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Review

Diagnosing epileptic seizures in patients with Alzheimer’s disease and deciding on the appropriate treatment plan

&
Pages 361-370 | Received 09 Nov 2023, Accepted 26 Feb 2024, Published online: 01 Mar 2024

References

  • Scheltens P, De Strooper B, Kivipelto M, et al. WM. Alzheimer’s disease. Lancet. 2021;397(10284):1577–1590. doi: 10.1016/S0140-6736(20)32205-4
  • Brigo F, Nardone R. Epilepsy associated with Alzheimer’s disease and other adult neurodegenerative disorders. In: Shorvon S, Guerrini R, Schachter S Trinka E, editors The causes of epilepsy: common and uncommon causes in adults and children. Cambridge: Cambridge University Press; 2019. p. 783–789.
  • Sosa-Ortiz AL, Acosta-Castillo I, Prince MJ. Epidemiology of dementias and Alzheimer’s disease. Arch Med Res. 2012;43(8):600–8. doi: 10.1016/j.arcmed.2012.11.003
  • Meng XF, Yu JT, Wang HF, et al. Midlife vascular risk factors and the risk of Alzheimer’s disease: a systematic review and meta-analysis. J Alzheimers Dis. 2014;42(4):1295–310. doi: 10.3233/JAD-140954
  • Davis KAS, Bishara D, Perera G, et al. Benefits and harms of statins in people with dementia: a systematic review and meta-analysis. J Am Geriatr Soc. 2020;68(3):650–658. doi: 10.1111/jgs.16342
  • Hyman BT, Phelps CH, Beach TG, et al. National Institute on Aging–Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease. Alzheimer’s Dementia. 2012;8(1):1–13. doi: 10.1016/j.jalz.2011.10.007
  • Cheng X, Wei Y, Qian Z, et al. Autophagy balances neuroinflammation in Alzheimer’s disease. Cell Mol Neurobiol. 2023;43(4):1537–1549. doi: 10.1007/s10571-022-01269-6
  • Montembeault M, Migliaccio R. Atypical forms of Alzheimer’s disease: patients not to forget. Curr Opin Neurol. 2023;36(4):245–252. doi: 10.1097/WCO.0000000000001182
  • Kumfor F, Halliday GM, Piguet O. Clinical aspects of Alzheimer’s disease. Adv Neurobiol. 2017;15:31–53.
  • Villain N, Dubois B. Alzheimer’s disease including focal presentations. Semin Neurol. 2019;39(2):213–226. doi: 10.1055/s-0039-1681041
  • Liang CS, Li DJ, Yang FC, et al. Mortality rates in Alzheimer’s disease and non-Alzheimer’s dementias: a systematic review and meta-analysis. Lancet Healthy Longev. 2021;2(8):e479–e488. doi: 10.1016/S2666-7568(21)00140-9
  • Romanelli MF, Morris JC, Ashkin K, et al. Advanced Alzheimer’s disease is a risk factor for late-onset seizures. Arch Neurol. 1990;47(8):847–850. doi: 10.1001/archneur.1990.00530080029006
  • Hesdorffer DC, Hauser WA, Annegers JF, et al. Dementia and adult-onset unprovoked seizures. Neurology. 1996;46(3):727–730. doi: 10.1212/WNL.46.3.727
  • Pandis D, Scarmeas N. Seizures in Alzheimer disease: clinical and epidemiological data. Epilepsy Curr. 2012;12(5):184–187. doi: 10.5698/1535-7511-12.5.184
  • Nicastro N, Assal F, Seeck M. From here to epilepsy: the risk of seizure in patients with Alzheimer’s disease. Epileptic Disord. 2016;18(1):1–12. doi: 10.1684/epd.2016.0808
