Journal of the European Optical Society-Rapid Publications, Volume. 19, Issue 1, 2023028(2023)

Brillouin scattering spectroscopy for studying human anatomy: Towards in situ mechanical characterization of soft tissue

Paata Pruidze1,2, Elena Chayleva3, Wolfgang J. Weninger1,2, and Kareem Elsayad1,2、*
Author Affiliations
  • 1Division of Anatomy, Center for Anatomy and Cell Biology, Medical University of Vienna, 1090 Vienna, Austria
  • 2Medical Imaging Cluster (MIC), Medical University of Vienna, 1090 Vienna, Austria
  • 3Max Perutz Laboratories, University of Vienna, 1030 Vienna, Austria
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    [1] N.M.E. Ayad, S. Kaushik, V.M. Weaver. Tissue mechanics, an important regulator of development and disease. Philos. Trans. Roy. Soc. B: Biol. Sci., 374, 20180215(2019).

    [2] K. Mukund, S. Subramaniam. Skeletal muscle: A review of molecular structure and function, in health and disease. WIREs Syst. Biol. Med., 12, e1462(2020).

    [3] N.A. Shirwany, M.-H. Zou. Arterial stiffness: A brief review. Acta Pharmacol. Sin., 31, 1267-1276(2010).

    [4] B. Spronck, J.D. Humphrey. Arterial stiffness: Different metrics, different meanings. J. Biomech. Eng., 141, 0910041-09100412(2019).

    [5] L.E. Bilston, K. Tan. Measurement of passive skeletal muscle mechanical properties in vivo: Recent progress, clinical applications, and remaining challenges. Ann. Biomed. Eng., 43, 261-273(2015).

    [6] B.F. Kennedy, P. Wijesinghe, D.D. Sampson. The emergence of optical elastography in biomedicine. Nat. Photon., 11, 215-221(2017).

    [7] G. Scarcelli, S.H. Yun. Confocal Brillouin microscopy for three-dimensional mechanical imaging. Nat. Photon., 2, 39-43(2007).

    [8] G. Antonacci, T. Beck, A. Bilenca, J. Czarske, K. Elsayad, J. Guck, K. Kim, B. Krug, F. Palombo, R. Prevedel, G. Scarcelli. Recent progress and current opinions in Brillouin microscopy for life science applications. Biophys. Rev., 12, 615-624(2020).

    [9] C. Poon, J. Chou, M. Cortie, I. Kabakova. Brillouin imaging for studies of micromechanics in biology and biomedicine: from current state-of-the-art to future clinical translation. J. Phys.: Photon., 3, 012002(2021).

    [10] K. Elsayad, S. Polakova, J. Gregan. Probing mechanical properties in biology using Brillouin microscopy. Trends Cell Biol., 29, 608-611(2019).

    [11] S. Mattana, S. Caponi, F. Tamagnini, D. Fioretto, F. Palombo. Viscoelasticity of amyloid plaques in transgenic mouse brain studied by Brillouin microspectroscopy and correlative Raman analysis. J. Innov. Opt. Health Sci., 10, 1742001(2017).

    [12] G. Antonacci, R.M. Pedrigi, A. Kondiboyina, V.V. Mehta, R. De Silva, C. Paterson, R. Krams, P. Török. Quantification of plaque stiffness by Brillouin microscopy in experimental thin cap fibroatheroma. J. R. Soc. Interf., 12, 20150843(2015).

    [13] D. Cikes, K. Elsayad, E. Sezgin, E. Koitai, T. Ferenc, M. Orthofer, R. Yarwood, L.X. Heinz, V. Sedlyarov, N.D. Miranda, A. Taylor, S. Grapentine, F. al-Murshedi, A. Abott, A. Weidinger, C. Kutchukian, C. Sanchez, S.J.F. Cronin, M. Novatchkova, A. Kavirayani, T. Schuetz, B. Haubner, L. Haas, A. Hagelkruys, S. Jackowski, A. Kozlov, V. Jacquemond, C. Knauf, G. Superti-Furga, E. Rullman, T. Gustafsson, J. McDermot, M. Lowe, Z. Radak, J.S. Chamberlain, M. Bakovic, S. Banka, J.M. Penninger. Critical role of PCYT2 in muscle health and aging. bioRxiv(2022).

