Abstract

Spatially resolved multiply excited autofluorescence spectroscopy is a valuable optical biopsy technique to investigate skin UV-Visible optical properties in vivo in clinics. However, it provides bulk fluorescence signals from which the individual endogenous fluorophore contributions need to be disentangled. Skin optical clearing allows for increasing tissue transparency, thus providing access to more accurate in-depth information. The aim of the present contribution was to study the time changes in skin spatially resolved and multiply excited autofluorescence spectra during skin optical clearing. The latter spectra were acquired on an ex vivo human skin strip lying on a fluorescent gel substrate during 37 minutes of the optical clearing process of a topically applied sucrose-based solution. A Non Negative Matrix Factorization-based blind source separation approach was proposed to unmix skin tissue intrinsic fluorophore contributions and to analyze the time evolution of this mixing throughout the optical clearing process. This spectral unmixing exploited the multidimensionality of the acquired data, i.e., spectra resolved in five excitation wavelengths, four source-to-detector separations, and eight measurement times. Best fitting results between experimental and estimated spectra were obtained for optimal numbers of 3 and 4 sources. These estimated spectral sources exhibited common identifiable shapes of fluorescence emission spectra related to the fluorescent gel substrate and to known skin intrinsic fluorophores matching namely dermis collagen/elastin and epidermis flavins. The time analysis of the fluorophore contributions allowed us to highlight how the clearing process towards the deepest skin layers impacts skin autofluorescence through time, namely with a strongest contribution to the bulk autofluorescence signal of dermis collagen (respectively epidermis flavins) fluorescence at shortest (respectively longest) excitation wavelengths and longest (respectively shortest) source-to-detector separations.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]

2018 (2)

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

D. Artemyev, “Mathematical model of skin autofluorescence induced by 450 nm laser,” J. Biomed. Photonics & Eng. 4, 020303 (2018).
[Crossref]

2017 (2)

C. Ash, M. Dubec, K. Donne, and T. Bashford, “Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods,” Lasers Med. Sci. 32, 1909–1918 (2017).
[Crossref] [PubMed]

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

2016 (2)

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

2015 (1)

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

2014 (4)

E. Borisova, L. Angelova, and E. Pavlova, “Endogenous and exogenous fluorescence skin cancer diagnostics for clinical applications,” IEEE J. Sel. Top. Quantum Electron. 20, 1–12 (2014).
[Crossref]

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

G. Zhou, A. Cichocki, Q. Zhao, and S. Xie, “Nonnegative matrix and tensor factorizations: an algorithmic perspective,” IEEE Sig. Proc. Mag. 31, 54–65 (2014).
[Crossref]

A. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58, 2461 (2014).
[Crossref]

2013 (3)

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

T. Pengo, A. Muñoz-Barrutia, I. Zudaire, and C. Ortiz-de Solorzano, “Efficient blind spectral unmixing of fluorescently labeled samples using multi-layer non-negative matrix factorization,” PLoS One 8, e78504 (2013).
[Crossref] [PubMed]

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[Crossref] [PubMed]

2012 (4)

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

F. Abdat, M. Amouroux, Y. Guermeur, and W. Blondel, “Hybrid feature selection and svm-based classification for mouse skin precancerous stages diagnosis from bimodal spectroscopy,” Opt. Express 20, 228–244 (2012).
[Crossref] [PubMed]

H. Liu, H. Gisquet, W. Blondel, and F. Guillemin, “Bimodal spectroscopy for in vivo characterization of hypertrophic skin tissue: pre-clinical experimentation, data selection and classification,” Biomed. Opt. Express 3, 3278–3290 (2012).
[Crossref] [PubMed]

2011 (1)

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

2010 (2)

E. Migacheva, A. Pravdin, and V. Tuchin, “Alterations in autofluorescence signal from rat skin ex vivo under optical immersion clearing,” J. Innov. Opt. Heal. Sci. 3, 147–152 (2010).
[Crossref]

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

2009 (2)

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

2008 (3)

G. Vargas, J. K. Barton, and A. J. Welch, “Use of hyperosmotic chemical agent to improve the laser treatment of cutaneous vascular lesions,” J. Biomed. Opt. 13, 021114 (2008).
[Crossref] [PubMed]

