Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties

Abstract Several theories have tried to elucidate the mechanisms behind the pathophysiology of chronic subdural hematoma (CSDH). However, this process is complex and remains mostly unknown. In this study we performed a retrospective randomised analysis comparing the cortical atrophy of 190 patients...

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Main Authors: Pietro Familiari, Pierfrancesco Lapolla, Michela Relucenti, Ezio Battaglione, Loredana Cristiano, Veronica Sorrentino, Sara Aversa, Alessia D’Amico, Pierfabrizio Puntorieri, Lucia Bruzzaniti, Andrea Mingoli, Gioia Brachini, Giuseppe Barbaro, Anthony Kevin Scafa, Giancarlo D’Andrea, Alessandro Frati, Veronica Picotti, Luigi Valentino Berra, Vincenzo Petrozza, Stefania Nottola, Antonio Santoro, Placido Bruzzaniti
Format: Article
Language:English
Published: Nature Portfolio 2023-02-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-30135-8
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author Pietro Familiari
Pierfrancesco Lapolla
Michela Relucenti
Ezio Battaglione
Loredana Cristiano
Veronica Sorrentino
Sara Aversa
Alessia D’Amico
Pierfabrizio Puntorieri
Lucia Bruzzaniti
Andrea Mingoli
Gioia Brachini
Giuseppe Barbaro
Anthony Kevin Scafa
Giancarlo D’Andrea
Alessandro Frati
Veronica Picotti
Luigi Valentino Berra
Vincenzo Petrozza
Stefania Nottola
Antonio Santoro
Placido Bruzzaniti
author_facet Pietro Familiari
Pierfrancesco Lapolla
Michela Relucenti
Ezio Battaglione
Loredana Cristiano
Veronica Sorrentino
Sara Aversa
Alessia D’Amico
Pierfabrizio Puntorieri
Lucia Bruzzaniti
Andrea Mingoli
Gioia Brachini
Giuseppe Barbaro
Anthony Kevin Scafa
Giancarlo D’Andrea
Alessandro Frati
Veronica Picotti
Luigi Valentino Berra
Vincenzo Petrozza
Stefania Nottola
Antonio Santoro
Placido Bruzzaniti
author_sort Pietro Familiari
collection DOAJ
description Abstract Several theories have tried to elucidate the mechanisms behind the pathophysiology of chronic subdural hematoma (CSDH). However, this process is complex and remains mostly unknown. In this study we performed a retrospective randomised analysis comparing the cortical atrophy of 190 patients with unilateral CSDH, with 190 healthy controls. To evaluate the extent of cortical atrophy, CT scan images were utilised to develop an index that is the ratio of the maximum diameter sum of 3 cisterns divided by the maximum diameter of the skull at the temporal lobe level. Also, we reported, for the first time, the ultrastructural analyses of the CSDH using a combination of immunohistochemistry methods and transmission electron microscopy techniques. Internal validation was performed to confirm the assessment of the different degrees of cortical atrophy. Relative Cortical Atrophy Index (RCA index) refers to the sum of the maximum diameter of three cisterns (insular cistern, longitudinal cerebral fissure and cerebral sulci greatest) with the temporal bones' greatest internal distance. This index, strongly related to age in healthy controls, is positively correlated to the preoperative and post-operative maximum diameter of hematoma and the midline shift in CSDH patients. On the contrary, it negatively correlates to the Karnofsky Performance Status (KPS). The Area Under the Receiver Operating Characteristics (AUROC) showed that RCA index effectively differentiated cases from controls. Immunohistochemistry analysis showed that the newly formed CD-31 positive microvessels are higher in number than the CD34-positive microvessels in the CSDH inner membrane than in the outer membrane. Ultrastructural observations highlight the presence of a chronic inflammatory state mainly in the CSDH inner membrane. Integrating these results, we have obtained an etiopathogenetic model of CSDH. Cortical atrophy appears to be the triggering factor activating the cascade of transendothelial cellular filtration, inflammation, membrane formation and neovascularisation leading to the CSDH formation.