    [14] C. Conrad, K.M. Gray, K.M. Stroka, I. Rizvi, G. Scarcelli. Mechanical characterization of 3D ovarian cancer nodules using Brillouin confocal microscopy. Cell Mol. Bioeng., 12, 215-226(2019).

    [15] J. Rix, O. Uckermann, K. Kirsche, G. Schackert, E. Koch, M. Kirsch, R. Galli. Correlation of biomechanics and cancer cell phenotype by combined Brillouin and Raman spectroscopy of U87-MG glioblastoma cells. J. Roy. Soc. Interf., 19, 20220209(2022).

    [16] J. Zhang, R. Raghunathan, J. Rippy, C. Wu, R.H. Finnell, K.V. Larin, G. Scarcelli. Tissue biomechanics during cranial neural tube closure measured by Brillouin microscopy and optical coherence tomography. Birth Defects Res., 111, 991-998(2019).

    [17] R.J.J. Rioboó, N. Gontán, D. Sanderson, M. Desco, M.V. Gómez-Gaviro. Brillouin spectroscopy: From biomedical research to new generation pathology diagnosis. Int. J. Mol. Sci., 22, 8055(2021).

    [18] M. Troyanova-Wood, Z. Meng, V.V. Yakovlev. Differentiating melanoma and healthy tissues based on elasticity-specific Brillouin microspectroscopy. Biomed. Opt. Express, 10, 1774-1781(2019).

    [19] S. Besner, G. Scarcelli, R. Pineda, S.H. Yun. In vivo Brillouin analysis of the aging crystalline lens. Invest. Ophthalmol. Vis. Sci., 57, 5093-5100(2016).

    [20] G. Scarcelli, S.H. Yun. In vivo Brillouin optical microscopy of the human eye. Opt. Express, 20, 9197-9202(2012).

    [21] I. Kabakova, Y. Xiang, C. Paterson, P. Török. Fiber-integrated Brillouin microspectroscopy: Towards Brillouin endoscopy. J. Innov. Opt. Health Sci., 10, 1742002(2017).

    [22] B.J. Berne, R. Pecora. Dynamic light scattering: With applications to chemistry, biology, and physics(2000).

    [23] F. Palombo, D. Fioretto. Brillouin light scattering: Applications in biomedical sciences. Chem. Rev., 119, 7833-7847(2019).

    [24] F. Palombo, C.P. Winlove, R.S. Edginton, E. Green, N. Stone, S. Caponi, M. Madami, D. Fioretto. Biomechanics of fibrous proteins of the extracellular matrix studied by Brillouin scattering. J. R. Soc. Interf., 11, 20140739(2014).

    [25] P.J. Wu, I.V. Kabakova, J.W. Ruberti, J.M. Sherwood, I.E. Dunlop, C. Paterson, P. Török, D.R. Overby. Water content, not stiffness, dominates Brillouin spectroscopy measurements in hydrated materials. Nat. Methods, 15, 561-562(2018).

    [26] O.G. Andriotis, K. Elsayad, D.E. Smart, M. Nalbach, D.E. Davies, P.J. Thurner. Hydration and nanomechanical changes in collagen fibrils bearing advanced glycation end-products. Biomed. Opt. Express, 10, 1841-1855(2019).

    [27] M. Bailey, M. Alunni-Cardinali, N. Correa, S. Caponi, T. Holsgrove, H. Barr, N. Stone, C.P. Winlove, D. Fioretto, F. Palombo. Viscoelastic properties of biopolymer hydrogels determined by Brillouin spectroscopy: A probe of tissue micromechanics. Science, Advances, 6, eabc1937(2020).

    [28] S.V. Adichtchev, Y.A. Karpegina, K.A. Okotrub, M.A. Surovtseva, V.A. Zykova, N.V. Surovtsev. Brillouin spectroscopy of biorelevant fluids in relation to viscosity and solute concentration. Phys. Rev. E, 99, 062410(2019).

