Multimodal imaging of the role of hyperglycemia following experimental subarachnoid hemorrhage

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Abstract

Hyperglycemia has been linked to worsening outcomes after subarachnoid hemorrhage (SAH). Nevertheless, the mechanisms involved in the pathogenesis of SAH have been scarcely evaluated so far. The role of hyperglycemia was assessed in an experimental model of SAH by T ₂ weighted, dynamic contrast-enhanced magnetic resonance imaging (T ₂W and DCE-MRI), [ ¹⁸F]BR-351 PET imaging and immunohistochemistry. Measures included the volume of bleeding, the extent of cerebral infarction and brain edema, blood brain barrier disruption (BBBd), neutrophil infiltration and matrix metalloprotease (MMP) activation. The neurofunctional outcome, neurodegeneration and myelinization were also investigated. The induction of hyperglycemia increased mortality, the size of the ischemic lesion, brain edema, neurodegeneration and worsened neurological outcome during the first 3 days after SAH in rats. In addition, these results show for the first time the exacerbating effect of hyperglycemia on in vivo MMP activation, Intercellular Adhesion Molecule 1 (ICAM-1) expression and neutrophil infiltration together with increased BBBd, bleeding volume and fibrinogen accumulation at days 1 and 3 after SAH. Notably, these data provide valuable insight into the detrimental effect of hyperglycemia on early BBB damage mediated by neutrophil infiltration and MMP activation that could explain the worse prognosis in SAH.

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Spontaneous subarachnoid haemorrhage

Tom A. Schweizer, R. Loch Macdonald (2017)

Subarachnoid haemorrhage is an uncommon and severe subtype of stroke affecting patients at a mean age of 55 years, leading to loss of many years of productive life. The rupture of an intracranial aneurysm is the underlining cause in 85% of cases. Survival from aneurysmal subarachnoid haemorrhage has increased by 17% in the past few decades, probably because of better diagnosis, early aneurysm repair, prescription of nimodipine, and advanced intensive care support. Nevertheless, survivors commonly have cognitive impairments, which in turn affect patients' daily functionality, working capacity, and quality of life. Additionally, those deficits are frequently accompanied by mood disorders, fatigue, and sleep disturbances. Management requires specialised neurological intensive care units and multidisciplinary clinical expertise, which is better provided in high-volume centres. Many clinical trials have been done, but only two interventions are shown to improve outcome. Challenges that remain relate to prevention of subarachnoid haemorrhage by improved screening and development of lower-risk methods to repair or stabilise aneurysms that have not yet ruptured. Multicentre cooperative efforts might increase the knowledge that can be gained from clinical trials, which is often limited by small studies with differing criteria and endpoints that are done in single centres. Outcome assessments that incorporate finer assessment of neurocognitive function and validated surrogate imaging or biomarkers for outcome could also help to advance the specialty.

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Early brain injury, an evolving frontier in subarachnoid hemorrhage research.

Mutsumi Fujii, Junhao Yan, William B Rolland … (2013)

Subarachnoid hemorrhage (SAH), predominantly caused by a ruptured aneurysm, is a devastating neurological disease that has a morbidity and mortality rate higher than 50%. Most of the traditional in vivo research has focused on the pathophysiological or morphological changes of large-arteries after intracisternal blood injection. This was due to a widely held assumption that delayed vasospasm following SAH was the major cause of delayed cerebral ischemia and poor outcome. However, the results of the CONSCIOUS-1 trial implicated some other pathophysiological factors, independent of angiographic vasospasm, in contributing to the poor clinical outcome. The term early brain injury (EBI) has been coined and describes the immediate injury to the brain after SAH, before onset of delayed vasospasm. During the EBI period, a ruptured aneurysm brings on many physiological derangements such as increasing intracranial pressure (ICP), decreased cerebral blood flow (CBF), and global cerebral ischemia. These events initiate secondary injuries such as blood-brain barrier disruption, inflammation, and oxidative cascades that all ultimately lead to cell death. Given the fact that the reversal of vasospasm does not appear to improve patient outcome, it could be argued that the treatment of EBI may successfully attenuate some of the devastating secondary injuries and improve the outcome of patients with SAH. In this review, we provide an overview of the major advances in EBI after SAH research.

