{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:22:49Z","timestamp":1760149369595,"version":"build-2065373602"},"reference-count":38,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,8,3]],"date-time":"2023-08-03T00:00:00Z","timestamp":1691020800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Brain Sciences"],"abstract":"<jats:p>Hemorrhagic complications arising from ventricular drainage procedures are typically asymptomatic and of low volume. A particular subset of these complications, known as delayed intracranial hemorrhage (DICH), is however recognized for its particularly poor prognosis. We primarily aimed to identify epidemiological characteristics associated with DICH, to shed light on its occurrence and potential risk factors. To do so, we performed a retrospective analysis of a series of ten patients who presented with DICH in the context of a ruptured brain arteriovenous malformation (bAVM) and a systematic literature review of all DICH cases reported in the literature. Our ten patients showed delayed neurological deterioration after a ventriculoperitoneal shunt (VPS) procedure, with a computed tomography (CT) scan revealing a DICH surrounding the ventricular catheter, distinct and away from the nidus of their previously ruptured bAVM. Four patients (40%) rapidly declined and passed away, three (30%) required surgical management and the remaining three (30%) demonstrated gradual clinical improvement with conservative management. In the literature, most patients presenting with DICH had hydrocephalus associated with neurovascular disorders (47% of cases), such as bAVM rupture in our present series. These constatations point out the significance of the underlying pathologies potentially being predisposed to these unusual complications.<\/jats:p>","DOI":"10.3390\/brainsci13081159","type":"journal-article","created":{"date-parts":[[2023,8,3]],"date-time":"2023-08-03T11:08:43Z","timestamp":1691060923000},"page":"1159","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Delayed Intracerebral Hematoma after Ventriculoperitoneal Shunt in the Context of Ruptured Brain Arteriovenous Malformation: A Literature Review"],"prefix":"10.3390","volume":"13","author":[{"given":"Guillaume","family":"Dannhoff","sequence":"first","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Salvatore","family":"Chibbaro","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8747-7332","authenticated-orcid":false,"given":"Charles-Henry","family":"Mallereau","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8676-1147","authenticated-orcid":false,"given":"Mario","family":"Ganau","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martial","family":"Agbo-Ponzo","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marie des Neiges","family":"Santin","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1924-1774","authenticated-orcid":false,"given":"Ir\u00e8ne","family":"Ollivier","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4417-1496","authenticated-orcid":false,"given":"Raoul","family":"Pop","sequence":"additional","affiliation":[{"name":"Department of Interventional Radiology, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fran\u00e7ois","family":"Proust","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julien","family":"Todeschi","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, Strasbourg University Hospital, 67000 Strasbourg, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"E11","DOI":"10.3171\/2013.2.FOCUS12368","article-title":"Hydrocephalus after Arteriovenous Malformation Rupture","volume":"34","author":"Gross","year":"2013","journal-title":"FOC"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.clineuro.2017.11.019","article-title":"Intraventricular Hemorrhage Related to AVM Rupture: Description, Outcomes and Impact of Intraventricular Fibrinolysis","volume":"164","author":"Gilard","year":"2018","journal-title":"Clin. Neurol. Neurosurg."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"188","DOI":"10.4103\/2152-7806.172533","article-title":"Role of External Ventricular Drainage in the Management of Intraventricular Hemorrhage; Its Complications and Management","volume":"6","author":"Kirmani","year":"2015","journal-title":"Surg. Neurol. Int."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/0090-3019(85)90006-0","article-title":"Postoperative Intracerebral Hemorrhages: A Survey of Computed Tomographic Findings after 1074 Intracranial Operations","volume":"23","author":"Fukamachi","year":"1985","journal-title":"Surg. Neurol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"931","DOI":"10.3171\/2013.12.JNS131685","article-title":"Hemorrhagic Complications of Ventriculostomy: Incidence and Predictors in Patients with Intracerebral Hemorrhage: Clinical Article","volume":"120","author":"Sussman","year":"2014","journal-title":"JNS"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"ONS-419","DOI":"10.1227\/01.NEU.0000222817.99752.E6","article-title":"Hemorrhagic Complications Of External Ventricular Drainage","volume":"59","author":"Maniker","year":"2006","journal-title":"Oper. Neurosurg."