Abstract

The most superficial layer of the epidermis, the stratum corneum, plays a crucial role in retaining hydration; if its structure or composition is compromised, dry skin may result as a consequence of poor water retention. Dry skin is typically treated with topical application of humectant agents that attract water into the skin. Corneometry, the industry standard for measuring skin hydration, works by assessing the bulk electrical properties of skin. However, this technique samples a large volume of tissue and thus does not resolve the biochemical changes that occur at the cellular level that may underlie mechanisms of dry skin. These limitations can be addressed using coherent Raman scattering (CRS) microscopy to probe the intrinsic vibrational modes of chemical groups such as lipids and water. In the present study, ex vivo human skin explants undergoing dehydration and humectant-induced rehydration were measured via CRS imaging and corneometry. Corneometry data and chemically specific images were obtained from the stratum corneum of each patient sample at each timepoint. The resulting data was statistically analyzed using linear mixed effect model regression analysis. The cellular imaging data revealed water loss in the stratum corneum during dehydration that was correlated with corneometer readings. Interestingly, the imaging data and corneometer readings show differences under the experimental rehydration conditions. The rehydration results suggest that hydration restored by the humectant agents may not be retained by the corneocytes in the ex vivo model system. Given the complementary nature of corneometry, a bulk assessment tool, and CRS microscopy, a modality with subcellular resolution implemented here in an en-face tissue imaging setup, these techniques can be used to measure uptake and efficacy of topical compounds in order to better understand their mode of action and improve therapeutic applications.

© 2018 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 (1)

C. L. Evans, “Nonlinear optical microscopy for melanoma: Challenges, tools and opportunities,” Photochem. Photobiol. 94, 624–632 (2018).
[Crossref] [PubMed]

2017 (2)

N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
[Crossref] [PubMed]

S. Osseiran, E. M. Roider, H. Wang, Y. Suita, M. Murphy, D. E. Fisher, and C. L. Evans, “Non-euclidean phasor analysis for quantification of oxidative stress in ex vivo human skin exposed to sun filters using fluorescence lifetime imaging microscopy,” J. Biomed. Opt. 22, 125004 (2017).
[Crossref]

2016 (4)

L. A. Austin, S. Osseiran, and C. L. Evans, “Raman technologies in cancer diagnostics,” Analyst 141, 476–503 (2016).
[Crossref]

I. Saytashev, R. Glenn, G. A. Murashova, S. Osseiran, D. Spence, C. L. Evans, and M. Dantus, “Multiphoton excited hemoglobin fluorescence and third harmonic generation for non-invasive microscopy of stored blood,” Biomed. Opt. Express 7, 3449–3460 (2016).
[Crossref] [PubMed]

H. Wang, S. Osseiran, V. Igras, A. J. Nichols, E. M. Roider, J. Pruessner, H. Tsao, D. E. Fisher, and C. L. Evans, “In vivo coherent raman imaging of the melanomagenesis-associated pigment pheomelanin,” Sci. Reports 6, 37986 (2016).
[Crossref]

X. Chen, P. Gasecka, F. Formanek, J.-B. Galey, and H. Rigneault, “In vivo single human sweat gland activity monitoring using coherent anti-stokes raman scattering and two-photon excited autofluorescence microscopy,” Br. J. Dermatol. 174, 803–812 (2016).
[Crossref]

2015 (1)

C. H. Camp and M. T. Cicerone, “Chemically sensitive bioimaging with coherent raman scattering,” Nat. Photonics 9, 295–305 (2015).
[Crossref]

2014 (4)

D. Zhang, P. Wang, M. N. Slipchenko, and J.-X. Cheng, “Fast vibrational imaging of single cells and tissues by stimulated raman scattering microscopy,” Accounts Chem. Res. 47, 2282–2290 (2014).
[Crossref]

A. A. Romanovsky, “Skin temperature: its role in thermoregulation,” Acta Physiol. 210, 498–507 (2014).
[Crossref]

Y. Belkaid and J. A. Segre, “Dialogue between skin microbiota and immunity,” Science 346, 954–959 (2014).
[Crossref] [PubMed]

A. Zimmerman, L. Bai, and D. D. Ginty, “The gentle touch receptors of mammalian skin,” Science 346, 950–954 (2014).
[Crossref] [PubMed]

2013 (1)

D. Fu, G. Holtom, C. Freudiger, X. Zhang, and X. S. Xie, “Hyperspectral imaging with stimulated raman scattering by chirped femtosecond lasers,” The J. Phys. Chem. B 117, 4634–4640 (2013).
[Crossref]

