Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients: A Pilot Study

Nina Eriksen; Bente Pakkenberg; Egill Rostrup; David O Okonkwo; Bruce Mathern; Lori A Shutter; Anthony J Strong; Johannes Woitzik; Clemens Pahl; Jens P Dreier; Peter Martus; Martin J Lauritzen; Martin Fabricius; Jed A Hartings

doi:10.1007/s12028-019-00692-w

Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients: A Pilot Study

Nina Eriksen, Bente Pakkenberg, Egill Rostrup, David O Okonkwo, Bruce Mathern, Lori A Shutter, Anthony J Strong, Johannes Woitzik, Clemens Pahl, Jens P Dreier, Peter Martus, Martin J Lauritzen, Martin Fabricius, Jed A Hartings

4 Citations (Scopus)

Abstract

Background: Spreading depolarizations (SDs) occur in 50–60% of patients after surgical treatment of severe traumatic brain injury (TBI) and are independently associated with unfavorable outcomes. Here we performed a pilot study to examine the relationship between SDs and various types of intracranial lesions, progression of parenchymal damage, and outcomes. Methods: In a multicenter study, fifty patients (76% male; median age 40) were monitored for SD by continuous electrocorticography (ECoG; median duration 79 h) following surgical treatment of severe TBI. Volumes of hemorrhage and parenchymal damage were estimated using unbiased stereologic assessment of preoperative, postoperative, and post-ECoG serial computed tomography (CT) studies. Neurologic outcomes were assessed at 6 months by the Glasgow Outcome Scale-Extended. Results: Preoperative volumes of subdural and subarachnoid hemorrhage, but not parenchymal damage, were significantly associated with the occurrence of SDs (P’s < 0.05). Parenchymal damage increased significantly (median 34 ml [Interquartile range (IQR) − 2, 74]) over 7 (5, 8) days from preoperative to post-ECoG CT studies. Patients with and without SDs did not differ in extent of parenchymal damage increase [47 ml (3, 101) vs. 30 ml (− 2, 50), P = 0.27], but those exhibiting the isoelectric subtype of SDs had greater initial parenchymal damage and greater increases than other patients (P’s < 0.05). Patients with temporal clusters of SDs (≥ 3 in 2 h; n = 10 patients), which included those with isoelectric SDs, had worse outcomes than those without clusters (P = 0.03), and parenchymal damage expansion also correlated with worse outcomes (P = 0.01). In multivariate regression with imputation, both clusters and lesion expansion were significant outcome predictors. Conclusions: These results suggest that subarachnoid and subdural blood are important primary injury factors in provoking SDs and that clustered SDs and parenchymal lesion expansion contribute independently to worse patient outcomes. These results warrant future prospective studies using detailed quantification of TBI lesion types to better understand the relationship between anatomic and physiologic measures of secondary injury.

Original language	English
Journal	Neurocritical Care
Volume	30
Issue number	3
Pages (from-to)	557-568
ISSN	1541-6933
DOIs	https://doi.org/10.1007/s12028-019-00692-w
Publication status	Published - 15 Jun 2019

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Eriksen, N., Pakkenberg, B., Rostrup, E., Okonkwo, D. O., Mathern, B., Shutter, L. A., Strong, A. J., Woitzik, J., Pahl, C., Dreier, J. P., Martus, P., Lauritzen, M. J., Fabricius, M., & Hartings, J. A. (2019). Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients: A Pilot Study. Neurocritical Care, 30(3), 557-568. https://doi.org/10.1007/s12028-019-00692-w

Eriksen, N, Pakkenberg, B, Rostrup, E, Okonkwo, DO, Mathern, B, Shutter, LA, Strong, AJ, Woitzik, J, Pahl, C, Dreier, JP, Martus, P, Lauritzen, MJ, Fabricius, M & Hartings, JA 2019, 'Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients: A Pilot Study', Neurocritical Care, vol. 30, no. 3, pp. 557-568. https://doi.org/10.1007/s12028-019-00692-w