  • Sen A, Jette N, Husain M, et al. Epilepsy in older people. Lancet. 2020;395(10225):735–748. doi: 10.1016/S0140-6736(19)33064-8
  • Scarmeas N, Honig LS, Choi H, et al. Seizures in Alzheimer disease: who, when, and how common? Arch Neurol. 2009;66(8):992–997. doi: 10.1001/archneurol.2009.130
  • Irizarry MC, Jin S, He F, et al. Incidence of new-onset seizures in mild to moderate Alzheimer disease. Arch Neurol. 2012;69(3):368–372. doi: 10.1001/archneurol.2011.830
  • Mendez MF, Catanzaro P, Doss RC, et al. Seizures in Alzheimer’s disease: clinicopathologic study. J Geriatr Psychiatry Neurol. 1994;7(4):230–233. doi: 10.1177/089198879400700407
  • Larner AJ, Doran M. Clinical phenotypic heterogeneity of Alzheimer’s disease associated with mutations of the presenilin–1 gene. J Neurol. 2006;253(2):139–158. doi: 10.1007/s00415-005-0019-5
  • Zarea A, Charbonnier C, Rovelet-Lecrux A, et al. PHRC GMAJ Collaborators. Seizures in dominantly inherited Alzheimer disease. Neurology. 2016 30;87(9):912–919. doi: 10.1212/WNL.0000000000003048
  • Johnson EL, Krauss GL, Lee AK, et al. Association between midlife risk factors and late-onset epilepsy: results from the atherosclerosis risk in communities study. JAMA Neurol. 2018;75(11):1375–1382. doi: 10.1001/jamaneurol.2018.1935
  • Chan J, Jones NC, Bush AI, et al. A mouse model of Alzheimer’s disease displays increased susceptibility to kindling and seizure-associated death. Epilepsia. 2015;56(6):e73–7. doi: 10.1111/epi.12993
  • Palop JJ, Mucke L. Network abnormalities and interneuron dysfunction in Alzheimer disease. Nat Rev Neurosci. 2016;17(12):777–792. doi: 10.1038/nrn.2016.141
  • Heggland I, Kvello P, Witter MP. Electrophysiological characterization of networks and single cells in the hippocampal region of a transgenic rat model of Alzheimer’s disease. eNeuro. 2019;6(1):ENEURO.0448–17.2019. doi: 10.1523/ENEURO.0448-17.2019
  • Kang JQ. Epileptic mechanisms shared by Alzheimer’s disease: viewed via the Unique lens of genetic epilepsy. Int J Mol Sci. 2021;22(13):7133. doi: 10.3390/ijms22137133
  • Rao SC, Dove G, Cascino GD, et al. Recurrent seizures in patients with dementia: frequency, seizure types, and treatment outcome. Epilepsy Behav. 2009;14(1):118–120. doi: 10.1016/j.yebeh.2008.08.012
  • Bernardi S, Scaldaferri N, Vanacore N, et al. Seizures in Alzheimer’s disease: a retrospective study of a cohort of outpatients. Epileptic Disord. 2010;12(1):16–21. doi: 10.1684/epd.2010.0290
  • Hauser WA, Morris ML, Heston LL, et al. Seizures and myoclonus in patients with Alzheimer’s disease. Neurology. 1986;36(9):1226–1230. doi: 10.1212/WNL.36.9.1226
  • 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(1):211–223. doi: 10.3233/JAD-170031
  • Brigo F, Mecarelli O. Aging and degenerative disorders. In: Mecarelli O, editor. Clinical electroencephalography. Cham, Switzerland: Springer; 2019. p. 661–676.