2012 (6)

I. Georgakoudi and K. P. Quinn, “Optical imaging using endogenous contrast to assess metabolic state,” Annu. Rev. Biomed. Eng. 14, 351–367 (2012).
[Crossref] [PubMed]

K. Koenig, “Hybrid multiphoton multimodal tomography of in vivo human skin,” IntraVital 1, 11–26 (2012).
[Crossref]

H. Schneckenburger, P. Weber, M. Wagner, T. Bruns, V. Richter, S. Schickinger, and R. Wittig, “Multidimensional fluorescence microscopy in live cell imaging — a mini review,” Photonics & Lasers Medicine 1, 35–40 (2012).
[Crossref]

M. Lodén, “Effect of moisturizers on epidermal barrier function,” Clin. Dermatol. 30, 286–296 (2012).
[Crossref] [PubMed]

P. Clarys, R. Clijsen, J. Taeymans, and A. O. Barel, “Hydration measurements of the stratum corneum: comparison between the capacitance method (digital version of the corneometer cm 825®) and the impedance method (skicon-200ex®),” Ski. Res. Technol. 18, 316–323 (2012).
[Crossref]

J. W. Fluhr, R. Darlenski, N. Lachmann, C. Baudouin, P. Msika, C. De Belilovsky, and J.-P. Hachem, “Infant epidermal skin physiology: adaptation after birth,” Br. J. Dermatol. 166, 483–490 (2012).
[Crossref]

2011 (4)

W. J. Lee, J. Y. Kim, C. H. Song, H. D. Jung, S. H. Lee, S.-J. Lee, and D. W. Kim, “Disruption of barrier function in dermatophytosis and pityriasis versicolor,” The J. Dermatol. 38, 1049–1053 (2011).
[Crossref] [PubMed]

D. D. Bikle, “Vitamin d metabolism and function in the skin,” Mol. Cell. Endocrinol. 347, 80–89 (2011).
[Crossref] [PubMed]

A. Ishida-Yamamoto, S. Igawa, and M. Kishibe, “Order and disorder in corneocyte adhesion,” The J. Dermatol. 38, 645–654 (2011).
[Crossref] [PubMed]

P. Clarys, R. Clijsen, and A. O. Barel, “Influence of probe application pressure on in vitro and in vivo capacitance (corneometer cm 825®) and conductance (skicon 200 ex®) measurements,” Ski. Res. Technol. 17, 445–450 (2011).
[Crossref]

2009 (3)

W. Langbein, I. Rocha-Mendoza, and P. Borri, “Coherent anti-stokes raman micro-spectroscopy using spectral focusing: theory and experiment,” J. Raman Spectrosc. 40, 800–808 (2009).
[Crossref]

K. M. Hanson and C. J. Bardeen, “Application of nonlinear optical microscopy for imaging skin,” Photochem. Photobiol. 85, 33–44 (2009).
[Crossref] [PubMed]

V. Andresen, S. Alexander, W.-M. Heupel, M. Hirschberg, R. M. Hoffman, and P. Friedl, “Infrared multiphoton microscopy: subcellular-resolved deep tissue imaging,” Curr. Opin. Biotechnol. 20, 54–62 (2009).
[Crossref] [PubMed]

2008 (3)

C. L. Evans and X. S. Xie, “Coherent anti-stokes raman scattering microscopy: Chemical imaging for biology and medicine,” Annu. Rev. Anal. Chem. 1, 883–909 (2008).
[Crossref]

J. W. Fluhr, R. Darlenski, and C. Surber, “Glycerol and the skin: holistic approach to its origin and functions,” Br. J. Dermatol. 159, 23–34 (2008).
[Crossref] [PubMed]

E. Proksch, J. M. Brandner, and J.-M. Jensen, “The skin: an indispensable barrier,” Exp. Dermatol. 17, 1063–1072 (2008).
[Crossref] [PubMed]

2007 (2)

S. Verdier-Sévrain and F. Bonté, “Skin hydration: a review on its molecular mechanisms,” J. Cosmet. Dermatol. 6, 75–82 (2007).
[Crossref] [PubMed]

B. Godin and E. Touitou, “Transdermal skin delivery: Predictions for humans from in vivo, ex vivo and animal models,” Adv. Drug Deliv. Rev. 59, 1152–1161 (2007).
[Crossref] [PubMed]

2006 (1)

J. W. Fluhr, K. R. Feingold, and P. M. Elias, “Transepidermal water loss reflects permeability barrier status: validation in human and rodent in vivo and ex vivo models,” Exp. Dermatol. 15, 483–492 (2006).
[Crossref] [PubMed]

