Deep structural brain lesions associated with consciousness impairment early after hemorrhagic stroke
Benjamin Rohaut, Kevin W Doyle, Alexandra S Reynolds, Kay Igwe, Caroline Couch, Adu Matory, Batool Rizvi, David Roh, Angela Velazquez, Murad Megjhani, Soojin Park, Sachin Agarwal, Christine M Mauro, Gen Li, Andrey Eliseyev, Vincent Perlbarg, Sander Connolly, Adam M Brickman, Jan Claassen, Benjamin Rohaut, Kevin W Doyle, Alexandra S Reynolds, Kay Igwe, Caroline Couch, Adu Matory, Batool Rizvi, David Roh, Angela Velazquez, Murad Megjhani, Soojin Park, Sachin Agarwal, Christine M Mauro, Gen Li, Andrey Eliseyev, Vincent Perlbarg, Sander Connolly, Adam M Brickman, Jan Claassen
Abstract
The purpose of this study was to determine the significance of deep structural lesions for impairment of consciousness following hemorrhagic stroke and recovery at ICU discharge. Our study focused on deep lesions that previously were implicated in studies of disorders of consciousness. We analyzed MRI measures obtained within the first week of the bleed and command following throughout the ICU stay. A machine learning approach was applied to identify MRI findings that best predicted the level consciousness. From 158 intracerebral hemorrhage patients that underwent MRI, one third was unconscious at the time of MRI and half of these patients recovered consciousness by ICU discharge. Deep structural lesions predicted both, impairment and recovery of consciousness, together with established measures of mass effect. Lesions in the midbrain peduncle and pontine tegmentum alongside the caudate nucleus were implicated as critical structures. Unconscious patients predicted to recover consciousness by ICU discharge had better long-term functional outcomes than those predicted to remain unconscious.
Conflict of interest statement
The authors declare no competing interests.
Figures
References
- Parvizi J, Damasio AR. Neuroanatomical correlates of brainstem coma. Brain J. Neurol. 2003;126:1524–1536. doi: 10.1093/brain/awg166.
- Posner, J. B., Saper, C. B., Schiff, N. & Plum, F. Plum and Posner’s Diagnosis of Stupor and Coma. (Oxford University Press, 2007).
- Fischer DB, et al. A human brain network derived from coma-causing brainstem lesions. Neurology. 2016;87:2427–2434. doi: 10.1212/WNL.0000000000003404.
- Adams JH, Graham DI, Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain J. Neurol. 2000;123(Pt 7):1327–1338. doi: 10.1093/brain/123.7.1327.
- Dehaene S, Naccache L. Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition. 2001;79:1–37. doi: 10.1016/S0010-0277(00)00123-2.
- Schiff ND. Recovery of consciousness after brain injury: a mesocircuit hypothesis. Trends Neurosci. 2010;33:1–9. doi: 10.1016/j.tins.2009.11.002.
- Giacino JT, Fins JJ, Laureys S, Schiff ND. Disorders of consciousness after acquired brain injury: the state of the science. Nat. Rev. Neurol. 2014;10:99–114. doi: 10.1038/nrneurol.2013.279.
- Lutkenhoff ES, et al. Thalamic and extrathalamic mechanisms of consciousness after severe brain injury. Ann. Neurol. 2015;78:68–76. doi: 10.1002/ana.24423.
- Mikell CB, et al. Frontal networks associated with command following after hemorrhagic stroke. Stroke J. Cereb. Circ. 2015;46:49–57. doi: 10.1161/STROKEAHA.114.007645.
- Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005;437:1257–1263. doi: 10.1038/nature04284.
- Saper, C. B. Diffuse cortical projection systems: anatomical organization and role in cortical function. Compr. Physiol (2011).
- Forgacs PB, et al. Dynamic regimes of neocortical activity linked to corticothalamic integrity correlate with outcomes in acute anoxic brain injury after cardiac arrest. Ann. Clin. Transl. Neurol. 2017;4:119–129. doi: 10.1002/acn3.385.
- Clarençon F, et al. Lesions in deep gray nuclei after severe traumatic brain injury predict neurologic outcome. PLOS ONE. 2017;12:e0186641. doi: 10.1371/journal.pone.0186641.
- Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet Lond. Engl. 2009;373:1632–1644. doi: 10.1016/S0140-6736(09)60371-8.
- Hemphill JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke. 2001;32:891–897. doi: 10.1161/01.STR.32.4.891.
- Rost NS, et al. Prediction of functional outcome in patients with primary intracerebral hemorrhage: the FUNC score. Stroke. 2008;39:2304–2309. doi: 10.1161/STROKEAHA.107.512202.
- Claassen J, et al. Recommendations on the use of EEG monitoring in critically ill patients: consensus statement from the neurointensive care section of the ESICM. Intensive Care Med. 2013;39:1337–1351. doi: 10.1007/s00134-013-2938-4.
- Le Roux, P. et al. The International Multidisciplinary Consensus Conference on Multimodality Monitoring in Neurocritical Care: evidentiary tables: a statement for healthcare professionals from the Neurocritical Care Society and the European Society of Intensive Care Medicine. Neurocrit. Care21 Suppl 2, S297–361 (2014).
