Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics

A special issue of Journal of Clinical Medicine (ISSN 2077-0383). This special issue belongs to the section "Clinical Neurology".

Deadline for manuscript submissions: closed (25 June 2021) | Viewed by 36073

Special Issue Editor


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Guest Editor
1. Department of Neuroradiology, University of Basel, Basel, Switzerland
2. Department of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
Interests: intracerebral hemorrhage; ischemic stroke; neuroimaging; neurointervention

Special Issue Information

Dear Colleagues,

Intracerebral hemorrhage (ICH) remains a major cause of morbidity and mortality worldwide. Several factors, such as hematoma volume and hematoma location have been reported to impact neurological outcome. In contrast to them, early hematoma growth is potentially modifiable if detected early enough and therefore presents an appealing therapeutic target. Hematoma Expansion can be predicted using clinical information and advanced neuroimaging techniques including machine learning approaches. This Special Issue will focus on the clinical and neuroimaging characteristics of intracerebral hemorrhage and their potential value for predicting neurological outcomes with the final aim of tailoring individual treatment approaches.

PD Dr. Peter Sporns

Guest Editor

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Keywords

  • Intracerebral hemorrhage
  • Hematoma growth
  • Neuroimaging
  • Outcome prediction
  • Machine learning

Published Papers (10 papers)