2005 (1)

A. V. Rawlings and P. J. Matts, “Stratum corneum moisturization at the molecular level: An update in relation to the dry skin cycle,” J. Investig. Dermatol. 124, 1099–1110 (2005).
[Crossref] [PubMed]

2004 (3)

A. V. Rawlings and C. R. Harding, “Moisturization and skin barrier function,” Dermatol. Ther. 17, 43–48 (2004).
[Crossref] [PubMed]

E. Alanen, J. Nuutinen, K. Nicklén, T. Lahtinen, and J. Mönkkönen, “Measurement of hydration in the stratum corneum with the moisturemeter and comparison with the corneometer,” Ski. Res. Technol. 10, 32–37 (2004).
[Crossref]

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85, 25–27 (2004).
[Crossref]

2003 (6)

P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21, 1356–1360 (2003).
[Crossref] [PubMed]

U. Heinrich, U. Koop, M.-C. Leneveu-Duchemin, K. Osterrieder, S. Bielfeldt, C. Chkarnat, J. Degwert, D. Häntschel, S. Jaspers, H.-P. Nissen, M. Rohr, G. Schneider, and H. Tronnier, “Multicentre comparison of skin hydration in terms of physical-, physiological-and product-dependent parameters by the capacitive method (corneometer cm 825),” Int. J. Cosmet. Sci. 25, 45–53 (2003).
[Crossref]

M. Lodén, “Role of topical emollients and moisturizers in the treatment of dry skin barrier disorders,” Am. J. Clin. Dermatol. 4, 771–788 (2003).
[Crossref] [PubMed]

A. V. Rawlings, “Trends in stratum corneum research and the management of dry skin conditions,” Int. J. Cosmet. Sci. 25, 63–95 (2003).
[Crossref]

J. L. Sugarman, J. W. Fluhr, A. J. Fowler, T. Bruckner, T. L. Diepgen, and M. L. Williams, “The objective severity assessment of atopic dermatitis score: An objective measure using permeability barrier function and stratum corneum hydration with computer-assisted estimates for extent of disease,” Arch. Dermatol. 139, 1417–1422 (2003).
[Crossref] [PubMed]

J. A. Bouwstra, A. de Graaff, G. S. Gooris, J. Nijsse, J. W. Wiechers, and A. C. van Aelst, “Water distribution and related morphology in human stratum corneum at different hydration levels,” J. Investig. Dermatol. 120, 750–758 (2003).
[Crossref] [PubMed]

2001 (2)

E. O. Potma, W. P. de Boeij, P. J. M. van Haastert, and D. A. Wiersma, “Real-time visualization of intracellular hydrodynamics in single living cells,” Proc. Natl. Acad. Sci. 98, 1577–1582 (2001).
[Crossref] [PubMed]

A. E. Sagiv, S. Dikstein, and A. Ingber, “The efficiency of humectants as skin moisturizers in the presence of oil,” Ski. Res. Technol. 7, 32–35 (2001).
[Crossref]

2000 (2)

C. R. Harding, A. Watkinson, A. V. Rawlings, and I. R. Scott, “Dry skin, moisturization and corneodesmolysis,” Int. J. Cosmet. Sci. 22, 21–52 (2000).
[Crossref]

S. Pfeiffer, G. Vielhaber, J.-P. Vietzke, K.-P. Wittern, U. Hintze, and R. Wepf, “High-pressure freezing provides new information on human epidermis: Simultaneous protein antigen and lamellar lipid structure preservation. study on human epidermis by cryoimmobilization,” J. Investig. Dermatol. 114, 1030–1038 (2000).
[Crossref] [PubMed]

1999 (1)

J. W. Fluhr, M. Gloor, S. Lazzerini, P. Kleesz, R. Grieshaber, and E. Berardesca, “Comparative study of five instruments measuring stratum corneum hydration (corneometer cm 820 and cm 825, skicon 200, nova dpm 9003, dermalab). part i. in vitro,” Ski. Res. Technol. 5, 161–170 (1999).
[Crossref]

1997 (1)

V. Liguori, C. Guillemin, G. F. Pesce, R. O. Mirimanoff, and J. Bernier, “Double-blind, randomized clinical study comparing hyaluronic acid cream to placebo in patients treated with radiotherapy,” Radiother. Oncol. 42, 155–161 (1997).
[Crossref] [PubMed]

1996 (1)

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. 93, 10763–10768 (1996).
[Crossref] [PubMed]

