Diffuse optical tomography for mapping cerebral hemodynamics and functional connectivity in delirium.
acute brain failure
delirium
diffuse optical tomography
encephalopathy
near‐infrared light
optical imaging
Journal
Alzheimer's & dementia : the journal of the Alzheimer's Association
ISSN: 1552-5279
Titre abrégé: Alzheimers Dement
Pays: United States
ID NLM: 101231978
Informations de publication
Date de publication:
03 May 2024
03 May 2024
Historique:
revised:
07
03
2024
received:
08
12
2023
accepted:
08
03
2024
medline:
3
5
2024
pubmed:
3
5
2024
entrez:
3
5
2024
Statut:
aheadofprint
Résumé
Delirium is associated with mortality and new onset dementia, yet the underlying pathophysiology remains poorly understood. Development of imaging biomarkers has been difficult given the challenging nature of imaging delirious patients. Diffuse optical tomography (DOT) offers a promising approach for investigating delirium given its portability and three-dimensional capabilities. Twenty-five delirious and matched non-delirious patients (n = 50) were examined using DOT, comparing cerebral oxygenation and functional connectivity in the prefrontal cortex during and after an episode of delirium. Total hemoglobin values were significantly decreased in the delirium group, even after delirium resolution. Functional connectivity between the dorsolateral prefrontal cortex and dorsomedial prefrontal cortex was strengthened post-resolution compared to during an episode; however, this relationship was still significantly weaker compared to controls. These findings highlight DOT's potential as an imaging biomarker to measure impaired cerebral oxygenation and functional dysconnectivity during and after delirium. Future studies should focus on the role of cerebral oxygenation in delirium pathogenesis and exploring the etiological link between delirium and dementias. We developed a portable diffuse optical tomography (DOT) system for bedside three-dimensional functional neuroimaging to study delirium in the hospital. We implemented a novel DOT task-focused seed-based correlation analysis. DOT revealed decreased cerebral oxygenation and functional connectivity strength in the delirium group, even after resolution of delirium.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : University of South Florida internal department funds
Informations de copyright
© 2024 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.
Références
Maldonado JR. Acute brain failure: pathophysiology, diagnosis, management, and sequelae of delirium. Crit Care Clin. 2017;33(3):461‐519. doi:10.1016/j.ccc.2017.03.013
Inouye SK, Westendorp RGJ, Saczynski JS. Delirium in elderly people. Lancet. 2014;383(9920):911‐922. doi:10.1016/S0140‐6736(13)60688‐1
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
Witlox J, Eurelings LSM, de Jonghe JFM, 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
Goldberg TE, Chen C, Wang Y, et al. Association of delirium with long‐term cognitive decline: a meta‐analysis. JAMA Neurol. 2020;77(11):1373‐1381. doi:10.1001/jamaneurol.2020.2273
Leighton SP, Herron JW, Jackson E, Sheridan M, Deligianni F, Cavanagh J. Delirium and the risk of developing dementia: a cohort study of 12 949 patients. J Neurol Neurosurg Psychiatry. 2022;93(8):822‐827. doi:10.1136/jnnp‐2022‐328903
Kunicki ZJ, Ngo LH, Marcantonio ER, et al. Six‐year cognitive trajectory in older adults following major surgery and delirium. JAMA Intern Med. 2023:e230144. doi:10.1001/jamainternmed.2023.0144. Published online March 20.
