Neuropathological interpretation of stimulated Raman histology images of brain and spine tumors: part B.

Diagnostic accuracy H&E-stained frozen section NIO Neuropathology Neurosurgery Stimulated Raman histology (SRH)

Journal

Neurosurgical review
ISSN: 1437-2320
Titre abrégé: Neurosurg Rev
Pays: Germany
ID NLM: 7908181

Informations de publication

Date de publication:
Apr 2022
Historique:
received: 25 10 2021
accepted: 26 11 2021
revised: 22 11 2021
pubmed: 11 12 2021
medline: 6 4 2022
entrez: 10 12 2021
Statut: ppublish

Résumé

Intraoperative histopathological examinations are routinely performed to provide neurosurgeons with information about the entity of tumor tissue. Here, we quantified the neuropathological interpretability of stimulated Raman histology (SRH) acquired using a Raman laser imaging system in a routine clinical setting without any specialized training or prior experience. Stimulated Raman scattering microscopy was performed on 117 samples of pathological tissue from 73 cases of brain and spine tumor surgeries. A board-certified neuropathologist - novice in the interpretation of SRH - assessed image quality by scoring subjective tumor infiltration and stated a diagnosis based on the SRH images. The diagnostic accuracy was determined by comparison to frozen hematoxylin-eosin (H&E)-stained sections and the ground truth defined as the definitive neuropathological diagnosis. The overall SRH imaging quality was rated high with the detection of tumor cells classified as inconclusive in only 4.2% of all images. The accuracy of neuropathological diagnosis based on SRH images was 87.7% and was non-inferior to the current standard of fast frozen H&E-stained sections (87.3 vs. 88.9%, p = 0.783). We found a substantial diagnostic correlation between SRH-based neuropathological diagnosis and H&E-stained frozen sections (κ = 0.8). The interpretability of intraoperative SRH imaging was demonstrated to be equivalent to the current standard method of H&E-stained frozen sections. Further research using this label-free innovative alternative vs. conventional staining is required to determine to which extent SRH-based intraoperative decision-making can be streamlined in order to facilitate the advancement of surgical neurooncology.

Identifiants

pubmed: 34890000
doi: 10.1007/s10143-021-01711-1
pii: 10.1007/s10143-021-01711-1
pmc: PMC8976804
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1721-1729

Subventions

Organisme : BMBF (German Ministry of Education and Research)
ID : 031L0260B

Informations de copyright

© 2021. The Author(s).