1990 (1)

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E. Alanen, J. Nuutinen, K. Nicklén, T. Lahtinen, and J. Mönkkönen, “Measurement of hydration in the stratum corneum with the moisturemeter and comparison with the corneometer,” Ski. Res. Technol. 10, 32–37 (2004).
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N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
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L. A. Austin, S. Osseiran, and C. L. Evans, “Raman technologies in cancer diagnostics,” Analyst 141, 476–503 (2016).
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A. Zimmerman, L. Bai, and D. D. Ginty, “The gentle touch receptors of mammalian skin,” Science 346, 950–954 (2014).
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K. M. Hanson and C. J. Bardeen, “Application of nonlinear optical microscopy for imaging skin,” Photochem. Photobiol. 85, 33–44 (2009).
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P. Clarys, R. Clijsen, J. Taeymans, and A. O. Barel, “Hydration measurements of the stratum corneum: comparison between the capacitance method (digital version of the corneometer cm 825®) and the impedance method (skicon-200ex®),” Ski. Res. Technol. 18, 316–323 (2012).
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P. Clarys, R. Clijsen, and A. O. Barel, “Influence of probe application pressure on in vitro and in vivo capacitance (corneometer cm 825®) and conductance (skicon 200 ex®) measurements,” Ski. Res. Technol. 17, 445–450 (2011).
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J. W. Fluhr, R. Darlenski, N. Lachmann, C. Baudouin, P. Msika, C. De Belilovsky, and J.-P. Hachem, “Infant epidermal skin physiology: adaptation after birth,” Br. J. Dermatol. 166, 483–490 (2012).
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J. W. Fluhr, M. Gloor, S. Lazzerini, P. Kleesz, R. Grieshaber, and E. Berardesca, “Comparative study of five instruments measuring stratum corneum hydration (corneometer cm 820 and cm 825, skicon 200, nova dpm 9003, dermalab). part i. in vitro,” Ski. Res. Technol. 5, 161–170 (1999).
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V. Liguori, C. Guillemin, G. F. Pesce, R. O. Mirimanoff, and J. Bernier, “Double-blind, randomized clinical study comparing hyaluronic acid cream to placebo in patients treated with radiotherapy,” Radiother. Oncol. 42, 155–161 (1997).
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U. Heinrich, U. Koop, M.-C. Leneveu-Duchemin, K. Osterrieder, S. Bielfeldt, C. Chkarnat, J. Degwert, D. Häntschel, S. Jaspers, H.-P. Nissen, M. Rohr, G. Schneider, and H. Tronnier, “Multicentre comparison of skin hydration in terms of physical-, physiological-and product-dependent parameters by the capacitive method (corneometer cm 825),” Int. J. Cosmet. Sci. 25, 45–53 (2003).
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J. L. Sugarman, J. W. Fluhr, A. J. Fowler, T. Bruckner, T. L. Diepgen, and M. L. Williams, “The objective severity assessment of atopic dermatitis score: An objective measure using permeability barrier function and stratum corneum hydration with computer-assisted estimates for extent of disease,” Arch. Dermatol. 139, 1417–1422 (2003).
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H. Schneckenburger, P. Weber, M. Wagner, T. Bruns, V. Richter, S. Schickinger, and R. Wittig, “Multidimensional fluorescence microscopy in live cell imaging — a mini review,” Photonics & Lasers Medicine 1, 35–40 (2012).
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Cagan, R. H.

C. L. Froebe, F. A. Simion, H. Ohlmeyer, L. D. Rhein, J. Mattai, R. H. Cagan, and S. E. Friberg, “Prevention of stratum corneum lipid phase transitions in vitro by glycerol — an alternative mechanism for skin moisturization,” J. Soc. Cosmet. Chem. 41, 51–65 (1990).

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C. H. Camp and M. T. Cicerone, “Chemically sensitive bioimaging with coherent raman scattering,” Nat. Photonics 9, 295–305 (2015).
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P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nat. Biotechnol. 21, 1356–1360 (2003).
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X. Chen, P. Gasecka, F. Formanek, J.-B. Galey, and H. Rigneault, “In vivo single human sweat gland activity monitoring using coherent anti-stokes raman scattering and two-photon excited autofluorescence microscopy,” Br. J. Dermatol. 174, 803–812 (2016).
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D. Zhang, P. Wang, M. N. Slipchenko, and J.-X. Cheng, “Fast vibrational imaging of single cells and tissues by stimulated raman scattering microscopy,” Accounts Chem. Res. 47, 2282–2290 (2014).
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N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
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Cicerone, M. T.

