Infarct-related structural disconnection and delirium in surgical aortic valve replacement patients.
Journal
Annals of clinical and translational neurology
ISSN: 2328-9503
Titre abrégé: Ann Clin Transl Neurol
Pays: United States
ID NLM: 101623278
Informations de publication
Date de publication:
28 Dec 2023
28 Dec 2023
Historique:
received:
06
10
2023
accepted:
28
10
2023
medline:
29
12
2023
pubmed:
29
12
2023
entrez:
29
12
2023
Statut:
aheadofprint
Résumé
Although acute brain infarcts are common after surgical aortic valve replacement (SAVR), they are often unassociated with clinical stroke symptoms. The relationship between clinically "silent" infarcts and in-hospital delirium remains uncertain; obscured, in part, by how infarcts have been traditionally summarized as global metrics, independent of location or structural consequence. We sought to determine if infarct location and related structural connectivity changes were associated with postoperative delirium after SAVR. A secondary analysis of a randomized multicenter SAVR trial of embolic protection devices (NCT02389894) was conducted, excluding participants with clinical stroke or incomplete neuroimaging (N = 298; 39% female, 7% non-White, 74 ± 7 years). Delirium during in-hospital recovery was serially screened using the Confusion Assessment Method. Parcellation and tractography atlas-based neuroimaging methods were used to determine infarct locations and cortical connectivity effects. Mixed-effect, zero-inflated gaussian modeling analyses, accounting for brain region-specific infarct characteristics, were conducted to examine for differences within and between groups by delirium status and perioperative neuroprotection device strategy. 23.5% participants experienced postoperative delirium. Delirium was associated with significantly increased lesion volumes in the right cerebellum and temporal lobe white matter, while diffusion weighted imaging infarct-related structural disconnection (DWI-ISD) was observed in frontal and temporal lobe regions (p-FDR < 0.05). Fewer brain regions demonstrated DWI-ISD loss in the suction-based neuroprotection device group, relative to filtration-based device or standard aortic cannula. Structural disconnection from acute infarcts was greater in patients who experienced postoperative delirium, suggesting that the impact from covert perioperative infarcts may not be as clinically "silent" as commonly assumed.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NHLBI NIH HHS
ID : R01-HL130443
Pays : United States
Organisme : NHLBI NIH HHS
ID : U01-HL088942
Pays : United States
Organisme : NIA NIH HHS
ID : R01-AG074185
Pays : United States
Investigateurs
Kathleen Fenton
(K)
Marissa A Miller
(MA)
Wendy C Taddei-Peters
(WC)
Neal O Jeffries
(NO)
Dennis Buxton
(D)
Nancy L Geller
(NL)
David Gordon
(D)
Catherine Burke
(C)
Albert Lee
(A)
Tyrone Smith
(T)
Claudia S Moy
(CS)
Ilana Kogan Gombos
(IK)
Marc Gillinov
(M)
Mariell Jessup
(M)
Richard Weisel
(R)
Timothy J Gardner
(TJ)
Eric A Rose
(EA)
Annetine C Gelijns
(AC)
Ellen Moquete
(E)
Helena L Chang
(HL)
Melissa Chase
(M)
Seth D Goldfarb
(SD)
Lopa Gupta
(L)
Edlira Dobrev
(E)
Ron Levitan
(R)
Milerva Santos
(M)
Xia Ye Michael K Parides
(XYMK)
Deborah D Ascheim
(DD)
Kinjal Shah