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Research

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14 pages, 1540 KiB  
Article
Perihematomal Edema and Clinical Outcome in Intracerebral Hemorrhage Related to Different Oral Anticoagulants
by Jawed Nawabi, Sarah Elsayed, Andrea Morotti, Anna Speth, Melanie Liu, Helge Kniep, Rosalie McDonough, Gabriel Broocks, Tobias Faizy, Elif Can, Peter B. Sporns, Jens Fiehler, Bernd Hamm, Tobias Penzkofer, Georg Bohner, Frieder Schlunk and Uta Hanning
J. Clin. Med. 2021, 10(11), 2234; https://doi.org/10.3390/jcm10112234 - 21 May 2021
Cited by 5 | Viewed by 2844
Abstract
Background: There is a need to examine the effects of different types of oral anticoagulant-associated intracerebral hemorrhage (OAC-ICH) on perihematomal edema (PHE), which is gaining considerable appeal as a biomarker for secondary brain injury and clinical outcome. Methods: In a large multicenter approach, [...] Read more.
Background: There is a need to examine the effects of different types of oral anticoagulant-associated intracerebral hemorrhage (OAC-ICH) on perihematomal edema (PHE), which is gaining considerable appeal as a biomarker for secondary brain injury and clinical outcome. Methods: In a large multicenter approach, computed tomography-derived imaging markers for PHE (absolute PHE, relative PHE (rPHE), edema expansion distance (EED)) were calculated for patients with OAC-ICH and NON-OAC-ICH. Exploratory analysis for non-vitamin-K-antagonist OAC (NOAC) and vitamin-K-antagonists (VKA) was performed. The predictive performance of logistic regression models, employing predictors of poor functional outcome (modified Rankin scale 4–6), was explored. Results: Of 811 retrospectively enrolled patients, 212 (26.14%) had an OAC-ICH. Mean rPHE and mean EED were significantly lower in patients with OAC-ICH compared to NON-OAC-ICH, p-value 0.001 and 0.007; whereas, mean absolute PHE did not differ, p-value 0.091. Mean EED was also significantly lower in NOAC compared to NON-OAC-ICH, p-value 0.05. Absolute PHE was an independent predictor of poor clinical outcome in NON-OAC-ICH (OR 1.02; 95%CI 1.002–1.028; p-value 0.027), but not in OAC-ICH (p-value 0.45). Conclusion: Quantitative markers of early PHE (rPHE and EED) were lower in patients with OAC-ICH compared to those with NON-OAC-ICH, with significantly lower levels of EED in NOAC compared to NON-OAC-ICH. Increase of early PHE volume did not increase the likelihood of poor outcome in OAC-ICH, but was independently associated with poor outcome in NON-OAC-ICH. The results underline the importance of etiology-specific treatment strategies. Further prospective studies are needed. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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15 pages, 1045 KiB  
Article
Circulating AQP4 Levels in Patients with Cerebral Amyloid Angiopathy-Associated Intracerebral Hemorrhage
by Paula Marazuela, Anna Bonaterra-Pastra, Júlia Faura, Anna Penalba, Jesús Pizarro, Olalla Pancorbo, David Rodríguez-Luna, Carla Vert, Alex Rovira, Francesc Pujadas, M. Mar Freijo, Silvia Tur, Maite Martínez-Zabaleta, Pere Cardona Portela, Rocío Vera, Lucia Lebrato-Hernández, Juan F. Arenillas, Soledad Pérez-Sánchez, Joan Montaner, Pilar Delgado and Mar Hernández-Guillamonadd Show full author list remove Hide full author list
J. Clin. Med. 2021, 10(5), 989; https://doi.org/10.3390/jcm10050989 - 02 Mar 2021
Cited by 5 | Viewed by 2146
Abstract
Cerebral amyloid angiopathy (CAA) is a major cause of lobar intracerebral hemorrhage (ICH) in elderly patients. Growing evidence suggests a potential role of aquaporin 4 (AQP4) in amyloid-beta-associated diseases, including CAA pathology. Our aim was to investigate the circulating levels of AQP4 in [...] Read more.
Cerebral amyloid angiopathy (CAA) is a major cause of lobar intracerebral hemorrhage (ICH) in elderly patients. Growing evidence suggests a potential role of aquaporin 4 (AQP4) in amyloid-beta-associated diseases, including CAA pathology. Our aim was to investigate the circulating levels of AQP4 in a cohort of patients who had suffered a lobar ICH with a clinical diagnosis of CAA. AQP4 levels were analyzed in the serum of 60 CAA-related ICH patients and 19 non-stroke subjects by enzyme-linked immunosorbent assay (ELISA). The CAA–ICH cohort was divided according to the time point of the functional outcome evaluation: mid-term (12 ± 18.6 months) and long-term (38.5 ± 32.9 months) after the last ICH. Although no differences were found in AQP4 serum levels between cases and controls, lower levels were found in CAA patients presenting specific hemorrhagic features such as ≥2 lobar ICHs and ≥5 lobar microbleeds detected by magnetic resonance imaging (MRI). In addition, CAA-related ICH patients who presented a long-term good functional outcome had higher circulating AQP4 levels than subjects with a poor outcome or controls. Our data suggest that AQP4 could potentially predict a long-term functional outcome and may play a protective role after a lobar ICH. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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8 pages, 440 KiB  
Article
Prolonged Mechanical Ventilation in Patients with Deep-Seated Intracerebral Hemorrhage: Risk Factors and Clinical Implications
by Felix Lehmann, Lorena M. Schenk, Inja Ilic, Christian Putensen, Alexis Hadjiathanasiou, Valeri Borger, Julian Zimmermann, Erdem Güresir, Hartmut Vatter, Christian Bode, Matthias Schneider and Patrick Schuss
J. Clin. Med. 2021, 10(5), 1015; https://doi.org/10.3390/jcm10051015 - 02 Mar 2021
Cited by 10 | Viewed by 1668
Abstract
While management of patients with deep-seated intracerebral hemorrhage (ICH) is well established, there are scarce data on patients with ICH who require prolonged mechanical ventilation (PMV) during the course of their acute disease. Therefore, we aimed to determine the influence of PMV on [...] Read more.
While management of patients with deep-seated intracerebral hemorrhage (ICH) is well established, there are scarce data on patients with ICH who require prolonged mechanical ventilation (PMV) during the course of their acute disease. Therefore, we aimed to determine the influence of PMV on mortality in patients with ICH and to identify associated risk factors. From 2014 to May 2020, all patients with deep-seated ICH who were admitted to intensive care for >3 days were included in further analyses. PMV is defined as receiving mechanical ventilation for more than 7 days. A total of 42 out of 94 patients (45%) with deep-seated ICH suffered from PMV during the course of treatment. The mortality rate after 90 days was significantly higher in patients with PMV than in those without (64% versus 22%, p < 0.0001). Multivariate analysis identified “ICH volume >30 mL” (p = 0.001, OR 5.3) and “admission SOFA score > 5” (p = 0.007, OR 4.2) as significant and independent predictors for PMV over the course of treatment in deep-seated ICH. With regard to the identified risk factors for PMV occurrence, these findings might enable improved guidance of adequate treatment at the earliest possible stage and lead to a better estimation of prognosis in the course of ICH treatment. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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17 pages, 3481 KiB  
Article
Intrahematomal Ultrasound Enhances RtPA-Fibrinolysis in a Porcine Model of Intracerebral Hemorrhage
by Julia Masomi-Bornwasser, Axel Heimann, Christian Schneider, Tristan Klodt, Hammoud Elmehdawi, Andrea Kronfeld, Harald Krenzlin, Yasemin Tanyildizi, Karl-Friedrich Kreitner, Oliver Kempski, Clemens Sommer, Florian Ringel and Naureen Keric
J. Clin. Med. 2021, 10(4), 563; https://doi.org/10.3390/jcm10040563 - 03 Feb 2021
Cited by 2 | Viewed by 1895
Abstract
Catheter-based ultrasound-thrombolysis has been successfully used in a small clinical trial in order to enhance recombinant tissue plasminogen activator (rtPA)-fibrinolysis, for the treatment of spontaneous intracerebral hemorrhages (ICHs). The aim of this study was to investigate the ultra-early effects of ultrasound on hematoma [...] Read more.
Catheter-based ultrasound-thrombolysis has been successfully used in a small clinical trial in order to enhance recombinant tissue plasminogen activator (rtPA)-fibrinolysis, for the treatment of spontaneous intracerebral hemorrhages (ICHs). The aim of this study was to investigate the ultra-early effects of ultrasound on hematoma and the surrounding brain tissue in a porcine ICH-model. To achieve this, 21 pigs with a right frontal ICH were randomly assigned to four groups: (1) drainage (n = 3), (2) drainage + rtPA (n = 6), (3) drainage + ultrasound (n = 6), and (4) drainage + ultrasound + rtPA (n = 6). The hematoma volume assessment was performed using cranial MRI before and after the treatments. Subsequently, the brain sections were analyzed using HE-staining and