    [29] G. Scarcelli, S. Kling, E. Quijano, R. Pineda, S. Marcos, S.H. Yun. Brillouin microscopy of collagen crosslinking: noncontact depth-dependent analysis of corneal elastic modulus. Invest. Ophthalmol. Vis. Sci., 54, 1418-1425(2013).

    [30] N.J. Tao, S.M. Lindsay, A. Rupprecht. Dynamic coupling between DNA and its primary hydration shell studied by Brillouin scattering. Biopolymers, 27, 1655-1671(1988).

    [31] S.A. Lee, S.M. Lindsay, J.W. Powell, T. Weidlich, N.J. Tao, G.D. Lewen, A. Rupprecht. A Brillouin scattering study of the hydration of Li- and Na-DNA films. Biopolymers, 26, 1637-1665(1987).

    [32] G. Scarcelli, W.J. Polacheck, H.T. Nia, K. Patel, A.J. Grodzinsky, R.D. Kamm, S.H. Yun. Noncontact three-dimensional mapping of intracellular hydromechanical properties by Brillouin microscopy. Nat. Methods, 12, 1132-1134(2015).

    [33] M. Samalova, K. Elsayad, A. Melnikava, A. Peaucelle, E. Gahurova, J. Gumulec, I. Spyroglou, E.V. Zemlyanskaya, E.V. Ubogoeva, J. Hejatko. Expansin-controlled cell wall stiffness regulates root growth in Arabidopsis. bioRxiv(2020).

    [34] R. Pethig, D.B. Kell. The passive electrical properties of biological systems: their significance in physiology, biophysics and biotechnology. Phys. Med. Biol., 32, 933(1987).

    [35] A. Carlton, R.M. Orr. The effects of fluid loss on physical performance: A critical review. J. Sport Health Sci., 4, 357-363(2015).

    [36] K.F.A. Ross, R.E. Gordon. Water in malignant tissue, measured by cell refractometry and nuclear magnetic resonance. J. Microscopy, 128, 7-21(1982).

    [37] N.M. Lacevic, J.E. Sader. Viscoelasticity of glycerol at ultra-high frequencies investigated via molecular dynamics simulations. J. Chem. Phys., 144, 054502(2016).

    [38] I. Remer, R. Shaashoua, N. Shemesh, A. Ben-Zvi, A. Bilenca. High-sensitivity and high-specificity biomechanical imaging by stimulated Brillouin scattering microscopy. Nat. Methods, 17, 913-916(2020).

    [39] B. Krug, N. Koukourakis, J.W. Czarske. Impulsive stimulated Brillouin microscopy for non-contact, fast mechanical investigations of hydrogels. Opt. Express, 27, 26910-26923(2019).

    [40] K. Elsayad, S. Werner, M. Gallemí, J. Kong, E.R. Sánchez Guajardo, L. Zhang, Y. Jaillais, T. Greb, Y. Belkhadir. Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission-Brillouin imaging. Sci. Signal, 9, rs5(2016).

    [41] Z. Meng, A.J. Traverso, V.V. Yakovlev. Background clean-up in Brillouin microspectroscopy of scattering medium. Opt. Express, 22, 5410-5415(2014).

    [42] E. Edrei, M.C. Gather, G. Scarcelli. Integration of spectral coronagraphy within VIPA-based spectrometers for high extinction Brillouin imaging. Opt. Express, 25, 6895-6903(2017).

    [43] R. Khan, B. Gul, S. Khan, H. Nisar, I. Ahmad. Refractive index of biological tissues: Review, measurement techniques, and applications. Photodiagn. Photodyn. Ther., 33, 102192(2021).

    [44] A.-D. Annexes. Adult reference computational phantoms. Ann. ICRP, 39, 47-70(2009).

    [45] F.P. Bolin, L.E. Preuss, R.C. Taylor, R.J. Ference. Refractive index of some mammalian tissues using a fiber optic cladding method. Appl. Opt., 28, 2297-2303(1989).

    [46] S. Gelman, D.S. Warner, M.A. Warner. Venous function and central venous pressure: A physiologic story. Anesthesiology, 108, 735-748(2008).

