Covert Cognition in Disorders of Consciousness: A Meta-Analysis.

[en] Covert cognition in patients with disorders of consciousness represents a real diagnostic conundrum for clinicians. In this meta-analysis, our main objective was to identify clinical and demographic variables that are more likely to be associated with responding to an active paradigm. Among 2018 citations found on PubMed, 60 observational studies were found relevant. Based on the QUADAS-2, 49 studies were considered. Data from 25 publications were extracted and included in the meta-analysis. Most of these studies used electrophysiology as well as counting tasks or mental imagery. According to our statistical analysis, patients clinically diagnosed as being in a vegetative state and in a minimally conscious state minus (MCS-) show similar likelihood in responding to active paradigm and responders are most likely suffering from a traumatic brain injury. In the future, multi-centric studies should be performed in order to increase sample size, with similar methodologies and include structural and functional neuroimaging in order to identify cerebral markers related to such a challenging diagnosis.

Disciplines :

Neurology

Author, co-author :

Schnakers, Caroline

Hirsch, Michaela

Noé, Enrique

Llorens, Roberto

Lejeune, Nicolas ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group

Veeramuthu, Vigneswaran

De Marco, Sabrina

Demertzi, Athina ; Université de Liège - ULiège > GIGA Consciousness - Physiology of Cognition

Duclos, Catherine

Morrissey, Ann-Marie

Chatelle, Camille

Estraneo, Anna

Language :

English

Title :

Covert Cognition in Disorders of Consciousness: A Meta-Analysis.

Publication date :

2020

Journal title :

Brain Sciences

eISSN :

2076-3425

Publisher :

