Terahertz Spectroscopy of Mouse Blood Serum in the Dynamics of Experimental Glioblastoma
Paper #8990 received 3 Apr 2023; accepted for publication 21 Jun 2023; published online 15 Aug 2023
Abstract
In this study terahertz (THz) absorption spectra of mouse blood serum in the dynamics of experimental U87 glioblastoma were investigated. Decrease of THz absorption with glioma growth was demonstrated. A two-component Debye model was used to analyze the experimental data. Analysis of the complex dielectric permittivity parameters of blood serum indicates an increase in the proportion of bound water in the samples in the dynamics of tumor growth.
Keywords
Full Text:
PDFReferences
1. Q. T. Ostrom, G. Cioffi, K. Waite, C. Kruchko, and J. C. Barnholtz-Sloan, “CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2014–2018,” Neuro-Oncology, 23(Supplement S3), iii1–iii105 (2021).
2. T. Tykocki, M. Eltayeb, “Ten-year survival in glioblastoma. A systematic review,” Journal of Clinical Neuroscience 54, 7–13 (2018).
3. M. Hishii, T. Matsumoto, and H. Arai, “Diagnosis and Treatment of Early-Stage Glioblastoma,” Asian Journal of Neurosurgery 14(2), 589–592 (2019).
4. L. Wang, X. Liu, and Q. Yang, “Application of Metabolomics in Cancer Research: As a Powerful Tool to Screen Biomarker for Diagnosis, Monitoring and Prognosis of Cancer,” Biomarkers Journal 4(3), 12 (2018).
5. V. Poinsignon, L. Mercier, K. Nakabayashi, M. D. David, A. Lalli, V. Penard- Lacronique, C. Quivoron, V. Saada, S. D. Botton, S. Broutin, and A. Paci, “Quantitation of isocitrate dehydrogenase (IDH)-induced D and L enantiomers of 2-hydroxyglutaric acid in biological fluids by a fully validated liquid tandem mass spectrometry method, suitable for clinical applications,” Journal of Chromatography B 1022, 290–297 (2016).
6. M. Touat, A. Duran-Peña, A. Alentorn, L. Lacroix, C. Massard, and A. Idbaih, “Emerging circulating biomarkers in glioblastoma: promises and challenges,” Expert Reviews 15(10), 1311–1323 (2015).
7. E. Miyauchi, T. Furuta, S. Ohtsuki, M. Tachikawa, Y. Uchida, H. Sabit, W. Obuchi, T. Baba, M. Watanabe, T. Terasaki, and M. Nakada, “Identification of blood biomarkers in glioblastoma by SWATH mass spectrometry and quantitative targeted absolute proteomics,” PLoS ONE 13(3), e0193799 (2018).
8. E. Baranovičová, T. Galanda, M. Galanda, J. Hatok, B. Kolarovszki, R. Richterová, and P. Račay, “Metabolomic profiling of blood plasma in patients with primary brain tumours: Basal plasma metabolites correlated with tumour grade and plasma biomarker analysis predicts feasibility of the successful statistical discrimination from healthy subjects – a preliminary study,” IUBMB Life 71(12), 1994–2002 (2019).
9. J. E. Lee, S. S. Jeun, S. H. Kim, C. Y. Yoo, H.-M. Baek, and S. H. Yang, “Metabolic profiling of human gliomas assessed with NMR,” Journal of Clinical Neuroscience 68, 275–280 (2019).
10. J. M. Figueroa, “Detection of glioblastoma in biofluids,” Journal of Neurosurgery 129(2), 334–340 (2018).
11. O. Cherkasova, Y. Peng, M. Konnikova, Y. Kistenev, C. Shi, D. Vrazhnov, O. Shevelev, E. Zavjalov, S. Kuznetsov, and A. Shkurinov, “Diagnosis of Glioma Molecular Markers by Terahertz Technologies,” Photonics 8(1), 22 (2021).
12. H. J. Butler, P. M. Brennan, J. M. Cameron, D. Finlayson, M. G. Hegarty, M. D. Jenkinson, D. S. Palmer, B. R. Smith, and M. J. Baker, “Development of high-throughput ATR-FTIR technology for rapid triage of brain cancer,” Nature Communications 10, 4501 (2019).
