{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T19:55:58Z","timestamp":1780084558682,"version":"3.54.0"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2025,3,18]],"date-time":"2025-03-18T00:00:00Z","timestamp":1742256000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,3,18]],"date-time":"2025-03-18T00:00:00Z","timestamp":1742256000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004047","name":"Karolinska Institute","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004047","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Int J Legal Med"],"published-print":{"date-parts":[[2025,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:p>Lethal rotational acceleration induced injury to the brain may leave few detectable intracerebral injuries if the survival time is short. Eighty-two Sprague Dawley rats were utilized in a validated model for standardized rotational acceleration traumatic brain injury to investigate the number and area of subarachnoid and intracerebral hemorrhages. The rats were divided into groups with survival times of 0, 5, 10, 20 and 60\u00a0min with equal amounts of experimental and sham operated rats in each group. In addition, a \u201cpostmortem\u201d group of rats were euthanizied 5\u00a0min before the trauma and samples collected 5\u00a0min after the trauma. From all rats, hemispheres were collected, cut and double stained with immunohistochemistry with anti-collagen IV and anti-hemoglobin. Brains from the 20- and 60-minutes groups were stained with immunohistochemistry for amyloid precursor protein beta. The 2 rats with the most and 2 rats with the least intracerebral hemorrhages from all time points were stained for fibrinogen and P-selectin. The group that sustained trauma postmortem and all sham operated rats showed either no bleedings or only a few, minimal, isolated hemorrhages. All other experimental groups showed widespread subarachnoid hemorrhages and few and small intracerebral hemorrhages. The hemorrhages were observed immediately after the rotational brain injury and did not change in number or size during the first hour. Amyloid precursor protein beta staining did not show any convincing axonal accumulation. Fibrinogen and P-selectin showed signs of hemostasis in all antemortem trauma groups. Our conclusion is that hemorrhages from rotatory traumatic brain injury develops immediately upon trauma and do not change during the first hour.<\/jats:p>","DOI":"10.1007\/s00414-025-03457-7","type":"journal-article","created":{"date-parts":[[2025,3,18]],"date-time":"2025-03-18T04:47:30Z","timestamp":1742273250000},"page":"1609-1621","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Bleeding pattern in the early phase after experimental rotational acceleration induced traumatic brain injury"],"prefix":"10.1007","volume":"139","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-2855-1320","authenticated-orcid":false,"given":"Daniel","family":"Andersson","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9154-5393","authenticated-orcid":false,"given":"Kanar","family":"Alkass","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia Anna","family":"Mielcarz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1717-1514","authenticated-orcid":false,"given":"Johan","family":"Davidsson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9198-023X","authenticated-orcid":false,"given":"Henrik","family":"Druid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,3,18]]},"reference":[{"issue":"2","key":"3457_CR1","doi-asserted-by":"publisher","first-page":"e76","DOI":"10.1016\/S2468-2667(16)30017-2","volume":"1","author":"M Majdan","year":"2016","unstructured":"Majdan M et al (2016) Epidemiology of traumatic brain injuries in Europe: a cross-sectional analysis. Lancet Public Health 1(2):e76\u2013e83","journal-title":"Lancet Public Health"},{"key":"3457_CR2","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/B978-0-444-52892-6.00004-0","volume":"127","author":"AC McKee","year":"2015","unstructured":"McKee AC, Daneshvar DH (2015) The neuropathology of traumatic brain injury. Handb Clin Neurol 127:45\u201366","journal-title":"Handb Clin Neurol"},{"issue":"2","key":"3457_CR3","first-page":"120","volume":"26","author":"J Sobrino","year":"2013","unstructured":"Sobrino J, Shafi S (2013) Timing and causes of death after