Leslie DL, Inouye SK. The importance of delirium: economic and societal costs. J Am Geriatr Soc. 2011;59(2):S241‐S243. doi:10.1111/j.1532‐5415.2011.03671.x
Burton JK, Craig LE, Yong SQ, et al. Non‐pharmacological interventions for preventing delirium in hospitalised non‐ICU patients. Cochrane Database Syst Rev. 2021;7(7):CD013307. doi:10.1002/14651858.CD013307.pub2
Burry L, Hutton B, Williamson DR, et al. Pharmacological interventions for the treatment of delirium in critically ill adults. Cochrane Database Syst Rev. 2019;9(9):CD011749. doi:10.1002/14651858.CD011749.pub2
Dunne SS, Coffey JC, Konje S, et al. Biomarkers in delirium: a systematic review. J Psychosom Res. 2021;147:110530. doi:10.1016/j.jpsychores.2021.110530
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
van Montfort SJT, van Dellen E, Stam CJ, et al. Brain network disintegration as a final common pathway for delirium: a systematic review and qualitative meta‐analysis. Neuroimage Clin. 2019;23:101809. doi:10.1016/j.nicl.2019.101809
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
Oh J, Shin JE, Yang KH, et al. Cortical and subcortical changes in resting‐state functional connectivity before and during an episode of postoperative delirium. Aust N Z J Psychiatry. 2019;53(8):794‐806. doi:10.1177/0004867419848826
Nitchingham A, Pereira JVB, Wegner EA, Oxenham V, Close J, Caplan GA. Regional cerebral hypometabolism on 18F‐FDG PET/CT scan in delirium is independent of acute illness and dementia. Alzheimers Dement. 2023;19(1):97‐106. doi:10.1002/alz.12604
Wiegand TLT, Rémi J, Dimitriadis K. Electroencephalography in delirium assessment: a scoping review. BMC Neurol. 2022;22(1):86. doi:10.1186/s12883‐022‐02557‐w
Jiang H. Diffuse Optical Tomography. CRC Press; 2018. doi:10.1201/b10482
Eggebrecht AT, White BR, Ferradal SL, et al. A quantitative spatial comparison of high‐density diffuse optical tomography and fMRI cortical mapping. Neuroimage. 2012;61(4):1120‐1128. doi:10.1016/j.neuroimage.2012.01.124
Eggebrecht AT, Ferradal SL, Robichaux‐Viehoever A, et al. Mapping distributed brain function and networks with diffuse optical tomography. Nat Photonics. 2014;8(6):448‐454. doi:10.1038/nphoton.2014.107
Obata T, Liu TT, Miller KL, et al. Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients. Neuroimage. 2004;21(1):144‐153. doi:10.1016/j.neuroimage.2003.08.040
White BR, Culver JP. Quantitative evaluation of high‐density diffuse optical tomography: in vivo resolution and mapping performance. J Biomed Opt. 2010;15(2):026006. doi:10.1117/1.3368999
Jasdzewski G, Strangman G, Wagner J, Kwong KK, Poldrack RA, Boas DA. Differences in the hemodynamic response to event‐related motor and visual paradigms as measured by near‐infrared spectroscopy. Neuroimage. 2003;20(1):479‐488. doi:10.1016/s1053‐8119(03)00311‐2
Toronov VY, Zhang X, Webb AG. A spatial and temporal comparison of hemodynamic signals measured using optical and functional magnetic resonance imaging during activation in the human primary visual cortex. Neuroimage. 2007;34(3):1136‐1148. doi:10.1016/j.neuroimage.2006.08.048
Wheelock MD, Culver JP, Eggebrecht AT. High‐density diffuse optical tomography for imaging human brain function. Rev Sci Instrum. 2019;90(5):051101. doi:10.1063/1.5086809
Dai X, Zhang T, Yang H, Tang J, Carney PR, Jiang H. Fast noninvasive functional diffuse optical tomography for brain imaging. J Biophotonics. 2018;11(3). doi:10.1002/jbio.201600267
White BR, Snyder AZ, Cohen AL, et al. Resting‐state functional connectivity in the human brain revealed with diffuse optical tomography. Neuroimage. 2009;47(1):148‐156. doi:10.1016/j.neuroimage.2009.03.058
Burke B, Bergonzi K, Sherafati A, et al. Bedside diffuse optical tomography of disrupted brain connectivity during acute stroke. Review. 2020. 10.21203/rs.3.rs‐107369/v1
Jiang S, Huang J, Yang H, et al. Neuroimaging of depression with diffuse optical tomography during repetitive transcranial magnetic stimulation. Sci Rep. 2021;11(1):7328. doi:10.1038/s41598‐021‐86751‐9
Huang J, Jiang S, Wagoner R, Yang H, Currier G, Jiang H. Three‐dimensional optical imaging of brain activation during transcranial magnetic stimulation. J Xray Sci Technol. 2021;29(5):891‐902. doi:10.3233/XST‐210900