C. H. Camp and M. T. Cicerone, “Chemically sensitive bioimaging with coherent raman scattering,” Nat. Photonics 9, 295–305 (2015).
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Clarys, P.

P. Clarys, R. Clijsen, J. Taeymans, and A. O. Barel, “Hydration measurements of the stratum corneum: comparison between the capacitance method (digital version of the corneometer cm 825®) and the impedance method (skicon-200ex®),” Ski. Res. Technol. 18, 316–323 (2012).
[Crossref]

P. Clarys, R. Clijsen, and A. O. Barel, “Influence of probe application pressure on in vitro and in vivo capacitance (corneometer cm 825®) and conductance (skicon 200 ex®) measurements,” Ski. Res. Technol. 17, 445–450 (2011).
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Clijsen, R.

P. Clarys, R. Clijsen, J. Taeymans, and A. O. Barel, “Hydration measurements of the stratum corneum: comparison between the capacitance method (digital version of the corneometer cm 825®) and the impedance method (skicon-200ex®),” Ski. Res. Technol. 18, 316–323 (2012).
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P. Clarys, R. Clijsen, and A. O. Barel, “Influence of probe application pressure on in vitro and in vivo capacitance (corneometer cm 825®) and conductance (skicon 200 ex®) measurements,” Ski. Res. Technol. 17, 445–450 (2011).
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Dantus, M.

Darlenski, R.

J. W. Fluhr, R. Darlenski, N. Lachmann, C. Baudouin, P. Msika, C. De Belilovsky, and J.-P. Hachem, “Infant epidermal skin physiology: adaptation after birth,” Br. J. Dermatol. 166, 483–490 (2012).
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J. W. Fluhr, R. Darlenski, and C. Surber, “Glycerol and the skin: holistic approach to its origin and functions,” Br. J. Dermatol. 159, 23–34 (2008).
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J. W. Fluhr, R. Darlenski, N. Lachmann, C. Baudouin, P. Msika, C. De Belilovsky, and J.-P. Hachem, “Infant epidermal skin physiology: adaptation after birth,” Br. J. Dermatol. 166, 483–490 (2012).
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Degwert, J.

U. Heinrich, U. Koop, M.-C. Leneveu-Duchemin, K. Osterrieder, S. Bielfeldt, C. Chkarnat, J. Degwert, D. Häntschel, S. Jaspers, H.-P. Nissen, M. Rohr, G. Schneider, and H. Tronnier, “Multicentre comparison of skin hydration in terms of physical-, physiological-and product-dependent parameters by the capacitive method (corneometer cm 825),” Int. J. Cosmet. Sci. 25, 45–53 (2003).
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Diepgen, T. L.

J. L. Sugarman, J. W. Fluhr, A. J. Fowler, T. Bruckner, T. L. Diepgen, and M. L. Williams, “The objective severity assessment of atopic dermatitis score: An objective measure using permeability barrier function and stratum corneum hydration with computer-assisted estimates for extent of disease,” Arch. Dermatol. 139, 1417–1422 (2003).
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N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
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Elias, P. M.

J. W. Fluhr, K. R. Feingold, and P. M. Elias, “Transepidermal water loss reflects permeability barrier status: validation in human and rodent in vivo and ex vivo models,” Exp. Dermatol. 15, 483–492 (2006).
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Enejder, A. M. K.

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85, 25–27 (2004).
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C. L. Evans, “Nonlinear optical microscopy for melanoma: Challenges, tools and opportunities,” Photochem. Photobiol. 94, 624–632 (2018).
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S. Osseiran, E. M. Roider, H. Wang, Y. Suita, M. Murphy, D. E. Fisher, and C. L. Evans, “Non-euclidean phasor analysis for quantification of oxidative stress in ex vivo human skin exposed to sun filters using fluorescence lifetime imaging microscopy,” J. Biomed. Opt. 22, 125004 (2017).
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L. A. Austin, S. Osseiran, and C. L. Evans, “Raman technologies in cancer diagnostics,” Analyst 141, 476–503 (2016).
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I. Saytashev, R. Glenn, G. A. Murashova, S. Osseiran, D. Spence, C. L. Evans, and M. Dantus, “Multiphoton excited hemoglobin fluorescence and third harmonic generation for non-invasive microscopy of stored blood,” Biomed. Opt. Express 7, 3449–3460 (2016).
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H. Wang, S. Osseiran, V. Igras, A. J. Nichols, E. M. Roider, J. Pruessner, H. Tsao, D. E. Fisher, and C. L. Evans, “In vivo coherent raman imaging of the melanomagenesis-associated pigment pheomelanin,” Sci. Reports 6, 37986 (2016).
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C. L. Evans and X. S. Xie, “Coherent anti-stokes raman scattering microscopy: Chemical imaging for biology and medicine,” Annu. Rev. Anal. Chem. 1, 883–909 (2008).
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Feingold, K. R.