(K)
Stephanie Pan
(S)
Katherine Kirkwood
(K)
Karen O'Sullivan
(K)
Michael Mack
(M)
Rachelle Winkle
(R)
Marc Gillinov
(M)
Carrie Geither
(C)
Michael Argenziano
(M)
Sowmya Sreekanth
(S)
Jock N McCullough
(JN)
Henry Stokes
(H)
Peter K Smith
(PK)
Stacey Welsh
(S)
Vinod H Thourani
(VH)
Kim Baio
(K)
Pierre Voisine
(P)
Gladys Dussault
(G)
Mark A Groh
(MA)
Ralph Mangusan
(R)
Robert E Michler
(RE)
Rebecca Meli
(R)
Louis P Perrault
(LP)
Sophie Robichaud
(S)
Keith A Horvath
(KA)
Margaret Iraola
(M)
Bryan A Whitson
(BA)
Denise Fadorsen
(D)
Maral Ouzounian
(M)
Shakira Christie
(S)
John C Mullen
(JC)
Alexandra Hripko
(A)
James S Gammie
(JS)
Manal Al-Suqi
(M)
Michael A Acker
(MA)
Steven Messé
(S)
Mary Lou Mayer
(ML)
Michael Bowdish
(M)
Edward Lozano
(E)
Gorav Ailawadi
(G)
Sandra Burks
(S)
David A Bull
(DA)
Patrice Desvigne-Nickens
(P)
Dennis O Dixon
(DO)
Rebecca Gottesman
(R)
Mark Haigney
(M)
Richard Holubkov
(R)
Constantino Iadecola
(C)
Alice Jacobs
(A)
Eric M Meslin
(EM)
John M Murkin
(JM)
John A Spertus
(JA)
Frank Sellke
(F)
Cheryl L McDonald
(CL)
John Canty
(J)
Neal Dickert
(N)
Dennis O Dixon
(DO)
John S Ikonomidis
(JS)
KyungMann Kim
(K)
David O Williams
(DO)
Clyde W Yancy
(CW)
Seemant Chaturvedi
(S)
Marc Chimowitz
(M)
James C Fang
(JC)
Wayne Richenbacher
(W)
Vivek Rao
(V)
Karen L Furie
(KL)
Rachel Miller
(R)
Jennifer Cook
(J)
David D'Alessandro
(D)
Frederick Han
(F)
Sean Pinney
(S)
Mary N Walsh
(MN)
David Greer
(D)
Koto Ishida
(K)
Christian Stapf
(C)
Judy Hung
(J)
Xin Zeng
(X)
David Hung
(D)
Sudarat Satitthummanid
(S)
Michel Billelo
(M)
Christos Davatzikos
(C)
Guray Erus
(G)
Lauren Karpf
(L)
Lisa Desiderio
(L)
Joseph P Mathew
(JP)
Jeffrey N Browndyke
(JN)
Michael L James
(ML)
Yanne Toulgoat-Dubois
(Y)
Rachele Brassard
(R)
Renu Virmanu
(R)
Maria E Romero
(ME)
Ryan Braumann
(R)
Informations de copyright
© 2023 The Authors. Annals of Clinical and Translational Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
Références
Messe SR, Acker MA, Kasner SE, et al. Stroke after aortic valve surgery: results from a prospective cohort. Circulation. 2014;129(22):2253-2261. doi:10.1161/CIRCULATIONAHA.113.005084
Samim M, Hendrikse J, van der Worp HB, et al. Silent ischemic brain lesions after transcatheter aortic valve replacement: lesion distribution and predictors. Clin Res Cardiol. 2015;104(5):430-438. doi:10.1007/s00392-014-0798-8
Stolz E, Gerriets T, Kluge A, Klovekorn WP, Kaps M, Bachmann G. Diffusion-weighted magnetic resonance imaging and neurobiochemical markers after aortic valve replacement: implications for future neuroprotective trials? Stroke. 2004;35(4):888-892. doi:10.1161/01.STR.0000120306.82787.5A
Evered L, Silbert B, Knopman DS, et al. Recommendations for the nomenclature of cognitive change associated with anaesthesia and surgery-2018. J Alzheimers Dis. 2018;66(1):1-10. doi:10.3233/JAD-189004
Shadvar K, Baastani F, Mahmoodpoor A, Bilehjani E. Evaluation of the prevalence and risk factors of delirium in cardiac surgery ICU. J Cardiovasc Thorac Res. 2013;5(4):157-161. doi:10.5681/jcvtr.2013.034
Witlox J, Eurelings LS, de Jonghe JF, Kalisvaart KJ, Eikelenboom P, van Gool WA. Delirium in elderly patients and the risk of postdischarge mortality, institutionalization, and dementia: a meta-analysis. JAMA. 2010;304(4):443-451. doi:10.1001/jama.2010.1013
