 1K23AG084893-01A1
Pays : United States
Organisme : Alzheimer's Association
ID : AACSFD-22-974008
Pays : United States
Organisme : American Epilepsy Society
ID : 1067206
Informations de copyright
© 2024 The Author(s). Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
Références
Hesdorffer DC, Hauser WA, Annegers JF, et al. Dementia and adult‐onset unprovoked seizures. Neurology 1996;46:727–730. https://doi.org/10.1212/WNL.46.3.727.
Scarmeas N, Honig LS, Choi H, et al. Seizures in Alzheimer disease: who, when, and how common? Arch Neurol 2009;66:992–997. https://doi.org/10.1001/ARCHNEUROL.2009.130.
Hauser WA, Morris ML, Heston LL, Anderson VE. Seizures and myoclonus in patients with Alzheimer's disease. Neurology 1986;36:1226. https://doi.org/10.1212/wnl.36.9.1226.
Johnson EL, Krauss GL, Kucharska‐Newton A, et al. Dementia in late‐onset epilepsy: the atherosclerosis risk in communities study. Neurology 2020;95:e3248–e3256. https://doi.org/10.1212/WNL.0000000000011080.
Breteler MMB, De Groot RRM, Van Romunde LKJ, Hofman A. Risk of dementia in patients with Parkinson's disease, epilepsy, and severe head trauma: a register‐based follow‐up study. Am J Epidemiol 1995;142:1300–1305. https://doi.org/10.1093/OXFORDJOURNALS.AJE.A117597.
Imfeld P, Bodmer M, Schuerch M, et al. Seizures in patients with Alzheimer's disease or vascular dementia: a population‐based nested case‐control analysis. Epilepsia 2013;54:700–707. https://doi.org/10.1111/EPI.12045.
Friedman D, Honig LS, Scarmeas N. Seizures and epilepsy in Alzheimer's disease. CNS Neurosci Ther 2012;18:285–294. https://doi.org/10.1111/j.1755-5949.2011.00251.x.
Breteler MM, van Duijn CM, Chandra V, et al. Medical history and the risk of Alzheimer's disease: a collaborative re‐analysis of case‐control studies. EURODEM risk factors research group. Int J Epidemiol 1991;20:S4–S12.
Zelano J, Brigo F, Garcia‐Patek S. Increased risk of epilepsy in patients registered in the Swedish dementia registry. Eur J Neurol 2020;27:129–135. https://doi.org/10.1111/ene.14043.
Zawar I. The interplay between epilepsy and Alzheimer's disease: a pas De Deux. Epilepsy Curr 2024;24:90–92. https://doi.org/10.1177/15357597231224652.
Vossel KA, Ranasinghe KG, Beagle AJ, et al. Incidence and impact of subclinical epileptiform activity in Alzheimer's disease. Ann Neurol 2016;80:858–870. https://doi.org/10.1002/ANA.24794.
Volicer L, Smith S, Volicer BJ. Effect of seizures on progression of dementia of the Alzheimer type. Dement Geriatr Cogn Disord 1995;6:258–263. https://doi.org/10.1159/000106956.
Zawar I, Kapur J, Mattos MK, et al. Association of Seizure Control with Cognition in people with Normal cognition and mild cognitive impairment. Neurology 2024;103:e209820. https://doi.org/10.1212/WNL.0000000000209820.
Subota A, Jetté N, Josephson CB, et al. Risk factors for dementia development, frailty, and mortality in older adults with epilepsy–a population‐based analysis. Epilepsy Behav 2021;120:108006. https://doi.org/10.1016/j.yebeh.2021.108006.
Beekly DL, Ramos EM, Lee WW, et al. The National Alzheimer's coordinating center (NACC) database: the uniform data set. Alzheimer Dis Assoc Disord 2007;21:249–258. https://doi.org/10.1097/WAD.0b013e318142774e.
Beekly DL, Ramos EM, Van Belle G, et al. The National Alzheimer's coordinating center (NACC) database: an Alzheimer disease database. Alzheimer Dis Assoc Disord 2004;18:270–277.