J. W. Fluhr, K. R. Feingold, and P. M. Elias, “Transepidermal water loss reflects permeability barrier status: validation in human and rodent in vivo and ex vivo models,” Exp. Dermatol. 15, 483–492 (2006).
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Fisher, D. E.

N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
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S. Osseiran, E. M. Roider, H. Wang, Y. Suita, M. Murphy, D. E. Fisher, and C. L. Evans, “Non-euclidean phasor analysis for quantification of oxidative stress in ex vivo human skin exposed to sun filters using fluorescence lifetime imaging microscopy,” J. Biomed. Opt. 22, 125004 (2017).
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H. Wang, S. Osseiran, V. Igras, A. J. Nichols, E. M. Roider, J. Pruessner, H. Tsao, D. E. Fisher, and C. L. Evans, “In vivo coherent raman imaging of the melanomagenesis-associated pigment pheomelanin,” Sci. Reports 6, 37986 (2016).
[Crossref]

Fluhr, J. W.

J. W. Fluhr, R. Darlenski, N. Lachmann, C. Baudouin, P. Msika, C. De Belilovsky, and J.-P. Hachem, “Infant epidermal skin physiology: adaptation after birth,” Br. J. Dermatol. 166, 483–490 (2012).
[Crossref]

J. W. Fluhr, R. Darlenski, and C. Surber, “Glycerol and the skin: holistic approach to its origin and functions,” Br. J. Dermatol. 159, 23–34 (2008).
[Crossref] [PubMed]

J. W. Fluhr, K. R. Feingold, and P. M. Elias, “Transepidermal water loss reflects permeability barrier status: validation in human and rodent in vivo and ex vivo models,” Exp. Dermatol. 15, 483–492 (2006).
[Crossref] [PubMed]

J. L. Sugarman, J. W. Fluhr, A. J. Fowler, T. Bruckner, T. L. Diepgen, and M. L. Williams, “The objective severity assessment of atopic dermatitis score: An objective measure using permeability barrier function and stratum corneum hydration with computer-assisted estimates for extent of disease,” Arch. Dermatol. 139, 1417–1422 (2003).
[Crossref] [PubMed]

J. W. Fluhr, M. Gloor, S. Lazzerini, P. Kleesz, R. Grieshaber, and E. Berardesca, “Comparative study of five instruments measuring stratum corneum hydration (corneometer cm 820 and cm 825, skicon 200, nova dpm 9003, dermalab). part i. in vitro,” Ski. Res. Technol. 5, 161–170 (1999).
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Formanek, F.

X. Chen, P. Gasecka, F. Formanek, J.-B. Galey, and H. Rigneault, “In vivo single human sweat gland activity monitoring using coherent anti-stokes raman scattering and two-photon excited autofluorescence microscopy,” Br. J. Dermatol. 174, 803–812 (2016).
[Crossref]

Fowler, A. J.

J. L. Sugarman, J. W. Fluhr, A. J. Fowler, T. Bruckner, T. L. Diepgen, and M. L. Williams, “The objective severity assessment of atopic dermatitis score: An objective measure using permeability barrier function and stratum corneum hydration with computer-assisted estimates for extent of disease,” Arch. Dermatol. 139, 1417–1422 (2003).
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Freudiger, C.

D. Fu, G. Holtom, C. Freudiger, X. Zhang, and X. S. Xie, “Hyperspectral imaging with stimulated raman scattering by chirped femtosecond lasers,” The J. Phys. Chem. B 117, 4634–4640 (2013).
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Friberg, S. E.

C. L. Froebe, F. A. Simion, H. Ohlmeyer, L. D. Rhein, J. Mattai, R. H. Cagan, and S. E. Friberg, “Prevention of stratum corneum lipid phase transitions in vitro by glycerol — an alternative mechanism for skin moisturization,” J. Soc. Cosmet. Chem. 41, 51–65 (1990).

Friedl, P.

V. Andresen, S. Alexander, W.-M. Heupel, M. Hirschberg, R. M. Hoffman, and P. Friedl, “Infrared multiphoton microscopy: subcellular-resolved deep tissue imaging,” Curr. Opin. Biotechnol. 20, 54–62 (2009).
[Crossref] [PubMed]

Froebe, C. L.