  • Silveira DC, Jehi L, Chapin J, et al. Seizure semiology and aging. Epilepsy Behav. 2011;20(2):375–377. doi: 10.1016/j.yebeh.2010.12.033
  • Kellinghaus C, Loddenkemper T, Dinner DS, et al. Seizure semiology in the elderly: a video analysis. Epilepsia. 2004;45(3):263–267. doi: 10.1111/j.0013-9580.2004.29003.x
  • Brodie MJ, Elder AT, Kwan P. Epilepsy in later life. Lancet Neurol. 2009;8(11):1019–1030. doi: 10.1016/S1474-4422(09)70240-6
  • Kinney MO, Craig JJ, Kaplan PW. Non-convulsive status epilepticus: mimics and chameleons. Pract Neurol. 2018;18(4):291–305. doi: 10.1136/practneurol-2017-001796
  • Kinney MO, Craig JJ, Kaplan PW. Hidden in plain sight: Non-convulsive status epilepticus-Recognition and management. Acta Neurol Scand. 2017;136(4):280–292. doi: 10.1111/ane.12732
  • Cretin B, Sellal F, Philippi N, et al. Epileptic prodromal Alzheimer’s disease, a retrospective study of 13 new cases: expanding the spectrum of Alzheimer’s disease to an epileptic variant? J Alzheimers Dis. 2016;52(3):1125–1133. doi: 10.3233/JAD-150096
  • Horváth A, Szűcs A, Barcs G, et al. Epileptic Seizures in Alzheimer Disease: A Review. Alzheimer Dis Assoc Disord. 2016;30(2):186–92. doi: 10.1097/WAD.0000000000000134
  • Vossel KA, Beagle AJ, Rabinovici GD, et al. Seizures and epileptiform activity in the early stages of Alzheimer disease. JAMA Neurol. 2013;70(9):1158–1166. doi: 10.1001/jamaneurol.2013.136
  • Horváth A, Szűcs A, Hidasi Z, et al. Prevalence, semiology, and risk factors of epilepsy in Alzheimer’s disease: an ambulatory EEG study. J Alzheimers Dis. 2018;63(3):1045–1054. doi: 10.3233/JAD-170925
  • Vossel KA, Ranasinghe KG, Beagle AJ, et al. Incidence and impact of subclinical epileptiform activity in Alzheimer’s disease. Ann Neurol. 2016;80(6):858–870. doi: 10.1002/ana.24794
  • Ciliento R, Gjini K, Dabbs K, et al. Prevalence and localization of nocturnal epileptiform discharges in mild cognitive impairment. Brain Commun. 2023;5(6):fcad302. doi: 10.1093/braincomms/fcad302
  • Lam AD, Deck G, Goldman A, et al. Silent hippocampal seizures and spikes identified by foramen ovale electrodes in Alzheimer’s disease. Nat Med. 2017;23(6):678–680. doi: 10.1038/nm.4330
  • Ranasinghe KG, Kudo K, Hinkley, et al. Neuronal synchrony abnormalities associated with subclinical epileptiform activity in early-onset Alzheimer’s disease. Brain. 2022;145(2):744–753. doi: 10.1093/brain/awab442
  • Brick JF, Gutierrez AR, Cheek JC, et al. Transient appearance of periodic EEG discharges in senile dementia. Clin Electroencephalogr. 1991;22(2):108–111. doi: 10.1177/155005949102200211
  • Tschampa HJ, Neumann M, Zerr I, et al. Patients with Alzheimer’s disease and dementia with Lewy bodies mistaken for Creutzfeldt-Jakob disease. J Neurol Neurosurg Psychiatry. 2001;71(1):33–39. 10.1136/jnnp.71.1.33
  • Doran M, Larner AJ. EEG findings in dementia with Lewy bodies causing diagnostic confusion with sporadic Creutzfeldt-Jakob disease. Eur J Neurol. 2004;11(12):838–841. doi: 10.1111/j.1468-1331.2004.00895.x
  • Musaeus CS, Kjaer TW, Cacic Hribljan M, et al. Subclinical epileptiform activity in dementia with Lewy Bodies. Mov Disord. 2023;38(10):1861–1870. doi: 10.1002/mds.29531
  • Brigo F, Storti M. Triphasic waves. Am J Electroneurodiagnostic Technol. 2011;51(1):16. doi: 10.1080/1086508X.2011.11079796
  • Brigo F. An evidence-based approach to proper diagnostic use of the electroencephalogram for suspected seizures. Epilepsy Behav. 2011;21(3):219–222. doi: 10.1016/j.yebeh.2011.04.004
  • Vossel KA, Tartaglia MC, Nygaard HB, et al. Epileptic activity in Alzheimer’s disease: causes and clinical relevance. Lancet Neurol. 2017;16(4):311–322. doi: 10.1016/S1474-4422(17)30044-3
  • McAreavey MJ, Ballinger BR, Fenton GW. Epileptic seizures in elderly patients with dementia. Epilepsia. 1992;33(4):657–660. doi: 10.1111/j.1528-1157.1992.tb02343.x
  • Vercueil L. Epilepsy and neurodegenerative diseases in adults: a clinical review. Epileptic Disord. 2006;8:S44–S54.