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

E. Borisova, P. Troyanova, P. Pavlova, and L. Avramov, “Diagnostics of pigmented skin tumors based on laser-induced autofluorescence and diffuse reflectance spectroscopy,” Quantum Electron. 38, 597 (2008).
[Crossref]

2007 (1)

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

2006 (1)

2002 (1)

N. Kollias, G. Zonios, and G. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002).
[Crossref]

1999 (3)

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

L. Brancaleon, G. Lin, and N. Kollias, “The in vivo fluorescence of tryptophan moieties in human skin increases with uv exposure and is a marker for epidermal proliferation,” J. Investig. Dermatol. 113, 977–982 (1999).
[Crossref] [PubMed]

D. D. Lee and H. S. Seung, “Learning the parts of objects by non-negative matrix factorization,” Nature 401, 788–791 (1999).
[Crossref] [PubMed]

1998 (1)

B. Masters, P. So, and E. Gratton, “Optical biopsy of in vivo human skin: multi-photon excitation microscopy,” Lasers Med. Sci. 13, 196–203 (1998).
[Crossref]

Abdat, F.

Amouroux, M.

F. Abdat, M. Amouroux, Y. Guermeur, and W. Blondel, “Hybrid feature selection and svm-based classification for mouse skin precancerous stages diagnosis from bimodal spectroscopy,” Opt. Express 20, 228–244 (2012).
[Crossref] [PubMed]

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

M. Amouroux, W. Blondel, and A. Delconte, “Medical device for fibred bimodal optical spectroscopy,” Tech. Rep. WO2017093316A1, University of Lorraine (2015).

Anders, A.

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

Angelova, L.

E. Borisova, L. Angelova, and E. Pavlova, “Endogenous and exogenous fluorescence skin cancer diagnostics for clinical applications,” IEEE J. Sel. Top. Quantum Electron. 20, 1–12 (2014).
[Crossref]

Artemyev, D.

D. Artemyev, “Mathematical model of skin autofluorescence induced by 450 nm laser,” J. Biomed. Photonics & Eng. 4, 020303 (2018).
[Crossref]

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Ash, C.

C. Ash, M. Dubec, K. Donne, and T. Bashford, “Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods,” Lasers Med. Sci. 32, 1909–1918 (2017).
[Crossref] [PubMed]

Avramov, L.

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

E. Borisova, P. Troyanova, P. Pavlova, and L. Avramov, “Diagnostics of pigmented skin tumors based on laser-induced autofluorescence and diffuse reflectance spectroscopy,” Quantum Electron. 38, 597 (2008).
[Crossref]

Bagnato, V. S.

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

Bain, A. J.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Barton, J. K.

G. Vargas, J. K. Barton, and A. J. Welch, “Use of hyperosmotic chemical agent to improve the laser treatment of cutaneous vascular lesions,” J. Biomed. Opt. 13, 021114 (2008).
[Crossref] [PubMed]

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

Bashford, T.

C. Ash, M. Dubec, K. Donne, and T. Bashford, “Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods,” Lasers Med. Sci. 32, 1909–1918 (2017).
[Crossref] [PubMed]

Bashkatov, A. G.

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Bashkatov, A. N.

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

Blacker, T. S.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Blondel, W.

F. Abdat, M. Amouroux, Y. Guermeur, and W. Blondel, “Hybrid feature selection and svm-based classification for mouse skin precancerous stages diagnosis from bimodal spectroscopy,” Opt. Express 20, 228–244 (2012).
[Crossref] [PubMed]

H. Liu, H. Gisquet, W. Blondel, and F. Guillemin, “Bimodal spectroscopy for in vivo characterization of hypertrophic skin tissue: pre-clinical experimentation, data selection and classification,” Biomed. Opt. Express 3, 3278–3290 (2012).
[Crossref] [PubMed]

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

M. Amouroux, W. Blondel, and A. Delconte, “Medical device for fibred bimodal optical spectroscopy,” Tech. Rep. WO2017093316A1, University of Lorraine (2015).

