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February 01, 2022; 98 (5) Research Article

Combining Transcranial Doppler and EEG Data to Predict Delayed Cerebral Ischemia After Subarachnoid Hemorrhage

View ORCID ProfileHsin Yi Chen, Jonathan Elmer, Sahar F. Zafar, Manohar Ghanta, View ORCID ProfileValdery Moura Junior, View ORCID ProfileEric S. Rosenthal, Emily J. Gilmore, View ORCID ProfileLawrence J. Hirsch, Hitten P. Zaveri, Kevin N. Sheth, View ORCID ProfileNils H. Petersen, View ORCID ProfileM. Brandon Westover, View ORCID ProfileJennifer A. Kim
First published November 29, 2021, DOI: https://doi.org/10.1212/WNL.0000000000013126
Hsin Yi Chen
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Jonathan Elmer
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Sahar F. Zafar
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Manohar Ghanta
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Valdery Moura Junior
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Eric S. Rosenthal
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Emily J. Gilmore
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Lawrence J. Hirsch
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Hitten P. Zaveri
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Kevin N. Sheth
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Nils H. Petersen
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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M. Brandon Westover
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Jennifer A. Kim
From the Department of Neurology (H.Y.C., E.J.G., L.J.H., H.P.Z., K.N.S., N.H.P., J.A.K.), Yale University, New Haven, CT; Department of Critical Care Medicine (J.E.), University of Pittsburgh Medical Center, PA; and Department of Neurology (S.F.Z., M.G., V.M.J., E.S.R., M.B.W.), Massachusetts General Hospital, Boston.
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Citation
Combining Transcranial Doppler and EEG Data to Predict Delayed Cerebral Ischemia After Subarachnoid Hemorrhage
Hsin Yi Chen, Jonathan Elmer, Sahar F. Zafar, Manohar Ghanta, Valdery Moura Junior, Eric S. Rosenthal, Emily J. Gilmore, Lawrence J. Hirsch, Hitten P. Zaveri, Kevin N. Sheth, Nils H. Petersen, M. Brandon Westover, Jennifer A. Kim
Neurology Feb 2022, 98 (5) e459-e469; DOI: 10.1212/WNL.0000000000013126

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Abstract

Background and Objectives Delayed cerebral ischemia (DCI) is the leading complication of subarachnoid hemorrhage (SAH). Because DCI was traditionally thought to be caused by large vessel vasospasm, transcranial Doppler ultrasounds (TCDs) have been the standard of care. Continuous EEG has emerged as a promising complementary monitoring modality and predicts increased DCI risk. Our objective was to determine whether combining EEG and TCD data improves prediction of DCI after SAH. We hypothesize that integrating these diagnostic modalities improves DCI prediction.

Methods We retrospectively assessed patients with moderate to severe SAH (2011–2015; Fisher 3–4 or Hunt-Hess 4–5) who had both prospective TCD and EEG acquisition during hospitalization. Middle cerebral artery (MCA) peak systolic velocities (PSVs) and the presence or absence of epileptiform abnormalities (EAs), defined as seizures, epileptiform discharges, and rhythmic/periodic activity, were recorded daily. Logistic regressions were used to identify significant covariates of EAs and TCD to predict DCI. Group-based trajectory modeling (GBTM) was used to account for changes over time by identifying distinct group trajectories of MCA PSV and EAs associated with DCI risk.

Results We assessed 107 patients; DCI developed in 56 (51.9%). Univariate predictors of DCI are presence of high-MCA velocity (PSV ≥200 cm/s, sensitivity 27%, specificity 89%) and EAs (sensitivity 66%, specificity 62%) on or before day 3. Two univariate GBTM trajectories of EAs predicted DCI (sensitivity 64%, specificity 62.75%). Logistic regression and GBTM models using both TCD and EEG monitoring performed better. The best logistic regression and GBTM models used both TCD and EEG data, Hunt-Hess score at admission, and aneurysm treatment as predictors of DCI (logistic regression: sensitivity 90%, specificity 70%; GBTM: sensitivity 89%, specificity 67%).

Discussion EEG and TCD biomarkers combined provide the best prediction of DCI. The conjunction of clinical variables with the timing of EAs and high MCA velocities improved model performance. These results suggest that TCD and cEEG are promising complementary monitoring modalities for DCI prediction. Our model has potential to serve as a decision support tool in SAH management.

Classification of Evidence This study provides Class II evidence that combined TCD and EEG monitoring can identify delayed cerebral ischemia after SAH.

Glossary

ACA=
anterior cerebral artery;
cEEG=
continuous EEG;
CI=
confidence interval;
DCI=
delayed cerebral ischemia;
EA=
epileptiform abnormality;
GBTM=
group-based trajectory modeling;
IRB=
institutional review board;
LOO-CV=
leave-one-out cross-validation;
MCA=
middle cerebral artery;
MGH=
Massachusetts General Hospital;
NPV=
negative predictive value;
OR=
odds ratio;
PCA=
posterior cerebral artery;
PPV=
positive predictive value;
PSV=
peak systolic velocity;
SAH=
subarachnoid hemorrhage;
TCD=
transcranial Doppler ultrasound

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* M. Brandon Westover and Jennifer A. Kim are co–senior authors.

  • Class of Evidence: NPub.org/coe

  • Received May 7, 2021.
  • Accepted in final form November 8, 2021.
  • © 2021 American Academy of Neurology
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