Impact of Aphasia on Brain Activation to Motor Commands in Patients with Acute Intracerebral Hemorrhage.
Aphasia
Cognitive motor dissociation
Electroencephalography
Language
Motor commands
Journal
Neurocritical care
ISSN: 1556-0961
Titre abrégé: Neurocrit Care
Pays: United States
ID NLM: 101156086
Informations de publication
Date de publication:
13 Aug 2024
13 Aug 2024
Historique:
received:
03
05
2024
accepted:
23
07
2024
medline:
14
8
2024
pubmed:
14
8
2024
entrez:
14
8
2024
Statut:
aheadofprint
Résumé
Brain activation to motor commands is seen in 15% of clinically unresponsive patients with acute brain injury. This state called cognitive motor dissociation (CMD) is detectable by electroencephalogram (EEG) or functional magnetic resonance imaging, predicts long-term recovery, and is recommended by recent guidelines to support prognostication. However, false negative CMD results are a particular concern, and occult aphasia in clinically unresponsive patients may be a major factor. This study aimed to quantify the impact of aphasia on CMD testing. We prospectively studied 61 intensive care unit patients admitted with acute primary intracerebral hemorrhage (ICH) who had behavioral evidence of command following or were able to mimic motor commands. All patients underwent an EEG-based motor command paradigm used to detect CMD and comprehensive aphasia assessments. Logistic regression was used to identify predictors of brain activation, including aphasia types and associations with recovery of independence (Glasgow Outcome Scale-Extended score ≥ 4). Of 61 patients, 50 completed aphasia and the EEG-based motor command paradigm. A total of 72% (n = 36) were diagnosed with aphasia. Patients with impaired comprehension (i.e., receptive or global aphasia) were less likely to show brain activation than those with intact comprehension (odds ratio [OR] 0.23 [95% confidence interval 0.05-0.89], p = 0.04). Brain activation was independently associated with Glasgow Outcome Scale-Extended ≥ 4 by 12 months (OR 2.4 [95% confidence interval 1.2-5.0], p = 0.01) accounting for the Functional Outcome in Patients with Primary ICH score (OR1.3 [95% confidence interval 1.0-1.8], p = 0.01). Brain activation to motor commands is four times less likely for patients with primary ICH with impaired comprehension. False negative results due to occult receptive aphasia need to be considered when interpreting CMD testing. Early detection of brain activation may help predict long-term recovery in conscious patients with ICH.
Sections du résumé
BACKGROUND
BACKGROUND
Brain activation to motor commands is seen in 15% of clinically unresponsive patients with acute brain injury. This state called cognitive motor dissociation (CMD) is detectable by electroencephalogram (EEG) or functional magnetic resonance imaging, predicts long-term recovery, and is recommended by recent guidelines to support prognostication. However, false negative CMD results are a particular concern, and occult aphasia in clinically unresponsive patients may be a major factor. This study aimed to quantify the impact of aphasia on CMD testing.
METHODS
METHODS
We prospectively studied 61 intensive care unit patients admitted with acute primary intracerebral hemorrhage (ICH) who had behavioral evidence of command following or were able to mimic motor commands. All patients underwent an EEG-based motor command paradigm used to detect CMD and comprehensive aphasia assessments. Logistic regression was used to identify predictors of brain activation, including aphasia types and associations with recovery of independence (Glasgow Outcome Scale-Extended score ≥ 4).
RESULTS
RESULTS
Of 61 patients, 50 completed aphasia and the EEG-based motor command paradigm. A total of 72% (n = 36) were diagnosed with aphasia. Patients with impaired comprehension (i.e., receptive or global aphasia) were less likely to show brain activation than those with intact comprehension (odds ratio [OR] 0.23 [95% confidence interval 0.05-0.89], p = 0.04). Brain activation was independently associated with Glasgow Outcome Scale-Extended ≥ 4 by 12 months (OR 2.4 [95% confidence interval 1.2-5.0], p = 0.01) accounting for the Functional Outcome in Patients with Primary ICH score (OR1.3 [95% confidence interval 1.0-1.8], p = 0.01).
CONCLUSIONS
CONCLUSIONS
Brain activation to motor commands is four times less likely for patients with primary ICH with impaired comprehension. False negative results due to occult receptive aphasia need to be considered when interpreting CMD testing. Early detection of brain activation may help predict long-term recovery in conscious patients with ICH.
Identifiants
pubmed: 39138716
doi: 10.1007/s12028-024-02086-z
pii: 10.1007/s12028-024-02086-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NINDS NIH HHS
ID : NS106014
Pays : United States
Organisme : U.S. National Library of Medicine
ID : LM011826
Informations de copyright
© 2024. Springer Science+Business Media, LLC, part of Springer Nature and Neurocritical Care Society.