Borisova, E.

E. Borisova, L. Angelova, and E. Pavlova, “Endogenous and exogenous fluorescence skin cancer diagnostics for clinical applications,” IEEE J. Sel. Top. Quantum Electron. 20, 1–12 (2014).
[Crossref]

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

E. Borisova, P. Troyanova, P. Pavlova, and L. Avramov, “Diagnostics of pigmented skin tumors based on laser-induced autofluorescence and diffuse reflectance spectroscopy,” Quantum Electron. 38, 597 (2008).
[Crossref]

Bottiroli, G.

A. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58, 2461 (2014).
[Crossref]

Bourg-Heckly, G.

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

Brancaleon, L.

L. Brancaleon, G. Lin, and N. Kollias, “The in vivo fluorescence of tryptophan moieties in human skin increases with uv exposure and is a marker for epidermal proliferation,” J. Investig. Dermatol. 113, 977–982 (1999).
[Crossref] [PubMed]

Bratchenko, I.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Calin, M.

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[Crossref] [PubMed]

Calin, R.

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[Crossref] [PubMed]

Chan, E. K.

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

Chen, L.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Choi, B.

J. Hirshburg, B. Choi, J. S. Nelson, and A. T. Yeh, “Correlation between collagen solubility and skin optical clearing using sugars,” Lasers Surg. Medicine 39, 140–144 (2007).
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G. Zhou, A. Cichocki, Q. Zhao, and S. Xie, “Nonnegative matrix and tensor factorizations: an algorithmic perspective,” IEEE Sig. Proc. Mag. 31, 54–65 (2014).
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A. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58, 2461 (2014).
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A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
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M. Amouroux, W. Blondel, and A. Delconte, “Medical device for fibred bimodal optical spectroscopy,” Tech. Rep. WO2017093316A1, University of Lorraine (2015).

Demidov, V.

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

Diaz-Ayil, G.

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

Ding, Z.

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

Dinten, J.

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

Dinten, J.-M.

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

Dolin, L. S.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Donne, K.

C. Ash, M. Dubec, K. Donne, and T. Bashford, “Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods,” Lasers Med. Sci. 32, 1909–1918 (2017).
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Dontu, S.

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
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Dubec, M.

C. Ash, M. Dubec, K. Donne, and T. Bashford, “Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods,” Lasers Med. Sci. 32, 1909–1918 (2017).
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Duchen, M. R.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
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Gale, J. E.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
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Gelikonov, G.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Gelikonov, V.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Genina, E. A.

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Gisquet, H.

Gladkova, N. D.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Gratton, E.

B. Masters, P. So, and E. Gratton, “Optical biopsy of in vivo human skin: multi-photon excitation microscopy,” Lasers Med. Sci. 13, 196–203 (1998).
[Crossref]

Guermeur, Y.

Guillemin, F.

H. Liu, H. Gisquet, W. Blondel, and F. Guillemin, “Bimodal spectroscopy for in vivo characterization of hypertrophic skin tissue: pre-clinical experimentation, data selection and classification,” Biomed. Opt. Express 3, 3278–3290 (2012).
[Crossref] [PubMed]

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

Guo, L.

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

Heinrich, U.

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

Herve, L.

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

Hirshburg, J.

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

Iksanov, R. R.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Kamensky, V.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Katika, K. M.

Khlebtsov, B. N.

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Kirchhoff, F.

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Kollias, N.

N. Kollias, G. Zonios, and G. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002).
[Crossref]

L. Brancaleon, G. Lin, and N. Kollias, “The in vivo fluorescence of tryptophan moieties in human skin increases with uv exposure and is a marker for epidermal proliferation,” J. Investig. Dermatol. 113, 977–982 (1999).
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Kozina, A. M.

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Kozlov, S.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Krebs, R.

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

Kurachi, C.

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

Kuranov, R. S.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Lademann, J.

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

Larin, K. V.

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

Lee, D. D.

D. D. Lee and H. S. Seung, “Learning the parts of objects by non-negative matrix factorization,” Nature 401, 788–791 (1999).
[Crossref] [PubMed]

Leroux, A.