C. L. Froebe, F. A. Simion, H. Ohlmeyer, L. D. Rhein, J. Mattai, R. H. Cagan, and S. E. Friberg, “Prevention of stratum corneum lipid phase transitions in vitro by glycerol — an alternative mechanism for skin moisturization,” J. Soc. Cosmet. Chem. 41, 51–65 (1990).

Fu, D.

D. Fu, G. Holtom, C. Freudiger, X. Zhang, and X. S. Xie, “Hyperspectral imaging with stimulated raman scattering by chirped femtosecond lasers,” The J. Phys. Chem. B 117, 4634–4640 (2013).
[Crossref]

Galey, J.-B.

X. Chen, P. Gasecka, F. Formanek, J.-B. Galey, and H. Rigneault, “In vivo single human sweat gland activity monitoring using coherent anti-stokes raman scattering and two-photon excited autofluorescence microscopy,” Br. J. Dermatol. 174, 803–812 (2016).
[Crossref]

Gasecka, P.

X. Chen, P. Gasecka, F. Formanek, J.-B. Galey, and H. Rigneault, “In vivo single human sweat gland activity monitoring using coherent anti-stokes raman scattering and two-photon excited autofluorescence microscopy,” Br. J. Dermatol. 174, 803–812 (2016).
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I. Georgakoudi and K. P. Quinn, “Optical imaging using endogenous contrast to assess metabolic state,” Annu. Rev. Biomed. Eng. 14, 351–367 (2012).
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Ginty, D. D.

A. Zimmerman, L. Bai, and D. D. Ginty, “The gentle touch receptors of mammalian skin,” Science 346, 950–954 (2014).
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Glenn, R.

Gloor, M.

J. W. Fluhr, M. Gloor, S. Lazzerini, P. Kleesz, R. Grieshaber, and E. Berardesca, “Comparative study of five instruments measuring stratum corneum hydration (corneometer cm 820 and cm 825, skicon 200, nova dpm 9003, dermalab). part i. in vitro,” Ski. Res. Technol. 5, 161–170 (1999).
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Gooris, G. S.

J. A. Bouwstra, A. de Graaff, G. S. Gooris, J. Nijsse, J. W. Wiechers, and A. C. van Aelst, “Water distribution and related morphology in human stratum corneum at different hydration levels,” J. Investig. Dermatol. 120, 750–758 (2003).
[Crossref] [PubMed]

Gray, N. S.

N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
[Crossref] [PubMed]

Grieshaber, R.

J. W. Fluhr, M. Gloor, S. Lazzerini, P. Kleesz, R. Grieshaber, and E. Berardesca, “Comparative study of five instruments measuring stratum corneum hydration (corneometer cm 820 and cm 825, skicon 200, nova dpm 9003, dermalab). part i. in vitro,” Ski. Res. Technol. 5, 161–170 (1999).
[Crossref]

Guillemin, C.

V. Liguori, C. Guillemin, G. F. Pesce, R. O. Mirimanoff, and J. Bernier, “Double-blind, randomized clinical study comparing hyaluronic acid cream to placebo in patients treated with radiotherapy,” Radiother. Oncol. 42, 155–161 (1997).
[Crossref] [PubMed]

Hachem, J.-P.

J. W. Fluhr, R. Darlenski, N. Lachmann, C. Baudouin, P. Msika, C. De Belilovsky, and J.-P. Hachem, “Infant epidermal skin physiology: adaptation after birth,” Br. J. Dermatol. 166, 483–490 (2012).
[Crossref]

Hanson, K. M.

K. M. Hanson and C. J. Bardeen, “Application of nonlinear optical microscopy for imaging skin,” Photochem. Photobiol. 85, 33–44 (2009).
[Crossref] [PubMed]

Häntschel, D.

U. Heinrich, U. Koop, M.-C. Leneveu-Duchemin, K. Osterrieder, S. Bielfeldt, C. Chkarnat, J. Degwert, D. Häntschel, S. Jaspers, H.-P. Nissen, M. Rohr, G. Schneider, and H. Tronnier, “Multicentre comparison of skin hydration in terms of physical-, physiological-and product-dependent parameters by the capacitive method (corneometer cm 825),” Int. J. Cosmet. Sci. 25, 45–53 (2003).
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U. Heinrich, U. Koop, M.-C. Leneveu-Duchemin, K. Osterrieder, S. Bielfeldt, C. Chkarnat, J. Degwert, D. Häntschel, S. Jaspers, H.-P. Nissen, M. Rohr, G. Schneider, and H. Tronnier, “Multicentre comparison of skin hydration in terms of physical-, physiological-and product-dependent parameters by the capacitive method (corneometer cm 825),” Int. J. Cosmet. Sci. 25, 45–53 (2003).
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Hellerer, T.

