• Journal of Innovative Optical Health Sciences
  • Vol. 14, Issue 5, 2142003 (2021)
Ali Jaafar1、2、3、*, Malik H. Mahmood1、2、4, Roman Holomb1、5, Laszló Himics1, Tamas Vaczi1, Anton Y. Sdobnov6、7, Valery V. Tuchin6、8、9, and Miklós Veres1
Author Affiliations
  • 1Institute for Solid State Physics and Optics Wigner Research Centre for Physics P.O. Box 49, H-1121 Budapest, Hungary
  • 2Institute of Physics, University of Szeged Dom ter 9, H-6720 Szeged, Hungary
  • 3Ministry of Higher Education and Scientific Research Baghdad 10065, Iraq
  • 4Physiology Department, College of Medicine University of Misan, Al-Amarah, Misan 62001, Iraq
  • 5Uzhhorod National University, Uzhhorod 88015 Transcarpathia, Ukraine
  • 6Science Medical Center, Saratov State University 83 Astrakhanskaya Str., Saratov 410012, Russia
  • 7Optoelectronics and Measurement Techniques Laboratory University of Oulu, 90570 Oulu, Finland
  • 8Laboratory of Laser Diagnostics of Technical and Living Systems Institute of Precision Mechanics and Control of the Russian Academy of Sciences 24 Rabochaya, Saratov 410028, Russia
  • 9Interdisciplinary Laboratory of Biophotonics National Research Tomsk State University 36 Lenin Avenue, Tomsk 634050, Russia
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    DOI: 10.1142/s1793545821420037 Cite this Article
    Ali Jaafar, Malik H. Mahmood, Roman Holomb, Laszló Himics, Tamas Vaczi, Anton Y. Sdobnov, Valery V. Tuchin, Miklós Veres. Ex-vivo confocal Raman microspectroscopy of porcine skin with 633/785-NM laser excitation and optical clearing with glycerol/water/DMSO solution[J]. Journal of Innovative Optical Health Sciences, 2021, 14(5): 2142003 Copy Citation Text show less
    References

    [1] R. Schulz et al., "Modeling of drug diffusion based on concentration profiles in healthy and damaged human skin," Biophys. J. 117, 998–1008 (2019).

    [2] M. K. Matta et al., "Effect of sunscreen application under maximal use conditions on plasma concentration of sunscreen active ingredients: A randomized clinical trial," JAMA 321, 2082–2091 (2019).

    [3] C. Choe, J. Lademann, M. E. Darvin, "Analysis of human and porcine skin in vivo/ex vivo for penetration of selected oils by confocal Raman microscopy," Skin Pharmacol. Physiol. 28, 318–330 (2015).

    [4] C. Kra?t, J. Popp, "The many facets of Raman spectroscopy for biomedical analysis," Anal. Bioanal. Chem. 407, 699–717 (2015).

    [5] S. Osseiran et al., "Characterizing stratum corneum structure, barrier function, and chemical content of human skin with coherent Raman scattering imaging," Biomed. Opt. Express 9, 6425–6443 (2018).

    [6] L. Zhang et al., "Resolving water, proteins, and lipids from in vivo confocal Raman spectra of stratum corneum through a chemometric approach," J. Vis. Exp. 2019(151), e60186 (2019).

    [7] R. Vyumvuhore et al., "Raman spectroscopy: In vivo quick response code of skin physiological status," J. Biomed. Opt. 19(11), 111603 (2014).

    [8] K. V. Berezin et al., "Optical clearing of human skin using some monosaccharides in vivo," Opt. Spectrosc. 127, 352–358 (2019).

    [9] J. Gallwas et al., "Effect of optical clearing agents on optical coherence tomography images of cervical epithelium," Lasers Med. Sci. 30, 517–525 (2015).

    [10] M. E. Shvachkina, D. D. Yakovlev, E. N. Lazareva, A. B. Pravdin, D. A. Yakovlev, "Monitoring of the process of immersion optical clearing of collagen bundles using optical coherence tomography," Opt. Spectrosc. 127, 359–367 (2019).