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

Li, C.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Li, P.

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

Li, Z.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Lin, G.

L. Brancaleon, G. Lin, and N. Kollias, “The in vivo fluorescence of tryptophan moieties in human skin increases with uv exposure and is a marker for epidermal proliferation,” J. Investig. Dermatol. 113, 977–982 (1999).
[Crossref] [PubMed]

Liu, H.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

H. Liu, H. Gisquet, W. Blondel, and F. Guillemin, “Bimodal spectroscopy for in vivo characterization of hypertrophic skin tissue: pre-clinical experimentation, data selection and classification,” Biomed. Opt. Express 3, 3278–3290 (2012).
[Crossref] [PubMed]

Luo, Q.

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

Mann, Z. F.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Mao, Y.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Mars, J.

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

Masters, B.

B. Masters, P. So, and E. Gratton, “Optical biopsy of in vivo human skin: multi-photon excitation microscopy,” Lasers Med. Sci. 13, 196–203 (1998).
[Crossref]

Meinhardt, M.

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

Migacheva, E.

E. Migacheva, A. Pravdin, and V. Tuchin, “Alterations in autofluorescence signal from rat skin ex vivo under optical immersion clearing,” J. Innov. Opt. Heal. Sci. 3, 147–152 (2010).
[Crossref]

Mitkovski, M.

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Montcuquet, A.

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

Montcuquet, A.-S.

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

Moryatov, A.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Muñoz-Barrutia, A.

T. Pengo, A. Muñoz-Barrutia, I. Zudaire, and C. Ortiz-de Solorzano, “Efficient blind spectral unmixing of fluorescently labeled samples using multi-layer non-negative matrix factorization,” PLoS One 8, e78504 (2013).
[Crossref] [PubMed]

Myakinin, O.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Navarro, F.

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

Navarro, F. P.

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

Neher, E.

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Neher, R. A.

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Nelson, J. S.

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

Ortiz-de Solorzano, C.

T. Pengo, A. Muñoz-Barrutia, I. Zudaire, and C. Ortiz-de Solorzano, “Efficient blind spectral unmixing of fluorescently labeled samples using multi-layer non-negative matrix factorization,” PLoS One 8, e78504 (2013).
[Crossref] [PubMed]

Parasca, S.

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[Crossref] [PubMed]

Pavlova, E.

E. Borisova, L. Angelova, and E. Pavlova, “Endogenous and exogenous fluorescence skin cancer diagnostics for clinical applications,” IEEE J. Sel. Top. Quantum Electron. 20, 1–12 (2014).
[Crossref]

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

Pavlova, P.

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

E. Borisova, P. Troyanova, P. Pavlova, and L. Avramov, “Diagnostics of pigmented skin tumors based on laser-induced autofluorescence and diffuse reflectance spectroscopy,” Quantum Electron. 38, 597 (2008).
[Crossref]

Pengo, T.

T. Pengo, A. Muñoz-Barrutia, I. Zudaire, and C. Ortiz-de Solorzano, “Efficient blind spectral unmixing of fluorescently labeled samples using multi-layer non-negative matrix factorization,” PLoS One 8, e78504 (2013).
[Crossref] [PubMed]

Pilon, L.

Pires, L.

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

Pravdin, A.

E. Migacheva, A. Pravdin, and V. Tuchin, “Alterations in autofluorescence signal from rat skin ex vivo under optical immersion clearing,” J. Innov. Opt. Heal. Sci. 3, 147–152 (2010).
[Crossref]

Rylander, H. G.

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

Savastru, R.

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[Crossref] [PubMed]

Sdobnov, A. Y.

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

Seung, H. S.

D. D. Lee and H. S. Seung, “Learning the parts of objects by non-negative matrix factorization,” Nature 401, 788–791 (1999).
[Crossref] [PubMed]

Shakhova, N. M.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Shi, R.

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

Shpuntenko, K.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

So, P.

B. Masters, P. So, and E. Gratton, “Optical biopsy of in vivo human skin: multi-photon excitation microscopy,” Lasers Med. Sci. 13, 196–203 (1998).
[Crossref]

Stamatas, G.