Références

Capper D, Jones DTW, Sill M, Hovestadt V, Schrimpf D, Sturm D, Koelsche C, Sahm F, Chavez L, Reuss DE, Kratz A, Wefers AK, Huang K, Pajtler KW, Schweizer L, Stichel D, Olar A, Engel NW, Lindenberg K, Harter PN, Braczynski AK, Plate KH, Dohmen H, Garvalov BK, Coras R, Hölsken A, Hewer E, Bewerunge-Hudler M, Schick M, Fischer R, Beschorner R, Schittenhelm J, Staszewski O, Wani K, Varlet P, Pages M, Temming P, Lohmann D, Selt F, Witt H, Milde T, Witt O, Aronica E, Giangaspero F, Rushing E, Scheurlen W, Geisenberger C, Rodriguez FJ, Becker A, Preusser M, Haberler C, Bjerkvig R, Cryan J, Farrell M, Deckert M, Hench J, Frank S, Serrano J, Kannan K, Tsirigos A, Brück W, Hofer S, Brehmer S, Seiz-Rosenhagen M, Hänggi D, Hans V, Rozsnoki S, Hansford JR, Kohlhof P, Kristensen BW, Lechner M, Lopes B, Mawrin C, Ketter R, Kulozik A, Khatib Z, Heppner F, Koch A, Jouvet A, Keohane C, Mühleisen H, Mueller W, Pohl U, Prinz M, Benner A, Zapatka M, Gottardo NG, Driever PH, Kramm CM, Müller HL, Rutkowski S, von Hoff K, Frühwald MC, Gnekow A, Fleischhack G, Tippelt S, Calaminus G, Monoranu C-M, Perry A, Jones C, Jacques TS, Radlwimmer B, Gessi M, Pietsch T, Schramm J, Schackert G, Westphal M, Reifenberger G, Wesseling P, Weller M, Collins VP, Blümcke I, Bendszus M, Debus J, Huang A, Jabado N, Northcott PA, Paulus W, Gajjar A, Robinson GW, Taylor MD, Jaunmuktane Z, Ryzhova M, Platten M, Unterberg A, Wick W, Karajannis MA, Mittelbronn M, Acker T, Hartmann C, Aldape K, Schüller U, Buslei R, Lichter P, Kool M, Herold-Mende C, Ellison DW, Hasselblatt M, Snuderl M, Brandner S, Korshunov A, von Deimling A, Pfister SM (2018) DNA methylation-based classification of central nervous system tumours. Nature 555:469–474. https://doi.org/10.1038/nature26000
doi: 10.1038/nature26000 pubmed: 29539639 pmcid: 6093218
Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Measur 20:37–46
doi: 10.1177/001316446002000104
Desroches J, Jermyn M, Mok K, Lemieux-Leduc C, Mercier J, St-Arnaud K, Urmey K, Guiot M-C, Marple E, Petrecca K (2015) Characterization of a Raman spectroscopy probe system for intraoperative brain tissue classification. Biomed Opt Express 6:2380–2397
doi: 10.1364/BOE.6.002380
Eichberg DG, Shah AH, Di L, Semonche AM, Jimsheleishvili G, Luther EM, Sarkiss CA, Levi AD, Gultekin SH, Komotar RJ (2019) Stimulated Raman histology for rapid and accurate intraoperative diagnosis of CNS tumors: prospective blinded study. J Neurosurg 134:137–143
doi: 10.3171/2019.9.JNS192075
Fountain DM, Bryant A, Barone DG, Waqar M, Hart MG, Bulbeck H, Kernohan A, Watts C, Jenkinson MD (2021) Intraoperative imaging technology to maximise extent of resection for glioma: a network meta‐analysis. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD013630.pub2
Freudiger CW, Min W, Saar BG, Lu S, Holtom GR, He C, Tsai JC, Kang JX, Xie XS (2008) Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy. Science 322:1857. https://doi.org/10.1126/science.1165758
doi: 10.1126/science.1165758 pubmed: 19095943 pmcid: 3576036
Freudiger CW, Yang W, Holtom GR, Peyghambarian N, Xie XS, Kieu KQ (2014) Stimulated Raman scattering microscopy with a robust fibre laser source. Nat Photonics 8:153–159. https://doi.org/10.1038/nphoton.2013.360
doi: 10.1038/nphoton.2013.360 pubmed: 25313312 pmcid: 4193905
Höhne J, Schebesch K-M, Zoubaa S, Proescholdt M, Riemenschneider MJ, Schmidt NO (2021) Intraoperative imaging of brain tumors with fluorescein: confocal laser endomicroscopy in neurosurgery. Clinical and user experience. Neurosurg Focus FOC 50:E19. https://doi.org/10.3171/2020.11.FOCUS20783
doi: 10.3171/2020.11.FOCUS20783
Hollon TC, Pandian B, Adapa AR, Urias E, Save AV, Khalsa SSS, Eichberg DG, D’Amico RS, Farooq ZU, Lewis S, Petridis PD, Marie T, Shah AH, Garton HJL, Maher CO, Heth JA, McKean EL, Sullivan SE, Hervey-Jumper SL, Patil PG, Thompson BG, Sagher O, McKhann GM, Komotar RJ, Ivan ME, Snuderl M, Otten ML, Johnson TD, Sisti MB, Bruce JN, Muraszko KM, Trautman J, Freudiger CW, Canoll P, Lee H, Camelo-Piragua S, Orringer DA (2020) Near real-time intraoperative brain tumor diagnosis using stimulated Raman histology and deep neural networks. Nat Med 26:52–58. https://doi.org/10.1038/s41591-019-0715-9
doi: 10.1038/s41591-019-0715-9 pubmed: 31907460 pmcid: 6960329
Jermyn M, Mercier J, Aubertin K, Desroches J, Urmey K, Karamchandiani J, Marple E, Guiot M-C, Leblond F, Petrecca K (2017) Highly accurate detection of cancer in situ with intraoperative, label-free, multimodal optical spectroscopy. Can Res 77:3942–3950