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Inflammatory Cytokine Concentrations Are Acutely Increased by Hyperglycemia in Humans: Role of Oxidative Stress

Katherine Esposito, Francesco Nappo, Raffaele Marfella … (2002)

Background— Circulating levels of interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α) are elevated in diabetic patients. We assessed the role of glucose in the regulation of circulating levels of IL-6, TNF-α, and interleukin-18 (IL-18) in subjects with normal or impaired glucose tolerance (IGT), as well as the effect of the antioxidant glutathione. Methods and Results— Plasma glucose levels were acutely raised in 20 control and 15 IGT subjects and maintained at 15 mmol/L for 5 hours while endogenous insulin secretion was blocked with octreotide. In control subjects, plasma IL-6, TNF-α, and IL-18 levels rose ( P <0.01) within 2 hours of the clamp and returned to basal values at 3 hours. In another study, the same subjects received 3 consecutive pulses of intravenous glucose (0.33 g/kg) separated by a 2-hour interval. Plasma cytokine levels obtained at 3, 4, and 5 hours were higher ( P <0.05) than the corresponding values obtained during the clamp. The IGT subjects had fasting plasma IL-6 and TNF-α levels higher ( P <0.05) than those of control subjects. The increase in plasma cytokine levels during the clamping lasted longer (4 hours versus 2 hours, P <0.01) in the IGT subjects than in the control subjects, and the cytokine peaks of IGT subjects after the first glucose pulse were higher ( P <0.05) than those of control subjects. On another occasion, 10 control and 8 IGT subjects received the same glucose pulses as above during an infusion of glutathione; plasma cytokine levels did not show any significant change from baseline after the 3 glucose pulses. Conclusions— Hyperglycemia acutely increases circulating cytokine concentrations by an oxidative mechanism, and this effect is more pronounced in subjects with IGT. This suggests a causal role for hyperglycemia in the immune activation of diabetes.

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Author and article information

Journal

Journal ID (nlm-ta): J Cereb Blood Flow Metab

Journal ID (iso-abbrev): J Cereb Blood Flow Metab

Journal ID (publisher-id): JCB

Journal ID (hwp): spjcb

Title: Journal of Cerebral Blood Flow & Metabolism

Publisher: SAGE Publications (Sage UK: London, England )

ISSN (Print): 0271-678X

ISSN (Electronic): 1559-7016

Publication date (Electronic): 20 September 2023

Publication date (Print): May 2024

Publication date PMC-release: 20 September 2023

Volume: 44

Issue: 5

Pages: 726-741

Affiliations

[1 ]Achucarro Basque Center for Neuroscience, Leioa, Spain

[2 ]CIC biomaGUNE, Basque Research and Technology Alliance, San Sebastian, Spain

[3 ]Neurovascular Group, Biocruces Health Research Institute, Barakaldo, Spain

[4 ]Institute of Neuroscience, Comprehensive Stroke Center, Hospital Clinic of Barcelona, Barcelona, Spain

[5 ]Institute of Neuroscience, Neurosurgery Department, Hospital Clinic of Barcelona, Spain

[6 ]Area of Neurosciences. Institut d'Investigacions Biomèdiques Agustí Pi i Sunyer (IDIBAPS), Barcelona, Spain

[7 ]Department of Neuroscience and Experimental Therapeutics, Institut d'Investigacions Biomèdiques de Barcelona (IIBB), Consejo Superior de Investigaciones Científicas (CSIC), Barcelona, Spain

[8 ]Centro de Investigación Biomédica en Red - Enfermedades Respiratorias, CIBERES, Madrid, Spain

[9 ]Ikerbasque Basque Foundation for Science, Bilbao, Spain

Author notes

[*]Abraham Martín, Achucarro Basque Center for Neuroscience, Science Park of the UPV/EHU, 48940 Leioa, Spain. Email: abraham.martin@ 123456achucarro.org

[*]Carles Justicia, Department of Neuroscience and Experimental Therapeutics, Institut d'Investigacions Biomèdiques de Barcelona (IIBB), Consejo Superior de Investigaciones Científicas (CSIC), Area of Neurosciences, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona 08036, Spain. Email: cjmfat@ 123456iibb.csic.es

Author information

Sergio Amaro https://orcid.org/0000-0001-6838-6390

Anna M Planas https://orcid.org/0000-0002-6147-1880

Article

Publisher ID: 10.1177_0271678X231197946

DOI: 10.1177/0271678X231197946

PMC ID: 11197138

PubMed ID: 37728631

SO-VID: efa6cc4e-9345-4398-8eb3-eb75e5c881ce

License:

This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License ( https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

History

Date received : 16 June 2023

Date revision received : 27 July 2023

Date accepted : 6 August 2023

Custom metadata

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ScienceOpen disciplines: Neurosciences

Keywords: bbbd,hyperglycemia,mri,pet,subarachnoid hemorrhage

Data availability:

ScienceOpen disciplines: Neurosciences

Keywords: bbbd, hyperglycemia, mri, pet, subarachnoid hemorrhage

Multimodal imaging of the role of hyperglycemia following experimental subarachnoid hemorrhage

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