N. Kollias, G. Zonios, and G. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002).
[Crossref]

Szabadkai, G.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Tang, J.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Terentyuk, A. N.

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Terentyuk, G. S.

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Theis, F. J.

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Tronnier, H.

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

Troyanova, P.

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

E. Borisova, P. Troyanova, P. Pavlova, and L. Avramov, “Diagnostics of pigmented skin tumors based on laser-induced autofluorescence and diffuse reflectance spectroscopy,” Quantum Electron. 38, 597 (2008).
[Crossref]

Tuchin, I.

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

Tuchin, V.

E. Migacheva, A. Pravdin, and V. Tuchin, “Alterations in autofluorescence signal from rat skin ex vivo under optical immersion clearing,” J. Innov. Opt. Heal. Sci. 3, 147–152 (2010).
[Crossref]

Tuchin, V. V.

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

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

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Vargas, G.

G. Vargas, J. K. Barton, and A. J. Welch, “Use of hyperosmotic chemical agent to improve the laser treatment of cutaneous vascular lesions,” J. Biomed. Opt. 13, 021114 (2008).
[Crossref] [PubMed]

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

Vitkin, I. A.

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

Vrakova, M.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Welch, A. J.

G. Vargas, J. K. Barton, and A. J. Welch, “Use of hyperosmotic chemical agent to improve the laser treatment of cutaneous vascular lesions,” J. Biomed. Opt. 13, 021114 (2008).
[Crossref] [PubMed]

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

Wilson, B. C.

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

Xie, S.

G. Zhou, A. Cichocki, Q. Zhao, and S. Xie, “Nonnegative matrix and tensor factorizations: an algorithmic perspective,” IEEE Sig. Proc. Mag. 31, 54–65 (2014).
[Crossref]

Yeh, A. T.

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

Zakharov, V.

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

Zeug, A.

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Zhang, C.

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

Zhang, R.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Zhang, Y.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Zhao, Q.

G. Zhou, A. Cichocki, Q. Zhao, and S. Xie, “Nonnegative matrix and tensor factorizations: an algorithmic perspective,” IEEE Sig. Proc. Mag. 31, 54–65 (2014).
[Crossref]

Zhou, G.

G. Zhou, A. Cichocki, Q. Zhao, and S. Xie, “Nonnegative matrix and tensor factorizations: an algorithmic perspective,” IEEE Sig. Proc. Mag. 31, 54–65 (2014).
[Crossref]

Zhou, X.

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Zhu, D.

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

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

Ziegler, M.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Zonios, G.

N. Kollias, G. Zonios, and G. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002).
[Crossref]

Zudaire, I.

T. Pengo, A. Muñoz-Barrutia, I. Zudaire, and C. Ortiz-de Solorzano, “Efficient blind spectral unmixing of fluorescently labeled samples using multi-layer non-negative matrix factorization,” PLoS One 8, e78504 (2013).
[Crossref] [PubMed]

ACS Appl. Mater. Interfaces (1)

Y. Zhang, H. Liu, J. Tang, Z. Li, X. Zhou, R. Zhang, L. Chen, Y. Mao, and C. Li, “Noninvasively imaging subcutaneous tumor xenograft by a handheld raman detector, with the assistance of an optical clearing agent,” ACS Appl. Mater. Interfaces 9, 17769–17776 (2017).
[Crossref] [PubMed]

Appl. Opt. (1)

Biomed. Opt. Express (1)

Biophys. J. (1)

R. A. Neher, M. Mitkovski, F. Kirchhoff, E. Neher, F. J. Theis, and A. Zeug, “Blind source separation techniques for the decomposition of multiply labeled fluorescence images,” Biophys. J. 96, 3791–3800 (2009).
[Crossref] [PubMed]

Eur. J. Histochem. (1)

A. Croce and G. Bottiroli, “Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis,” Eur. J. Histochem. 58, 2461 (2014).
[Crossref]

IEEE J. Sel. Top. Quantum Electron. (1)

E. Borisova, L. Angelova, and E. Pavlova, “Endogenous and exogenous fluorescence skin cancer diagnostics for clinical applications,” IEEE J. Sel. Top. Quantum Electron. 20, 1–12 (2014).
[Crossref]