13. A. G. Theakstone, P. M. Brennan, M. D. Jenkinson, S. J. Mills, K. Syed, C. Rinaldi, Y. Xu, R. Goodacre, H. J. Butler, D. S. Palmer, B. R. Smith, and M. J. Baker, “Rapid Spectroscopic Liquid Biopsy for the Universal Detection of Brain Tumours,” Cancers 13(15), 3851 (2021).
14. G. R. Musina, P. V. Nikitin, N. V. Chernomyrdin, I. N. Dolganova, A. A. Gavdush, G. A. Komandin, D. S. Ponomarev, A. A. Potapov, I. V. Reshetov, V. V. Tuchin, and K. I. Zaytsev, “Prospects of terahertz technology in diagnosis of human brain tumors – a review,” Journal of Biomedical Photonics & Engineering 6(2), 020201 (2020).
15. O. A. Smolyanskaya, N. V. Chernomyrdin, A. A. Konovko, K. I. Zaytsev, I. A. Ozheredov, O. P. Cherkasova, M. M. Nazarov, J.-P. Guillet, S. A. Kozlov, Yu. V. Kistenev, J.-L. Coutaz, P. Mounaix, V. L. Vaks, J.-H. Son, H. Cheon, V. P. Wallace, Yu. Feldman, I. Popov, and V. V. Tuchin, “Terahertz biophotonics as a tool for studies of dielectric and spectral properties of biological tissues and liquids,” Progress in Quantum Electronics 62, 1–77 (2018).
16. K. I. Zaytsev, I. N. Dolganova, N. V. Chernomyrdin, G. M. Katyba, A. A. Gavdush, O. P. Cherkasova, G. A. Komandin, M. A. Shchedrina, A. N. Khodan, D. S. Ponomarev, I. V. Reshetov, V. E. Karasik, M. Skorobogatiy, V.N. Kurlov, and V. V. Tuchin, “The progress and perspectives of terahertz technology for diagnosis of neoplasms: A review,” Journal of Optics 22(1), 013001 (2020).
17. K. P. Cheung, D. H. Auston, “A novel technique for measuring far-infrared absorption and dispersion,” Infrared Physics 26(1), 23–27 (1986).
18. D. Grischkowsky, S. Keiding, M. van Exter, and Ch. Fattinger, “Far-infrared time-domain spectroscopy with terahertz beams of dielectrics and semiconductors,” Journal of the Optical Society of America B 7(10), 2006–2015 (1990).
19. O. Cherkasova, M. Nazarov, and A. Shkurinov, “Noninvasive blood glucose monitoring in the terahertz frequency range,” Optical and Quantum Electronics 48(3), 217 (2016).
20. A. Gavdush, N. Chernomyrdin, K. Malakhov, S.-I. Beshplav, I. Dolganova, A. Kosyrkova, P. Nikitin, G. Musina, G. Katyba, I. Reshetov, O. Cherkasova, G. Komandin, V. Karasik, A. Potapov, V. Tuchin, and K. Zaytsev, “Terahertz spectroscopy of gelatin-embedded human brain gliomas of different grades: a road toward intraoperative THz diagnosis,” Journal of Biomedical Optics 24(2), 027001 (2019).
21. A. A. Gavdush, N. V. Chernomyrdin, G. A. Komandin, I. N. Dolganova, P. V. Nikitin, G. R. Musina, G. M. Katyba, A. S. Kucheryavenko, I. V. Reshetov, A. A. Potapov, V. V. Tuchin, and K. I. Zaytsev, “Terahertz dielectric spectroscopy of human brain gliomas and intact tissues ex vivo: double-Debye and double-overdamped-oscillator models of dielectric response,” Biomedical Optics Express 12(1), 69–83 (2020).
22. S. J. Oh, S.-H. Kim, Y. B. Ji, K. Jeong, Y. Park, J. Yang, D. W. Park, S. K. Noh, S.-G. Kang, Y.-M. Huh, J.-H. Son, and J.-S. Suh, “Study of freshly excised brain tissues using terahertz imaging,” Biomedical Optics Express 5(8), 2837–2842 (2014).
23. K. Meng, T.-N. Chen, T. Chen, L.-G. Zhu, Q. Liu, Z. Li, F. Li, S.-C. Zhong, Z.-R. Li, H. Feng, and J.-H. Zhao, “Terahertz pulsed spectroscopy of paraffin-embedded brain glioma,” Journal of Biomedical Optics 19(7), 077001 (2014).