doi: 10.1158/0008-5472.CAN-17-0668
Ji M, Lewis S, Camelo-Piragua S, Ramkissoon SH, Snuderl M, Venneti S, Fisher-Hubbard A, Garrard M, Fu D, Wang AC (2015) Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy. Sci Transl Med 7:309ra163
doi: 10.1126/scitranslmed.aab0195
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
Louis DN, Wesseling P, Aldape K, Brat DJ, Capper D, Cree IA, Eberhart C, Figarella‐Branger D, Fouladi M, Fuller GN, Giannini C, Haberler C, Hawkins C, Komori T, Kros JM, Ng H, Orr BA, Park S, Paulus W, Perry A, Pietsch T, Reifenberger G, Rosenblum M, Rous B, Sahm F, Sarkar C, Solomon DA, Tabori U, Bent MJ, Deimling A, Weller M, White VA, Ellison DW (2020) cIMPACT‐NOW update 6: new entity and diagnostic principle recommendations of the cIMPACT‐Utrecht meeting on future CNS tumor classification and grading. Brain Pathol 30:844–856. https://doi.org/10.1111/bpa.12832
Martirosyan NL, Eschbacher JM, Kalani MYS, Turner JD, Belykh E, Spetzler RF, Nakaji P, Preul MC (2016) Prospective evaluation of the utility of intraoperative confocal laser endomicroscopy in patients with brain neoplasms using fluorescein sodium: experience with 74 cases. Neurosurg Focus FOC 40:E11. https://doi.org/10.3171/2016.1.FOCUS15559
doi: 10.3171/2016.1.FOCUS15559
Meyer M, Keith-Rokosh J, Reddy H, Megyesi J, Hammond RR (2010) Sources of error in neuropathology intraoperative diagnosis. Can J Neurol Sci 37:620–624. https://doi.org/10.1017/S0317167100010799
doi: 10.1017/S0317167100010799 pubmed: 21059508
Neidert N, Straehle J, Erny D, Sacalean V, El Rahal A, Steybe D, Schmelzeisen R, Vlachos A, Reinacher PC, Coenen VA, Mizaikoff B, Heiland DH, Prinz M, Beck J, Schnell O (2021) Stimulated Raman histology in the neurosurgical workflow of a major European neurosurgical center — part A (in press)
Orringer DA, Pandian B, Niknafs YS, Hollon TC, Boyle J, Lewis S, Garrard M, Hervey-Jumper SL, Garton HJL, Maher CO, Heth JA, Sagher O, Wilkinson DA, Snuderl M, Venneti S, Ramkissoon SH, McFadden KA, Fisher-Hubbard A, Lieberman AP, Johnson TD, Xie XS, Trautman JK, Freudiger CW, Camelo-Piragua S (2017) Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy. Nat Biomed Eng 1:0027. https://doi.org/10.1038/s41551-016-0027
doi: 10.1038/s41551-016-0027 pubmed: 28955599 pmcid: 5612414
Pekmezci M, Morshed RA, Chunduru P, Pandian B, Young J, Villanueva-Meyer JE, Tihan T, Sloan EA, Aghi MK, Molinaro AM, Berger MS, Hervey-Jumper SL (2021) Detection of glioma infiltration at the tumor margin using quantitative stimulated Raman scattering histology. Sci Rep 11:12162. https://doi.org/10.1038/s41598-021-91648-8
doi: 10.1038/s41598-021-91648-8 pubmed: 34108566 pmcid: 8190264
Raabe A, Beck J, Schucht P, Seidel K (2014) Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg 120:1015–1024
doi: 10.3171/2014.1.JNS13909
Ringel F, Ingerl D, Ott S, Meyer B (2009) VarioGuide: a new frameless image-guided stereotactic system —accuracy study and clinical assessment. Oper Neurosurg 64:ons365–ons373. https://doi.org/10.1227/01.NEU.0000341532.15867.1C
doi: 10.1227/01.NEU.0000341532.15867.1C
Seidel K, Schucht P, Beck J, Raabe A (2020) Continuous dynamic mapping to identify the corticospinal tract in motor eloquent brain tumors: an update. J Neurol Surg A Cent Eur Neurosurg 81:105–110
doi: 10.1055/s-0039-1698384
Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12:997–1003
doi: 10.1016/S1470-2045(11)70196-6
Stieglitz LH, Fichtner J, Andres R, Schucht P, Krähenbühl A-K, Raabe A, Beck J (2013) The silent loss of neuronavigation accuracy: a systematic retrospective analysis of factors influencing the mismatch of frameless stereotactic systems in cranial neurosurgery. Neurosurgery 72:796–807
doi: 10.1227/NEU.0b013e318287072d
Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen H-J (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol 7:392–401. https://doi.org/10.1016/S1470-2045(06)70665-9
doi: 10.1016/S1470-2045(06)70665-9 pubmed: 16648043
Tofte K, Berger C, Torp SH, Solheim O (2014) The diagnostic properties of frozen sections in suspected intracranial tumors: a study of 578 consecutive cases. Surg Neurol Int 5(1):170
doi: 10.4103/2152-7806.146153
Uematsu Y, Owai Y, Okita R, Tanaka Y, Itakura T (2007) The usefulness and problem of intraoperative rapid diagnosis in surgical neuropathology. Brain Tumor Pathol 24:47–52
doi: 10.1007/s10014-007-0219-z