IEEE Sig. Proc. Mag. (1)

G. Zhou, A. Cichocki, Q. Zhao, and S. Xie, “Nonnegative matrix and tensor factorizations: an algorithmic perspective,” IEEE Sig. Proc. Mag. 31, 54–65 (2014).
[Crossref]

IEEE Transactions on Biomed. Eng. (1)

A. Montcuquet, L. Herve, F. Navarro, J. Dinten, and J. Mars, “In vivo fluorescence spectra unmixing and autofluorescence removal by sparse nonnegative matrix factorization,” IEEE Transactions on Biomed. Eng. 58, 2554–2565 (2011).
[Crossref]

Int. J. Bioautomation (1)

E. Borisova, P. Pavlova, E. Pavlova, P. Troyanova, and L. Avramov, “Optical biopsy of human skin-a tool for cutaneous tumours’ diagnosis,” Int. J. Bioautomation 16, 53–72 (2012).

J. Biomed. Opt. (6)

L. Guo, R. Shi, C. Zhang, D. Zhu, Z. Ding, and P. Li, “Optical coherence tomography angiography offers comprehensive evaluation of skin optical clearing in vivo by quantifying optical properties and blood flow imaging simultaneously,” J. Biomed. Opt. 21, 1–6 (2016).
[Crossref]

M. Amouroux, G. Diaz-Ayil, W. Blondel, G. Bourg-Heckly, A. Leroux, and F. Guillemin, “Classification of ultraviolet irradiated mouse skin histological stages by bimodal spectroscopy: multiple excitation autofluorescence and diffuse reflectance,” J. Biomed. Opt. 14, 014011 (2009).
[Crossref] [PubMed]

M. Meinhardt, R. Krebs, A. Anders, U. Heinrich, and H. Tronnier, “Wavelength-dependent penetration depths of ultraviolet radiation in human skin,” J. Biomed. Opt. 13, 044030 (2008).
[Crossref] [PubMed]

A.-S. Montcuquet, L. Herve, F. P. Navarro, J.-M. Dinten, and J. Mars, “Nonnegative matrix factorization: a blind spectra separation method for in vivo fluorescent optical imaging,” J. Biomed. Opt. 15, 1–14 (2010).

L. Pires, V. Demidov, I. A. Vitkin, V. S. Bagnato, C. Kurachi, and B. C. Wilson, “Optical clearing of melanoma in vivo: characterization by diffuse reflectance spectroscopy and optical coherence tomography,” J. Biomed. Opt. 21, 081210 (2016).
[Crossref] [PubMed]

G. Vargas, J. K. Barton, and A. J. Welch, “Use of hyperosmotic chemical agent to improve the laser treatment of cutaneous vascular lesions,” J. Biomed. Opt. 13, 021114 (2008).
[Crossref] [PubMed]

J. Biomed. Photonics & Eng. (2)

I. Bratchenko, D. Artemyev, O. Myakinin, M. Vrakova, K. Shpuntenko, A. Moryatov, S. Kozlov, and V. Zakharov, “Malignant melanoma and basal cell carcinoma detection with 457 nm laser-induced fluorescence,” J. Biomed. Photonics & Eng. 1, 180–185 (2015).
[Crossref]

D. Artemyev, “Mathematical model of skin autofluorescence induced by 450 nm laser,” J. Biomed. Photonics & Eng. 4, 020303 (2018).
[Crossref]

J. Cancer Res. Clin. Oncol. (1)

M. Calin, S. Parasca, R. Savastru, R. Calin, and S. Dontu, “Optical techniques for the noninvasive diagnosis of skin cancer,” J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[Crossref] [PubMed]

J. Innov. Opt. Heal. Sci. (1)

E. Migacheva, A. Pravdin, and V. Tuchin, “Alterations in autofluorescence signal from rat skin ex vivo under optical immersion clearing,” J. Innov. Opt. Heal. Sci. 3, 147–152 (2010).
[Crossref]