Jiang S, Carpenter LL, Jiang H. Optical neuroimaging: advancing transcranial magnetic stimulation treatments of psychiatric disorders. Vis Comput Ind Biomed Art. 2022;5(1):22. doi:10.1186/s42492‐022‐00119‐y
Regier DA, Kuhl EA, Kupfer DJ. The DSM‐5: classification and criteria changes. World Psychiatry. 2013;12(2):92‐98. doi:10.1002/wps.20050
Bellelli G, Morandi A, Davis DHJ, et al. Validation of the 4AT, a new instrument for rapid delirium screening: a study in 234 hospitalised older people. Age Ageing. 2014;43(4):496‐502. doi:10.1093/ageing/afu021
Jorm AF. The informant questionnaire on cognitive decline in the elderly (IQCODE): a review. Int Psychogeriatr. 2004;16(3):275‐293. doi:10.1017/s1041610204000390
Folstein MF, Folstein SE, McHugh PR. “Mini‐mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189‐198. doi:10.1016/0022‐3956(75)90026‐6
Collin C, Wade DT, Davies S, Horne V. The Barthel ADL Index: a reliability study. Int Disabil Stud. 1988;10(2):61‐63. doi:10.3109/09638288809164103
Knaus WA, Wagner DP, Draper EA, et al. The APACHE III prognostic system. Risk prediction of hospital mortality for critically ill hospitalized adults. Chest. 1991;100(6):1619‐1636. doi:10.1378/chest.100.6.1619
Charlson M, Szatrowski TP, Peterson J, Gold J. Validation of a combined comorbidity index. J Clin Epidemiol. 1994;47(11):1245‐1251. doi:10.1016/0895‐4356(94)90129‐5
Liptzin B, Levkoff SE, Cleary PD, et al. An empirical study of diagnostic criteria for delirium. Am J Psychiatry. 1991;148(4):454‐457. doi:10.1176/ajp.148.4.454
Trzepacz PT, Mittal D, Torres R, Kanary K, Norton J, Jimerson N. Validation of the Delirium Rating Scale‐revised‐98: comparison with the delirium rating scale and the cognitive test for delirium. J Neuropsychiatry Clin Neurosci. 2001;13(2):229‐242. doi:10.1176/jnp.13.2.229
Mulligan M, Lally L, Adamis D, et al. Comparison of verbal and computerised months backwards tests in a hospitalized older population. Aging Clin Exp Res. 2022;34(11):2713‐2719. doi:10.1007/s40520‐022‐02205‐w
Meagher J, Leonard M, Donoghue L, et al. Months backward test: a review of its use in clinical studies. World J Psychiatry. 2015;5(3):305‐314. doi:10.5498/wjp.v5.i3.305
Delpy DT, Cope M. Quantification in tissue near‐infrared spectroscopy. Philos Trans R Soc Lond B Biol Sci. 1997;352(1354):649‐659. doi:10.1098/rstb.1997.0046
Gagnon L, Yücel MA, Dehaes M, et al. Quantification of the cortical contribution to the NIRS signal over the motor cortex using concurrent NIRS‐fMRI measurements. Neuroimage. 2012;59(4):3933‐3940. doi:10.1016/j.neuroimage.2011.10.054
Mazziotta J, Toga A, Evans A, et al. A probabilistic atlas and reference system for the human brain: international Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci. 2001;356(1412):1293‐1322. doi:10.1098/rstb.2001.0915
Pompei P, Foreman M, Rudberg MA, Inouye SK, Braund V, Cassel CK. Delirium in hospitalized older persons: outcomes and predictors. J Am Geriatr Soc. 1994;42(8):809‐815. doi:10.1111/j.1532‐5415.1994.tb06551.x
Salluh JIF, Wang H, Schneider EB, et al. Outcome of delirium in critically ill patients: systematic review and meta‐analysis. BMJ. 2015;350:h2538. doi:10.1136/bmj.h2538
Maldonado JR. Delirium pathophysiology: an updated hypothesis of the etiology of acute brain failure. Int J Geriatr Psychiatry. 2018;33(11):1428‐1457. doi:10.1002/gps.4823
Haggstrom L, Welschinger R, Caplan GA. Functional neuroimaging offers insights into delirium pathophysiology: a systematic review. Australas J Ageing. 2017;36(3):186‐192. doi:10.1111/ajag.12417
Daffner KR, Mesulam MM, Scinto LF, et al. The central role of the prefrontal cortex in directing attention to novel events. Brain. 2000;123(Pt 5):927‐939. doi:10.1093/brain/123.5.927
Barbey AK, Koenigs M, Grafman J. Dorsolateral prefrontal contributions to human working memory. Cortex. 2013;49(5):1195‐1205. doi:10.1016/j.cortex.2012.05.022
Friedman NP, Robbins TW. The role of prefrontal cortex in cognitive control and executive function. Neuropsychopharmacology. 2022;47(1):72‐89. doi:10.1038/s41386‐021‐01132‐0
Eickhoff SB, Laird AR, Fox PT, Bzdok D, Hensel L. Functional segregation of the human dorsomedial prefrontal cortex. Cereb Cortex. 2016;26(1):304‐321. doi:10.1093/cercor/bhu250