    [11] M. Balu, H. Mikami, J. Hou, E. O. Potma, B. J. Tromberg, "Rapid mesoscale multiphoton microscopy of human skin," Biomed. Opt. Express 7, 4375–4387 (2016).

    [12] K. Koenig, I. Riemann, "High-resolution multiphoton tomography of human skin with subcellular spatial resolution and picosecond time resolution," J. Biomed. Opt. 8(3), 432–439 (2003).

    [13] E. A. Shirshin et al., "In vivo optical imaging of the viable epidermis around the nailfold capillaries for the assessment of heart failure severity in humans," J. Biophotonics 11(9), e201800066 (2018).

    [14] E. A. Shirshin et al., "Two-photon autofluorescence lifetime imaging of human skin papillary dermis in vivo: Assessment of blood capillaries and structural proteins localization," Sci. Rep. 7, 1171 (2017).

    [15] M. Rajadhyaksha, M. Grossman, D. Esterowitz, R. H. Webb, R. R. Anderson, "In vivo confocal scanning laser microscopy of human skin: Melanin provides strong contrast," J. Invest. Dermatol. 104, 946–952 (1995).

    [16] V. H. Maciel, W. R. Correr, C. Kurachi, V. S. Bagnato, C. da Silva Souza, "Fluorescence spectroscopy as a tool to in vivo discrimination of distinctive skin disorders," Photodiagnosis Photodyn. Ther. 19, 45–50 (2017).

    [17] I. Ferulova, A. Lihachev, J. Spigulis, "Photobleaching effects on in vivo skin auto- fluorescence lifetime," J. Biomed. Opt. 20(5), 051031 (2015).

    [18] D. I. Ramos-Soto, A. K. Singh, E. Saucedo-Casas, E. Castro-Camus, M. Alfaro-Gomez, "Visualization of moisturizer effects in stratum corneum in vitro using THz spectroscopic imaging," Appl. Opt. 58, 6581–6585 (2019).

    [19] K. I. Zaytsev et al., "The progress and perspectives of terahertz technology for diagnosis of neoplasms: A review," J. Opt. (United Kingdom) 22, 013001 (2020).

    [20] C. Merle, C. Laugel, P. Chaminade, A. Baillet- Gu?roy, "Quantitative study of the stratum corneum lipid classes by normal phase liquid chromatography: Comparison between two universal detectors," J. Liq. Chromatogr. Relat. Technol. 33, 629–644 (2010).

    [21] V. Kalchenko, I. Meglinski, A. Sdobnov, Y. Kuznetsov, A. Harmelin, "Combined laser speckle imaging and fluorescent intravital microscopy for monitoring acute vascular permeability reaction," J. Biomed. Opt. 24(6), 060501 (2019).

    [22] B. Gotter, W. Faubel, R. H. H. Neubert, "Optical methods for measurements of skin penetration," Skin Pharmacol. Physiol. 21, 156–165 (2008).

    [23] C. V. Raman, K. S. Krishnan, "A new type of secondary radiation," Nature 121, 501–502 (1928).

    [24] A. Quatela, L. Miloudi, A. Tfayli, A. Baillet- Gu?roy, "In vivo Raman microspectroscopy: Intraand intersubject variability of stratum corneum spectral markers," Skin Pharmacol. Physiol. 29, 102–109 (2016).

    [25] D. Huang et al., "Optical clearing of porcine skin tissue in vitro studied by Raman microspectroscopy," J. Biomed. Opt. 17, 015004 (2012).

    [26] V. V. Tuchin, Tissue Optics: Light Scattering Methods and Instruments for Medical Diagnosis, SPIE Press, Bellingham (2015).

    [27] E. Gratton, "Deeper tissue imaging with total detection," Science 331, 1016–1017 (2011).

    [28] B. E. Bouma, G. J. Tearney, Handbook of Optical Coherence Tomography, Marcel Dekker, New York (2002).

    [29] A. Y. Sdobnov et al., "Recent progress in tissue optical clearing for spectroscopic application," Spectrochim. Acta A, Mol. Biomol. Spectrosc. 197, 216–229 (2018).

    [30] D. A. Boas, "A fundamental limitation of linearized algorithms for diffuse optical tomography," Opt. Express 1, 404–413 (1997).

