Prolonged course of brain edema and neurological recovery in a translational model of decompressive craniectomy after closed head injury in mice

Jacek Szczygielski; Vanessa Hubertus; Eduard Kruchten; Andreas Müller; Lisa Franziska Albrecht; Karsten Schwerdtfeger; Joachim Oertel

doi:10.3389/fneur.2023.1308683

Prolonged course of brain edema and neurological recovery in a translational model of decompressive craniectomy after closed head injury in mice

Front Neurol. 2023 Nov 20:14:1308683. doi: 10.3389/fneur.2023.1308683. eCollection 2023.

Authors

Jacek Szczygielski^{1

2

3}, Vanessa Hubertus^{1

4

5}, Eduard Kruchten^{1

6}, Andreas Müller⁷, Lisa Franziska Albrecht¹, Karsten Schwerdtfeger¹, Joachim Oertel¹

Affiliations

¹ Department of Neurosurgery, Saarland University Medical Center and Saarland University Faculty of Medicine, Homburg, Germany.
² Instutute of Neuropathology, Saarland University Medical Center and Saarland University Faculty of Medicine, Homburg, Germany.
³ Institute of Medical Sciences, University of Rzeszów, Rzeszow, Poland.
⁴ Department of Neurosurgery, Charité University Medicine, Berlin, Germany.
⁵ Berlin Institute of Health at Charité, Berlin, Germany.
⁶ Institute of Interventional and Diagnostic Radiology, Karlsruhe, Germany.
⁷ Department of Radiology, Saarland University Medical Center and Saarland University Faculty of Medicine, Homburg, Germany.

Abstract

Background: The use of decompressive craniectomy in traumatic brain injury (TBI) remains a matter of debate. According to the DECRA trial, craniectomy may have a negative impact on functional outcome, while the RescueICP trial revealed a positive effect of surgical decompression, which is evolving over time. This ambivalence of craniectomy has not been studied extensively in controlled laboratory experiments.

Objective: The goal of the current study was to investigate the prolonged effects of decompressive craniectomy (both positive and negative) in an animal model.

Methods: Male mice were assigned to the following groups: sham, decompressive craniectomy, TBI and TBI followed by craniectomy. The analysis of functional outcome was performed at time points 3d, 7d, 14d and 28d post trauma according to the Neurological Severity Score and Beam Balance Score. At the same time points, magnetic resonance imaging was performed, and brain edema was analyzed.

Results: Animals subjected to both trauma and craniectomy presented the exacerbation of the neurological impairment that was apparent mostly in the early course (up to 7d) after injury. Decompressive craniectomy also caused a significant increase in brain edema volume (initially cytotoxic with a secondary shift to vasogenic edema and gliosis). Notably, delayed edema plus gliosis appeared also after decompression even without preceding trauma.

Conclusion: In prolonged outcomes, craniectomy applied after closed head injury in mice aggravates posttraumatic brain edema, leading to additional functional impairment. This effect is, however, transient. Treatment options that reduce brain swelling after decompression may accelerate neurological recovery and should be explored in future experiments.

Keywords: brain edema; closed head injury; decompressive craniectomy; magnetic resonance imaging; mouse model; traumatic brain injury.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work has been supported by financial award of voluntary association “Friends of Saarland University Medical Center” for JS.