24. S. Yamaguchi, Y. Fukushi, O. Kubota, T. Itsuji, T. Ouchi, and S. Yamamoto, “Brain tumor imaging of rat fresh tissue using terahertz spectroscopy,” Scientific Reports 6, 30124 (2016).
25. L. Wu, D. Xu, Y. Wang, B. Liao, Z. Jiang, L. Zhao, Z. Sun, N. Wu, T. Chen, H. Feng, and J. Yao, “Study of in vivo brain glioma in a mouse model using continuous-wave terahertz reflection imaging,” Biomedical Optics Express 10(8), 3953–3962 (2019).
26. Y. B. Ji, S. J. Oh, S.-G. Kang, J. Heo, S.-H. Kim, Y. Choi, S. Song, H. Y. Son, S. H. Kim, J. H. Lee, S. J. Haam, Y. M. Huh, J. H. Chang, C. Joo, and J.-S. Suh, “Terahertz reflectometry imaging for low and high grade gliomas,” Scientific Reports 6, 36040 (2016).
27. L. Wu, Y. Wang, B. Liao, L. Zhao, K. Chen, M. Ge, H. Li, T. Chen, H. Feng, D. Xu, and J. Yao, “Temperature dependent terahertz spectroscopy and imaging of orthotopic brain gliomas in mouse models,” Biomedical Optics Express 13(1), 93–104 (2022).
28. A. S. Kucheryavenko, N. V. Chernomyrdin, A. A. Gavdush, A. I. Alekseeva, P. V. Nikitin, I. N. Dolganova, P. A. Karalkin, A. S. Khalansky, I. E. Spektor, M. Skorobogatiy, V. V. Tuchin, and K. I. Zaytsev, “Terahertz dielectric spectroscopy and solid immersion microscopy of ex vivo glioma model 101.8: brain tissue heterogeneity,” Biomedical Optics Express 12(8), 5272–5289 (2021).
29. A. G. Kamkin, A. A. Kamensky (Eds.), Fundamental and Clinical Physiology, Training manual, The Academy Moscow (2004). ISBN: 5-7695-1675-5.
30. O. P. Cherkasova, M. M. Nazarov, and A. P. Shkurinov, “Study of blood and its components by terahertz pulsed spectroscopy,” EPJ Web of Conferences 195, 10003 (2018).
31. M. M. Nazarov, O. P. Cherkasova, E. N. Lazareva, A. B. Bucharskaya, N. A. Navolokin, V. V. Tuchin, and A. P. Shkurinov, “A complex study of the peculiarities of blood serum absorption of rats with experimental liver cancer,” Optics and Spectroscopy 126(6), 721–729 (2019).
32. M. R. Konnikova, O. P. Cherkasova, M. M. Nazarov, D. A. Vrazhnov, Yu. V. Kistenev, S. E. Titov, E. V. Kopeikina, S. P. Shevchenko, and A. P. Shkurinov, “Malignant and benign thyroid nodule differentiation through the analysis of blood plasma with terahertz spectroscopy,” Biomedical Optics Express 12(2), 1020–1035 (2021).
33. J. A. Koutcher, X. Hu, S. Xu, T. P. Gade, N. Leeds, X. J. Zhou, D. Zagzag, and E. S. Holland, “MRI of Mouse Models for Gliomas Shows Similarities to Humans and Can Be Used to Identify Mice for Preclinical Trials,” Neoplasia 4(6), 480–485 (2002).
34. E. L. Zavjalov, I. A. Razumov, L. A. Gerlinskaya, and A. V. Romashchenko, “In vivo MRI Visualization of U87 Glioblastoma Development Dynamics in the Model of Orthotopic Xenotransplantation to the SCID Mouse,” Russian Journal of Genetics: Applied Research 6, 448–453 (2016).
35. M. M. Nazarov, A. P. Shkurinov, E. A. Kuleshov, and V. V. Tuchin, “Terahertz time-domain spectroscopy of biological tissues,” Quantum Electronics 38(7), 647 (2008).
36. O. P. Cherkasova, M. M. Nazarov, A. P. Shkurinov, and V. I. Fedorov, “Terahertz spectroscopy of biological molecules,” Radiophysics and Quantum Electronics 52(7), 518–523 (2009).
