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Metabolic Pattern of the Acute Phase of Subarachnoid Hemorrhage in a Novel Porcine Model: Studies with Cerebral Microdialysis with High Temporal Resolution
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Neurosurgery.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Surgical Sciences, Anaesthesiology and Intensive Care.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Neurosurgery.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Neurosurgery.
2014 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 6, e99904- p.Article in journal (Refereed) Published
Abstract [en]

Background: Aneurysmal subarachnoid hemorrhage (SAH) may produce cerebral ischemia and systemic responses including stress. To study immediate cerebral and systemic changes in response to aneurysm rupture, animal models are needed. Objective: To study early cerebral energy changes in an animal model. Methods: Experimental SAH was induced in 11 pigs by autologous blood injection to the anterior skull base, with simultaneous control of intracranial and cerebral perfusion pressures. Intracerebral microdialysis was used to monitor concentrations of glucose, pyruvate and lactate. Results: In nine of the pigs, a pattern of transient ischemia was produced, with a dramatic reduction of cerebral perfusion pressure soon after blood injection, associated with a quick glucose and pyruvate decrease. This was followed by a lactate increase and a delayed pyruvate increase, producing a marked but short elevation of the lactate/pyruvate ratio. Glucose, pyruvate, lactate and lactate/pyruvate ratio thereafter returned toward baseline. The two remaining pigs had a more severe metabolic reaction with glucose and pyruvate rapidly decreasing to undetectable levels while lactate increased and remained elevated, suggesting persisting ischemia. Conclusion: The animal model simulates the conditions of SAH not only by deposition of blood in the basal cisterns, but also creating the transient global ischemic impact of aneurysmal SAH. The metabolic cerebral changes suggest immediate transient substrate failure followed by hypermetabolism of glucose upon reperfusion. The model has features that resemble spontaneous bleeding, and is suitable for future research of the early cerebral and systemic responses to SAH that are difficult to study in humans.

Place, publisher, year, edition, pages
2014. Vol. 9, no 6, e99904- p.
National Category
Surgery
Identifiers
URN: urn:nbn:se:uu:diva-229957DOI: 10.1371/journal.pone.0099904ISI: 000338508200053PubMedID: 24940881OAI: oai:DiVA.org:uu-229957DiVA: diva2:738616
Available from: 2014-08-18 Created: 2014-08-18 Last updated: 2017-12-05Bibliographically approved
In thesis
1. Metabolic and Endocrine Response in the Acute Stage of Subarachnoid Hemorrhage
Open this publication in new window or tab >>Metabolic and Endocrine Response in the Acute Stage of Subarachnoid Hemorrhage
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The rupture of an aneurysm in subarachnoid hemorrhage (SAH) is a dramatic event causing a severe impact on the brain and a transient or permanent ischemic condition. Several types of responses to meet the challenges of SAH have been found in the acute phase, including activation of the hypothalamic-pituitary-adrenal (HPA) axis and the sympathetic nervous system, elevated levels of brain natriuretic peptide (BNP), and disturbances in cerebral and systemic metabolism.

Cerebral metabolism and the endocrine stress response in the ultra-early phase was investigated in a novel porcine model of SAH in which autologous blood was injected to the anterior skull base. Early activation of the HPA axis was found with rapid elevation of adrenocorticotrophic hormone, cortisol and aldosterone. The peak values of these hormones were early and may be impossible to catch in patients. There were indications of a sympathetic nervous response with excretion of catecholamines in urine as well as plasma chromogranin-A elevation. Cerebral microdialysis suggested immediate substrate failure followed by hypermetabolism of glucose. The animal model seems suited for further studies of aneurysmal SAH.

NT-proBNP was investigated in 156 patients with SAH, there was a dynamic course with increasing levels during the first 4 days of the disease. Factors predicting high NT-proBNP load included female sex, high age, high Troponin-I at admission, angiographic finding of an aneurysm and worse clinical condition at admission. High levels of NT-proBNP were correlated to factors indicating a more severe disease, suggesting the initial injury in aneurysmal SAH is an important factor in predicting high NT-proBNP during the acute stage of the disease.

Measurements with indirect calorimetry were performed daily during the first week after SAH on 32 patients with SAH. There was a dynamic course with increasing energy expenditure (EE) the first week after SAH. Comparisons with three predictive equations indicated that measured EE generally is higher than predicted, but considerable variation exists within and between patients, indicating that prediction of EE in SAH is difficult.

Altogether, the studies demonstrate a complicated response in acute SAH that needs to be further studied to increase possibility of good outcome in SAH patients.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. 61 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1357
Keyword
Subarachnoid hemorrhage, Energy Expenditure, BNP, Animal Model, Cortisol, Microdialysis
National Category
Neurology Anesthesiology and Intensive Care
Research subject
Neurosurgery
Identifiers
urn:nbn:se:uu:diva-328121 (URN)978-91-513-0038-2 (ISBN)
Public defence
2017-10-06, Grönwallsalen, Akademiska sjukhuset, Uppsala, 09:15 (Swedish)
Opponent
Supervisors
Available from: 2017-09-15 Created: 2017-08-17 Last updated: 2017-10-17

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Nyberg, ChristofferKarlsson, TorbjörnHillered, LarsRonne-Engström, Elisabeth

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