injuries. Proc (Bayl Univ Med Cent) 26(2):120\u2013123","journal-title":"Proc (Bayl Univ Med Cent)"},{"key":"3457_CR4","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.expneurol.2012.01.013","volume":"246","author":"VE Johnson","year":"2013","unstructured":"Johnson VE, Stewart W, Smith DH (2013) Axonal pathology in traumatic brain injury. Exp Neurol 246:35\u201343","journal-title":"Exp Neurol"},{"issue":"1","key":"3457_CR5","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1111\/j.1365-2559.1989.tb03040.x","volume":"15","author":"JH Adams","year":"1989","unstructured":"Adams JH et al (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15(1):49\u201359","journal-title":"Histopathology"},{"issue":"6","key":"3457_CR6","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1136\/jnnp.54.6.481","volume":"54","author":"JH Adams","year":"1991","unstructured":"Adams JH et al (1991) Diffuse axonal injury in non-missile head injury. J Neurol Neurosurg Psychiatry 54(6):481\u2013483","journal-title":"J Neurol Neurosurg Psychiatry"},{"issue":"4","key":"3457_CR7","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1111\/j.1365-2990.1997.tb01305.x","volume":"23","author":"JF Geddes","year":"1997","unstructured":"Geddes JF et al (1997) The diagnosis of diffuse axonal injury: implications for forensic practice. Neuropathol Appl Neurobiol 23(4):339\u2013347","journal-title":"Neuropathol Appl Neurobiol"},{"issue":"2","key":"3457_CR8","first-page":"309","volume":"66","author":"N Yoganandan","year":"2009","unstructured":"Yoganandan N et al (2009) Association of contact loading in diffuse axonal injuries from motor vehicle crashes. J Trauma 66(2):309\u2013315","journal-title":"J Trauma"},{"issue":"2","key":"3457_CR9","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1089\/neu.1994.11.173","volume":"11","author":"CW Christman","year":"1994","unstructured":"Christman CW et al (1994) Ultrastructural studies of diffuse axonal injury in humans. J Neurotrauma 11(2):173\u2013186","journal-title":"J Neurotrauma"},{"issue":"2","key":"3457_CR10","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1111\/j.1365-2990.2006.00794.x","volume":"33","author":"T Hortob\u00e1gyi","year":"2007","unstructured":"Hortob\u00e1gyi T et al (2007) Traumatic axonal damage in the brain can be detected using beta-APP immunohistochemistry within 35 min after head injury to human adults. Neuropathol Appl Neurobiol 33(2):226\u2013237","journal-title":"Neuropathol Appl Neurobiol"},{"issue":"1","key":"3457_CR11","doi-asserted-by":"publisher","first-page":"S171","DOI":"10.1016\/j.legalmed.2009.01.076","volume":"11","author":"T Hayashi","year":"2009","unstructured":"Hayashi T et al (2009) Two patterns of beta-amyloid precursor protein (APP) immunoreactivity in cases of blunt head injury. Leg Med (Tokyo) 11(1):S171\u2013S173","journal-title":"Leg Med (Tokyo)"},{"issue":"2\u20133","key":"3457_CR12","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/S0379-0738(03)00274-3","volume":"146","author":"DI Graham","year":"2004","unstructured":"Graham DI et al (2004) Trials and tribulations of using beta-amyloid precursor protein immunohistochemistry to evaluate traumatic brain injury in adults. Forensic Sci Int 146(2\u20133):89\u201396","journal-title":"Forensic Sci Int"},{"issue":"4","key":"3457_CR13","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1089\/neu.1995.12.565","volume":"12","author":"PC Blumbergs","year":"1995","unstructured":"Blumbergs PC et al (1995) Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J Neurotrauma 12(4):565\u2013572","journal-title":"J Neurotrauma"},{"issue":"1","key":"3457_CR14","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/0303-8467(94)90025-6","volume":"96","author":"HK Ng","year":"1994","unstructured":"Ng HK, Mahaliyana RD, Poon WS (1994) The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and Myelin strains. Clin Neurol Neurosurg 96(1):24\u201331","journal-title":"Clin Neurol Neurosurg"},{"issue":"9","key":"3457_CR15","doi-asserted-by":"publisher","first-page":"840","DOI":"10.1136\/jcp.45.9.840","volume":"45","author":"DI Graham","year":"1992","unstructured":"Graham DI et al (1992) Diffuse axonal injury caused by assault. J Clin Pathol 45(9):840\u2013841","journal-title":"J Clin Pathol"},{"issue":"6","key":"3457_CR16","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1182\/blood-2018-07-818211","volume":"133","author":"JP