An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke

Abstract High intracranial pressure (ICP) can impede cerebral blood flow resulting in secondary injury or death following severe stroke. Compensatory mechanisms include reduced cerebral blood and cerebrospinal fluid volumes, but these often fail to prevent raised ICP. Serendipitous observations in i...

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Autores principales: Anna C. J. Kalisvaart, Cassandra M. Wilkinson, Sherry Gu, Tiffany F. C. Kung, Jerome Yager, Ian R. Winship, Frank K. H. van Landeghem, Frederick Colbourne
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Publicado: Nature Portfolio 2020
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spelling oai:doaj.org-article:0cfda1b4ad5d4c7287732a62aeecb83d2021-12-02T12:40:40ZAn update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke10.1038/s41598-020-78880-42045-2322https://doaj.org/article/0cfda1b4ad5d4c7287732a62aeecb83d2020-12-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-78880-4https://doaj.org/toc/2045-2322Abstract High intracranial pressure (ICP) can impede cerebral blood flow resulting in secondary injury or death following severe stroke. Compensatory mechanisms include reduced cerebral blood and cerebrospinal fluid volumes, but these often fail to prevent raised ICP. Serendipitous observations in intracerebral hemorrhage (ICH) suggest that neurons far removed from a hematoma may shrink as an ICP compliance mechanism. Here, we sought to critically test this observation. We tracked the timing of distal tissue shrinkage (e.g. CA1) after collagenase-induced striatal ICH in rat; cell volume and density alterations (42% volume reduction, 34% density increase; p < 0.0001) were highest day one post-stroke, and rebounded over a week across brain regions. Similar effects were seen in the filament model of middle cerebral artery occlusion (22% volume reduction, 22% density increase; p ≤ 0.007), but not with the Vannucci-Rice model of hypoxic-ischemic encephalopathy (2.5% volume increase, 14% density increase; p ≥ 0.05). Concerningly, this ‘tissue compliance’ appears to cause sub-lethal damage, as revealed by electron microscopy after ICH. Our data challenge the long-held assumption that ‘healthy’ brain tissue outside the injured area maintains its volume. Given the magnitude of these effects, we posit that ‘tissue compliance’ is an important mechanism invoked after severe strokes.Anna C. J. KalisvaartCassandra M. WilkinsonSherry GuTiffany F. C. KungJerome YagerIan R. WinshipFrank K. H. van LandeghemFrederick ColbourneNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 10, Iss 1, Pp 1-15 (2020)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Anna C. J. Kalisvaart
Cassandra M. Wilkinson
Sherry Gu
Tiffany F. C. Kung
Jerome Yager
Ian R. Winship
Frank K. H. van Landeghem
Frederick Colbourne
An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
description Abstract High intracranial pressure (ICP) can impede cerebral blood flow resulting in secondary injury or death following severe stroke. Compensatory mechanisms include reduced cerebral blood and cerebrospinal fluid volumes, but these often fail to prevent raised ICP. Serendipitous observations in intracerebral hemorrhage (ICH) suggest that neurons far removed from a hematoma may shrink as an ICP compliance mechanism. Here, we sought to critically test this observation. We tracked the timing of distal tissue shrinkage (e.g. CA1) after collagenase-induced striatal ICH in rat; cell volume and density alterations (42% volume reduction, 34% density increase; p < 0.0001) were highest day one post-stroke, and rebounded over a week across brain regions. Similar effects were seen in the filament model of middle cerebral artery occlusion (22% volume reduction, 22% density increase; p ≤ 0.007), but not with the Vannucci-Rice model of hypoxic-ischemic encephalopathy (2.5% volume increase, 14% density increase; p ≥ 0.05). Concerningly, this ‘tissue compliance’ appears to cause sub-lethal damage, as revealed by electron microscopy after ICH. Our data challenge the long-held assumption that ‘healthy’ brain tissue outside the injured area maintains its volume. Given the magnitude of these effects, we posit that ‘tissue compliance’ is an important mechanism invoked after severe strokes.
format article
author Anna C. J. Kalisvaart
Cassandra M. Wilkinson
Sherry Gu
Tiffany F. C. Kung
Jerome Yager
Ian R. Winship
Frank K. H. van Landeghem
Frederick Colbourne
author_facet Anna C. J. Kalisvaart
Cassandra M. Wilkinson
Sherry Gu
Tiffany F. C. Kung
Jerome Yager
Ian R. Winship
Frank K. H. van Landeghem
Frederick Colbourne
author_sort Anna C. J. Kalisvaart
title An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
title_short An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
title_full An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
title_fullStr An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
title_full_unstemmed An update to the Monro–Kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
title_sort update to the monro–kellie doctrine to reflect tissue compliance after severe ischemic and hemorrhagic stroke
publisher Nature Portfolio
publishDate 2020
url https://doaj.org/article/0cfda1b4ad5d4c7287732a62aeecb83d
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