    [31] C. L. Smithpeter, A. K. Dunn, A. J. Welch, R. Richards-Kortum, "Penetration depth limits of in vivo confocal reflectance imaging," Appl. Opt. 37, 2749–2754 (1998).

    [32] V. V. Tuchin, "Light propagation in tissues with controlled optical properties," J. Biomed. Opt. 2, 401–417 (1997).

    [33] E. A. Genina, A. N. Bashkatov, V. V. Tuchin, "Tissue optical immersion clearing," Expert Rev. Med. Devices 7, 825–842 (2010).

    [34] V. V. Tuchin, X. Xu, R. K. Wang, "Dynamic optical coherence tomography in studies of optical clearing, sedimentation, and aggregation of immersed blood," Appl. Opt. 41, 258–271 (2002).

    [35] D. K. Tuchina et al., "Ex vivo optical measurements of glucose diffusion kinetics in native and diabetic mouse skin," J. Biophotonics 8, 332–346 (2015).

    [36] K. V. Larin et al., "Optical clearing for OCT image enhancement and in-depth monitoring of molecular diffusion," IEEE J. Sel. Top. Quantum Electron. 18, 1244–1259 (2012).

    [37] H. Hama et al., "Scale: A chemical approach for fluorescence imaging and reconstruction of transparent mouse brain," Nat. Neurosci. 14, 1481–1488 (2011).

    [38] H. Hama et al., "ScaleS: An optical clearing palette for biological imaging," Nat. Neurosci. 18, 1518– 1529 (2015).

    [39] D. Zhu, K. V. Larin, Q. Luo, V. V. Tuchin, "Recent progress in tissue optical clearing," Laser Photonics Rev. 7, 732–757 (2013).

    [40] A. K. Bui et al., "Revisiting optical clearing with dimethyl sulfoxide DMSO," Lasers Surg. Med. 41, 142–148 (2009).

    [41] V. V. Tuchin, "A clear vision for laser diagnostics (review)," IEEE J. Sel. Top. Quantum Electron. 13, 1621–1628 (2007).

    [42] X. Weny, Z. Maoy, Z. Han, V. V. Tuchin, D. Zhu, "In vivo skin optical clearing by glycerol solutions: Mechanism," J. Biophotonics 3, 44–52 (2010).

    [43] J. Hirshburg, B. Choi, J. S. Nelson, A. T. Yeh, "Collagen solubility correlates with skin optical clearing," J. Biomed. Opt. 11, 040501 (2006).

    [44] J. Hirshburg, B. Choi, J. S. Nelson, A. T. Yeh, "Correlation between collagen solubility and skin optical clearing using sugars," Lasers Surg. Med. 39, 140–144 (2007).

    [45] J. M. Hirshburg, K. M. Ravikumar, W. Hwang, A. T. Yeh, "Molecular basis for optical clearing of collagenous tissues," J. Biomed. Opt. 15, 055002 (2010).

    [46] A. T. Yeh, B. Choi, J. S. Nelson, B. J. Tromberg, "Reversible dissociation of collagen in tissues," J. Invest. Dermatol. 121, 1332–1335 (2003).

    [47] L. M. C. Oliveira and V. V. Tuchin, The Optical Clearing Method: A New Tool for Clinical Practice and Biomedical Engineering, Springer International Publishing, Switzerland (2019).

    [48] X. Wen, S. L. Jacques, V. V. Tuchin, D. Zhu, "Enhanced optical clearing of skin in vivo and optical coherence tomography in-depth imaging," J. Biomed. Opt. 17, 066022 (2012).

    [49] Y. Y. Fu, S. C. Tang, "Optical clearing facilitates integrated 3D visualization of mouse ileal microstructure and vascular network with high definition," Microvasc. Res. 80, 512–521 (2010).

    [50] O. Nadiarnykh, P. J. Campagnola, "Retention of polarization signatures in SHG microscopy of scattering tissues through optical clearing," Opt. Express 17, 5794–5806 (2009).

    [51] M. V. Schulmerich et al., "Optical clearing in transcutaneous Raman spectroscopy of murine cortical bone tissue," J. Biomed. Opt. 13, 021108 (2008).

