Dura mater and survival time determination in individuals who died after traumatic brain injury: a preliminary study.

Dura mater Survival time Traumatic brain injury

Journal

Forensic science, medicine, and pathology
ISSN: 1556-2891
Titre abrégé: Forensic Sci Med Pathol
Pays: United States
ID NLM: 101236111

Informations de publication

Date de publication:
22 Jun 2024
Historique:
accepted: 11 05 2024
medline: 22 6 2024
pubmed: 22 6 2024
entrez: 22 6 2024
Statut: aheadofprint

Résumé

Traumatic brain injury (TBI) is one of the major causes of morbidity and mortality among young people and is a matter of concern for forensic pathologists. Many authors have tried to estimate a person's survival time (ST) after TBI using different approaches. The present study aimed to present an innovative workflow to estimate the ST after TBI by observing the inflammatory reaction of the dura mater (DM). The authors collected DM samples from 36 cadavers (20 with TBI and 16 with no history or signs of TBI). Each sample was labelled via immunohistochemistry with three different primary antibodies, CD15, CD68, and CD3, yielding 108 slides in total. The slides were digitalized and analysed using QuPath software. The DM is involved in the inflammatory response after TBI. CD15 immunoreactivity allowed us to distinguish between subjects who died immediately after TBI and those with an ST of minutes or hours. CD3 immunoreactivity can be used to differentiate subjects with an ST of days from those with other STs. Moreover, the DM samples showed an acceptable diagnostic yield even in samples with signs of putrefaction.

Sections du résumé

BACKGROUND BACKGROUND
Traumatic brain injury (TBI) is one of the major causes of morbidity and mortality among young people and is a matter of concern for forensic pathologists. Many authors have tried to estimate a person's survival time (ST) after TBI using different approaches.
OBJECTIVE OBJECTIVE
The present study aimed to present an innovative workflow to estimate the ST after TBI by observing the inflammatory reaction of the dura mater (DM).
METHODS METHODS
The authors collected DM samples from 36 cadavers (20 with TBI and 16 with no history or signs of TBI). Each sample was labelled via immunohistochemistry with three different primary antibodies, CD15, CD68, and CD3, yielding 108 slides in total. The slides were digitalized and analysed using QuPath software.
RESULTS RESULTS
The DM is involved in the inflammatory response after TBI. CD15 immunoreactivity allowed us to distinguish between subjects who died immediately after TBI and those with an ST of minutes or hours. CD3 immunoreactivity can be used to differentiate subjects with an ST of days from those with other STs. Moreover, the DM samples showed an acceptable diagnostic yield even in samples with signs of putrefaction.