immunohistochemistry. The combined treatment using rtPA and ultrasound led to a significantly higher hematoma reduction (62 ± 5%) compared to the other groups (Group 1: 2 ± 1%; Group 2: 30 ± 12%; Group 3: 18 ± 8% (p < 0.0001)). In all groups, the MRI revealed an increase in diffusion restriction but neither hyper- or hypoperfusion, nor perihematomal edema. HE stains showed perihematomal microhemorrhages were equally distributed in each group, while edema was more pronounced within the control group. Immunohistochemistry did not reveal any ultra-early side effects. The combined therapy of drainage, rtPA and ultrasound is a safe and effective technique for hematoma-reduction and protection of the perihematomal tissue in regard to ultra-early effects. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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15 pages, 2329 KiB  
Article
Clinical and Imaging Characteristics in Patients with SARS-CoV-2 Infection and Acute Intracranial Hemorrhage
by Jawed Nawabi, Andrea Morotti, Moritz Wildgruber, Gregoire Boulouis, Hermann Kraehling, Frieder Schlunk, Elif Can, Helge Kniep, Götz Thomalla, Marios Psychogios, Bernd Hamm, Jens Fiehler, Uta Hanning and Peter Sporns
J. Clin. Med. 2020, 9(8), 2543; https://doi.org/10.3390/jcm9082543 - 06 Aug 2020
Cited by 33 | Viewed by 5049
Abstract
Background and Purpose: Intracranial hemorrhage has been observed in patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection (COVID-19), but the clinical, imaging, and pathophysiological features of intracranial bleeding during COVID-19 infection remain poorly characterized. This study describes clinical and imaging characteristics [...] Read more.
Background and Purpose: Intracranial hemorrhage has been observed in patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection (COVID-19), but the clinical, imaging, and pathophysiological features of intracranial bleeding during COVID-19 infection remain poorly characterized. This study describes clinical and imaging characteristics of patients with COVID-19 infection who presented with intracranial bleeding in a European multicenter cohort. Methods: This is a multicenter retrospective, observational case series including 18 consecutive patients with COVID-19 infection and intracranial hemorrhage. Data were collected from February to May 2020 at five designated European special care centers for COVID-19. The diagnosis of COVID-19 was based on laboratory-confirmed diagnosis of SARS-CoV-2. Intracranial bleeding was diagnosed on computed tomography (CT) of the brain within one month of the date of COVID-19 diagnosis. The clinical, laboratory, radiologic, and pathologic findings, therapy and outcomes in COVID-19 patients presenting with intracranial bleeding were analyzed. Results: Eighteen patients had evidence of acute intracranial bleeding within 11 days (IQR 9–29) of admission. Six patients had parenchymal hemorrhage (33.3%), 11 had subarachnoid hemorrhage (SAH) (61.1%), and one patient had subdural hemorrhage (5.6%). Three patients presented with intraventricular hemorrhage (IVH) (16.7%). Conclusion: This study represents the largest case series of patients with intracranial hemorrhage diagnosed with COVID-19 based on key European countries with geospatial hotspots of SARS-CoV-2. Isolated SAH along the convexity may be a predominant bleeding manifestation and may occur in a late temporal course of severe COVID-19. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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8 pages, 236 KiB  
Article
Prognostic Value of Non-Contrast CT Markers and Spot Sign for Outcome Prediction in Patients with Intracerebral Hemorrhage under Oral Anticoagulation
by Sebastian Zimmer, Jörn Meier, Jens Minnerup, Moritz Wildgruber, Gabriel Broocks, Jawed Nawabi, Andrea Morotti, Andre Kemmling, Marios Psychogios, Uta Hanning and Peter B. Sporns
J. Clin. Med. 2020, 9(4), 1077; https://doi.org/10.3390/jcm9041077 - 10 Apr 2020
Cited by 5 | Viewed by 2221
Abstract
Introduction: In patients with spontaneous intracerebral hemorrhage (ICH), several non-contrast computed tomography (NCCT) markers and the spot sign (SS) in computed tomography (CT) angiography (CTA) have been established for the prediction of hematoma growth and neurological outcome. However, the prognostic value of these [...] Read more.