Auteurs

Jakob Straehle (J)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.

Daniel Erny (D)

Institute of Neuropathology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Nicolas Neidert (N)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.
Microenvironment and Immunology Research Laboratory, Medical Center, University of Freiburg, Freiburg, Germany.

Dieter Henrik Heiland (DH)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.
Microenvironment and Immunology Research Laboratory, Medical Center, University of Freiburg, Freiburg, Germany.
Comprehensive Cancer Center Freiburg (CCCF), Faculty of Medicine and Medical Center, University of Freiburg, Freiburg, Germany.
German Cancer Consortium (DKTK), partner site Freiburg, Freiburg, Germany.
Medical Faculty of Freiburg University, Freiburg, Germany.

Amir El Rahal (A)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.

Vlad Sacalean (V)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.
Microenvironment and Immunology Research Laboratory, Medical Center, University of Freiburg, Freiburg, Germany.

David Steybe (D)

Department of Oral and Maxillofacial Surgery, Medical Center, University of Freiburg, Freiburg, Germany.

Rainer Schmelzeisen (R)

Medical Faculty of Freiburg University, Freiburg, Germany.
Department of Oral and Maxillofacial Surgery, Medical Center, University of Freiburg, Freiburg, Germany.

Andreas Vlachos (A)

Medical Faculty of Freiburg University, Freiburg, Germany.
Department of Neuroanatomy, Institute of Anatomy and Cell Biology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Basics in NeuroModulation (NeuroModulBasics), Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center Brain Links Brain Tools, University of Freiburg, Freiburg, Germany.

Boris Mizaikoff (B)

Institute of Analytical and Bioanalytical Chemistry, Ulm University, Ulm, Germany.
Hahn-Schickard Institute for Microanalysis Systems, Ulm, Germany.

Peter Christoph Reinacher (PC)

Medical Faculty of Freiburg University, Freiburg, Germany.
Department of Stereotactic and Functional Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.
Fraunhofer Institute for Laser Technology (ILT), Aachen, Germany.

Volker Arnd Coenen (VA)

Medical Faculty of Freiburg University, Freiburg, Germany.
Department of Stereotactic and Functional Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.

Marco Prinz (M)

Institute of Neuropathology, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Medical Faculty of Freiburg University, Freiburg, Germany.
Center for Basics in NeuroModulation (NeuroModulBasics), Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Freiburg, Germany.

Jürgen Beck (J)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany.
Comprehensive Cancer Center Freiburg (CCCF), Faculty of Medicine and Medical Center, University of Freiburg, Freiburg, Germany.
Medical Faculty of Freiburg University, Freiburg, Germany.
Center for Basics in NeuroModulation (NeuroModulBasics), Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Oliver Schnell (O)

Department of Neurosurgery, Medical Center, University of Freiburg, Freiburg, Germany. oliver.schnell@uniklinik-freiburg.de.
Medical Faculty of Freiburg University, Freiburg, Germany. oliver.schnell@uniklinik-freiburg.de.

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