Drysdale AT, Grosenick L, Downar J, et al. Resting‐state connectivity biomarkers define neurophysiological subtypes of depression. Nat Med. 2017;23(1):28‐38. doi:10.1038/nm.4246
Downar J, Geraci J, Salomons TV, et al. Anhedonia and reward‐circuit connectivity distinguish nonresponders from responders to dorsomedial prefrontal repetitive transcranial magnetic stimulation in major depression. Biol Psychiatry. 2014;76(3):176‐185. doi:10.1016/j.biopsych.2013.10.026
Bakker N, Shahab S, Giacobbe P, et al. rTMS of the dorsomedial prefrontal cortex for major depression: safety, tolerability, effectiveness, and outcome predictors for 10 Hz versus intermittent theta‐burst stimulation. Brain Stimul. 2015;8(2):208‐215. doi:10.1016/j.brs.2014.11.002
Wood MD, Boyd JG, Wood N, et al. The use of near‐infrared spectroscopy and/or transcranial doppler as non‐invasive markers of cerebral perfusion in adult sepsis patients with delirium: a systematic review. J Intensive Care Med. 2022;37(3):408‐422. doi:10.1177/0885066621997090
Cerebral Oxygenation and Neurological Outcomes Following Critical Illness (CONFOCAL) Research Group, Canadian Critical Care Trials Group, Wood MD, et al, Cerebral Oxygenation and Neurological Outcomes Following Critical Illness (CONFOCAL) Research Group. Low brain tissue oxygenation contributes to the development of delirium in critically ill patients: a prospective observational study. J Crit Care. 2017;41:289‐295. doi:10.1016/j.jcrc.2017.06.009
Lee KF, Wood MD, Maslove DM, Muscedere JG, Boyd JG. Dysfunctional cerebral autoregulation is associated with delirium in critically ill adults. J Cereb Blood Flow Metab. 2019;39(12):2512‐2520. doi:10.1177/0271678X18803081
Somjen GG, Aitken PG, Balestrino M, Herreras O, Kawasaki K. Spreading depression‐like depolarization and selective vulnerability of neurons. A brief review. Stroke. 1990;21(11):III179‐III183.
Globus MY, Busto R, Dietrich WD, Martinez E, Valdes I, Ginsberg MD. Effect of ischemia on the in vivo release of striatal dopamine, glutamate, and gamma‐aminobutyric acid studied by intracerebral microdialysis. J Neurochem. 1988;51(5):1455‐1464. doi:10.1111/j.1471‐4159.1988.tb01111.x
Moghaddam B, Schenk JO, Stewart WB, Hansen AJ. Temporal relationship between neurotransmitter release and ion flux during spreading depression and anoxia. Can J Physiol Pharmacol. 1987;65(5):1105‐1110. doi:10.1139/y87‐173
Maldonado JR. Neuropathogenesis of delirium: review of current etiologic theories and common pathways. Am J Geriatr Psychiatry. 2013;21(12):1190‐1222. doi:10.1016/j.jagp.2013.09.005
Ionescu‐Tucker A, Cotman CW. Emerging roles of oxidative stress in brain aging and Alzheimer's disease. Neurobiol Aging. 2021;107:86‐95. doi:10.1016/j.neurobiolaging.2021.07.014
Bennett S, Grant MM, Aldred S. Oxidative stress in vascular dementia and Alzheimer's disease: a common pathology. J Alzheimers Dis. 2009;17(2):245‐257. doi:10.3233/JAD‐2009‐1041
Strangman GE, Zhang Q, Li Z. Scalp and skull influence on near infrared photon propagation in the Colin27 brain template. Neuroimage. 2014;85(Pt 1):136‐149. doi:10.1016/j.neuroimage.2013.04.090
Okada E, Delpy DT. Near‐infrared light propagation in an adult head model. II. Effect of superficial tissue thickness on the sensitivity of the near‐infrared spectroscopy signal. Appl Opt. 2003;42(16):2915‐2922. doi:10.1364/ao.42.002915
Tedford CE, DeLapp S, Jacques S, Anders J. Quantitative analysis of transcranial and intraparenchymal light penetration in human cadaver brain tissue. Lasers Surg Med. 2015;47(4):312‐322. doi:10.1002/lsm.22343
Pitzschke A, Lovisa B, Seydoux O, et al. Red and NIR light dosimetry in the human deep brain. Phys Med Biol. 2015;60(7):2921‐2937. doi:10.1088/0031‐9155/60/7/2921
Yaroslavsky AN, Schulze PC, Yaroslavsky IV, Schober R, Ulrich F, Schwarzmaier HJ. Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range. Phys Med Biol. 2002;47(12):2059‐2073. doi:10.1088/0031‐9155/47/12/305
Khan AF, Zhang F, Yuan H, Ding L. Brain‐wide functional diffuse optical tomography of resting state networks. J Neural Eng. 2021;18(4). doi:10.1088/1741‐2552/abfdf9
Khan AF, Zhang F, Shou G, Yuan H, Ding L. Transient brain‐wide coactivations and structured transitions revealed in hemodynamic imaging data. Neuroimage. 2022;260:119460. doi:10.1016/j.neuroimage.2022.119460