Luyendyk","year":"2019","unstructured":"Luyendyk JP, Schoenecker JG, Flick MJ (2019) The multifaceted role of fibrinogen in tissue injury and inflammation. Blood 133(6):511\u2013520","journal-title":"Blood"},{"issue":"3","key":"3457_CR17","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1111\/j.1365-2141.2004.05032.x","volume":"126","author":"P Andr\u00e9","year":"2004","unstructured":"Andr\u00e9 P (2004) P-selectin in haemostasis. Br J Haematol 126(3):298\u2013306","journal-title":"Br J Haematol"},{"issue":"6","key":"3457_CR18","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1016\/j.jflm.2008.02.011","volume":"15","author":"JA Ortiz-Rey","year":"2008","unstructured":"Ortiz-Rey JA et al (2008) Immunohistochemical analysis of P-Selectin as a possible marker of vitality in human cutaneous wounds. J Forensic Leg Med 15(6):368\u2013372","journal-title":"J Forensic Leg Med"},{"issue":"11","key":"3457_CR19","doi-asserted-by":"publisher","first-page":"1724","DOI":"10.1089\/neu.2018.6261","volume":"36","author":"DV Agoston","year":"2019","unstructured":"Agoston DV et al (2019) How to translate time: the Temporal aspects of rodent and human Pathobiological processes in traumatic brain injury. J Neurotrauma 36(11):1724\u20131737","journal-title":"J Neurotrauma"},{"issue":"1","key":"3457_CR20","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.expneurol.2004.05.022","volume":"190","author":"JR Stone","year":"2004","unstructured":"Stone JR et al (2004) Impaired axonal transport and altered axolemmal permeability occur in distinct populations of damaged axons following traumatic brain injury. Exp Neurol 190(1):59\u201369","journal-title":"Exp Neurol"},{"key":"3457_CR21","doi-asserted-by":"crossref","unstructured":"Losurdo M, Davidsson J, Sk\u00f6ld MK (2020) Diffuse axonal injury in the rat brain: axonal injury and oligodendrocyte activity following rotational injury. Brain Sci, 10(4)","DOI":"10.3390\/brainsci10040229"},{"key":"3457_CR22","doi-asserted-by":"publisher","first-page":"41","DOI":"10.3389\/fneur.2011.00041","volume":"2","author":"J Davidsson","year":"2011","unstructured":"Davidsson J, Risling M (2011) A new model to produce sagittal plane rotational induced diffuse axonal injuries. Front Neurol 2:41","journal-title":"Front Neurol"},{"issue":"1","key":"3457_CR23","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","volume":"57","author":"Y Benjamini","year":"2018","unstructured":"Benjamini Y, Hochberg Y (2018) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J Roy Stat Soc: Ser B (Methodol) 57(1):289\u2013300","journal-title":"J Roy Stat Soc: Ser B (Methodol)"},{"issue":"2","key":"3457_CR24","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1097\/PAF.0b013e31828877f0","volume":"34","author":"L Xiang","year":"2013","unstructured":"Xiang L et al (2013) Could postmortem hemorrhage occur in the brain? A preliminary study on the establishment and investigation of postmortem hypostatic hemorrhage using rabbit models. Am J Forensic Med Pathol 34(2):147\u2013149","journal-title":"Am J Forensic Med Pathol"},{"issue":"1","key":"3457_CR25","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1186\/s12915-021-00972-y","volume":"19","author":"DA Ammendolia","year":"2021","unstructured":"Ammendolia DA, Bement WM, Brumell JH (2021) Plasma membrane integrity: implications for health and disease. BMC Biol 19(1):71","journal-title":"BMC Biol"},{"issue":"3","key":"3457_CR26","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1089\/08977150151070892","volume":"18","author":"M Runnerstam","year":"2001","unstructured":"Runnerstam M et al (2001) A new model for diffuse brain injury by rotational acceleration: II. Effects on extracellular glutamate, intracranial pressure, and neuronal apoptosis. J Neurotrauma 18(3):259\u2013273","journal-title":"J Neurotrauma"},{"issue":"3","key":"3457_CR27","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1089\/08977150151070874","volume":"18","author":"E Gutierrez","year":"2001","unstructured":"Gutierrez E et al (2001) A new model for diffuse brain injury by rotational acceleration: I model, gross appearance, and astrocytosis. J Neurotrauma 18(3):247\u2013257","journal-title":"J Neurotrauma"},{"issue":"4","key":"3457_CR28","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1002\/jnr.24079","volume":"96","author":"R