    [52] Q. Lin, E. N. Lazareva, V. I. Kochubey, Y. Duan, V. V. Tuchin, "Kinetics of optical clearing of human skin studied in vivo using portable Raman spectroscopy," Laser Phys. Lett. 17, 105601 (2020).

    [53] P. Liu et al., "Discrimination of dimethyl sulphoxide diffusion coefficient in the process of optical clearing by confocal micro-Raman spectroscopy," J. Biomed. Opt. 18, 020507 (2013).

    [54] A. Y. Sdobnov, M. E. Darvin, J. Schleusener, J. Lademann, V. V. Tuchin, "Hydrogen bound water profiles in the skin influenced by optical clearing molecular agents — Quantitative analysis using confocal Raman microscopy," J. Biophotonics 12(5), e201800283 (2019), doi: 10.1002/ jbio.201800283.

    [55] K. V. Larin, V. V. Tuchin, "Functional imaging and assessment of the glucose diffusion rate in epithelial tissues in optical coherence tomography," Quantum Electron. 38, 551–556 (2008).

    [56] J. Jiang, M. Boese, P. Turner, R. K. Wang, "Penetration kinetics of dimethyl sulphoxide and glycerol in dynamic optical clearing of porcine skin tissue in vitro studied by Fourier transform infrared spectroscopic imaging," J. Biomed. Opt. 13, 021105 (2008).

    [57] N. J. Yang, M. J. Hinner, "Getting across the cell membrane: An overview for small molecules, peptides, and proteins," Methods Mol. Biol. 1266, 29– 53 (2015).

    [58] S. R. Utz, V. V. Tuchin, E. M. Galkina, "The dynamics of some human skin biophysical parameters in the process of optical clearing after hyperosmotic solutions topical application," Vestn. Dermatol. Venerol. 91(4), 60–68 (2015).

    [59] P. J. Caspers et al., "Monitoring the penetration enhancer dimethyl sulfoxide in human stratum corneum in vivo by confocal Raman spectroscopy," Pharm. Res. 19, 1577–1580 (2002).

    [60] M. H. Khan et al., "Optical clearing of in vivo human skin: Implications for light-based diagnostic imaging and therapeutics," Lasers Surg. Med. 34, 83–85 (2004).

    [61] V. Genin et al., "Ex vivo investigation of glycerol diffusion in skin tissue," J. Biomed. Photonics Eng. 2, 010303-1–010303-5 (2016).

    [62] A. Sdobnov, M. E. Darvin, J. Lademann, V. V. Tuchin, "A comparative study of ex vivo skin optical clearing using two-photon microscopy," J. Biophotonics 10, 1115–1123 (2017).

    [63] S. Debeer et al., "Comparative histology and immunohistochemistry of porcine versus human skin," Eur. J. Dermatol. 23, 456–466 (2013).

    [64] S. Mangelsdorf, T. Vergou, W. Sterry, J. Lademann, A. Patzelt, "Comparative study of hair follicle morphology in eight mammalian species and humans," Ski. Res. Technol. 20, 147–154 (2014).

    [65] M. E. Darvin et al., "Comparison of in vivo and ex vivo laser scanning microscopy and multiphoton tomography application for human and porcine skin imaging," Quantum Electron. 44, 646– 651 (2014).

    [66] T. Sullivan, W. H. Eaglstein, S. C. Davis, P. Mertz, "The pig as a model for human wound healing," Wound Repair Regen. 9, 66–76 (2001).

    [67] C. S. Choe, J. Schleusener, J. Lademann, M. E. Darvin, "Human skin in vivo has a higher skin barrier function than porcine skin ex vivo — Comprehensive Raman microscopic study of the stratum corneum," J. Biophotonics 11, e201700355 (2018).

    [68] V. V. Tuchin et al., "Optical clearing of skin using flashlamp-induced enhancement of epidermal permeability," Lasers Surg. Med. 38, 824–836 (2006).

    [69] J. Schleusener, J. Lademann, M. E. Darvin, "Depthdependent autofluorescence photobleaching using 325, 473, 633, and 785 nm of porcine ear skin ex vivo," J. Biomed. Opt. 22, 091503 (2017).