Morris JC, Weintraub S, Chui HC, et al. The uniform data set (UDS): clinical and cognitive variables and descriptive data from Alzheimer disease centers. Alzheimer Dis Assoc Disord 2006;20:210–216. https://doi.org/10.1097/01.wad.0000213865.09806.92.
Weintraub S, Salmon D, Mercaldo N, et al. The Alzheimer's disease Centers' uniform data set (UDS): the neuropsychologic test battery. Alzheimer Dis Assoc Disord 2009;23:91–101. https://doi.org/10.1097/WAD.0b013e318191c7dd.
Besser L, Kukull W, Knopman DS, et al. Version 3 of the national Alzheimer's coordinating center's uniform data set. Alzheimer Dis Assoc Disord 2018;32:351–358. https://doi.org/10.1097/WAD.0000000000000279.
von Elm E, Altman DG, Egger M, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg 2014;12:1495–1499. https://doi.org/10.1016/j.ijsu.2014.07.013.
Fisher RS, Acevedo C, Arzimanoglou A, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014;55:475–482. https://doi.org/10.1111/EPI.12550.
Morris JC. The clinical dementia rating (CDR). Neurology 1993;43:2412‐A. https://doi.org/10.1212/WNL.43.11.2412-A.
Tractenberg RE, Schafer K, Morris C. Interobserver disagreements on clinical dementia rating assessment: interpretation and implications for. Training 2001;15:155–161.
Brown LM, Schinka JA. Development and initial validation of a 15‐item informant version of the Geriatric depression scale. Int J Geriatr Psychiatry 2005;20:911–918. https://doi.org/10.1002/gps.1375.
Swindell WR. Accelerated failure time models provide a useful statistical framework for aging research. Exp Gerontol 2009;44:190–200. https://doi.org/10.1016/j.exger.2008.10.005.
Marawar R, Wakim N, Albin RL, Dodge H. Seizure occurrence and related mortality in dementia with Lewy bodies. Epilepsy Behav 2020;111:107311. https://doi.org/10.1016/j.yebeh.2020.107311.
Altuna M, Giménez S, Fortea J. Epilepsy in down syndrome: a highly prevalent comorbidity. J Clin Med 2021;10:1–17. https://doi.org/10.3390/jcm10132776.
Zawar I. Seizing off this mortal coil: a matter of epilepsy and death. Epilepsy Curr 2023;23:360–362. https://doi.org/10.1177/15357597231205198.
Devinsky O, Singh A, Friedman D. Deaths in epilepsy: what we are missing. JAMA Neurol 2018;75:913–915. https://doi.org/10.1001/JAMANEUROL.2018.0002.
Salam MT, Montandon G, Genov R, et al. Mortality with brainstem seizures from focal 4‐aminopyridine‐induced recurrent hippocampal seizures. Epilepsia 2017;58:1637–1644. https://doi.org/10.1111/EPI.13846.
Ryvlin P, Nashef L, Lhatoo SD, et al. Incidence and mechanisms of cardiorespiratory arrests in epilepsy monitoring units (MORTEMUS): a retrospective study. Lancet Neurol 2013;12:966–977. https://doi.org/10.1016/S1474-4422(13)70214-X.
Rhone AE, Kovach CK, Harmata GIS, et al. A human amygdala site that inhibits respiration and elicits apnea in pediatric epilepsy. JCI Insight 2020;5:e134852. https://doi.org/10.1172/JCI.INSIGHT.134852.
Strzelczyk A, Griebel C, Lux W, et al. The burden of severely drug‐refractory epilepsy: a comparative longitudinal evaluation of mortality, morbidity, resource use, and cost using German health insurance data. Front Neurol 2017;8:712. https://doi.org/10.3389/FNEUR.2017.00712.
Fang YT, Lee TL, Tu YH, et al. Factors associated with mortality in patients with super‐refractory status epilepticus. Sci Rep 2022;12:1–10. https://doi.org/10.1038/s41598-022-13726-9.
Teran FA, Sainju RK, Bravo E, et al. Seizures cause prolonged impairment of ventilation, CO2 chemoreception and thermoregulation. J Neurosci 2023;43:4959–4971. https://doi.org/10.1523/JNEUROSCI.0450-23.2023.