@article{87332f0d8ccc446c8043b7bbaab3e46e,

title = "Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients: A Pilot Study",

abstract = "Background: Spreading depolarizations (SDs) occur in 50–60% of patients after surgical treatment of severe traumatic brain injury (TBI) and are independently associated with unfavorable outcomes. Here we performed a pilot study to examine the relationship between SDs and various types of intracranial lesions, progression of parenchymal damage, and outcomes. Methods: In a multicenter study, fifty patients (76% male; median age 40) were monitored for SD by continuous electrocorticography (ECoG; median duration 79 h) following surgical treatment of severe TBI. Volumes of hemorrhage and parenchymal damage were estimated using unbiased stereologic assessment of preoperative, postoperative, and post-ECoG serial computed tomography (CT) studies. Neurologic outcomes were assessed at 6 months by the Glasgow Outcome Scale-Extended. Results: Preoperative volumes of subdural and subarachnoid hemorrhage, but not parenchymal damage, were significantly associated with the occurrence of SDs (P{\textquoteright}s < 0.05). Parenchymal damage increased significantly (median 34 ml [Interquartile range (IQR) − 2, 74]) over 7 (5, 8) days from preoperative to post-ECoG CT studies. Patients with and without SDs did not differ in extent of parenchymal damage increase [47 ml (3, 101) vs. 30 ml (− 2, 50), P = 0.27], but those exhibiting the isoelectric subtype of SDs had greater initial parenchymal damage and greater increases than other patients (P{\textquoteright}s < 0.05). Patients with temporal clusters of SDs (≥ 3 in 2 h; n = 10 patients), which included those with isoelectric SDs, had worse outcomes than those without clusters (P = 0.03), and parenchymal damage expansion also correlated with worse outcomes (P = 0.01). In multivariate regression with imputation, both clusters and lesion expansion were significant outcome predictors. Conclusions: These results suggest that subarachnoid and subdural blood are important primary injury factors in provoking SDs and that clustered SDs and parenchymal lesion expansion contribute independently to worse patient outcomes. These results warrant future prospective studies using detailed quantification of TBI lesion types to better understand the relationship between anatomic and physiologic measures of secondary injury.",

author = "Nina Eriksen and Bente Pakkenberg and Egill Rostrup and Okonkwo, {David O} and Bruce Mathern and Shutter, {Lori A} and Strong, {Anthony J} and Johannes Woitzik and Clemens Pahl and Dreier, {Jens P} and Peter Martus and Lauritzen, {Martin J} and Martin Fabricius and Hartings, {Jed A}",