    [70] F. Menges, "Spectragryph: Optical spectroscopy software: Description," https://www.e?emm2.de/ spectragryph/about descr.html (2020).

    [71] A. Y. Sdobnov, V. V. Tuchin, J. Lademann, M. E. Darvin, "Confocal Raman microscopy supported by optical clearing treatment of the skin— influence on collagen hydration," J. Phys. D, Appl. Phys. 50, 285401 (2017).

    [72] R. Na, I. M. Stender, M. Henriksen, H. C. Wulf, "Autofluorescence of human skin is age-related after correction for skin pigmentation and redness," J. Invest. Dermatol. 116, 536–540 (2001).

    [73] T. Dai, B. M. Pikkula, L. V. Wang, B. Anvari, "Comparison of human skin opto-thermal response to near-infrared and visible laser irradiations: A theoretical investigation," Phys. Med. Biol. 49, 4861–4877 (2004).

    [74] E. Guillard, A. Tfayli, M. Manfait, A. Baillet- Gu?roy, "Thermal dependence of Raman descriptors of ceramides — Part II: Effect of chains lengths and head group structures," Anal. Bioanal. Chem. 399, 1201–1213 (2011).

    [75] P. J. Caspers, G. W. Lucassen, E. A. Carter, H. A. Bruining, G. J. Puppels, "In vivo confocal Raman microspectroscopy of the skin: Noninvasive determination of molecular concentration profiles," J. Invest. Dermatol. 116, 434–442 (2001).

    [76] N. Nakagawa, M. Matsumoto, S. Sakai, "In vivo measurement of the water content in the dermis by confocal Raman spectroscopy," Skin Res. Technol. 16, 137–141 (2010).

    [77] T. T.Nguyen et al., "Characterization of type I and IV collagens by Raman microspectroscopy: Identification of spectral markers of the dermo-epidermal junction," J. Spectrosc. (New York) 27, 686183 (2012).

    [78] B. G. Frushour, J. L. Koenig, "Raman scattering of collagen, gelatin, and elastin," Biopolymers 14, 379– 391 (1975).

    [79] A. Nijssen et al., "Discriminating basal cell carcinoma from its surrounding tissue by Raman spectroscopy," J. Invest. Dermatol. 119, 64–69 (2002).

    [80] M. Gniadecka, H. C. Wulf, O. F. Nielsen, D. H. Christensen, J. Hercogova, "Distinctive molecular abnormalities in benign and malignant skin lesions: Studies by Raman spectroscopy," Photochem. Photobiol. 66, 418–423 (1997).

    [81] B. H. Hokr, V. V. Yakovlev, "Raman signal enhancement via elastic light scattering," Opt. Express 21, 11757 (2013).

    [82] P. Matousek, "Raman signal enhancement in deep spectroscopy of turbid media," Appl. Spectrosc. 61, 845–854 (2007).

    [83] D. Oelkrug, B. Boldrini, K. Rebner, "Comparative Raman study of transparent and turbid materials: Models and experiments in the remote sensing mode," Anal. Bioanal. Chem. 409, 673–681 (2017).

    [84] J. Jiang, R. K. Wang, "Comparing the synergistic effects of oleic acid and dimethyl sulfoxide as vehicles for optical clearing of skin tissue in vitro," Phys. Med. Biol. 49, 5283–5294 (2004).

    [85] A. Liopo, R. Su, D. A. Tsyboulski, A. A. Oraevsky, "Optical clearing of skin enhanced with hyaluronic acid for increased contrast of optoacoustic imaging," J. Biomed. Opt. 21, 081208 (2016).

    Ali Jaafar, Malik H. Mahmood, Roman Holomb, Laszló Himics, Tamas Vaczi, Anton Y. Sdobnov, Valery V. Tuchin, Miklós Veres. Ex-vivo confocal Raman microspectroscopy of porcine skin with 633/785-NM laser excitation and optical clearing with glycerol/water/DMSO solution[J]. Journal of Innovative Optical Health Sciences, 2021, 14(5): 2142003
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