Diagnostic criteria for prolonged and chronic disturbances of consciousness after aneurysmal subarachnoid hemorrhages

Close metadata

BACKGROUND

In recent years, prolonged states of impaired consciousness became widespread among patients with aneurysmal subarachnoid hemorrhage. Treatment and maintenance of vital functions in such patients represent a complex medical, economic and social problem. In this regard, searching for the causes of prolonged states of impaired consciousness and predicting the outcomes are important.

OBJECTIVE

To analyze available literature data on prevention and treatment of prolonged states of impaired consciousness after aneurysmal subarachnoid hemorrhage.

RESULTS

We reviewed the PubMed database using the keywords «unresponsive wakefulness syndrome», «persistent vegetative state2, «minimal consciousness state» and «outcome of subarachnoid hemorrhage». Only 4 reports devoted to the causes and treatment outcomes in patients with prolonged impairment of consciousness after aneurysmal subarachnoid hemorrhage were found. At the same time, patients with aneurysmal subarachnoid hemorrhage comprise up to 11% among all cases of prolonged states of impaired consciousness. Examination, management and treatment of patients with prolonged impairment of consciousness after aneurysmal subarachnoid hemorrhage are carried out according to general principles without taking into account specific etiological and pathogenetic factors.

CONCLUSION

Increased number of patients with prolonged impairment of consciousness after aneurysmal subarachnoid hemorrhage necessitates analysis of etiopathogenesis and outcomes of these disorders based on modern clinical, instrumental and laboratory assessment of the brain.

Keywords:

long-term disturbances of consciousness

vegetative state

non-reactive wakefulness syndrome

state of minimal consciousness plus and minus

subarachnoid hemorrhage

Authors:

Sergeenko E.V.

Burdenko Neurosurgical Center

ORCID: 0000-0003-3858-5617

Belousova O.B.

Burdenko Neurosurgical Center

ORCID: 0000-0003-4908-8923

Pilipenko Yu.V.

Burdenko Neurosurgical Center

ORCID: 0000-0003-4001-3212

Received:

09.07.2023

Accepted:

31.05.2024

List of references:

Jennett B, Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet. 1972;1(7753):734-737. https://doi.org/10.1016/s0140-6736(72)90242-5
Kretschmer E. Das apallische Syndrom. Zeitschrift fur die gesamte. Neurologen und Psychiater. 1940;169(1):576-479.
Katayama Y, Nakamura T, Becker DP, Hayes RL. Intracranial pressure variations associated with activation of the cholinoceptive pontine inhibitory area in the unanesthetized drug-free cat. Journal of Neurosurgery. 1984;61(4):713-724. https://doi.org/10.3171/jns.1984.61.4.0713
Trulson ME. Activity of dopamine-containing substantia nigra neurons in freely moving cats. Neuroscience and Biobehavioral Reviews. 1985;9(2):283-297. https://doi.org/10.1016/0149-7634(85)90051-x
Legostaeva LA, Mochalova EG, Suponeva NA, Sergeev DV, Ryabinkina YuV, Samorukov VYu, Domashenko MA, Pryanikov IV, Gnedovskaya EV, Piradov MA. Slozhnosti klinicheskoj diagnostiki hronicheskih narushenij soznaniya i rekomendacii po kliniko-instrumental’noj ocenke pacientov posle ih vyhoda iz komy. Anesteziologiya i reanimatologiya. 2017;62(6):449-456. (In Russ.). https://doi.org/10.18821/0201-7563-2017-62-6-449-456
Kondziella D, Bender A, Diserens K, van Erp W, Estraneo A, Formisano R. European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. European Journal of Neurology. 2020;27(5):741-756.
Estraneo A, Moretta P, Loreto V, Lanzillo B, Santoro L, Trojano L. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology. 2010;75(3):239-245.
Katz DI, Polyak M, Coughlan D, Nichols M, Roche A. Natural history of recovery from brain injury after prolonged disorders of consciousness: outcome of patients admitted to inpatient rehabilitation with 1-4 year follow-up. Progress in Brain Research. 2009;177:73-88. https://doi.org/10.1016/S0079-6123(09)17707-5
Samuels OB, Sadan O, Feng C, Martin K, Medani K, Mei Y, Barrow DL. Aneurysmal Subarachnoid Hemorrhage: Trends, Outcomes, and Predictions from a 15-Year Perspective of a Single Neurocritical Care Unit. Neurosurgery. 2021;88(3):574-583. https://doi.org/10.1093/neuros/nyaa465
Klein AM, Howell K, Straube A, Pfefferkorn T, Bender A. Rehabilitation outcome of patients with severe and prolonged disorders of consciousness after aneurysmal subarachnoid hemorrhage (aSAH). Clinical Neurology and Neurosurgery. 2013;115(10):2136-2141. https://doi.org/10.1016/j.clineuro.2013.08.004
Forgacs PB, Allen BB, Wu X, Gerber LM, Boddu S, Fakhar M, Stieg PE, Schiff ND, Mangat HS. Corticothalamic Connectivity in Aneurysmal Subarachnoid Hemorrhage: Relationship with Disordered Consciousness and Clinical Outcomes. Neurocritical Care. 2022;36(3):760-771. https://doi.org/10.1007/s12028-021-01354-6
Edlow BL, Claassen J, Schiff ND, Greer DM. Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nature Reviews Neurology. 2021;17(3):135-156. https://doi.org/10.1038/s41582-020-00428-x
Laureys S, Celesia GG, Cohadon F, Lavrijsen J, León-Carrión J, Sannita WG, Sazbon L, Schmutzhard E, von Wild KR, Zeman A, Dolce G; European Task Force on Disorders of Consciousness. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Medicine. 2010;8:68. https://doi.org/10.1186/1741-7015-8-68
Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD, Zasler ND. The minimally conscious state: definition and diagnostic criteria. Neurology. 2002;58(3):349-353. https://doi.org/10.1212/WNL.58.3.349
Kotchoubey B, Vogel D, Lang S, Müller F. What kind of consciousness is minimal? Brain injury. 2014;28(9):1156-1163. https://doi.org/10.3109/02699052.2014.920523
Gosseries O, Bruno MA, Chatelle C, Vanhaudenhuyse A, Schnakers C, Soddu A, Laureys S. Disorders of consciousness: what’s in a name? NeuroRehabilitation. 2011;28(1):3-14. https://doi.org/10.3233/NRE-2011-0625
Bruno MA, Vanhaudenhuyse A, Thibaut A, Moonen G, Laureys S. From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: recent advances in our understanding of disorders of consciousness. Journal of Neurology. 2011;258(7):1373-1384. https://doi.org/10.1007/s00415-011-6114-x
Gosseries O, Thibaut A, Boly M, Rosanova M, Massimini M, Laureys S. Assessing consciousness in coma and related states using transcranial magnetic stimulation combined with electroencephalography. Annales Françaises d’Anesthésie et de Réanimation. 2014;33(2):65-71. https://doi.org/10.1016/j.annfar.2013.11.002
Bodart O, Laureys S, Gosseries O. Coma and disorders of consciousness: scientific advances and practical considerations for clinicians. Seminars in Neurology. 2013;33(2):83-90. https://doi.org/10.1055/s-0033-1348965