  • Salinsky M, Kanter R, Dasheiff RM. Effectiveness of multiple EEGs in supporting the diagnosis of epilepsy: an operational curve. Epilepsia. 1987;28(4):331–334. doi: 10.1111/j.1528-1157.1987.tb03652.x
  • Burkholder DB, Britton JW, Rajasekaran V, et al. Routine vs extended outpatient EEG for the detection of interictal epileptiform discharges. Neurology. 2016;86(16):1524–1530. doi: 10.1212/WNL.0000000000002592
  • Lam AD, Sarkis RA, Pellerin KR, et al. Association of epileptiform abnormalities and seizures in Alzheimer disease. Neurology. 2020;95(16):e2259–e2270. doi: 10.1212/WNL.0000000000010612
  • Ghosh S, Jehi LE. New-onset epilepsy in the elderly: challenges for the internist. Cleve Clin J Med. 2014;81(8):490–498. doi: 10.3949/ccjm.81a.13148
  • Howland RH. Drug therapies for cognitive impairment and dementia. J Psychosoc Nurs Ment Health Serv. 2010;48(4):11–14. doi: 10.3928/02793695-20100311-01
  • Kumlien E, Lundberg PO. Seizure risk associated with neuroactive drugs: data from the WHO adverse drug reactions database. Seizure. 2010;19(2):69–73. doi: 10.1016/j.seizure.2009.11.005
  • McShane R, Areosa Sastre A, Minakaran N. Memantine for dementia. Cochrane Database Syst Rev. 2006 2. CD003154. doi: 10.1002/14651858.CD003154.pub5
  • Harms SL, Garrard J, Schwinghammer P, et al. Ginkgo biloba use in nursing home elderly with epilepsy or seizure disorder. Epilepsia. 2006;47(2):323–329. doi: 10.1111/j.1528-1167.2006.00424.x
  • Zhai Y, Yin S, Zhang D, et al. Association between Antipsychotic drugs and mortality in older persons with Alzheimer’s disease: a systematic review and meta-analysis. J Alzheimers Dis. 2016;52(2):631–639. doi: 10.3233/JAD-151207
  • Bloechliger M, Rüegg S, Jick SS, et al. Antipsychotic drug use and the risk of seizures: follow-up study with a nested case–control analysis. CNS Drugs. 2015;29(7):591–603. doi: 10.1007/s40263-015-0262-y
  • Ruffmann C, Bogliun G, Beghi E. Epileptogenic drugs: a systematic review. Expert Rev Neurother. 2006;6(4):575–589. doi: 10.1586/14737175.6.4.575
  • Lertxundi U, Hernandez R, Medrano J, et al. Antipsychotics and seizures: higher risk with atypicals? Seizure. 2013;22(2):141–143. doi: 10.1016/j.seizure.2012.10.009
  • Montgomery SA. Antidepressants and seizures: emphasis on newer agents and clinical implications. Int J Clin Pract. 2005;59(12):1435–1440. doi: 10.1111/j.1368-5031.2005.00731.x
  • Hill T, Coupland C, Morriss R, et al. Antidepressant use and risk of epilepsy and seizures in people aged 20 to 64 years: cohort study using a primary care database. BMC Psychiatry. 2015;15(1):315. doi: 10.1186/s12888-015-0701-9
  • Chandra V, Bharucha NE, Schoenberg BS. Conditions associated with Alzheimer’s disease at death: case-control study. Neurology. 1987;36(2):209–211. doi: 10.1212/WNL.36.2.209
  • Volicer L, Smith S, Volicer BJ. Effect of seizures on progression of dementia of the Alzheimer type. Dementia. 1995;6(5):258–263. doi: 10.1159/000106956
  • Brigo F, Lattanzi S, Zelano J, et al. Randomized controlled trials of antiepileptic drugs for the treatment of post-stroke seizures: a systematic review with network meta-analysis. Seizure. 2018;61:57–62. doi: 10.1016/j.seizure.2018.08.001
  • Belcastro V, Costa C, Galletti F, et al. Levetiracetam monotherapy in Alzheimer patients with late-onset seizures: a prospective observational study. Eur J Neurol. 2007;14(10):1176–1178. doi: 10.1111/j.1468-1331.2007.01907.x
  • Liu J, Wang LN. Treatment of epilepsy for people with Alzheimer’s disease. Cochrane Database Syst Rev. 2021 May 11;5(5):CD011922. doi: 10.1002/14651858.CD011922.pub4
  • Cumbo E, Ligori LD. Levetiracetam, lamotrigine, and phenobarbital in patients with epileptic seizures and Alzheimer’s disease. Epilepsy Behav. 2010;17(4):461–466.