Zhang X, Guo B, Yi N. Zero-inflated gaussian mixed models for analyzing longitudinal microbiome data. PLoS ONE. 2020;15(11):e0242073. doi:10.1371/journal.pone.0242073
Mack MJ, Acker MA, Gelijns AC, et al. Effect of cerebral embolic protection devices on CNS infarction in surgical aortic valve replacement: a randomized clinical trial. JAMA. 2017;318(6):536-547. doi:10.1001/jama.2017.9479
Marcantonio ER, Ngo LH, O'Connor M, et al. 3D-CAM: derivation and validation of a 3-minute diagnostic interview for CAM-defined delirium: a cross-sectional diagnostic test study. Ann Intern Med. 2014;161(8):554-561. doi:10.7326/M14-0865
Ely EW, Inouye SK, Bernard GR, et al. Delirium in mechanically ventilated patients: validity and reliability of the confusion assessment method for the intensive care unit (CAM-ICU). JAMA. 2001;286(21):2703-2710. doi:10.1001/jama.286.21.2703
Zacharaki EI, Kanterakis S, Bryan RN, Davatzikos C. Measuring brain lesion progression with a supervised tissue classification system. Med Image Comput Comput Assist Interv. 2008;11(Pt 1):620-627. doi:10.1007/978-3-540-85988-8_74
Doshi J, Erus G, Ou Y, et al. MUSE: MUlti-atlas region segmentation utilizing ensembles of registration algorithms and parameters, and locally optimal atlas selection. Neuroimage. 2016;127:186-195. doi:10.1016/j.neuroimage.2015.11.073
Adams RL, Bischof L. Seeded region growing. IEEE Trans Pattern Anal Mach Intell. 1994;16(6):641-647. doi:10.1109/34.295913
Johansen-Berg H, Scholz J, Stagg CJ. Relevance of structural brain connectivity to learning and recovery from stroke. Front Syst Neurosci. 2010;4:146. doi:10.3389/fnsys.2010.00146
Sotelo MR, Kalinosky BT, Goodfriend K, Hyngstrom AS, Schmit BD. Indirect structural connectivity identifies changes in brain networks after stroke. Brain Connect. 2020;10(8):399-410. doi:10.1089/brain.2019.0725
Kuceyeski A, Maruta J, Relkin N, Raj A. The network modification (NeMo) tool: elucidating the effect of white matter integrity changes on cortical and subcortical structural connectivity. Brain Connect. 2013;3(5):451-463. doi:10.1089/brain.2013.0147
Kuceyeski A, Navi BB, Kamel H, et al. Exploring the brain's structural connectome: a quantitative stroke lesion-dysfunction mapping study. Hum Brain Mapp. 2015;36(6):2147-2160. doi:10.1002/hbm.22761
Fazekas F, Schmidt R, Scheltens P. Pathophysiologic mechanisms in the development of age-related white matter changes of the brain. Dement Geriatr Cogn Disord. 1998;9(suppl. 1):2-5. doi:10.1159/000051182
Hatano Y, Narumoto J, Shibata K, et al. White-matter hyperintensities predict delirium after cardiac surgery. Am J Geriatr Psychiatry. 2013;21(10):938-945. doi:10.1016/j.jagp.2013.01.061
Kant IMJ, de Bresser J, van Montfort SJT, et al. Preoperative brain MRI features and occurrence of postoperative delirium. J Psychosom Res. 2021;140:110301. doi:10.1016/j.jpsychores.2020.110301
Shibagaki K, Shirasaka T, Sawada J, et al. Silent cerebral ischemia detected by magnetic resonance imaging can predict postoperative delirium after total arch replacement for aneurysm. JTCVS Open. 2022;10:87-96. doi:10.1016/j.xjon.2022.02.026
