Localization of protoporphyrin IX in glioma patients with paired stimulated Raman histology and two-photon excitation fluorescence microscopy

Mustafa Nasir-Moin, Lisa Wadiura, Devin Juros, Misha Movahed-Ezazi, Matthew Lee, Hannah Weiss, Michael Müther, Daniel Alber, Sujay Ratna, Camila Fang, Eric Suero-Molina, Sonke Hellwig, Walter Stummer, Karl Rössler, Johannes Hainfellner, Georg Widhalm, Barbara Kiesel, David Reichert, Marlo Mischkulnig, Rajan JainAndrew Smith, Jakob Straehle, Nicholas Neidert, Oliver Schnell, Jurgen Beck, Jay Trautman, Steve Pastore, Donato Pacione, Dimitris Placantonakis, Eric Oermann, John Golfinos, Todd Hollon, Matija Snuderl, Christian Freudiger, Dieter Henrik Heiland, D. Orringer

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Abstract

Fluorescence guidance is widely utilized to improve the precision of cancer surgery. 5-aminolevulinic acid, the most widely used fluorophore in glioma surgery, is thought to cause selective accumulation of fluorescent protoporphyrin IX (PpIX) in tumor cells. 5-aminolevulinic acid is highly specific for densely tumor-infiltrated tissue but less effective for visualizing the tumor periphery. To improve clinical detection of PpIX, we developed a microscope to perform paired stimulated Raman histology and two-photon excitation fluorescence microscopy (TPEF) and validated it in 175 fresh tumor specimens from 75 high-grade glioma patients across three institutions. Here, we demonstrate that intracellular PpIX accumulation occurs most prominently in histiocytic, rather than neoplastic, appearing cells. Spatially resolved metabolomics, transcriptomics and RNA sequencing revealed that PPIX is most avidly concentrated in tumor associated macrophages. There was no correlation between the degree of tissue cellularity and PpIX concentration across all imaged specimens (R=-0.21). Our findings encourage reconsideration of the existing theory of 5-ALA-induced glioma cell fluorescence and demonstrate how 5-ALA and TPEF imaging can provide a window into the immune microenvironment of human gliomas.
Original languageEnglish
Number of pages28
DOIs
Publication statusSubmitted - 2022
Externally publishedYes

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