Förstl H, Burns A, Levy R, et al. Neurologic signs in Alzheimer's disease: results of a prospective clinical and Neuropathologic study. Arch Neurol 1992;49:1038. https://doi.org/10.1001/archneur.1992.00530340054018.
Degiorgio CM, Curtis A, Carapetian A, et al. Why are epilepsy mortality rates rising in the United States? A population‐based multiple cause‐of‐death study. BMJ Open 2020;10:e035767. https://doi.org/10.1136/bmjopen-2019-035767.
Vöglein J, Ricard I, Noachtar S, et al. Seizures in Alzheimer's disease are highly recurrent and associated with a poor disease course. J Neurol 2020;267:2941–2948. https://doi.org/10.1007/S00415-020-09937-7.
Thompson PJ, Duncan JS. Cognitive decline in severe intractable epilepsy. Epilepsia 2005;46:1780–1787. https://doi.org/10.1111/J.1528-1167.2005.00279.X.
Kleen JK, Scott RC, Holmes GL, et al. Hippocampal interictal epileptiform activity disrupts cognition in humans. Neurology 2013;81:18–24. https://doi.org/10.1212/WNL.0B013E318297EE50.
Kleen J, Lenck‐Santini PP, Scott R, et al. Hippocampal interictal epileptiform activity disrupts cognition in humans. Transient cognitive impairment due hippocampal interictal epileptiform activity in humans. Vol 81. Epilepsy Currents: SAGE publisher, 2013:18‐24.
Zawar I, Kapur J. Does Alzheimer's disease with mesial temporal lobe epilepsy represent a distinct disease subtype? Alzheimers Dement 2023;17:2697–2706. https://doi.org/10.1002/ALZ.12943.
Romanelli MF, Ashkin K, Morris JC, Coben LA. Advanced Alzheimer's disease is a risk factor for late‐onset seizures. Arch Neurol 1990;47:847–850. https://doi.org/10.1001/archneur.1990.00530080029006.
Beagle AJ, Darwish SM, Ranasinghe KG, et al. Relative incidence of seizures and myoclonus in Alzheimer's disease, dementia with lewy bodies, and frontotemporal dementia. J Alzheimers Dis 2017;60:211–223. https://doi.org/10.3233/JAD-170031.
Altwaijri WA, Yahya BJ, Alasmari LB, et al. Quality of life in paediatrics with intractable epilepsy in a large paediatric university hospital in Riyadh, Saudi Arabia. J Family Med Primary Care 2020;9:5523. https://doi.org/10.4103/JFMPC.JFMPC_1172_20.
Attarian H, Carter VJ, Hykes E, Gilliam F. Relationship between depression and intractability of seizures. Epilepsy Behav 2003;4:298–301. https://doi.org/10.1016/S1525-5050(03)00083-0.
Sarycheva T, Lavikainen P, Taipale H, et al. Antiepileptic drug use and mortality among community‐dwelling persons with Alzheimer disease. Neurology 2020;94:E2099–E2108. https://doi.org/10.1212/WNL.0000000000009435/ASSET/E5C4E312‐3A8E‐45FA‐A54E‐5CFBCFEA380E/ASSETS/GRAPHIC/8TTU1A.JPEG.
Johnson EL, Krauss GL, Kucharska‐Newton A, et al. Mortality in patients with late‐onset epilepsy: results from the atherosclerosis risk in communities study. Neurology 2021;97:E1132–E1140. https://doi.org/10.1212/WNL.0000000000012483.
Brodie MJ, Elder AT, Kwan P. Epilepsy in later life. Lancet Neurol 2009;8:1019–1030. https://doi.org/10.1016/S1474-4422(09)70240-6.
Stefan H. Epilepsy in the elderly: facts and challenges. Acta Neurol Scand 2011;124:223–237. https://doi.org/10.1111/j.1600-0404.2010.01464.x.
Baker J, Libretto T, Henley W, Zeman A. The prevalence and clinical features of epileptic seizures in a memory clinic population. Seizure 2019;71:83–92. https://doi.org/10.1016/j.seizure.2019.06.016.