Identifiants

pubmed: 38907772
doi: 10.1007/s12024-024-00834-3
pii: 10.1007/s12024-024-00834-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Blennow K, Brody DL, Kochanek PM, Levin H, McKee A, Ribbers GM, et al. Traumatic brain injuries. Nat Rev Dis Prim Nat Publishing Group. 2016;2:1–19.
de Souza RS, Pinheiro PP, Neto MLR, Machado Filho JA. Traumatic brain injury (TBI): morbidity, mortality and economic implications. Int Arch Med. 2015;8.
Silver JM, McAllister TW, Arciniegas DB. Textbook of traumatic brain injury. American Psychiatric Pub. 2018.
Zwirner J, Kulakofsky R, Fitzek A, Schröder AS, Bohnert S, Franke H, et al. Forensic biomarkers of lethal traumatic brain injury. Int J Legal Med Springer. 2022;136:871–86.
doi: 10.1007/s00414-022-02785-2
Capizzi A, Woo J, Verduzco-Gutierrez M. Traumatic Brain Injury: An Overview of Epidemiology, Pathophysiology, and Medical Management. Med Clin North Am [Internet]. 2020;104:213–38. https://www.sciencedirect.com/science/article/pii/S0025712519301294 .
Brazinova A, Rehorcikova V, Taylor MS, Buckova V, Majdan M, Psota M et al. Epidemiology of Traumatic Brain Injury in Europe: A Living Systematic Review. J Neurotrauma [Internet]. 2021;38:1411–40. https://www.liebertpub.com/doi/ https://doi.org/10.1089/neu.2015.4126 .
Oura P, Hakkarainen A, Sajantila A. Forensic neuropathology in the past decade: a scoping literature review. Forensic Sci Med Pathol. Springer. 2023;1–12.
Trautz F, Franke H, Bohnert S, Hammer N, Müller W, Stassart R et al. Survival-time dependent increase in neuronal IL-6 and astroglial GFAP expression in fatally injured human brain tissue. Sci Rep [Internet]. 2019;9:11771. https://doi.org/10.1038/s41598-019-48145-w .
Lesnikova I, Schreckenbach MN, Kristensen MP, Papanikolaou LL, Hamilton-Dutoit S. Usability of immunohistochemistry in forensic samples with varying decomposition. Am J Forensic Med Pathol LWW. 2018;39:185–91.
doi: 10.1097/PAF.0000000000000408
Donaldson AE, Lamont IL. Biochemistry changes that occur after death: potential markers for determining post-mortem interval. PLoS One. Public Library of Science San Francisco, USA. 2013;8:e82011.
Niestrawska JA, Rodewald M, Schultz C, Quansah E, Meyer-Zedler T, Schmitt M, et al. Morpho-mechanical mapping of human dura mater microstructure. Acta Biomater Elsevier. 2023;170:86–96.
doi: 10.1016/j.actbio.2023.08.024
De Kegel D, Vastmans J, Fehervary H, Depreitere B, Vander Sloten J, Famaey N. Biomechanical characterization of human dura mater. J Mech Behav Biomed Mater Elsevier. 2018;79:122–34.
doi: 10.1016/j.jmbbm.2017.12.023
Louveau A, Harris TH, Kipnis J. Revisiting the mechanisms of CNS Immune Privilege. Trends Immunol Engl. 2015;36:569–77.
doi: 10.1016/j.it.2015.08.006
Smits HJG, Swartz JE, Philippens MEP, de Bree R, Kaanders JHAM, Koppes SA et al. Validation of automated positive cell and region detection of immunohistochemically stained laryngeal tumor tissue using digital image analysis. J Pathol Inform [Internet]. 2023;14:100198. https://www.sciencedirect.com/science/article/pii/S2153353923000123 .
Dell’Aquila M, Maiese A, De Matteis A, Viola RV, Arcangeli M, La Russa R, et al. Traumatic brain injury: Estimate of the age of the injury based on neuroinflammation, endothelial activation markers and adhesion molecules. Volume 36. Madrid: Histol Histopathol. Francisco Hernández, Juan F. 2021. p. 18319.
Pennisi G, Torrisi M, Cocimano G, Esposito M, Salerno M, Sessa F. Vitality markers in forensic investigations: A literature review. Forensic Sci Med Pathol. Springer. 2023;19:103–16.
Bankhead P, Loughrey MB, Fernández JA, Dombrowski Y, McArt DG, Dunne PD, et al. QuPath: open source software for digital pathology image analysis. Sci Rep Engl. 2017;7:16878.
doi: 10.1038/s41598-017-17204-5
Loughrey MB, Bankhead P, Coleman HG, Hagan RS, Craig S, McCorry AMB, et al. Validation of the systematic scoring of immunohistochemically stained tumour tissue microarrays using QuPath digital image analysis. Histopathology Engl. 2018;73:327–38.
doi: 10.1111/his.13516
Mandrekar JN. Receiver Operating Characteristic Curve in Diagnostic Test Assessment. J Thorac Oncol [Internet]. 2010;5:1315–6. https://www.sciencedirect.com/science/article/pii/S1556086415306043 .
Unal I. Defining an optimal cut-point value in ROC analysis: an alternative approach. Comput Math Methods Med. Hindawi. 2017;2017.
Hosmer DW Jr, Lemeshow S, Sturdivant RX. Applied logistic regression. Wiley; 2013.
Adeeb N, Mortazavi MM, Tubbs S, Cohen-Gadol AA, Tubbs RS, Cohen-Gadol AA. The cranial dura mater: a review of its history, embryology, and anatomy. Child’s Nerv Syst Springer. 2012;28:827–37.
doi: 10.1007/s00381-012-1744-6
Coureuil M, Lécuyer H, Bourdoulous S, Nassif X. A journey into the brain: insight into how bacterial pathogens cross blood–brain barriers. Nat Rev Microbiol Nat Publishing Group UK Lond. 2017;15:149–59.
doi: 10.1038/nrmicro.2016.178
Ng SY, Lee AYW. Traumatic brain injuries: pathophysiology and potential therapeutic targets. Front Cell Neurosci Front Media SA. 2019;13:528.
doi: 10.3389/fncel.2019.00528
Kobek M, Jankowski Z, Szala J, Gąszczyk-Ożarowski Z, Pałasz A, Skowronek R. Time-related morphometric studies of neurofilaments in brain contusions. Folia Neuropathol Pol. 2016;54:50–8.
doi: 10.5114/fn.2016.58915