  • SANAD II collaborators, Marson A, Burnside G, et al. The SANAD II study of the effectiveness and cost-effectiveness of levetiracetam, zonisamide, or lamotrigine for newly diagnosed focal epilepsy: an open-label, non-inferiority, multicentre, phase 4, randomised controlled trial. Lancet. 2021;397(10282):1363–1374.
  • Larner AJ, Marson AG. Epileptic seizures in Alzheimer’s disease: what are the implications of SANAD II? J Alzheimers Dis. 2022;85(2):527–529. doi: 10.3233/JAD-215154
  • Lattanzi S, Trinka E, Del Giovane C, et al. Antiepileptic drug monotherapy for epilepsy in the elderly: a systematic review and network meta-analysis. Epilepsia. 2019;60(11):2245–2254. doi: 10.1111/epi.16366
  • Rohracher A, Kalss G, Kuchukhidze G, et al. New anti-seizure medication for elderly epilepsy patients - a critical narrative review. Expert Opin Pharmacother. 2021;22(5):621–634. doi: 10.1080/14656566.2020.1843636
  • Piccenna L, O’Dwyer R, Leppik I, et al. Management of epilepsy in older adults: a critical review by the ILAE task force on epilepsy in the elderly. Epilepsia. 2023;64(3):567–585. doi: 10.1111/epi.17426
  • Minkeviciene R, Rheims S, Dobszay MB, et al. Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J Neurosci. 2009;29(11):3453–3462. doi: 10.1523/JNEUROSCI.5215-08.2009
  • Liao WP, Shi YW, Long YS, et al. Partial epilepsy with antecedent febrile seizures and seizure aggravation by antiepileptic drugs: associated with loss of function of Na(v) 1.1. Epilepsia. 2010;51(9):1669–1678. doi: 10.1111/j.1528-1167.2010.02645.x
  • Bakker A, Krauss GL, Albert MS, et al. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron. 2012;74(3):467–474. doi: 10.1016/j.neuron.2012.03.023
  • Sanchez PE, Zhu L, Verret L, et al. Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer’s disease model. Proc Natl Acad Sci U S A. 2012;109(42):E2895–903. doi: 10.1073/pnas.1121081109
  • Bakker A, Albert MS, Krauss G, et al. Response of the medial temporal lobe network in amnestic mild cognitive impairment to therapeutic intervention assessed by fMRI and memory task performance. NeuroImage Clin. 2015;7:688–698. doi: 10.1016/j.nicl.2015.02.009
  • Vossel K, Ranasinghe KG, Beagle AJ, et al. Effect of Levetiracetam on cognition in patients with Alzheimer disease with and without epileptiform activity: a randomized clinical trial. JAMA Neurol. 2021;78(11):1345–1354. doi: 10.1001/jamaneurol.2021.3310
  • Hautecloque-Raysz G, Sellal F, Bousiges O, et al. Epileptic prodromal Alzheimer’s disease treated with antiseizure medications: medium-term outcome of seizures and cognition. J Alzheimers Dis. 2023;94(3):1057–1074. doi: 10.3233/JAD-221197
  • Hesdorffer DC, Benn EK, Cascino GD, et al. Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia. 2009;50(5):1102–1108. doi: 10.1111/j.1528-1167.2008.01945.x
  • Mauritz M, Hirsch LJ, Camfield P, et al. Acute symptomatic seizures: an educational, evidence-based review. Epileptic Disord. 2022;24(1):26–49. doi: 10.1684/epd.2021.1376
  • Mahamud Z, Mononen CP, Brigo F, et al. Risk of epilepsy diagnosis after a first unprovoked seizure in dementia. Seizure. 2020;82:118–124. doi: 10.1016/j.seizure.2020.09.001