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1016\/0090-3019(85)90264-2","article-title":"Delayed Intracerebral Hemorrhage after Ventriculoperitoneal Shunt","volume":"24","author":"Matsumura","year":"1985","journal-title":"Surg. Neurol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"42693","DOI":"10.18632\/oncotarget.17444","article-title":"Characteristics of Delayed Intracerebral Hemorrhage after Ventriculoperitoneal Shunt Insertion","volume":"8","author":"Gong","year":"2017","journal-title":"Oncotarget"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.wneu.2017.07.133","article-title":"Delayed Intracerebral Hemorrhage Secondary to Ventriculoperitoneal Shunt: A Retrospective Study","volume":"107","author":"Guo","year":"2017","journal-title":"World Neurosurg."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e2029","DOI":"10.1097\/MD.0000000000002029","article-title":"Delayed Intracerebral Hemorrhage Secondary to Ventriculoperitoneal Shunt: A Case Report and Literature Review","volume":"94","author":"Ma","year":"2015","journal-title":"Medicine"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"65","DOI":"10.7150\/ijms.9.65","article-title":"Delayed Intracerebral Hemorrhage Secondary to Ventriculoperitoneal Shunt: Two Case Reports and a Literature Review","volume":"9","author":"Zhou","year":"2012","journal-title":"Int. J. Med. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1016\/j.wneu.2017.07.005","article-title":"Symptomatic Intracerebral Hemorrhage Secondary to Ventriculoperitoneal Shunt in Adults without Bleeding Tendency","volume":"106","author":"Hou","year":"2017","journal-title":"World Neurosurg."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"32","DOI":"10.3171\/jns.1999.91.1.0032","article-title":"Low Incidence of Delayed Intracerebral Hemorrhage Secondary to Ventriculoperitoneal Shunt Insertion","volume":"91","author":"Savitz","year":"1999","journal-title":"J. Neurosurg."},{"key":"ref_14","first-page":"6093","article-title":"Delayed Intracerebral Hemorrhage after Ventriculo-Peritoneal Shunt Procedure: Two Case Reports and a Review of Literature","volume":"25","author":"Wang","year":"2021","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/S0140-6736(74)91639-0","article-title":"Assessment of Coma and Impaired Consciousness. A Practical Scale","volume":"2","author":"Teasdale","year":"1974","journal-title":"Lancet"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/S0140-6736(75)92830-5","article-title":"Assessment of Outcome after Severe Brain Damage: A Practical Scale","volume":"305","author":"Jennett","year":"1975","journal-title":"Lancet"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1227\/00006123-198001000-00001","article-title":"Relation of Cerebral Vasospasm to Subarachnoid Hemorrhage Visualized by Computerized Tomographic Scanning","volume":"6","author":"Fisher","year":"1980","journal-title":"Neurosurgery"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"476","DOI":"10.3171\/jns.1986.65.4.0476","article-title":"A Proposed Grading System for Arteriovenous Malformations","volume":"65","author":"Spetzler","year":"1986","journal-title":"J. Neurosurg."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/S0140-6736(07)61602-X","article-title":"The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for Reporting Observational Studies","volume":"370","author":"Altman","year":"2007","journal-title":"Lancet"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"n71","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.surneu.2007.06.081","article-title":"Safety of Deep Venous Thrombosis Prophylaxis with Low-Molecular-Weight Heparin in Brain Surgery. Prospective Study on 746 Patients","volume":"70","author":"Chibbaro","year":"2008","journal-title":"Surg. Neurol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e510","DOI":"10.1016\/j.wneu.2017.10.012","article-title":"Evolution of Prophylaxis Protocols for Venous Thromboembolism in Neurosurgery: Results from a Prospective Comparative Study on Low-Molecular-Weight Heparin, Elastic Stockings, and Intermittent Pneumatic Compression Devices","volume":"109","author":"Chibbaro","year":"2018","journal-title":"World Neurosurg."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.jocn.2017.08.008","article-title":"Risk of Deep Vein Thrombosis in Neurosurgery: State of the Art on Prophylaxis Protocols and Best Clinical Practices","volume":"45","author":"Ganau","year":"2017","journal-title":"J. Clin. Neurosci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"S224","DOI":"10.21037\/atm.2019.08.44","article-title":"Efficacy and Safety Profiles of Mechanical and Pharmacological Thromboprophylaxis","volume":"7","author":"Ganau","year":"2019","journal-title":"Ann. Transl. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1227\/00006123-198608000-00026","article-title":"Delayed Intracerebral Hemorrhage after Ventriculoperitoneal Shunting","volume":"19","author":"Snow","year":"1986","journal-title":"Neurosurgery"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1227\/00006123-198804000-00025","article-title":"Detection of Shunt-Induced Intracerebral Hemorrhage by Postoperative Skull Films: A Report of Two Cases","volume":"22","author":"Derdeyn","year":"1988","journal-title":"Neurosurgery"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1007\/BF02337623","article-title":"Delayed Intracerebral Hemorrhage after CSF Shunt for Communicating \u201cNormal-Pressure\u201d Hydrocephalus. Case Report","volume":"12","author":"Mascalchi","year":"1991","journal-title":"Ital. J. Neurol. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/S1130-1473(07)70299-3","article-title":"Delayed Intracerebral Hemorrhage after Ventriculoperitoneal Shunt Insertion. Case Report and Literature Review","volume":"18","author":"Alfaro","year":"2007","journal-title":"Neurocirug\u00eda"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"76","DOI":"10.2176\/nmc.50.76","article-title":"Intracerebral Hemorrhage Secondary to Ventriculoperitoneal Shunt Insertion -Four Case Reports\u2014Four Case Reports","volume":"50","author":"Misaki","year":"2010","journal-title":"Neurol. Med. Chir."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1055\/s-0039-1697769","article-title":"Delayed Intracerebral Hemorrhage after Placement of a Ventriculoperitoneal Shunt in a Case of Hydrocephalus: A Rare Case Report and Review of Literature","volume":"10","author":"Musali","year":"2019","journal-title":"J. Neurosci. Rural Pract."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"545","DOI":"10.2176\/nmc.oa.2013-0178","article-title":"Hemorrhage Rates Associated with Two Methods of Ventriculostomy: External Ventricular Drainage vs. Ventriculoperitoneal Shunt Procedure","volume":"54","author":"Ko","year":"2014","journal-title":"Neurol. Med. Chir."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"289","DOI":"10.3171\/2015.12.JNS152341","article-title":"Risk Factors for Hemorrhage Associated with External Ventricular Drain Placement and Removal","volume":"126","author":"Miller","year":"2017","journal-title":"JNS"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"13763","DOI":"10.1038\/s41598-021-93315-4","article-title":"A New Inflammatory Parameter Can Predict Delayed Intracranial Hemorrhage Following Ventriculoperitoneal Shunt","volume":"11","author":"Li","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_34","first-page":"124","article-title":"Evidence of Increased Endothelial Cell Turnover in Brain Arteriovenous Malformations","volume":"49","author":"Hashimoto","year":"2001","journal-title":"Neurosurgery"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"E10","DOI":"10.3171\/2009.2.FOCUS09316","article-title":"Cerebral Arteriovenous Malformations. Part 1: Cellular and Molecular Biology","volume":"26","author":"Moftakhar","year":"2009","journal-title":"FOC"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1007\/s12975-014-0343-0","article-title":"Brain Arteriovenous Malformation Modeling, Pathogenesis, and Novel Therapeutic Targets","volume":"5","author":"Chen","year":"2014","journal-title":"Transl. Stroke Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2294","DOI":"10.1161\/01.STR.0000141932.44613.b1","article-title":"Polymorphisms in Genes Involved in Inflammatory and Angiogenic Pathways and the Risk of Hemorrhagic Presentation of Brain Arteriovenous Malformations","volume":"35","author":"Pawlikowska","year":"2004","journal-title":"Stroke"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.jstrokecerebrovasdis.2015.11.034","article-title":"Alternatively Activated Macrophages Play an Important Role in Vascular Remodeling and Hemorrhaging in Patients with Brain Arteriovenous Malformation","volume":"25","author":"Nakamura","year":"2016","journal-title":"J. Stroke Cerebrovasc. Dis."}],"container-title":["Brain Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3425\/13\/8\/1159\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:24:56Z","timestamp":1760127896000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3425\/13\/8\/1159"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,3]]},"references-count":38,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["brainsci13081159"],"URL":"https:\/\/doi.org\/10.3390\/brainsci13081159","relation":{},"ISSN":["2076-3425"],"issn-type":[{"type":"electronic","value":"2076-3425"}],"subject":[],"published":{"date-parts":[[2023,8,3]]}}}