- Claassen J, et al. Bedside quantitative electroencephalography improves assessment of consciousness in comatose subarachnoid hemorrhage patients. Ann. Neurol. 2016;80:541–553. doi: 10.1002/ana.24752.
- Nieuwenhuys, R., Voogd, J. & Van Huijzen, C. The human central nervous system: a synopsis and atlas. (Springer Science & Business Media, 2007).
- Yang, W.-S. et al. Defining the Optimal Midline Shift Threshold to Predict Poor Outcome in Patients with Supratentorial Spontaneous Intracerebral Hemorrhage. Neurocrit. Care (2017).
- 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;15:573–585. doi: 10.1089/neu.1998.15.573.
- Friedman J, Hastie T, Tibshirani R. Regularization Paths for Generalized Linear Models via Coordinate Descent. J. Stat. Softw. 2010;33:1–22. doi: 10.18637/jss.v033.i01.
- Kriegeskorte N, Simmons WK, Bellgowan PSF, Baker CI. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 2009;12:535–540. doi: 10.1038/nn.2303.
- R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing (2017).
- de Oliveira Manoel AL, et al. The critical care management of spontaneous intracranial hemorrhage: a contemporary review. Crit. Care Lond. Engl. 2016;20:272. doi: 10.1186/s13054-016-1432-0.
- Jacobs BS, Poggesi A, Terry JB. Max-ICH score: Can it prevent self-fulfilling prophecy in ICH? Neurology. 2017;89:417–418. doi: 10.1212/WNL.0000000000004195.
- Rohaut B, Claassen J. Decision making in perceived devastating brain injury: a call to explore the impact of cognitive biases. Br. J. Anaesth. 2018;120:5–9. doi: 10.1016/j.bja.2017.11.007.
- Qiu M-H, Vetrivelan R, Fuller PM, Lu J. Basal ganglia control of sleep-wake behavior and cortical activation. Eur. J. Neurosci. 2010;31:499–507. doi: 10.1111/j.1460-9568.2009.07062.x.
- Bruno M-A, et al. Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J. Neurol. 2012;259:1087–1098. doi: 10.1007/s00415-011-6303-7.
- Schnakers, C. et al. Acute EEG spectra characteristics predict thalamic atrophy after severe TBI. J Neurol Neurosurg Psychiatry jnnp-2017-317829 (2018).
- Annen J, et al. Regional brain volumetry and brain function in severely brain-injured patients. Ann. Neurol. 2018;83:842–853. doi: 10.1002/ana.25214.
- den Heijer T, Ruitenberg A, Bakker J, Hertzberger L, Kerkhoff H. Neurological picture. Bilateral caudate nucleus infarction associated with variant in circle of Willis. J. Neurol. Neurosurg. Psychiatry. 2007;78:1175. doi: 10.1136/jnnp.2006.112656.
- Fukuoka T, et al. Bilateral caudate nucleus infarction associated with a missing A1 segment. J. Stroke Cerebrovasc. Dis. Off. J. Natl. Stroke Assoc. 2012;21:908.e11–12.
- Kumral E, Evyapan D, Balkir K. Acute caudate vascular lesions. Stroke. 1999;30:100–108. doi: 10.1161/01.STR.30.1.100.
- Chung CS, et al. Striatocapsular haemorrhage. Brain J. Neurol. 2000;123(Pt 9):1850–1862. doi: 10.1093/brain/123.9.1850.
- Hindman J, et al. Thalamic strokes that severely impair arousal extend into the brainstem. Ann. Neurol. 2018;84:926–930. doi: 10.1002/ana.25377.
- Giacino JT, et al. The minimally conscious state: definition and diagnostic criteria. Neurology. 2002;58:349–53. doi: 10.1212/WNL.58.3.349.
- Schiff ND. Uncovering hidden integrative cerebral function in the intensive care unit. Brain. 2017;140:2259–2262. doi: 10.1093/brain/awx209.
- Rohaut, B., Eliseyev, A. & Claassen, J. Uncovering consciousness in unresponsive ICU patients: technical, medical and ethical consideration. Crit. Care (2019).
- Hosker C, Ward D. Hypoactive delirium. BMJ. 2017;357:j2047. doi: 10.1136/bmj.j2047.
- Barr J, et al. Clinical Practice Guidelines for the Management of Pain, Agitation, and Delirium in Adult Patients in the Intensive Care Unit. Crit. Care Med. 2013;41:278–280. doi: 10.1097/CCM.0b013e3182783b72.
- Kidwell CS, Wintermark M. Imaging of intracranial haemorrhage. Lancet Neurol. 2008;7:256–267. doi: 10.1016/S1474-4422(08)70041-3.
- Velly L, et al. Use of brain diffusion tensor imaging for the prediction of long-term neurological outcomes in patients after cardiac arrest: a multicentre, international, prospective, observational, cohort study. Lancet Neurol. 2018;17:317–326. doi: 10.1016/S1474-4422(18)30027-9.
Source: PubMed