Brown CH, Faigle R, Klinker L, et al. The association of brain MRI characteristics and postoperative delirium in cardiac surgery patients. Clin Ther. 2015;37(12):2686-2699.e9. doi:10.1016/j.clinthera.2015.10.021
Cavallari M, Hshieh TT, Guttmann CR, et al. Brain atrophy and white-matter hyperintensities are not significantly associated with incidence and severity of postoperative delirium in older persons without dementia. Neurobiol Aging. 2015;36(6):2122-2129. doi:10.1016/j.neurobiolaging.2015.02.024
Otomo S, Maekawa K, Goto T, Baba T, Yoshitake A. Pre-existing cerebral infarcts as a risk factor for delirium after coronary artery bypass graft surgery. Interact Cardiovasc Thorac Surg. 2013;17(5):799-804. doi:10.1093/icvts/ivt304
Irimia P, Martinez-Vila E, Martinez-Cuesta A, Zulueta J. Delirium due to brain microembolism: diagnostic value of diffusion-weighted MRI. J Neuroimaging. 2007;17(2):175-177. doi:10.1111/j.1552-6569.2006.00067.x
Bendszus M, Stoll G. Silent cerebral ischaemia: hidden fingerprints of invasive medical procedures. Lancet Neurol. 2006;5(4):364-372. doi:10.1016/S1474-4422(06)70412-4
Sun X, Lindsay J, Monsein LH, Hill PC, Corso PJ. Silent brain injury after cardiac surgery: a review: cognitive dysfunction and magnetic resonance imaging diffusion-weighted imaging findings. J Am Coll Cardiol. 2012;60(9):791-797. doi:10.1016/j.jacc.2012.02.079
Meller SM, Baumbach A, Brickman AM, Lansky AJ. Clinical implications for diffusion-weighted MRI brain lesions associated with transcatheter aortic valve replacement. Catheter Cardiovasc Interv. 2014;83(3):502-508. doi:10.1002/ccd.24904
Chen CH, Peterson MD, Mazer CD, et al. Acute infarcts on brain MRI following aortic arch repair with circulatory arrest: insights from the ACE CardioLink-3 randomized trial. Stroke. 2022;54:67-77. doi:10.1161/STROKEAHA.122.041612
Ito H, Uchida M, Kaji T, et al. Risk factors of cerebellar microembolic infarctions after carotid artery stenting. World Neurosurg. 2020;142:e290-e296. doi:10.1016/j.wneu.2020.06.207
Lammers F, Zacharias N, Borchers F, Morgeli R, Spies CD, Winterer G. Functional connectivity of the supplementary motor network is associated with Fried's modified frailty score in older adults. J Gerontol A Biol Sci Med Sci. 2020;75(12):2239-2248. doi:10.1093/gerona/glz297
Lammers-Lietz F, Zacharias N, Morgeli R, Spies CD, Winterer G. Functional connectivity of the supplementary and presupplementary motor areas in postoperative transition between stages of frailty. J Gerontol A Biol Sci Med Sci. 2022;77:2464-2473. doi:10.1093/gerona/glac012
Nomura Y, Nakano M, Bush B, et al. Observational study examining the association of baseline frailty and postcardiac surgery delirium and cognitive change. Anesth Analg. 2019;129(2):507-514. doi:10.1213/ANE.0000000000003967
Song R, Song G, Xie P, et al. Diffusion tensor imaging and resting-state functional magnetic resonance imaging in patients with delirium in intensive care unit. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 2020;32(1):88-93. doi:10.3760/cma.j.cn121430-20190905-00016
Cavallari M, Dai W, Guttmann CR, et al. Neural substrates of vulnerability to postsurgical delirium as revealed by presurgical diffusion MRI. Brain. 2016;139(Pt 4):1282-1294. doi:10.1093/brain/aww010