MDPI AG, Basel, Switzerland

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 03 February 2022

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Bibliography

The Multi-Society Task Force on Persistent Vegetative State. Medical aspects of the persistent vegetative state. NEJM 1994, 330, 1499–1508. [CrossRef]
Giacino, J.; Ashwal, S.; Childs, N.; Cranford, R.; Jennett, B.; Katz, D.I.; Kelly, J.P.; Rosenberg, J.H.; Whyte, J.; Zafonte, R.D.; et al. The minimally conscious state: Definition and diagnostic criteria. Neurology 2002, 58, 349–353. [CrossRef]
Thibaut, A.; Bodien, Y.G.; Laureys, S.; Giacino, J.T. Minimally conscious state “plus”: Diagnostic criteria and relation to functional recovery. J. Neurol. 2020, 267, 1245–1254. [CrossRef]
Wade, D.T. How often is the diagnosis of the permanent vegetative state incorrect? A review of the evidence. Eur. J. Neurol. 2018, 25, 619–625. [CrossRef] [PubMed]
Schnakers, C. Update on diagnosis in disorders of consciousness. Expert Rev. Neurother. 2020, 20, 997–1004. [CrossRef] [PubMed]
Kondziella, D.; Bender, A.; Diserens, K.; van Erp, W.; Estraneo, A.; Formisano, R.; Laureys, S.; Naccache, L.; Ozturk, S.; Rohaut, B.; et al. EAN Panel on Coma, Disorders of Consciousness. Eur. J. Neurol. 2020, 27, 741–756. [CrossRef] [PubMed]
American Congress of Rehabilitation Medicine, Brain Injury-Interdisciplinary Special Interest Group. Assessment scales for disorders of consciousness: Evidence-based recommendations for clinical practice and research. Arch. Phys. Med. Rehabil. 2010, 91, 1795–1813. [CrossRef]
Owen, A.M.; Coleman, M.R.; Boly, M.; Davis, M.H.; Laureys, S.; Pickard, J.D. Detecting awareness in the vegetative state. Science 2006, 313, 1402. [CrossRef]
Monti, M.M.; Vanhaudenhuyse, A.; Coleman, M.R.; Boly, M.; Pickard, J.D.; Tshibanda, L.; Owen, A.M.; Laureys, S. Willful modulation of brain activity in disorders of consciousness. N. Engl. J. Med. 2010, 362, 579–589. [CrossRef]
Owen, A.M. The Search for Consciousness. Neuron 2019, 102, 526–528. [CrossRef]
Schiff, N.D. Cognitive Motor Dissociation Following Severe Brain Injuries. JAMA Neurol. 2015, 72, 1413–1415. [CrossRef]
Kondziella, D.; Friberg, C.K.; Frokjaer, V.G.; Fabricius, M.; Møller, K. Preserved consciousness in vegetative and minimal conscious states: Systematic review and meta-analysis. J. Neurol. Neurosurg. Psychiatry 2016, 87, 485–492. [CrossRef]
Schardt, C.; Adams, M.B.; Owens, T.; Keitz, S.; Fontelo, P. Utilization of the PICO framework to improve searching PubMed for clinical questions. BMC Med. Inform. Decis. Mak. 2007, 7, 16. [CrossRef]
Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ 2009, 339, b2700. [CrossRef]
Whiting, P.F.; Rutjes, A.W.; Westwood, M.E.; Mallett, S.; Deeks, J.J.; Reitsma, J.B.; Leeflang, M.M.; Sterne, J.A.; Bossuyt, P.M. QUADAS-2 Group. QUADAS-2: A revised tool for the quality assessment of diagnostic accuracy studies. Ann. Intern. Med. 2011, 155, 529–536. [CrossRef]
Giacino, J.T.; Katz, D.I.; Schiff, N.D.; Whyte, J.; Ashman, E.J.; Ashwal, S.; Barbano, R.; Hammond, F.M.; Laureys, S.; Ling, G.S.F.; 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. Neurology 2018, 91, 450–460.
Bekinschtein, T.A.; Dehaene, S.; Rohaut, B.; Tadel, F.; Cohen, L.; Naccache, L. Neural signature of the conscious processing of auditory regularities. Proc. Natl. Acad. Sci. USA 2009, 106, 1672–1677. [CrossRef]
Chennu, S.; Finoia, P.; Kamau, E.; Monti, M.M.; Allanson, J.; Pickard, J.D.; Owen, A.M.; Bekinschtein, T.A. Dissociable endogenous and exogenous attention in disorders of consciousness. Neuroimage Clin. 2013, 3, 450–461. [CrossRef]
