ORIGINAL RESEARCH

Ambient MS profiling of meningiomas: intraoperative oncometabolite-based monitoring

Bormotov DS1, Shamraeva MA1, Kuzin AA1, Shamarina EV1, Eliferov VA1, Silkin SV1, Zhdanova EV1, Pekov SI2,3, Popov IA1
About authors

1 Moscow Institute of Physics and Technology, Dolgoprudny, Russia

2 Skoltech, Moscow, Russia

3 Siberian State Medical University, Tomsk, Russia

Correspondence should be addressed: Stanislav I. Pekov
Bolshoy Blvd., 30, стр. 1, 121205, Moscow, Russia; ur.ewrof@vokep.valsinats

About paper

Funding: The study was conducted as part of the state task of the Ministry of Science and Higher Education (agreement №075-00337-20-02. project № 0714- 2020-0006), using the equipment of the N. N. Semenov Federal Research Center for Chemical Physics of the Russian Academy of Sciences.

Author contribution: Bormotov DS — experiment, data analysis, manuscript editing; Shamraeva MA — data analysis, preparation of illustrations, manuscript writing; Kuzin AA — experiment; Shamarina EV — experiment, ion source development; Eliferov VA — ion source development; Silkin SV — experiments, data analysis; Zhdanova EV — data analysis; Pekov SI — study concept, manuscript writing; Popov IA — search for sources of funding, project management, manuscript editing.

Compliance with ethical standards: the study was approved by the Ethics Committee of N. N. Burdenko National Medical Research Center of Neurosurgery (protocols №40 of 12 April 2016 and №131 of 17 July 2018) and conducted in accordance with the Declaration of Helsinki (2000 and subsequent revisions). All patients signed a voluntary informed consent form to participate in the study with use of biomaterials for research purposes.

