Optical tissue clearing and machine learning can precisely characterize extravasation and blood vessel architecture in brain tumors

Serhii Kostrikov, Kasper B. Johnsen, Thomas H. Braunstein, Johann M. Gudbergsson, Frederikke P. Fliedner, Elisabeth A. A. Obara, Petra Hamerlik, Anders E. Hansen, Andreas Kjaer, Casper Hempel & Thomas L. Andresen - Section for Biotherapeutic Engineering and Drug Targeting, Department of Health Technology, Technical University of Denmark, Lyngby, Denmark ; Section for Biotherapeutic Engineering and Drug Targeting, Department of Health Technology, Technical University of Denmark, Lyngby, Denmark ; Core Facility for Integrated Microscopy, Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark ; Department of Biomedical Sciences, Rigshospitalet and University of Copenhagen, Copenhagen, Denmark ; Brain Tumor Biology, Danish Cancer Society Research Center, Copenhagen, Denmark ;

Precise methods for quantifying drug accumulation in brain tissue are currently very limited, challenging the development of new therapeutics for brain disorders. Transcardial perfusion is instrumental for removing the intravascular fraction of an injected compound, thereby allowing for ex vivo assessment of extravasation into the brain. However, pathological remodeling of tissue microenvironment can affect the efficiency of transcardial perfusion, which has been largely overlooked.

We show that, in contrast to healthy vasculature, transcardial perfusion cannot remove an injected compound from the tumor vasculature to a sufficient extent leading to considerable overestimation of compound extravasation. We demonstrate that 3D deep imaging of optically cleared tumor samples overcomes this limitation. We developed two machine learning-based semi-automated image analysis workflows, which provide detailed quantitative characterization of compound extravasation patterns as well as tumor angioarchitecture in large three-dimensional datasets from optically cleared samples. This methodology provides a precise and comprehensive analysis of extravasation in brain tumors and allows for correlation of extravasation patterns with specific features of the heterogeneous brain tumor vasculature.

How Amira-Avizo Software is used

Afterward, images were imported to Amira and extravasation spots were recognized and measured using Label analysis module. Spots smaller than 10,000 µm3 were excluded from the analysis. For method validation, two image subsets 2 mm3 in volume were selected from two different tumors, number of extravasation spots was counted manually by human annotator and by using developed workflow. Postprocessed datasets were imported to Amira and the vasculature was traced by the AutoSkeleton module employing method developed by Fouard et al.