Giacino JT, Katz DI, Schiff ND, Whyte J, Ashman EJ, Ashwal S, Barbano R, Hammond FM, Laureys S, Ling GSF, Nakase-Richardson R, Seel RT, Yablon S, Getchius TSD, Gronseth GS, Armstrong MJ. 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(10):450-460. https://doi.org/10.1212/WNL.0000000000005926
Royal College of Physicians. Prolonged disorders of consciousness following sudden onset brain injury: National clinical guidelines. London: RCP; 2020.
Piradov MA, Suponeva NA, Voznyuk IA, Kondrat’ev AN, Shhyogolev AV, Belkin AA, Zajcev OS, Pryanikov IV, Petrova MV, Ivanova NE, Gnedovskaya EV, Ryabinkina YuV, Sergeev DV, Yazeva EG, Legostaeva LA, Fufaeva EV, Petrikov SS, Rossijskaya rabochaya gruppa po problemam xronicheskix narushenij soznaniya. Xronicheskie narusheniya soznaniya: terminologiya i diagnosticheskie kriterii. Rezul’taty’ pervogo zasedaniya Rossijskoj rabochej gruppy’ po problemam xronicheskix narushenij soznaniya. Annaly’ klinicheskoj i e’ksperimental’noj nevrologii. 2020;14(1):5-16. (In Russ.). https://doi.org/10.25692/ACEN.2020.1.1
Wade DT. How many patients in a prolonged disorder of consciousness might need a best interests meeting about starting or continuing gastrostomy feeding? Clinical Rehabilitation. 2018;32(11):1551-1564. https://doi.org/10.1177/0269215518777285
Pichler G, Fazekas F. Cardiopulmonary arrest is the most frequent cause of the unresponsive wakefulness syndrome: A prospective population-based cohort study in Austria. Resuscitation. 2016;103:94-98. https://doi.org/10.1016/j.resuscitation.2016.02.023
Turner-Stokes L, Rose H, Knight A, Williams H, Siegert RJ, Ashford SA. Prolonged disorders of consciousness: identification using the UK FIM + FAM and cohort analysis of outcomes from a UK national clinical database. Disability and Rehabilitation. 2023;45(4):620-629. https://doi.org/10.1080/09638288.2022.2037754
Multi-Society Task Force on PVS. Medical aspects of the persistent vegetative state (1). The New England Journal of Medicine. 1994;330(21):1499-1508. https://doi.org/10.1056/NEJM199405263302107
Royal College of Physicians. Prolonged disorders of consciousness: National clinical guidelines. London: RCP; 2013.
Giacino JT, Kezmarsky MA, DeLuca J, Cicerone KD. Monitoring rate of recovery to predict outcome in minimally responsive patients. Archives of physical medicine and rehabilitation. 1991;72(11):897-901.
Portaccio E, Morrocchesi A, Romoli AM, Hakiki B, Taglioli MP, Lippi E, Di Renzone M, Grippo A, Macchi C. Score on Coma Recovery Scale-Revised at admission predicts outcome at discharge in intensive rehabilitation after severe brain injury. Brain Injury. 2018;32(6):730-734. https://doi.org/10.1080/02699052.2018.1440420
Mochalova EG, Legostaeva LA, Zimin AA, Yusupova DG, Sergeev DV, Ryabinkina YuV, Bodien Y, Suponeva NA, Piradov MA. The Russian version of Coma Recovery Scale-revised — a standardized method for assessment of patients with disorders of consciousness. S.S. Korsakov Journal of Neurology and Psychiatry. 2018;118(3-2):25-31. (In Russ.).
Noé E, Olaya J, Navarro MD, Noguera P, Colomer C, García-Panach J, Rivero S, Moliner B, Ferri J. Behavioral recovery in disorders of consciousness: a prospective study with the Spanish version of the Coma Recovery Scale-Revised. Archives of Physical Medicine and Rehabilitation. 2012;93(3):428-33.e12.
Hansotia PL. Persistent vegetative state. Review and report of electrodiagnostic studies in eight cases. Archives of Neurology. 1985;42(11):1048-1052. https://doi.org/10.1001/archneur.1985.04060100030015
Kanno T, Kamei Y, Yokoyama T, Jain VK. Neurostimulation for patients in vegetative status. Pacing and Clinical Electrophysiology. 1987;10(1 Pt 2):207-208. https://doi.org/10.1111/j.1540-8159.1987.tb05949.x
Grindel’ OM, Romanova NV, Zajcev OS, Voronov VG, Skoryatina IG. Matematicheskij analiz e’lektroe’ncefalogramm v processe vosstanovleniya soznaniya posle tyazheloj cherepno-mozgovoj travmy. S.S. Korsakov Journal of Neurology and Psychiatry. 2006;12:47-51. (In Russ.).
Schiff ND, Nauvel T, Victor JD. Large-scale brain dynamics in disorders of consciousness. Current Opinion in Neurobiology. 2014;25:7-14. https://doi.org/10.1016/j.conb.2013.10.007
Edlow BL, Claassen J, Schiff ND, Greer DM. Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nature Reviews Neurology. 2021;17(3):135-156. https://doi.org/10.1038/s41582-020-00428-x
Estraneo A, Loreto V, Guarino I, Boemia V, Paone G, Moretta P, Trojano L. Standard EEG in diagnostic process of prolonged disorders of consciousness. Clin Neurophysiol. 2016;127(6):2379-2385. https://doi.org/10.1016/j.clinph.2016.03.021
Piarulli A, Bergamasco M, Thibaut A, Cologan V, Gosseries O, Laureys S. EEG ultradian rhythmicity differences in disorders of consciousness during wakefulness. Journal of Neurology. 2016;263(9):1746-1760. https://doi.org/10.1007/s00415-016-8196-y