Introduction: In patients with spontaneous intracerebral hemorrhage (ICH), several non-contrast computed tomography (NCCT) markers and the spot sign (SS) in computed tomography (CT) angiography (CTA) have been established for the prediction of hematoma growth and neurological outcome. However, the prognostic value of these markers in patients under oral anticoagulation (ORAC) is unclear. We hypothesized that outcome prediction by these imaging markers may be significantly different between patients with and without ORAC. Therefore, we aimed to investigate the predictive value of NCCT markers and SS in patients with ICH under ORAC. Methods: This is a retrospective study of the database for patients with ICH at a German tertiary stroke center. Inclusion criteria were (1) patients with ICH, (2) oral anticoagulation within the therapeutic range, and (3) NCCT and CTA performed on admission within 6 h after onset of symptoms. We defined a binary outcome: modified Rankin Scale (mRS) ≤ 3 = good outcome versus mRS > 3 = poor outcome at discharge. The predictive value of each sign was assessed in uni- and multivariable logistic regression models. Results: Of 129 patients with ICH under ORAC, 76 (58.9%) presented with hypodensities within the hematoma in admission NCCT, 64 (52.7%) presented with an irregular shape of the hematoma, 60 (46.5%) presented with a swirl sign, 49 (38.0%) presented with a black hole sign, and 46 (35.7%) presented with a heterogeneous density of the hematoma. Moreover, 44 (34.1%) patients had a satellite sign, in 20 (15.5%) patients, an island sign was detected, 18 (14.0%) patients were blend-sign positive, and 14 (10.9%) patients presented with a CTA spot sign. Inter-rater agreement was very high for all included characteristics between the two readers. Multivariable logistic regression analysis identified the presence of black hole sign (odds ratio 10.59; p < 0.001), swirl sign (odds ratio 14.06; p < 0.001), and satellite sign (odds ratio 6.38; p = 0.011) as independent predictors of poor outcome. Conclusions: The distribution and prognostic value of several NCCT markers and CTA spot sign in ICH patients under ORAC is comparable to those with spontaneous ICH, even though these parameters are partly based on coagulant status. These findings suggest that a similar approach can be used for further research regarding outcome prediction in ICH patients under ORAC and those with spontaneous ICH. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
10 pages, 3853 KiB  
Article
Inter- and Intrarater Agreement of Spot Sign and Noncontrast CT Markers for Early Intracerebral Hemorrhage Expansion
by Jawed Nawabi, Sarah Elsayed, Helge Kniep, Peter Sporns, Frieder Schlunk, Rosalie McDonough, Gabriel Broocks, Lasse Dührsen, Gerhard Schön, Thomalla Götz, Jens Fiehler and Uta Hanning
J. Clin. Med. 2020, 9(4), 1020; https://doi.org/10.3390/jcm9041020 - 04 Apr 2020
Cited by 12 | Viewed by 3633
Abstract
Background: The aim of this study was to assess the inter- and intrarater reliability of noncontrast CT (NCCT) markers [Black Hole Sign (BH), Blend Sign (BS), Island Sign (IS), and Hypodensities (HD)] and Spot Sign (SS) on CTA in patients with spontaneous intracerebral [...] Read more.
Background: The aim of this study was to assess the inter- and intrarater reliability of noncontrast CT (NCCT) markers [Black Hole Sign (BH), Blend Sign (BS), Island Sign (IS), and Hypodensities (HD)] and Spot Sign (SS) on CTA in patients with spontaneous intracerebral hemorrhage (ICH). Methods: Patients with spontaneous ICH at three German tertiary stroke centers were retrospectively included. Each CT scan was rated for four NCCT markers and SS on CTA by two radiology residents. Raters were blind to all demographic and outcome data. Inter- and intrarater agreement was determined by Cohen’s kappa (κ) coefficient and percentage of agreement. Results: Interrater agreement was excellent in 473 included patients, ranging from 96% to 99%. Interrater κ ranged from 0.85 (95% CI [0.78–0.91]) to 0.97 (95% CI [0.94–0.99]) for NCCT markers and 0.93 (95% CI [0.88–0.98]) for SS, all p-values < 0.001. Intrarrater agreement ranged from 96% to 100%, with κ ranging from 0.85 (95% CI [0.78–0.91]) to 1.00 (95% CI [0.10–0.85]) for NCCT markers and 0.96 (95% CI [0.92–1.00]) for SS, all p-values < 0.001. Conclusions: NCCT imaging findings and SS on CTA have good-to-excellent inter- and intrarater reliabilities, with the highest agreement for BH and SS. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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Review