J. Investig. Dermatol. (1)

L. Brancaleon, G. Lin, and N. Kollias, “The in vivo fluorescence of tryptophan moieties in human skin increases with uv exposure and is a marker for epidermal proliferation,” J. Investig. Dermatol. 113, 977–982 (1999).
[Crossref] [PubMed]

Laser Photonics Rev. (1)

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

Lasers Med. Sci. (2)

B. Masters, P. So, and E. Gratton, “Optical biopsy of in vivo human skin: multi-photon excitation microscopy,” Lasers Med. Sci. 13, 196–203 (1998).
[Crossref]

C. Ash, M. Dubec, K. Donne, and T. Bashford, “Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods,” Lasers Med. Sci. 32, 1909–1918 (2017).
[Crossref] [PubMed]

Lasers Surg. Medicine (2)

G. Vargas, E. K. Chan, J. K. Barton, H. G. Rylander, and A. J. Welch, “Use of an agent to reduce scattering in skin,” Lasers Surg. Medicine 24, 133–141 (1999).
[Crossref]

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

Nat. Commun. (1)

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating nadh and nadph fluorescence in live cells and tissues using flim,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Nature (1)

D. D. Lee and H. S. Seung, “Learning the parts of objects by non-negative matrix factorization,” Nature 401, 788–791 (1999).
[Crossref] [PubMed]

Opt. Express (1)

PLoS One (1)

T. Pengo, A. Muñoz-Barrutia, I. Zudaire, and C. Ortiz-de Solorzano, “Efficient blind spectral unmixing of fluorescently labeled samples using multi-layer non-negative matrix factorization,” PLoS One 8, e78504 (2013).
[Crossref] [PubMed]

Quantum Electron. (1)

E. Borisova, P. Troyanova, P. Pavlova, and L. Avramov, “Diagnostics of pigmented skin tumors based on laser-induced autofluorescence and diffuse reflectance spectroscopy,” Quantum Electron. 38, 597 (2008).
[Crossref]

Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. (1)

A. Y. Sdobnov, M. E. Darvin, E. A. Genina, A. N. Bashkatov, J. Lademann, and V. V. Tuchin, “Recent progress in tissue optical clearing for spectroscopic application,” Spectrochimica Acta Part A: Mol. Biomol. Spectrosc. 197, 216–229 (2018).
[Crossref]

SPIE Proc. (1)

A. M. Kozina, E. A. Genina, G. S. Terentyuk, A. N. Terentyuk, A. G. Bashkatov, V. V. Tuchin, and B. N. Khlebtsov, “The development of skin immersion clearing method for increasing of laser exposure efficiency on subcutaneous objects,” SPIE Proc. 8427, 842726 (2012).
[Crossref]

Vib. Spectrosc. (1)

N. Kollias, G. Zonios, and G. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002).
[Crossref]

Other (3)

M. Amouroux, W. Blondel, and A. Delconte, “Medical device for fibred bimodal optical spectroscopy,” Tech. Rep. WO2017093316A1, University of Lorraine (2015).

P. Comon and C. Jutten, eds., Handbook of Blind Source Separation, Independent Component Analysis and Applications (Academic Press, 2010).

L. S. Dolin, G. Gelikonov, V. Gelikonov, N. D. Gladkova, R. R. Iksanov, V. Kamensky, R. S. Kuranov, N. M. Shakhova, and I. Tuchin, Handbook of Coherent-Domain Optical Methods: Biomedical Diagnostics, Environmental Monitoring and Material Science., vol. 2 (Springer-Verlag, 2012).

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Figures (6)