Binder M, Papiernik J, Griskova-Bulanova I, Frycz S, Chojnacki B, Górska-Klimowska U. Diagnosing awareness in disorders of consciousness with gamma-band auditory responses. Frontiers in Human Neuroscience. 2024;17:1243051. https://doi.org/10.3389/fnhum.2023.1243051
Sonnet ML, Perrot D, Bouffard Y, Floret D, Fournet A, Motin J. Les potentiels évoqués somesthésiques et auditifs précoces dans les comas anoxiques. Intérêt dans le bilan lésionnel et valeur pronostique [Early somatosensory and auditory evoked potentials in anoxic coma. Role in evaluating and prognostic value]. La Presse Médicale. 1990;19(4):166-169. French.
Bonanni E, Di Coscio E, Maestri M, Carnicelli L, Tsekou H, Economou NT, Paparrigopoulos T, Bonakis A, Papageorgiou SG, Vassilopoulos D, Soldatos CR, Murri L, Ktonas PY. Differences in EEG delta frequency characteristics and patterns in slow-wave sleep between dementia patients and controls: a pilot study. Journal of Clinical Neurophysiology. 2012;29(1):50-54. https://doi.org/10.1097/WNP.0b013e318246b56d
Gottselig JM, Bassetti CL, Achermann P. Power and coherence of sleep spindle frequency activity following hemispheric stroke. Brain. 2002;125(Pt 2):373-283. https://doi.org/10.1093/brain/awf021
Shpichko AI, Shpichko NP, Zinchenko DV, Petrova MV. Polisomnografiya i klinicheskaya ocenka xronicheskix narushenij soznaniya. Trudny’j pacient. 2019;4(17):36-38. (In Russ).
Landsness E, Bruno MA, Noirhomme Q, Riedner B, Gosseries O, Schnakers C, Massimini M, Laureys S, Tononi G, Boly M. Electrophysiological correlates of behavioural changes in vigilance in vegetative state and minimally conscious state. Brain. 2011;134(Pt 8):2222-2232. https://doi.org/10.1093/brain/awr152
Owen AM, Coleman MR. Detecting awareness in the vegetative state. Annals of the New York Academy of Sciences. 2008;1129:130-138. https://doi.org/10.1196/annals.1417.018
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Ledoux D, Brichant JF, Moonen G, Maquet P, Greicius MD, Laureys S, Boly M. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain. 2010;133(Pt 1):161-171. https://doi.org/10.1093/brain/awp313
Greicius MD, Krasnow B, Reiss AL, Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences. 2003;100(1):253-258. https://doi.org/10.1073/pnas.0135058100
Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proceedings of the National Academy of Sciences. 2001;98(2):676-682.
Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends in Cognitive Sciences. 2005;9(12):556-559.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, Schnakers C, Soddu A, Perlbarg V, Ledoux D, Brichant JF, Moonen G, Maquet P, Greicius MD, Laureys S, Boly M. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain. 2010;133(Pt 1):161-171. https://doi.org/10.1093/brain/awp313
Monti MM, Vanhaudenhuyse A, Coleman MR, Boly M, Pickard JD, Tshibanda L, Owen AM, Laureys S. Willful modulation of brain activity in disorders of consciousness. The New England Journal of Medicine. 2010;362(7):579-589. https://doi.org/10.1056/NEJMoa0905370
Fernández-Espejo D, Norton L, Owen AM. The clinical utility of fMRI for identifying covert awareness in the vegetative state: a comparison of sensitivity between 3T and 1.5T. PLoS One. 2014;9(4):e95082. https://doi.org/10.1371/journal.pone.0095082
Di Perri C, Stender J, Laureys S, Gosseries O. Functional neuroanatomy of disorders of consciousness. Epilepsy and Behavior. 2014;30:28-32. https://doi.org/10.1016/j.yebeh.2013.09.014
Levy DE, Sidtis JJ, Rottenberg DA, Jarden JO, Strother SC, Dhawan V, Ginos JZ, Tramo MJ, Evans AC, Plum F. Plum Differences in cerebral blood flow and glucose utilization in vegetative versus locked-in patients. Annals of Neurology. 1987;22(6):673-682. https://doi.org/10.1002/ana.410220602
Stender J, Gosseries O, Bruno MA, Charland-Verville V, Vanhaudenhuyse A, Demertzi A, Chatelle C, Thonnard M, Thibaut A, Heine L, Soddu A, Boly M, Schnakers C, Gjedde A, Laureys S. Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study. Lancet. 2014;384(9942):514-522. https://doi.org/10.1016/S0140-6736(14)60042-8
Aleksandrova EV, Tenedieva VD, Potapov AA. Posttravmaticheskie bessoznatel’ny’e sostoyaniya: fundamental’ny’e i klinicheskie aspekty’. M.: GEOTAR-Media; 2015. (In Russ.).
Kondratieva EA, Kondratev SA, Denisova AA, Ivanova NE, Kondratiev AN. Results of treatment with intravenous amantadine sulfate (PK-Merz) patients with chronic disorders of consciousness. S.S. Korsakov Journal of Neurology and Psychiatry. 2020;120(12):102-108. (In Russ.).

Close metadata