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15 pages, 895 KiB  
Review
Ischemic Stroke and Heart Failure: Facts and Numbers. An Update
by Anush Barkhudaryan, Wolfram Doehner and Nadja Scherbakov
J. Clin. Med. 2021, 10(5), 1146; https://doi.org/10.3390/jcm10051146 - 09 Mar 2021
Cited by 9 | Viewed by 6985
Abstract
Heart failure (HF) is a severe clinical syndrome accompanied by a number of comorbidities. Ischemic stroke occurs frequently in patients with HF as a complication of the disease. In the present review, we aimed to summarize the current state of research on the [...] Read more.
Heart failure (HF) is a severe clinical syndrome accompanied by a number of comorbidities. Ischemic stroke occurs frequently in patients with HF as a complication of the disease. In the present review, we aimed to summarize the current state of research on the role of cardio–cerebral interactions in the prevalence, etiology, and prognosis of both diseases. The main pathophysiological mechanisms underlying the development of stroke in HF and vice versa are discussed. In addition, we reviewed the results of recent clinical trials investigating the prevalence and prevention of stroke in patients with HF. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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13 pages, 5194 KiB  
Review
Neuroimaging of Acute Intracerebral Hemorrhage
by Peter B. Sporns, Marios-Nikos Psychogios, Grégoire Boulouis, Andreas Charidimou, Qi Li, Enrico Fainardi, Dar Dowlatshahi, Joshua N. Goldstein and Andrea Morotti
J. Clin. Med. 2021, 10(5), 1086; https://doi.org/10.3390/jcm10051086 - 05 Mar 2021
Cited by 10 | Viewed by 4498
Abstract
Intracerebral hemorrhage (ICH) accounts for 10% to 20% of all strokes worldwide and is associated with high morbidity and mortality. Neuroimaging is clinically important for the rapid diagnosis of ICH and underlying etiologies, but also for identification of ICH expansion, often as-sociated with [...] Read more.
Intracerebral hemorrhage (ICH) accounts for 10% to 20% of all strokes worldwide and is associated with high morbidity and mortality. Neuroimaging is clinically important for the rapid diagnosis of ICH and underlying etiologies, but also for identification of ICH expansion, often as-sociated with an increased risk for poor outcome. In this context, rapid assessment of early hema-toma expansion risk is both an opportunity for therapeutic intervention and a potential hazard for hematoma evacuation surgery. In this review, we provide an overview of the current literature surrounding the use of multimodal neuroimaging of ICH for etiological diagnosis, prediction of early hematoma expansion, and prognostication of neurological outcome. Specifically, we discuss standard imaging using computed tomography, the value of different vascular imaging modalities to identify underlying causes and present recent advances in magnetic resonance imaging and computed tomography perfusion. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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10 pages, 4108 KiB  
Review
Neuroimaging of Pediatric Intracerebral Hemorrhage
by Peter B. Sporns, Marios-Nikos Psychogios, Heather J. Fullerton, Sarah Lee, Olivier Naggara and Grégoire Boulouis
J. Clin. Med. 2020, 9(5), 1518; https://doi.org/10.3390/jcm9051518 - 18 May 2020
Cited by 9 | Viewed by 3870
Abstract
Hemorrhagic strokes account for half of all strokes seen in children, and the etiologies of these hemorrhagic strokes differ greatly from those seen in adult patients. This review gives an overview about incidence and etiologies as well as presentation of children with intracerebral [...] Read more.
Hemorrhagic strokes account for half of all strokes seen in children, and the etiologies of these hemorrhagic strokes differ greatly from those seen in adult patients. This review gives an overview about incidence and etiologies as well as presentation of children with intracerebral hemorrhage and with differential diagnoses in the emergency department. Most importantly it describes how neuroimaging of children with intracerebral hemorrhage should be tailored to specific situations and clinical contexts and recommends specific imaging protocols for acute and repeat imaging. In this context it is important to keep in mind the high prevalence of underlying vascular lesions and adapt the imaging protocol accordingly, meaning that vascular imaging plays a key role regardless of modality. Magnetic resonance imaging (MRI), including advanced sequences, should be favored whenever possible at the acute phase. Full article
(This article belongs to the Special Issue Intracerebral Hemorrhage: Clinical and Neuroimaging Characteristics)
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