Fig. 1
Fig. 1 Schematic representation (left) and picture (middle) of the experimental configuration including the hybrid two-layer model made of an ex vivo skin strip lying on a fluorescent gel substrate and the multi-fiber optics probe in contact with skin epidermis. Fluorescence spectra x(λ; Di, λ j exc, tk) are collected according to four SDS Di (i ∈ {1, . . ., ND = 4}), five fluorescence excitation wavelengths λ j exc (j ∈ {1, . . ., Nexc = 5}) and eight time measurement points tk (k ∈ {1, . . ., Nt = 8}). Right picture: Hematoxylin and Eosin stained histological slide of the skin strip tested (scale bar = 200 μm).
Fig. 2
Fig. 2 Absorption (left) and emission (right) fluorescence spectra of Chlorin e6 normalized to their respective maximum peak values. The emission spectra was obtained under 403 nm excitation wavelength (corresponding to the wavelength of maximum absorption).
Fig. 3
Fig. 3 Measured (continuous lines) and recovered (dashed lines) fluorescence spectra using ALS-based NMF algorithm with a fixed number of 4 sources (NS = 4). Blue, red, yellow and purple color correspond to the curves at SDS D1:4 respectively. Results are plotted (i) for the 5 fluorescence excitation wavelengths λ 1 : 5 exc in rows from top to bottom and (ii) for 4 time points during the Optical Clearing process at T0, +13, +20 and +25 minutes respectively from left to right columns.
Fig. 4
Fig. 4 Estimated spectral sources Ŝ obtained by the ALS-based NMF method, for NS = 3 (left) and NS = 4 (right), according to all SDS D1:4, all fluorescence excitation wavelengths λ 1 : 5 exc and all time points during the Optical Clearing process t1:8.
Fig. 5
Fig. 5 Time evolution of the weight coefficients in the estimated abundance matrix A ^ with a total number of sources fixed at NS = 3. Each point correspond to the value of a coefficient al,m = ai+ND×(j−1)+ND×Nexc×(k−1),m with i ∈ {1, . . ., ND = 4}, j ∈ {1, . . ., Nexc = 5}, k ∈ {1, . . ., Nt = 8} and m ∈ {1, . . ., NS = 3} the SDS, the excitation wavelength, the time point and the source numbers respectively. Results (weights normalized to their initial values at T0) are plotted in blue, red, yellow and purple colors corresponding to SDS D1:4 respectively, (i) for the 5 fluorescence excitation wavelengths λ 1 : 5 exc in rows from top to bottom and (ii) for the 3 sources S1:3 from left to right columns.
Fig. 6
Fig. 6 Time evolution of the weight coefficients in the estimated abundance matrix A ^ with a total number of sources fixed at NS = 4. Each point correspond to the value of a coefficient al,m = ai+ND×(j−1)+ND×Nexc×(k−1),m with i ∈ {1, . . ., ND = 4}, j ∈ {1, . . ., Nexc = 5}, k ∈ {1, . . ., Nt = 8} and m ∈ {1, . . ., NS = 3} the SDS, the excitation wavelength, the time point and the source numbers respectively. Results (weights normalized to their initial values at T0) are plotted in blue, red, yellow and purple colors corresponding to SDS D1:4 respectively, (i) for the 5 fluorescence excitation wavelengths λ 1 : 5 exc in rows from top to bottom and (ii) for the 4 sources S1:4 from left to right columns.

Tables (1)

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Algorithm 1 Alternating Least Squares algorithm

Equations (6)

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X A S ( x ( λ ; D 1 , λ 1 exc , t 1 ) x ( λ ; D i , λ j exc , t k ) x ( λ ; D N D , λ N exc exc , t N t ) ( a 1 , 1 a 1 , m a 1 , N S a l , 1 a l , m a l , N S a N S p , 1 a N S p , m a N S p , N S ) ( s 1 ( λ ) s m ( λ ) s N S ( λ ) )
x l ( λ ) = m = 1 N S a l , m s m ( λ ) .
( A ^ , S ^ ) = arg min A 0 S 0 { f ( A , S ) = X A S F 2 = l = 1 N S p x l ( λ ) m = 1 N S a l , m s m ( λ ) 2 2 }
A ( iter ) = A ( iter 1 ) ( XS ( iter 1 ) T ) ( A ( iter 1 ) S ( iter 1 ) S ( iter 1 ) T )
S ( iter ) = S ( iter 1 ) ( A ( iter ) T X ) ( A ( iter ) T A ( iter ) S ( iter ) )
ε = f ( A ( iter 1 ) , S ( iter 1 ) ) f ( A ( iter ) , S ( iter ) ) f ( A ( iter 1 ) , S ( iter 1 ) )

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