37. M. M. Nazarov, O. P. Cherkasova, and A. P. Shkurinov, “A Comprehensive Study of Albumin Solutions in the Extended Terahertz Frequency Range,” Journal of Infrared, Millimeter, and Terahertz Waves 39, 840–853 (2018).
38. M. R. Konnikova, O. P. Cherkasova, T. A. Geints, E. S. Dizer, A. A. Man’kova, I. S. Vasilievskii, A. A. Butylin, Yu. V. Kistenev, V. V. Tuchin, and A. P. Shkurinov, “Study of adsorption of the SARS-CoV-2 virus spike protein by vibrational spectroscopy using terahertz metamaterials,” Quantum Electronics 52(1), 2 (2022).
39. D. Vrazhnov, A. Knyazkova, M. Konnikova, O. Shevelev, I. Razumov, E. Zavjalov, Y. Kistenev, A. Shkurinov, and O. Cherkasova, “Analysis of Mouse Blood Serum in the Dynamics of U87 Glioblastoma by Terahertz Spectroscopy and Machine Learning,” Applied Sciences 12(20), 10533 (2022).
40. O. B. Shevelev, A. A. Seryapina, E. L. Zavjalov, L. A. Gerlinskaya, T. N. Goryachkovskaya, N. M. Slynko, L. V. Kuibida, S. E. Peltek, A. L. Markel, and M. P. Moshkin, “Hypotensive and neurometabolic effects of intragastric Reishi (Ganoderma lucidum) administration in hypertensive ISIAH rat strain,” Phytomedicine 41, 1–6 (2018).
41. M. Nazarov, A. Shkurinov, V. V. Tuchin, and X.-C. Zhang, Handbook of Photonics for Biomedical Science. Series in Medical Physics and Biomedical Engineering, V. V. Tuchin (Ed.), 1st ed., CRC Press, Boca Raton (2010). ISBN: 9780429131271.
42. T.-F. Tseng, B. You, H.-C. Gao, T.-D. Wang, and C.-K. Sun, “Pilot clinical study to investigate the human whole blood spectrum characteristics in the sub-THz region,” Optics Express 23(7), 9440–9451 (2015).
43. O. P. Cherkasova, M. M. Nazarov, A. A. Angeluts, and A. P. Shkurinov, “Analysis of blood plasma at terahertz frequencies,” Optics and Spectroscopy 120, 50–57 (2016).
44. O. P. Cherkasova, M. M. Nazarov, I. N. Smirnova, A. A. Angeluts, and A. P. Shkurinov, “Application of time-domain THz spectroscopy for studying blood plasma of rats with experimental diabetes,” Physics of Wave Phenomena 22, 185–188 (2014).
45. Y. Wang, G. Wang, D. Xu, B. Jiang, M. Ge, L. Wu, C. Yang, N. Mu, S. Wang, C. Chang, T. Chen, H. Feng, and J. Yao, “Terahertz spectroscopic diagnosis of early blast-induced traumatic brain injury in rats,” Biomedical Optics Express 11(8), 4085–4098 (2020).
46. D. Vrazhnov, A. Mankova, E. Stupak, Y. Kistenev, A. Shkurinov, and O. Cherkasova, “Discovering Glioma Tissue through Its Biomarkers’ Detection in Blood by Raman Spectroscopy and Machine Learning,” Pharmaceutics 15(1), 203 (2023).
47. M. M. Nazarov, O. P. Cherkasova, and A. P. Shkurinov, “Study of the dielectric function of aqueous solutions of glucose and albumin by THz time-domain spectroscopy,” Quantum Electronics 46 (6), 488 (2016).
48. O. Cherkasova, M. Nazarov, and A. Shkurinov, “Properties of aqueous solutions in THz frequency range,” Journal of Physics: Conference Series 793(1), 012005 (2017).
49. O. P. Cherkasova, M. M. Nazarov, M. R. Konnikova, and A. P. Shkurinov, “THz Spectroscopy of Bound Water in Glucose: Direct Measurements from Crystalline to Dissolved State,” Journal of Infrared, Millimeter, and Terahertz Waves 41, 1057–1068 (2020).
50. H. Yada, M. Nagai, and K. Tanaka, “Origin of the fast relaxation component of water and heavy water revealed by terahertz time-domain attenuated total reflection spectroscopy,” Chemical Physics Letters 464 (4–6), 166–170 (2009).
© 2014-2023 Samara National Research University. All Rights Reserved.
Public Media Certificate (RUS). 12+