Received: 2022-11-27 Accepted: 2023-01-14 Published online: 2022-12-30
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  1. Islim AI, Mohan M, Moon RDC, Srikandarajah N, Mills SJ, Brodbelt AR, et al. Incidental intracranial meningiomas: a systematic review and meta-analysis of prognostic factors and outcomes. J Neurooncol. 2019; 142: 211–21. Available from: https://doi.org/10.1007/ s11060-019-03104-3.
  2. Ostrom QT, Patil N, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2013– 2017. Neuro Oncol. 2020; 22: iv1–96. Available from: https://doi. org/10.1093/neuonc/noaa200.
  3. Buerki RA, Horbinski CM, Kruser T, Horowitz PM, James CD, Lukas R v. An overview of meningiomas. Future Oncology. 2018; 14: 2161–77. Available from: https://doi.org/10.2217/fon-2018- 0006.
  4. Ogasawara C, Philbrick BD, Adamson DC. Meningioma: A Review of Epidemiology, Pathology, Diagnosis, Treatment, and Future Directions. Biomedicines. 2021; 9: 319. Available from: https://doi.org/10.3390/biomedicines9030319.
  5. Nguyen PX, Thi-Ngoc Doan H, van Vu H. Neuronavigation in falcine meningiomasare surgery: Initial results from a Vietnamese multi-center study. Annals of Medicine and Surgery. 2022: 104905. Available from: https://doi.org/10.1016/j.amsu.2022.104905.
  6. Bir SC, Konar SK, Maiti TK, Thakur JD, Guthikonda B, Nanda A. Utility of Neuronavigation in Intracranial Meningioma Resection: A Single-Center Retrospective Study. World Neurosurg. 2016; 90: 546-555.e1. Available from: https://doi.org/10.1016/j. wneu.2015.12.101.
  7. Stummer W, Koch R, Valle RD, Roberts DW, Sanai N, Kalkanis S, et al. Intraoperative fluorescence diagnosis in the brain: a systematic review and suggestions for future standards on reporting diagnostic accuracy and clinical utility. Acta Neurochir (Wien). 2019; 161: 2083–98. Available from: https://doi.org/10.1007/ s00701-019-04007-y.
  8. Ifa DR, Eberlin LS. Ambient ionization mass spectrometry for cancer diagnosis and surgical margin evaluation. Clin Chem. 2016; 62: 111–23. Available from: https://doi.org/10.1373/ clinchem.2014.237172.
  9. Kiritani S, Yoshimura K, Arita J, Kokudo T, Hakoda H, Tanimoto M, et al. A new rapid diagnostic system with ambient mass spectrometry and machine learning for colorectal liver metastasis. BMC Cancer. 2021; 21: 262. Available from: https://doi.org/10.1186/s12885- 021-08001-5.
  10. Huang Y-C, Chung H-H, Dutkiewicz EP, Chen C-L, Hsieh H-Y, Chen B-R, et al. Predicting Breast Cancer by Paper Spray Ion Mobility Spectrometry Mass Spectrometry and Machine Learning. Anal Chem. 2020; 92: 1653–7. Available from: https://doi. org/10.1021/acs.analchem.9b03966.
  11. Phelps DL, Balog J, Gildea LF, Bodai Z, Savage A, El-Bahrawy MA, et al. The surgical intelligent knife distinguishes normal, borderline and malignant gynaecological tissues using rapid evaporative ionisation mass spectrometry (REIMS). Br J Cancer. 2018; 118: 1349–58. Available from: https://doi.org/10.1038/s41416-018- 0048-3.
  12. Ogrinc N, Attencourt C, Colin E, Boudahi A, Tebbakha R, Salzet M, et al. Mass Spectrometry-Based Differentiation of Oral Tongue Squamous Cell Carcinoma and Nontumor Regions With the SpiderMass Technology. Frontiers in Oral Health. 2022; 3. Available from: https://doi.org/10.3389/froh.2022.827360.
  13. Pekov SI, Bormotov DS, Nikitin PV, Sorokin AA, Shurkhay VA, Eliferov VA, et al. Rapid estimation of tumor cell percentage in brain tissue biopsy samples using inline cartridge extraction mass spectrometry. Anal Bioanal Chem. 2021; 413: 2913–22. Available from: https://doi.org/10.1007/s00216-021-03220-y.
  14. Eberlin LS, Dill AL, Golby AJ, Ligon KL, Wiseman JM, Cooks RG, et al. Discrimination of human astrocytoma subtypes by lipid analysis using desorption electrospray ionization imaging mass spectrometry. Angewandte Chemie — International Edition. 2010; 49: 5953–6. Available from: https://doi.org/10.1002/ anie.201001452.
  15. Pirro V, Llor RS, Jarmusch AK, Alfaro CM, Cohen-Gadol AA, Hattab EM, et al. Analysis of human gliomas by swab touch spray-mass spectrometry: Applications to intraoperative assessment of surgical margins and presence of oncometabolites. Analyst. 2017; 142: 4058–66. Available from: https://doi.org/10.1039/ c7an01334e.
  16. Jarmusch AK, Pirro V, Baird Z, Hattab EM, Cohen-Gadol AA, Cooks RG. Lipid and metabolite profiles of human brain tumors by desorption electrospray ionization-MS. Proceedings of the National Academy of Sciences. 2016; 113: 1486–91. Available from: https://doi.org/10.1073/pnas.1523306113.
  17. Pekov SI, Eliferov VA, Sorokin AA, Shurkhay VA, Zhvansky ES, Vorobyev AS, et al. Inline cartridge extraction for rapid brain tumor tissue identification by molecular profiling. Sci Rep. 2019; 9: 18960. Available from: https://doi.org/10.1038/s41598-019- 55597-7.
  18. Pirro V, Jarmusch AK, Alfaro CM, Hattab EM, Cohen-Gadol AA, Cooks RG. Utility of neurological smears for intrasurgical brain cancer diagnostics and tumour cell percentage by DESI-MS. Analyst. 2017; 142: 449–54. Available from: https://doi. org/10.1039/c6an02645a.
  19. Keating MF, Zhang J, Feider CL, Retailleau S, Reid R, Antaris A, et al. Integrating the MasSpec Pen to the da Vinci Surgical System for in Vivo Tissue Analysis during a Robotic Assisted Porcine Surgery. Anal Chem. 2020; 92: 11535–42. Available from: https:// doi.org/10.1021/acs.analchem.0c02037.
  20. Shamraeva MA, Pekov SI, Bormotov DS, Levin RE, Larina IM, Nikolaev EN, et al. The lightweight spherical samplers for simplified collection, storage, and ambient ionization of drugs from saliva and blood. Acta Astronaut. 2022; 195: 556–60. Available from: https://doi.org/10.1016/j.actaastro.2022.03.026.
  21. Shamraeva MA, Bormotov DS, Shamarina EV, Bocharov KV, Peregudova OV, Pekov SI, et al. Spherical Sampler Probes Enhance the Robustness of Ambient Ionization Mass Spectrometry for Rapid Drugs Screening. Molecules. 2022; 27: 945. Available from: https://doi.org/10.3390/molecules27030945.
  22. Chagovets V, Wang Z, Kononikhin A, Starodubtseva N, Borisova A, Salimova D, et al. A Comparison of Tissue Spray and Lipid Extract Direct Injection Electrospray Ionization Mass Spectrometry for the Differentiation of Eutopic and Ectopic Endometrial Tissues. J Am Soc Mass Spectrom. 2017: 6–8. Available from: https://doi. org/10.1007/s13361-017-1792-y.
  23. Adamyan L, Starodubtseva N, Borisova A, Stepanian A, Chagovets V, Salimova D, et al. Direct Mass Spectrometry Differentiation of Ectopic and Eutopic Endometrium in Patients with Endometriosis. J Minim Invasive Gynecol. 2017. Available from: https://doi.org/10.1016/j.jmig.2017.08.658.
  24. Hutchins PD, Russell JD, Coon JJ. LipiDex: An Integrated Software Package for High-Confidence Lipid Identification. Cell Syst. 2018; 6: 621–5.e5. Available from: https://doi.org/10.1016/j. cels.2018.03.011.
  25. Bogner-Strauss JG. N-acetylaspartate metabolism outside the brain: Lipogenesis, histone acetylation, and cancer. Front Endocrinol (Lausanne). 2017; 8: 1–5. Available from: https://doi. org/10.3389/fendo.2017.00240.
  26. Pirro V, Alfaro CM, Jarmusch AK, Hattab EM, Cohen-Gadol AA, Cooks RG. Intraoperative assessment of tumor margins during glioma resection by desorption electrospray ionization-mass spectrometry. Proceedings of the National Academy of Sciences. 2017; 114: 201706459. Available from: https://doi.org/10.1073/ pnas.1706459114.