Chennu, S.; Finoia, P.; Kamau, E.; Allanson, J.; Williams, G.B.; Monti, M.M.; Noreika, V.; Arnatkeviciute, A.; Canales-Johnson, A.; Olivares, F.; et al. Spectral signatures of reorganised brain networks in disorders of consciousness. PLoS Comput. Biol. 2014, 10, e1003887. [CrossRef]
Cruse, D.; Chennu, S.; Chatelle, C.; Bekinschtein, T.A.; Fernández-Espejo, D.; Pickard, J.D.; Laureys, S.; Owen, A.M. Bedside detection of awareness in the vegetative state: A cohort study. Lancet 2011, 378, 2088–2094. [CrossRef]
Cruse, D.; Chennu, S.; Chatelle, C.; Fernández-Espejo, D.; Bekinschtein, T.A.; Pickard, J.D.; Laureys, S.; Owen, A.M. Relationship between etiology and covert cognition in the minimally conscious state. Neurology 2012, 78, 816–822. [CrossRef]
Edlow, B.L.; Chatelle, C.; Spencer, C.A.; Chu, C.J.; Bodien, Y.G.; O’Connor, K.L.; Hirschberg, R.E.; Hochberg, L.R.; Giacino, J.T.; Rosenthal, E.S.; et al. Early detection of consciousness in patients with acute severe traumatic brain injury. Brain 2017, 140, 2399–2414. [CrossRef]
Faugeras, F.; Rohaut, B.; Weiss, N.; Bekinschtein, T.A.; Galanaud, D.; Puybasset, L.; Bolgert, F.; Sergent, C.; Cohen, L.; Dehaene, S.; et al. Probing consciousness with event-related potentials in the vegetative state. Neurology 2011, 77, 264–268. [CrossRef]
Gibson, R.M.; Fernández-Espejo, D.; Gonzalez-Lara, L.E.; Kwan, B.Y.; Lee, D.H.; Owen, A.M.; Cruse, D. Multiple tasks and neuroimaging modalities increase the likelihood of detecting covert awareness in patients with disorders of consciousness. Front. Hum. Neurosci. 2014, 8, 950. [CrossRef]
Habbal, D.; Gosseries, O.; Noirhomme, Q.; Renaux, J.; Lesenfants, D.; Bekinschtein, T.A.; Majerus, S.; Laureys, S.; Schnakers, C. Volitional electromyographic responses in disorders of consciousness. Brain Inj. 2014, 28, 1171–1179. [CrossRef]
Hauger, S.L.; Schnakers, C.; Andersson, S.; Becker, F.; Moberget, T.; Giacino, J.T.; Schanke, A.K.; Løvstad, M. Neurophysiological Indicators of Residual Cognitive Capacity in the Minimally Conscious State. Behav. Neurol. 2015, 2015, 145913. [CrossRef]
Hauger, S.L.; Schanke, A.K.; Andersson, S.; Chatelle, C.; Schnakers, C.; Løvstad, M. The Clinical Diagnostic Utility of Electrophysiological Techniques in Assessment of Patients with Disorders of Consciousness Following Acquired Brain Injury: A Systematic Review. J. Head Trauma Rehabil. 2017, 32, 185–196. [CrossRef]
Höller, Y.; Bergmann, J.; Thomschewski, A.; Kronbichler, M.; Höller, P.; Crone, J.S.; Schmid, E.V.; Butz, K.; Nardone, R.; Trinka, E. Comparison of EEG-features and classification methods for motor imagery in patients with disorders of consciousness. PLoS ONE 2013, 8, e80479. [CrossRef]
King, J.R.; Faugeras, F.; Gramfort, A.; Schurger, A.; El Karoui, I.; Sitt, J.D.; Rohaut, B.; Wacongne, C.; Labyt, E.; Bekinschtein, T.; et al. Single-trial decoding of auditory novelty responses facilitates the detection of residual consciousness. Neuroimage 2013, 83, 726–738. [CrossRef]
Li, Y.; Pan, J.; He, Y.; Wang, F.; Laureys, S.; Xie, Q.; Yu, R. Detecting number processing and mental calculation in patients with disorders of consciousness using a hybrid brain-computer interface system. BMC Neurol. 2015, 15, 259. [CrossRef]
Schnakers, C.; Giacino, J.T.; Løvstad, M.; Habbal, D.; Boly, M.; Di, H.; Majerus, S.; Laureys, S. Preserved covert cognition in noncommunicative patients with severe brain injury? Neurorehabil. Neural Repair 2015, 29, 308–317. [CrossRef]
Schnakers, C.; Perrin, F.; Schabus, M.; Majerus, S.; Ledoux, D.; Damas, P.; Boly, M.; Vanhaudenhuyse, A.; Bruno, M.A.; Moonen, G.; et al. Voluntary brain processing in disorders of consciousness. Neurology 2008, 71, 1614–1620. [CrossRef]