Georgescu Margarint EL, Georgescu IA, Zahiu CD, et al. Reduced interhemispheric coherence after cerebellar vermis output perturbation. Brain Sci. 2020;10(9):621. doi:10.3390/brainsci10090621
Schmahmann JD, Pandya DN. Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems. Cortex. 2008;44(8):1037-1066. doi:10.1016/j.cortex.2008.04.004
Schmahmann JD, Guell X, Stoodley CJ, Halko MA. The theory and neuroscience of cerebellar cognition. Annu Rev Neurosci. 2019;42:337-364. doi:10.1146/annurev-neuro-070918-050258
Abderrakib A, Ligot N, Naeije G. Cerebellar cognitive affective syndrome after acute cerebellar stroke. Front Neurol. 2022;13:906293. doi:10.3389/fneur.2022.906293
Bodranghien F, Bastian A, Casali C, et al. Consensus paper: revisiting the symptoms and signs of cerebellar syndrome. Cerebellum. 2016;15(3):369-391. doi:10.1007/s12311-015-0687-3
Taskiran-Sag A, Uzuncakmak Uyanik H, Uyanik SA, Oztekin N. Prospective investigation of cerebellar cognitive affective syndrome in a previously non-demented population of acute cerebellar stroke. J Stroke Cerebrovasc Dis. 2020;29(8):104923. doi:10.1016/j.jstrokecerebrovasdis.2020.104923
Goulden N, Khusnulina A, Davis NJ, et al. The salience network is responsible for switching between the default mode network and the central executive network: replication from DCM. Neuroimage. 2014;99:180-190. doi:10.1016/j.neuroimage.2014.05.052
Chen H, Li Y, Liu Q, et al. Abnormal interactions of the salience network, central executive network, and default-mode network in patients with different cognitive impairment loads caused by leukoaraiosis. Front Neural Circuits. 2019;13:42. doi:10.3389/fncir.2019.00042
Choi SH, Lee H, Chung TS, et al. Neural network functional connectivity during and after an episode of delirium. Am J Psychiatry. 2012;169(5):498-507. doi:10.1176/appi.ajp.2012.11060976
Nitchingham A, Kumar V, Shenkin S, Ferguson KJ, Caplan GA. A systematic review of neuroimaging in delirium: predictors, correlates and consequences. Int J Geriatr Psychiatry. 2018;33(11):1458-1478. doi:10.1002/gps.4724
Cavallari M, Fong TG, Touroutoglou A, et al. Assessment of potential selection bias in neuroimaging studies of postoperative delirium and cognitive decline: lessons from the SAGES study. Brain Imaging Behav. 2022;16(4):1732-1740. doi:10.1007/s11682-022-00644-7
Browndyke JN, Moser DJ, Cohen RA, et al. Acute neuropsychological functioning following cardiosurgical interventions associated with the production of intraoperative cerebral microemboli. Clin Neuropsychol. 2002;16(4):463-471. doi:10.1076/clin.16.4.463.13910
Patel N, Minhas JS, Chung EM. Intraoperative embolization and cognitive decline after cardiac surgery: a systematic review. Semin Cardiothorac Vasc Anesth. 2016;20(3):225-231. doi:10.1177/1089253215626728
Knipp SC, Matatko N, Schlamann M, et al. Small ischemic brain lesions after cardiac valve replacement detected by diffusion-weighted magnetic resonance imaging: relation to neurocognitive function. Eur J Cardiothorac Surg. 2005;28(1):88-96. doi:10.1016/j.ejcts.2005.02.043
Abu-Omar Y, Balacumaraswami L, Pigott DW, Matthews PM, Taggart DP. Solid and gaseous cerebral microembolization during off-pump, on-pump, and open cardiac surgery procedures. J Thorac Cardiovasc Surg. 2004;127(6):1759-1765. doi:10.1016/j.jtcvs.2003.09.048