  • Zelano J, Brigo F, Garcia-Patek S. Increased risk of epilepsy in patients registered in the Swedish dementia registry. Eur J Neurol. 2020;27(1):129–135. doi: 10.1111/ene.14043
  • 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(11):e1132–e1140. doi: 10.1212/WNL.0000000000012483
  • Hesdorffer DC, Tomson T. Sudden unexpected death in epilepsy. Potential role of antiepileptic drugs. CNS Drugs. 2013;27(2):113–119. doi: 10.1007/s40263-012-0006-1
  • Opeskin K, Berkovic SF. Risk factors for sudden unexpected death in epilepsy: a controlled prospective study based on coroners cases. Seizure. 2003;12(7):456–464. doi: 10.1016/S1059-1311(02)00352-7
  • Bergey GK. Initial treatment of epilepsy. Special issues in treating the elderly. Neurology. 2004;63(10 suppl 4):S40–S48. doi: 10.1212/WNL.63.10_suppl_4.S40
  • Zelano J, Holtkamp M, Agarwal N, et al. How to diagnose and treat post-stroke seizures and epilepsy. Epileptic Disord. 2020;22(3):252–263. doi: 10.1684/epd.2020.1159
  • Galovic M, Ferreira-Atuesta C, Abraira L, et al. Seizures and epilepsy after stroke: epidemiology biomarkers and management. Drugs Aging. 2021;38(4):285–299. doi: 10.1007/s40266-021-00837-7
  • Seo JG, Cho YW, Kim KT, et al. Pharmacological treatment of epilepsy in elderly patients. J Clin Neurol. 2020;16(4):556–561. doi: 10.3988/jcn.2020.16.4.556
  • Josephson CB, Wiebe S, Delgado-Garcia G, et al. Association of enzyme-inducing antiseizure drug use with Long-term cardiovascular disease. JAMA Neurol. 2021;78(11):1367–1374. doi: 10.1001/jamaneurol.2021.3424
  • Huang R. Alzheimer’s disease diagnosis based on the EEG analysis. Stud Health Technol Inform. 2023;308:574–582. doi: 10.3233/SHTI230887
  • Tveit J, Aurlien H, Plis S, et al. Automated interpretation of clinical electroencephalograms using artificial intelligence. JAMA Neurol. 2023;80(8):805–812. doi: 10.1001/jamaneurol.2023.1645
  • AlSharabi K, Salamah YB, Aljalal M, et al. EEG-based clinical decision support system for Alzheimer’s disorders diagnosis using EMD and deep learning techniques. Front Hum Neurosci. 2023;17:1190203. doi: 10.3389/fnhum.2023.1190203
  • Dogan S, Baygin M, Tasci B, et al. Primate brain pattern-based automated Alzheimer’s disease detection model using EEG signals. Cogn Neurodyn. 2023;17(3):647–659. doi: 10.1007/s11571-022-09859-2
  • Chen Y, Wang H, Zhang D, et al. Multi-feature fusion learning for Alzheimer’s disease prediction using EEG signals in resting state. Front Neurosci. 2023;17:1272834. doi: 10.3389/fnins.2023.1272834
  • Illakiya T, Karthik R. Automatic detection of Alzheimer’s disease using deep learning models and neuro-imaging: Current trends and future perspectives. Neuroinformatics. 2023;21(2):339–364. doi: 10.1007/s12021-023-09625-7
  • Lattanzi S, Zaccara G, Giovannelli F, et al. Antiepileptic monotherapy in newly diagnosed focal epilepsy. A network meta-analysis. Acta Neurol Scand. 2019;139(1):33–41. doi: 10.1111/ane.13025
  • Bosco F, Guarnieri L, Rania V, et al. Antiseizure Medications in Alzheimer’s Disease from Preclinical to Clinical Evidence. Int J Mol Sci. 2023;24(16):12639. doi: 10.3390/ijms241612639

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