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spelling doaj.art-1ca8b9754bc943e0a7bc1b9607e097072023-03-22T10:58:46ZengNature PortfolioScientific Reports2045-23222023-02-0113112210.1038/s41598-023-30135-8Cortical atrophy in chronic subdural hematoma from ultra-structures to physical propertiesPietro Familiari0Pierfrancesco Lapolla1Michela Relucenti2Ezio Battaglione3Loredana Cristiano4Veronica Sorrentino5Sara Aversa6Alessia D’Amico7Pierfabrizio Puntorieri8Lucia Bruzzaniti9Andrea Mingoli10Gioia Brachini11Giuseppe Barbaro12Anthony Kevin Scafa13Giancarlo D’Andrea14Alessandro Frati15Veronica Picotti16Luigi Valentino Berra17Vincenzo Petrozza18Stefania Nottola19Antonio Santoro20Placido Bruzzaniti21Department of Human Neuroscience, Sapienza University of RomeNuffield Department of Surgical Sciences, University of Oxford, John Radcliffe Oxford University HospitalDepartment of Anatomical, Histological, Medical Legal Sciences and Locomotor Apparatus, Sapienza University of RomeDepartment of Medico-Surgical Sciences and Biotechnologies, Sapienza University of RomeDepartment of Life, Health and Environmental Sciences, University of L’AquilaDepartment of Medico-Surgical Sciences and Biotechnologies, Sapienza University of RomeDepartment of Medico-Surgical Sciences and Biotechnologies, Sapienza University of RomeDepartment of Experimental Medicine, Sapienza, University of RomeDICEAM Department, University Mediterranea of Reggio CalabriaDICEAM Department, University Mediterranea of Reggio CalabriaDepartment of Surgery “Pietro Valdoni”, Sapienza University of RomeDepartment of Surgery “Pietro Valdoni”, Sapienza University of RomeDICEAM Department, University Mediterranea of Reggio CalabriaDepartment of Human Neuroscience, Sapienza University of RomeNeurosurgery Division of “Spaziani” HospitalDepartment of Human Neuroscience, Sapienza University of RomeDepartment of Human Neuroscience, Sapienza University of RomeDepartment of Human Neuroscience, Sapienza University of RomeDepartment of Medico-Surgical Sciences and Biotechnologies, Sapienza University of RomeDepartment of Anatomical, Histological, Medical Legal Sciences and Locomotor Apparatus, Sapienza University of RomeDepartment of Human Neuroscience, Sapienza University of RomeDepartment of Human Neuroscience, Sapienza University of RomeAbstract Several theories have tried to elucidate the mechanisms behind the pathophysiology of chronic subdural hematoma (CSDH). However, this process is complex and remains mostly unknown. In this study we performed a retrospective randomised analysis comparing the cortical atrophy of 190 patients with unilateral CSDH, with 190 healthy controls. To evaluate the extent of cortical atrophy, CT scan images were utilised to develop an index that is the ratio of the maximum diameter sum of 3 cisterns divided by the maximum diameter of the skull at the temporal lobe level. Also, we reported, for the first time, the ultrastructural analyses of the CSDH using a combination of immunohistochemistry methods and transmission electron microscopy techniques. Internal validation was performed to confirm the assessment of the different degrees of cortical atrophy. Relative Cortical Atrophy Index (RCA index) refers to the sum of the maximum diameter of three cisterns (insular cistern, longitudinal cerebral fissure and cerebral sulci greatest) with the temporal bones' greatest internal distance. This index, strongly related to age in healthy controls, is positively correlated to the preoperative and post-operative maximum diameter of hematoma and the midline shift in CSDH patients. On the contrary, it negatively correlates to the Karnofsky Performance Status (KPS). The Area Under the Receiver Operating Characteristics (AUROC) showed that RCA index effectively differentiated cases from controls. Immunohistochemistry analysis showed that the newly formed CD-31 positive microvessels are higher in number than the CD34-positive microvessels in the CSDH inner membrane than in the outer membrane. Ultrastructural observations highlight the presence of a chronic inflammatory state mainly in the CSDH inner membrane. Integrating these results, we have obtained an etiopathogenetic model of CSDH. Cortical atrophy appears to be the triggering factor activating the cascade of transendothelial cellular filtration, inflammation, membrane formation and neovascularisation leading to the CSDH formation.https://doi.org/10.1038/s41598-023-30135-8
spellingShingle Pietro Familiari
Pierfrancesco Lapolla
Michela Relucenti
Ezio Battaglione
Loredana Cristiano
Veronica Sorrentino
Sara Aversa
Alessia D’Amico
Pierfabrizio Puntorieri
Lucia Bruzzaniti
Andrea Mingoli
Gioia Brachini
Giuseppe Barbaro
Anthony Kevin Scafa
Giancarlo D’Andrea
Alessandro Frati
Veronica Picotti
Luigi Valentino Berra
Vincenzo Petrozza
Stefania Nottola
Antonio Santoro
Placido Bruzzaniti
Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties
Scientific Reports
title Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties
title_full Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties
title_fullStr Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties
title_full_unstemmed Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties
title_short Cortical atrophy in chronic subdural hematoma from ultra-structures to physical properties
title_sort cortical atrophy in chronic subdural hematoma from ultra structures to physical properties
url https://doi.org/10.1038/s41598-023-30135-8
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