    [47] I.V. Ogneva, D.V. Lebedev, B.S. Shenkman. Transversal stiffness and Young’s modulus of single fibers from rat soleus muscle probed by atomic force microscopy. Biophys. J., 98, 418-424(2010).

    [48] D.B. Camasão, D. Mantovani. The mechanical characterization of blood vessels and their substitutes in the continuous quest for physiological-relevant performances. A critical review. Mater. Today Bio., 10, 100106(2021).

    [49] F. Troiani, K. Nikolic, T.G. Constandinou. Simulating optical coherence tomography for observing nerve activity: A finite difference time domain bi-dimensional model. PLoS One, 13, e0200392(2018).

    [50] M. Lin, Y. Chen, W. Deng, H. Liang, S. Yu, Z. Zhang, C. Liu. Quantifying the elasticity properties of the median nerve during the upper limb neurodynamic test 1. Appl. Bionics. Biomech., 2022, 3300835(2022).

    [51] D. Sicard, L.E. Fredenburgh, D.J. Tschumperlin. Measured pulmonary arterial tissue stiffness is highly sensitive to AFM indenter dimensions. J. Mech. Behav. Biomed. Mater., 74, 118-127(2017).

    [52] S. Ryu, N. Martino, S.J.J. Kwok, L. Bernstein, S.-H. Yun. Label-free histological imaging of tissues using Brillouin light scattering contrast. Biomed. Opt. Express, 12, 1437-1448(2021).

    [53] P.S. Timashev, S.L. Kotova, G.V. Belkova, E.V. Gubar’kova, L.B. Timofeeva, N.D. Gladkova, A.B. Solovieva. Atomic force microscopy study of atherosclerosis progression in arterial walls. Microsc. Microanal., 22, 311-325(2016).

    [54] J. Margueritat, A. Virgone-Carlotta, S. Monnier, H. Delanoë-Ayari, H.C. Mertani, A. Berthelot, Q. Martinet, X. Dagany, C. Rivière, J.P. Rieu, T. Dehoux. High-frequency mechanical properties of tumors measured by Brillouin light scattering. Phys. Rev. Lett., 122, 018101(2019).

    [55] L.D. Landau, E.M. Lifshitz. Landau L.D., Lifshitz E.M. (eds), Fluid Mechanics, 263-324(1987).

    [56] M.J. Holmes, N.G. Parker, M.J.W. Povey. Temperature dependence of bulk viscosity in water using acoustic spectroscopy. J. Phys.: Conf. Ser., 269, 012011(2011).

    [57] G. Antonacci, M.R. Foreman, C. Paterson, P. Török. Spectral broadening in Brillouin imaging. Appl. Phys. Lett., 103, 012011(2013).

    [58] M. Mattarelli, G. Capponi, A.A. Passeri, D. Fioretto, S. Caponi. Disentanglement of multiple scattering contribution in Brillouin microscopy. ACS Photon., 9, 2087-2091(2022).

    [59] S. Ryu, N. Martino, S.J.J. Kwok, L. Bernstein, S.H. Yun. Label-free histological imaging of tissues using Brillouin light scattering contrast. Biomed. Opt. Express, 12, 1437-1448(2021).

    [60] R. Schlüßler, K. Kim, M. Nötzel, A. Taubenberger, S. Abuhattum, T. Beck, P. Müller, S. Maharana, G. Cojoc, S. Girardo, A. Hermann. Correlative all-optical quantification of mass density and mechanics of sub-cellular compartments with fluorescence specificity. eLife, 11, e68490(2022).

    [61] C.J. Chan, C. Bevilacqua, R. Prevedel. Mechanical mapping of mammalian follicle development using Brillouin microscopy. Commun. Biol., 4, 1133(2021).


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    Paata Pruidze, Elena Chayleva, Wolfgang J. Weninger, Kareem Elsayad. Brillouin scattering spectroscopy for studying human anatomy: Towards in situ mechanical characterization of soft tissue[J]. Journal of the European Optical Society-Rapid Publications, 2023, 19(1): 2023028

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    Paper Information

    Category: Research Articles

    Received: Mar. 27, 2023

    Accepted: Apr. 29, 2023

    Published Online: Aug. 31, 2023

    The Author Email: Elsayad Kareem (