Références
Hammond FM, Giacino JT, Nakase Richardson R, et al. Disorders of consciousness due to traumatic brain injury: functional status ten years post-injury. J Neurotrauma. 2019;36(7):1136–46. https://doi.org/10.1089/NEU.2018.5954/ASSET/IMAGES/LARGE/FIGURE2.JPEG .
doi: 10.1089/NEU.2018.5954/ASSET/IMAGES/LARGE/FIGURE2.JPEG
Giacino J, Kalmar K. The vegetative and minimally conscious states: a comparison of clinical features and functional outcome. J Head Trauma Rehabil. 1997;12(4):36–51.
doi: 10.1097/00001199-199708000-00005
Rost NS, Smith EE, Chang Y, et al. Prediction of functional outcome in patients with primary intracerebral hemorrhage: the FUNC score. Stroke. 2008;39(8):2304–9. https://doi.org/10.1161/STROKEAHA.107.512202 .
doi: 10.1161/STROKEAHA.107.512202
Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974;2(7872):81–4. https://doi.org/10.1016/S0140-6736(74)91639-0 .
doi: 10.1016/S0140-6736(74)91639-0
Wijdicks EFM, Bamlet WR, Maramattom BV, Manno EM, McClelland RL. Validation of a new coma scale: the FOUR score. Ann Neurol. 2005;58(4):585–93. https://doi.org/10.1002/ANA.20611 .
doi: 10.1002/ANA.20611
Witsch J, Siegerink B, Nolte CH, et al. Prognostication after intracerebral hemorrhage: a review. Neurol Res Pract. 2021;3(1):22. https://doi.org/10.1186/s42466-021-00120-5 .
doi: 10.1186/s42466-021-00120-5
CG D. Report of world federation of neurological surgeons committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg. 1988. https://doi.org/10.3171/JNS.1988.68.6.0985 .
doi: 10.3171/JNS.1988.68.6.0985
Hemphill JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke. 2001;32(4):891–6. https://doi.org/10.1161/01.STR.32.4.891 .
doi: 10.1161/01.STR.32.4.891
Edlow BL, Chatelle C, Spencer CA, et al. Early detection of consciousness in patients with acute severe traumatic brain injury. Brain. 2017;140(9):2399–414. https://doi.org/10.1093/BRAIN/AWX176 .
doi: 10.1093/BRAIN/AWX176
Bodien YG, Giacino JT, Edlow BL. Functional MRI motor imagery tasks to detect command following in traumatic disorders of consciousness. Front Neurol. 2017;8:299515. https://doi.org/10.3389/FNEUR.2017.00688/BIBTEX .
doi: 10.3389/FNEUR.2017.00688/BIBTEX
Claassen J, Doyle K, Matory A, et al. Detection of brain activation in unresponsive patients with acute brain injury. N Engl J Med. 2019;380(26):2497–505. https://doi.org/10.1056/NEJMOA1812757/SUPPL_FILE/NEJMOA1812757_DATA-SHARING.PDF .
doi: 10.1056/NEJMOA1812757/SUPPL_FILE/NEJMOA1812757_DATA-SHARING.PDF
Cruse D, Chennu S, Chatelle C, et al. Bedside detection of awareness in the vegetative state: a cohort study. Lancet. 2011;378(9809):2088–94. https://doi.org/10.1016/S0140-6736(11)61224-5 .
doi: 10.1016/S0140-6736(11)61224-5
Egbebike J, Shen Q, Doyle K, et al. Cognitive-motor dissociation and time to functional recovery in patients with acute brain injury in the USA: a prospective observational cohort study. Lancet Neurol. 2022;21(8):704–13. https://doi.org/10.1016/S1474-4422(22)00212-5 .
doi: 10.1016/S1474-4422(22)00212-5
Majerus S, Bruno MA, Schnakers C, Giacino JT, Laureys S. The problem of aphasia in the assessment of consciousness in brain-damaged patients. Prog Brain Res. 2009;177(C):49–61. https://doi.org/10.1016/S0079-6123(09)17705-1 .
doi: 10.1016/S0079-6123(09)17705-1
Giacino JT, Katz DI, Schiff ND, et al. Practice guideline update recommendations summary: disorders of consciousness: report of the guideline development, dissemination, and implementation subcommittee of the American academy of neurology; the american congress of rehabilitation medicine; and the national institute on disability, independent living, and rehabilitation research. Arch Phys Med Rehabil. 2018. https://doi.org/10.1016/j.apmr.2018.07.001 .
doi: 10.1016/j.apmr.2018.07.001
Kondziella D, Bender A, Diserens K, et al. European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol. 2020;27(5):741–56. https://doi.org/10.1111/ene.14151 .
doi: 10.1111/ene.14151
Peterson A, Cruse D, Naci L, Weijer C, Owen AM. Risk, diagnostic error, and the clinical science of consciousness. Neuroimage Clin. 2015;7:588–97. https://doi.org/10.1016/J.NICL.2015.02.008 .
doi: 10.1016/J.NICL.2015.02.008
Kim N, O’Sullivan J, Olafson E, et al. Cognitive-motor dissociation following pediatric brain injury: What about the children? Neurol Clin Pract. 2022;12(3):248. https://doi.org/10.1212/CPJ.0000000000001169 .