Krohn M, Dreßler J, Bauer M, Schober K, Franke H, Ondruschka B. Immunohistochemical investigation of S100 and NSE in cases of traumatic brain injury and its application for survival time determination. J Neurotrauma Mary Ann Liebert Inc. 2015;32:430–40. 140 Huguenot Street, 3rd Floor New Rochelle, NY 10801 USA.
Krywanczyk A, Bundock EA. Quantifying macrophages and Hemosiderin in Pediatric Dura Mater. J Forensic Sci United States. 2018;63:902–5.
doi: 10.1111/1556-4029.13634
Bohnert S, Seiffert A, Trella S, Bohnert M, Distel L, Ondruschka B, et al. TMEM119 as a specific marker of microglia reaction in traumatic brain injury in postmortem examination. Int J Legal Med. 2020;134:2167–76.
doi: 10.1007/s00414-020-02384-z pubmed: 32719959 pmcid: 7578160
Romero Tirado M, de LÁ, Blanco Pampin JM, Gallego Gómez R. Dating of traumatic brain Injury in forensic cases using immunohistochemical markers (I): neurofilaments and β-Amyloid precursor protein. Am J Forensic Med Pathol United States. 2018;39:201–7.
doi: 10.1097/PAF.0000000000000412
Hausmann R. Age determination of brain contusions. Forensic Sci Med Pathol Springer. 2006;2:85–93.
doi: 10.1385/FSMP:2:2:85
Oehmichen M, Walter T, Meissner C, Friedrich H-J. Time course of cortical hemorrhages after closed traumatic brain injury: statistical analysis of posttraumatic histomorphological alterations. J Neurotrauma Mary Ann Liebert Inc. 2003;20:87–103.
Hausmann R, Kaiser A, Lang C, Bohnert M, Betz P. A quantitative immunohistochemical study on the time-dependent course of acute inflammatory cellular response to human brain injury. Int J Legal Med Ger. 1999;112:227–32.
doi: 10.1007/s004140050241
Esposito-Fava A, Marchand E, Gauchotte G. Skin injuries in forensic histopathology: a descriptive study. Forensic Sci Med Pathol. United States; 2023.
Gauchotte G, Wissler M-P, Casse J-M, Pujo J, Minetti C, Gisquet H, et al. FVIIIra, CD15, and tryptase performance in the diagnosis of skin stab wound vitality in forensic pathology. Int J Legal Med Springer. 2013;127:957–65.
doi: 10.1007/s00414-013-0880-1
Li N, Du Q, Bai R, Sun J. Vitality and wound-age estimation in forensic pathology: review and future prospects. Forensic Sci Res. Oxford University Press. 2020;5:15–24.
Friesen L, Kroc E, Zumbo BD. Psychometrics & Post-Data Analysis: Test ROC.[jamovi module]. 2019.
Thiele C, Hirschfeld G. Cutpointr: improved estimation and validation of optimal cutpoints in R. arXiv Prepr arXiv200209209. 2020.
Oehmichen M, Eisenmenger W, Raff G, Berghaus G. Brain macrophages in human cortical contusions as indicator of survival period. Forensic Sci Int Elsevier. 1986;30:281–301.
doi: 10.1016/0379-0738(86)90136-2
Oehmichen M, Jakob S, Mann S, Saternus KS, Pedal I, Meissner C. Macrophage subsets in mechanical brain injury (MBI)–a contribution to timing of MBI based on immunohistochemical methods: a pilot study. Leg Med Elsevier. 2009;11:118–24.
doi: 10.1016/j.legalmed.2008.11.003
Hsieh CL, Kim CC, Ryba BE, Niemi EC, Bando JK, Locksley RM, et al. Traumatic brain injury induces macrophage subsets in the brain. Eur J Immunol Wiley Online Libr. 2013;43:2010–22.
doi: 10.1002/eji.201243084
Schläger C, Körner H, Krueger M, Vidoli S, Haberl M, Mielke D, et al. Effector T-cell trafficking between the leptomeninges and the cerebrospinal fluid. Nat Nat Publishing Group UK Lond. 2016;530:349–53.
Alam A, Thelin EP, Tajsic T, Khan DZ, Khellaf A, Patani R, et al. Cellular infiltration in traumatic brain injury. J Neuroinflammation Springer. 2020;17:1–17.
Janaway RC, Percival SL, Wilson AS. Decomposition of human remains. Microbiol aging Clin manifestations. Springer. 2009;313–34.
MacKenzie JM. Examining the decomposed brain. Am J Forensic Med Pathol LWW. 2014;35:265–70.
doi: 10.1097/PAF.0000000000000111
Courts C, Sauer E, Hofmann Y, Madea B, Schyma C. Assessment of DNA profilability from putrefied bodies based on a newly developed quantitative grading system for putrefaction. Forensic Sci Int Genet Suppl Ser Elsevier. 2013;4:e262–3.
doi: 10.1016/j.fsigss.2013.10.134
Courts C, Sauer E, Hofmann Y, Madea B, Schyma C. Assessment of STR typing success rate in soft tissues from putrefied bodies based on a quantitative grading system for putrefaction. J Forensic Sci Wiley Online Libr. 2015;60:1016–21.
doi: 10.1111/1556-4029.12746
Motani H, Sakurada K, Akutsu T, Ikegaya H, Hayakawa M, Sato Y, et al. Usefulness of dura mater in providing DNA samples for identifying cadavers. J Forensic Sci Wiley Online Libr. 2006;51:888–92.
doi: 10.1111/j.1556-4029.2006.00157.x

Auteurs

Marcello Benevento (M)

Section of Legal Medicine, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy. m.benevento3@studenti.uniba.it.

Antonio d'Amati (A)

Section of Pathology, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy.

Simona Nicolì (S)

Section of Legal Medicine, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy.

Laura Ambrosi (L)

Section of Legal Medicine, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy.

Jacek Baj (J)

Chair and Department of Anatomy, Medical University of Lublin, Lublin, 20-090, Poland.

Davide Ferorelli (D)

Section of Legal Medicine, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy.

Giuseppe Ingravallo (G)

Section of Pathology, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy.

Biagio Solarino (B)

Section of Legal Medicine, University of Bari, piazza Giulio Cesare, 11, Bari, 70124, Italy.

Classifications MeSH