Stender, J.; Gosseries, O.; Bruno, M.A.; Charland-Verville, V.; Vanhaudenhuyse, A.; Demertzi, A.; Chatelle, C.; Thonnard, M.; Thibaut, A.; Heine, L.; et al. Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: A clinical validation study. Lancet 2014, 384, 514–522. [CrossRef]
Vogel, D.; Markl, A.; Yu, T.; Kotchoubey, B.; Lang, S.; Müller, F. Can mental imagery functional magnetic resonance imaging predict recovery in patients with disorders of consciousness? Arch. Phys. Med. Rehabil. 2013, 94, 1891–1898. [CrossRef]
Wang, F.; He, Y.; Pan, J.; Xie, Q.; Yu, R.; Zhang, R.; Li, Y. A Novel Audiovisual Brain-Computer Interface and Its Application in Awareness Detection. Sci. Rep. 2015, 5, 9962. [CrossRef]
Yu, T.; Lang, S.; Vogel, D.; Markl, A.; Müller, F.; Kotchoubey, B. Patients with unresponsive wakefulness syndrome respond to the pain cries of other people. Neurology 2013, 80, 345–352. [CrossRef]
Chatelle, C.; Spencer, C.A.; Cash, S.S.; Hochberg, L.R.; Edlow, B.L. Feasibility of an EEG-based brain-computer interface in the intensive care unit. Clin. Neurophysiol. 2018, 129, 1519–1525. [CrossRef]
Curley, W.H.; Forgacs, P.B.; Voss, H.U.; Conte, M.M.; Schiff, N.D. Characterization of EEG signals revealing covert cognition in the injured brain. Brain 2018, 141, 1404–1421. [CrossRef]
Spataro, R.; Heilinger, A.; Allison, B.; De Cicco, D.; Marchese, S.; Gregoretti, C.; La Bella, V.; Guger, C. Preserved somatosensory discrimination predicts consciousness recovery in unresponsive wakefulness syndrome. Clin. Neurophysiol. 2018, 129, 1130–1136. [CrossRef]
Xie, Q.; Pan, J.; Chen, Y.; He, Y.; Ni, X.; Zhang, J.; Wang, F.; Li, Y.; Yu, R. A gaze-independent audiovisual brain-computer Interface for detecting awareness of patients with disorders of consciousness. BMC Neurol. 2018, 18, 144. [CrossRef]
Aubinet, C.; Murphy, L.; Bahri, M.A.; Larroque, S.K.; Cassol, H.; Annen, J.; Carrière, M.; Wannez, S.; Thibaut, A.; Laureys, S.; et al. Brain, Behavior, and Cognitive Interplay in Disorders of Consciousness: A Multiple Case Study. Front. Neurol. 2018, 9, 665. [CrossRef]
Aubinet, C.; Larroque, S.K.; Heine, L.; Martial, C.; Majerus, S.; Laureys, S.; Di Perri, C. Clinical subcategorization of minimally conscious state according to resting functional connectivity. Hum. Brain Mapp. 2018, 39, 4519–4532. [CrossRef]
Aubinet, C.; Cassol, H.; Gosseries, O.; Bahri, M.A.; Larroque, S.K.; Majerus, S.; Martial, C.; Martens, G.; Carrière, M.; Chatelle, C.; et al. Brain Metabolism but Not Gray Matter Volume Underlies the Presence of Language Function in the Minimally Conscious State (MCS): MCS+ Versus MCS-Neuroimaging Differences. Neurorehabil. Neural Repair 2020, 34, 172–184. [CrossRef]
Fernández-Espejo, D.; Rossit, S.; Owen, A.M. A Thalamocortical Mechanism for the Absence of Overt Motor Behavior in Covertly Aware Patients. JAMA Neurol. 2015, 72, 1442–1450. [CrossRef]
Schnakers, C.; Monti, M.M. Disorders of consciousness after severe brain injury: Therapeutic options. Curr. Opin. Neurol. 2017, 30, 573–579. [CrossRef]
Pignat, J.M.; Mauron, E.; Jöhr, J.; Gilart de Keranflech, C.; Van De Ville, D.; Preti, M.G.; Meskaldji, D.E.; Hömberg, V.; Laureys, S.; Draganski, B.; et al. Outcome Prediction of Consciousness Disorders in the Acute Stage Based on a Complementary Motor Behavioural Tool. PLoS ONE 2016, 11, e0156882. [CrossRef]
Pincherle, A.; Jöhr, J.; Chatelle, C.; Pignat, J.M.; Du Pasquier, R.; Ryvlin, P.; Oddo, M.; Diserens, K. Motor behavior unmasks residual cognition in disorders of consciousness. Ann. Neurol. 2019, 85, 443–447. [CrossRef]
Pincherle, A.; Rossi, F.; Jöhr, J.; Dunet, V.; Ryvlin, P.; Oddo, M.; Schiff, N.; Diserens, K. Early discrimination of cognitive motor dissociation from disorders of consciousness: Pitfalls and clues. J. Neurol. 2020. [CrossRef]