doi: 10.1212/CPJ.0000000000001169
Flowers HL, Skoretz SA, Silver FL, et al. Poststroke aphasia frequency, recovery, and outcomes: a systematic review and meta-analysis. Arch Phys Med Rehabil. 2016;97(12):2188-2201.e8. https://doi.org/10.1016/J.APMR.2016.03.006 .
doi: 10.1016/J.APMR.2016.03.006
Fridriksson J, Den Ouden DB, Hillis AE, et al. Anatomy of aphasia revisited. Brain. 2018;141(3):848–62. https://doi.org/10.1093/BRAIN/AWX363 .
doi: 10.1093/BRAIN/AWX363
Mohr JP. The evaluation of aphasia. Stroke. 1982;13(3):399–401. https://doi.org/10.1161/01.STR.13.3.399 .
doi: 10.1161/01.STR.13.3.399
Goldfine AM, Victor JD, Conte MM, Bardin JC, Schiff ND. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clin Neurophysiol. 2011;122(11):2157–68. https://doi.org/10.1016/J.CLINPH.2011.03.022 .
doi: 10.1016/J.CLINPH.2011.03.022
Jones RD, Benton AL. Use of the multilingual aphasia examination in the detection of language disorders. J Int Neuropsychol Soc. 1995;1:364.
Arthur L, Benton P (2024) Multilingual aphasia examination, 3rd edn | MAE. Published 1989. https://www.parinc.com/Products/Pkey/222 . Accessed 6 Jan 2024
Kertesz A (2007) The western Aphasia battery- revised [Measurement instrument]. https://search.worldcat.org/title/77061826 . Accessed 6 Jan 2024
Claus W. Acute aphasias. In: Handbook of the neuroscience of language. New Jersey: Elsevier; 2008. p. 269–78.
Strauss E, Sherman EMS, Spreen O. A compendium of neuropsychological tests: administration, norms, and commentary. 3rd ed. Oxford: Oxford University Press; 2006.
Meretoja A, Strbian D, Putaala J, et al. SMASH-U. Stroke. 2012;43(10):2592–7. https://doi.org/10.1161/STROKEAHA.112.661603 .
doi: 10.1161/STROKEAHA.112.661603
Wilson JTL, Pettigrew LEL, Teasdale GM. Structured interviews for the glasgow outcome scale and the extended glasgow outcome scale: guidelines for their use. J Neurotrauma. 1998;15(8):573–80. https://doi.org/10.1089/NEU.1998.15.573 .
doi: 10.1089/NEU.1998.15.573
Van Swieten JC, Koudstaal PJ, Visser MC, Schouten H, Van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19(5):604–7. https://doi.org/10.1161/01.STR.19.5.604 .
doi: 10.1161/01.STR.19.5.604
Hanna-Pladdy B, Heilman KM, Foundas AL. Cortical and subcortical contributions to ideomotor apraxia: analysis of task demands and error types. Brain. 2001;124(Pt 12):2513–27. https://doi.org/10.1093/brain/124.12.2513 .
doi: 10.1093/brain/124.12.2513
Pedersen PM, Vinter K, Olsen TS. Aphasia after stroke: type, severity and prognosis. The copenhagen aphasia study. Cerebrovasc Dis. 2004;17(1):35–43. https://doi.org/10.1159/000073896 .
doi: 10.1159/000073896
Brust JC, Shafer SQ, Richter RW, Bruun B. Aphasia in acute stroke. Stroke. 1976;7(2):167–74. https://doi.org/10.1161/01.STR.7.2.167 .
doi: 10.1161/01.STR.7.2.167
Heeley E, Anderson CS, Woodward M, et al. Poor utility of grading scales in acute intracerebral hemorrhage: results from the INTERACT2 trial. Int J Stroke. 2015;10(7):1101–7. https://doi.org/10.1111/ijs.12518 .
doi: 10.1111/ijs.12518
Hwang DY, Dell CA, Sparks MJ, et al. Clinician judgment vs formal scales for predicting intracerebral hemorrhage outcomes. Neurology. 2016;86(2):126–33. https://doi.org/10.1212/WNL.0000000000002266 .
doi: 10.1212/WNL.0000000000002266
Perlovsky L, Sakai KL. Language and cognition. Front Behav Neurosci. 2014. https://doi.org/10.3389/fnbeh.2014.00436 .
doi: 10.3389/fnbeh.2014.00436
Schiff ND, Diringer M, Diserens K, et al. Brain-computer interfaces for communication in patients with disorders of consciousness: A gap analysis and scientific roadmap. Neurocrit Care. 2024. https://doi.org/10.1007/s12028-023-01924-w .
doi: 10.1007/s12028-023-01924-w
Curley WH, Forgacs PB, Voss HU, Conte MM, Schiff ND. Characterization of EEG signals revealing covert cognition in the injured brain. Brain. 2018;141(5):1404–21. https://doi.org/10.1093/brain/awy070 .
doi: 10.1093/brain/awy070