Vink","year":"2018","unstructured":"Vink R (2018) Large animal models of traumatic brain injury. J Neurosci Res 96(4):527\u2013535","journal-title":"J Neurosci Res"},{"issue":"7","key":"3457_CR29","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1016\/0020-711X(93)90114-T","volume":"25","author":"A Herr\u00e1ez","year":"1993","unstructured":"Herr\u00e1ez A et al (1993) Immunological relationship among rat erythrocyte membrane sialoglycoproteins and with human glycophorins. Int J Biochem 25(7):1009\u20131014","journal-title":"Int J Biochem"},{"key":"3457_CR30","doi-asserted-by":"publisher","first-page":"102228","DOI":"10.1016\/j.jflm.2021.102228","volume":"82","author":"GD Luigi Crudele","year":"2021","unstructured":"Luigi Crudele GD et al (2021) The forensic application of the Glycophorin A on the Amussat\u2019s sign with a brief review of the literature. J Forensic Leg Med 82:102228","journal-title":"J Forensic Leg Med"},{"key":"3457_CR31","doi-asserted-by":"crossref","unstructured":"Baldari B et al (2021) Forensic application of monoclonal Anti-Human Glycophorin A antibody in samples from decomposed bodies to Establish vitality of the injuries. A preliminary experimental study, vol 9. Healthcare (Basel), 5","DOI":"10.3390\/healthcare9050514"},{"issue":"2","key":"3457_CR32","first-page":"22","volume":"45","author":"P Kl\u00edr","year":"2000","unstructured":"Kl\u00edr P et al (2000) [Glycophorin in forensic medicine]. Soud Lek 45(2):22\u201325","journal-title":"Soud Lek"},{"issue":"6","key":"3457_CR33","doi-asserted-by":"publisher","first-page":"1615","DOI":"10.1208\/s12248-017-0123-3","volume":"19","author":"B Rodriguez-Grande","year":"2017","unstructured":"Rodriguez-Grande B et al (2017) Early to Long-Term alterations of CNS barriers after traumatic brain injury: considerations for drug development. Aaps J 19(6):1615\u20131625","journal-title":"Aaps J"},{"key":"3457_CR34","doi-asserted-by":"crossref","unstructured":"Ferrara M et al (2022) Glymphatic system a window on TBI pathophysiology: A systematic review. Int J Mol Sci, 23(16)","DOI":"10.3390\/ijms23169138"},{"key":"3457_CR35","doi-asserted-by":"publisher","first-page":"107866","DOI":"10.1016\/j.dib.2022.107866","volume":"41","author":"K Akeret","year":"2022","unstructured":"Akeret K et al (2022) Spatial transcriptome data from coronal mouse brain sections after striatal injection of Heme and Heme-hemopexin. Data Brief 41:107866","journal-title":"Data Brief"},{"key":"3457_CR36","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1016\/j.freeradbiomed.2021.11.011","volume":"179","author":"RM Buzzi","year":"2022","unstructured":"Buzzi RM et al (2022) Spatial transcriptome analysis defines Heme as a hemopexin-targetable Inflammatoxin in the brain. Free Radic Biol Med 179:277\u2013287","journal-title":"Free Radic Biol Med"}],"container-title":["International Journal of Legal Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00414-025-03457-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00414-025-03457-7\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00414-025-03457-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,6,16]],"date-time":"2025-06-16T04:04:43Z","timestamp":1750046683000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00414-025-03457-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,18]]},"references-count":36,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2025,7]]}},"alternative-id":["3457"],"URL":"https:\/\/doi.org\/10.1007\/s00414-025-03457-7","relation":{},"ISSN":["0937-9827","1437-1596"],"issn-type":[{"value":"0937-9827","type":"print"},{"value":"1437-1596","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,18]]},"assertion":[{"value":"6 August 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 February 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 March 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All animal procedures were approved by the Swedish Agricultural Agency\u2019s animal ethical committee in Stockholm (Dnr 398\u20132020).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Animal ethics"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Informed consent"}},{"value":"The authors have no relevant financial or non-financial.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}