Polygenic Vulnerability to Intracranial Hypertension, Hemorrhage Progression, and Outcome in Traumatic Brain Injury

Authors

Margaux E. Miller, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Benjamin E. Zusman, Department of Neurology, Massachusetts General Hospital, Brigham and Women's Hospital, Harvard Medical School, Boston, MA.
Chia-Ling Phuah, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Erin McNally, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
David O. Okonkwo, Department of Neurological Surgery, School of Medicine, University of Pittsburgh, Pittsburgh, PA.
Matthew Pease, Department of Neurological Surgery, School of Medicine, Indiana University, Bloomington, IN.
Shashvat M. Desai, HonorHealth Research Institute, Scottsdale, AZ.
Anupama Rani, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Nasathapot Namphol, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Aditya Kumar, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Raemier A. Javelosa, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Adam T. Eberle, Departments of Neurological Surgery, Barrow Neurological Institute, Phoenix, AZ.
Semeon Afework, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.
Joshua Catapano, Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA.
Charles S. Cox, Department of Neurosciences, McGovern Medical School, University of Texas, Houston, TX.
Patrick M. Kochanek, Department of Critical Care Medicine, University of Pittsburgh, Pittsburgh, PA.
Yvette P. Conley, School of Nursing, University of Pittsburgh, Pittsburgh, PA.
Ava M. Puccio, Department of Neurological Surgery, School of Medicine, Indiana University, Bloomington, IN.
Ruchira M. Jha, Department of Neurology, Barrow Neurological Institute, Phoenix, AZ.

Document Type

Article

Abstract

OBJECTIVE: Growing evidence underscores the importance of host-response/secondary-injury-likely influenced by genetics-in outcome variability post-traumatic brain injury (TBI). Intracranial hypertension and hemorrhage progression are critical secondary injuries in severe TBI; these are mediated by the SUR1-TRPM4 channel (a target in clinical trials). We aimed to deconstruct the complex network surrounding SUR1-TRPM4 and define the cumulative impact of key genetic variants on mechanistically connected secondary injuries/outcomes after severe TBI. METHODS: This exploratory study analyzed 492 prospectively enrolled patients with severe TBI. A network of regulators, mediators, and effectors upstream/downstream of SUR1-TRPM4 was bioinformatically constructed. Single nucleotide variants (SNVs) were evaluated for multivariable model association with intracranial pressure, intraparenchymal hemorrhage progression, and Glasgow Outcome Scale (GOS) score. Weighted/unweighted polygenic-risk scores (PRS) were constructed and interrogated. Spatial modeling and functional predictions were determined. Single-cell cortical transcriptomic differences were assessed in a parallel murine TBI model. RESULTS: Ninety-seven genes (625 SNVs) were analyzed. Nineteen genes contained variants associated with all outcomes (intracranial pressure, hemorrhage progression, and GOS score; p < 0.05). Twenty-two genes (42 SNVs) retained significance for ≥ 1 outcome, with overlap across outcomes. Functions included Ca-transport/signaling, glutamate-clearance, neuroinflammation, and cell death. Single-cell analyses revealed cell-specific gene-expression differences. SNVs were brain-specific cis-expression quantitative trait locus (eQTLs)/missense/frameshift mutations suggesting high likelihood of biological impact. PRSs were associated with all outcomes with large effects, and markedly improved model explanatory power/performance (R, receiver operating characteristic [ROC]). INTERPRETATION: Polygenic variability in key nodes linked to SUR1-TRPM4 were associated with mechanistically related secondary injuries and outcome after severe TBI; findings suggest a major role of heritability. Functional implications indicate biological plausibility and identify novel targets. The data, whereas requiring validation, support a shift toward incorporating biologically relevant genetics in advancing precision medicine. ANN NEUROL 2025.

Publication Date

11-14-2025

Publication Title

Annals of neurology

E-ISSN

1531-8249

PubMed ID

41235589

Digital Object Identifier (DOI)

10.1002/ana.78064

Share

COinS