year = "2019",

month = jun,

day = "15",

doi = "10.1007/s12028-019-00692-w",

language = "English",

volume = "30",

pages = "557--568",

journal = "Neurocritical Care",

issn = "1541-6933",

publisher = "Springer",

number = "3",

}

TY - JOUR

T1 - Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients

T2 - A Pilot Study

AU - Eriksen, Nina

AU - Pakkenberg, Bente

AU - Rostrup, Egill

AU - Okonkwo, David O

AU - Mathern, Bruce

AU - Shutter, Lori A

AU - Strong, Anthony J

AU - Woitzik, Johannes

AU - Pahl, Clemens

AU - Dreier, Jens P

AU - Martus, Peter

AU - Lauritzen, Martin J

AU - Fabricius, Martin

AU - Hartings, Jed A

PY - 2019/6/15

Y1 - 2019/6/15

N2 - Background: Spreading depolarizations (SDs) occur in 50–60% of patients after surgical treatment of severe traumatic brain injury (TBI) and are independently associated with unfavorable outcomes. Here we performed a pilot study to examine the relationship between SDs and various types of intracranial lesions, progression of parenchymal damage, and outcomes. Methods: In a multicenter study, fifty patients (76% male; median age 40) were monitored for SD by continuous electrocorticography (ECoG; median duration 79 h) following surgical treatment of severe TBI. Volumes of hemorrhage and parenchymal damage were estimated using unbiased stereologic assessment of preoperative, postoperative, and post-ECoG serial computed tomography (CT) studies. Neurologic outcomes were assessed at 6 months by the Glasgow Outcome Scale-Extended. Results: Preoperative volumes of subdural and subarachnoid hemorrhage, but not parenchymal damage, were significantly associated with the occurrence of SDs (P’s < 0.05). Parenchymal damage increased significantly (median 34 ml [Interquartile range (IQR) − 2, 74]) over 7 (5, 8) days from preoperative to post-ECoG CT studies. Patients with and without SDs did not differ in extent of parenchymal damage increase [47 ml (3, 101) vs. 30 ml (− 2, 50), P = 0.27], but those exhibiting the isoelectric subtype of SDs had greater initial parenchymal damage and greater increases than other patients (P’s < 0.05). Patients with temporal clusters of SDs (≥ 3 in 2 h; n = 10 patients), which included those with isoelectric SDs, had worse outcomes than those without clusters (P = 0.03), and parenchymal damage expansion also correlated with worse outcomes (P = 0.01). In multivariate regression with imputation, both clusters and lesion expansion were significant outcome predictors. Conclusions: These results suggest that subarachnoid and subdural blood are important primary injury factors in provoking SDs and that clustered SDs and parenchymal lesion expansion contribute independently to worse patient outcomes. These results warrant future prospective studies using detailed quantification of TBI lesion types to better understand the relationship between anatomic and physiologic measures of secondary injury.

AB - Background: Spreading depolarizations (SDs) occur in 50–60% of patients after surgical treatment of severe traumatic brain injury (TBI) and are independently associated with unfavorable outcomes. Here we performed a pilot study to examine the relationship between SDs and various types of intracranial lesions, progression of parenchymal damage, and outcomes. Methods: In a multicenter study, fifty patients (76% male; median age 40) were monitored for SD by continuous electrocorticography (ECoG; median duration 79 h) following surgical treatment of severe TBI. Volumes of hemorrhage and parenchymal damage were estimated using unbiased stereologic assessment of preoperative, postoperative, and post-ECoG serial computed tomography (CT) studies. Neurologic outcomes were assessed at 6 months by the Glasgow Outcome Scale-Extended. Results: Preoperative volumes of subdural and subarachnoid hemorrhage, but not parenchymal damage, were significantly associated with the occurrence of SDs (P’s < 0.05). Parenchymal damage increased significantly (median 34 ml [Interquartile range (IQR) − 2, 74]) over 7 (5, 8) days from preoperative to post-ECoG CT studies. Patients with and without SDs did not differ in extent of parenchymal damage increase [47 ml (3, 101) vs. 30 ml (− 2, 50), P = 0.27], but those exhibiting the isoelectric subtype of SDs had greater initial parenchymal damage and greater increases than other patients (P’s < 0.05). Patients with temporal clusters of SDs (≥ 3 in 2 h; n = 10 patients), which included those with isoelectric SDs, had worse outcomes than those without clusters (P = 0.03), and parenchymal damage expansion also correlated with worse outcomes (P = 0.01). In multivariate regression with imputation, both clusters and lesion expansion were significant outcome predictors. Conclusions: These results suggest that subarachnoid and subdural blood are important primary injury factors in provoking SDs and that clustered SDs and parenchymal lesion expansion contribute independently to worse patient outcomes. These results warrant future prospective studies using detailed quantification of TBI lesion types to better understand the relationship between anatomic and physiologic measures of secondary injury.

U2 - 10.1007/s12028-019-00692-w

DO - 10.1007/s12028-019-00692-w

M3 - Journal article

C2 - 30972614

SN - 1541-6933

VL - 30

SP - 557

EP - 568

JO - Neurocritical Care

JF - Neurocritical Care

IS - 3

ER -

Neurostereologic Lesion Volumes and Spreading Depolarizations in Severe Traumatic Brain Injury Patients: A Pilot Study

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