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85, 25–27 (2004).
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Hermann, A. L.

N. Mujahid, Y. Liang, R. Murakami, H. G. Choi, A. S. Dobry, J. Wang, Y. Suita, Q. Y. Weng, J. Allouche, L. V. Kemeny, A. L. Hermann, E. M. Roider, N. S. Gray, and D. E. Fisher, “A uv-independent topical small-molecule approach for melanin production in human skin,” Cell Reports 19, 2177–2184 (2017).
[Crossref] [PubMed]

Heupel, W.-M.

V. Andresen, S. Alexander, W.-M. Heupel, M. Hirschberg, R. M. Hoffman, and P. Friedl, “Infrared multiphoton microscopy: subcellular-resolved deep tissue imaging,” Curr. Opin. Biotechnol. 20, 54–62 (2009).
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S. Pfeiffer, G. Vielhaber, J.-P. Vietzke, K.-P. Wittern, U. Hintze, and R. Wepf, “High-pressure freezing provides new information on human epidermis: Simultaneous protein antigen and lamellar lipid structure preservation. study on human epidermis by cryoimmobilization,” J. Investig. Dermatol. 114, 1030–1038 (2000).
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U. Heinrich, U. Koop, M.-C. Leneveu-Duchemin, K. Osterrieder, S. Bielfeldt, C. Chkarnat, J. Degwert, D. Häntschel, S. Jaspers, H.-P. Nissen, M. Rohr, G. Schneider, and H. Tronnier, “Multicentre comparison of skin hydration in terms of physical-, physiological-and product-dependent parameters by the capacitive method (corneometer cm 825),” Int. J. Cosmet. Sci. 25, 45–53 (2003).
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H. Wang, S. Osseiran, V. Igras, A. J. Nichols, E. M. Roider, J. Pruessner, H. Tsao, D. E. Fisher, and C. L. Evans, “In vivo coherent raman imaging of the melanomagenesis-associated pigment pheomelanin,” Sci. Reports 6, 37986 (2016).
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J. A. Bouwstra, A. de Graaff, G. S. Gooris, J. Nijsse, J. W. Wiechers, and A. C. van Aelst, “Water distribution and related morphology in human stratum corneum at different hydration levels,” J. Investig. Dermatol. 120, 750–758 (2003).
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E. O. Potma, W. P. de Boeij, P. J. M. van Haastert, and D. A. Wiersma, “Real-time visualization of intracellular hydrodynamics in single living cells,” Proc. Natl. Acad. Sci. 98, 1577–1582 (2001).
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S. Verdier-Sévrain and F. Bonté, “Skin hydration: a review on its molecular mechanisms,” J. Cosmet. Dermatol. 6, 75–82 (2007).
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S. Pfeiffer, G. Vielhaber, J.-P. Vietzke, K.-P. Wittern, U. Hintze, and R. Wepf, “High-pressure freezing provides new information on human epidermis: Simultaneous protein antigen and lamellar lipid structure preservation. study on human epidermis by cryoimmobilization,” J. Investig. Dermatol. 114, 1030–1038 (2000).
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S. Pfeiffer, G. Vielhaber, J.-P. Vietzke, K.-P. Wittern, U. Hintze, and R. Wepf, “High-pressure freezing provides new information on human epidermis: Simultaneous protein antigen and lamellar lipid structure preservation. study on human epidermis by cryoimmobilization,” J. Investig. Dermatol. 114, 1030–1038 (2000).
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J. A. Bouwstra, A. de Graaff, G. S. Gooris, J. Nijsse, J. W. Wiechers, and A. C. van Aelst, “Water distribution and related morphology in human stratum corneum at different hydration levels,” J. Investig. Dermatol. 120, 750–758 (2003).
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D. Zhang, P. Wang, M. N. Slipchenko, and J.-X. Cheng, “Fast vibrational imaging of single cells and tissues by stimulated raman scattering microscopy,” Accounts Chem. Res. 47, 2282–2290 (2014).
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D. Fu, G. Holtom, C. Freudiger, X. Zhang, and X. S. Xie, “Hyperspectral imaging with stimulated raman scattering by chirped femtosecond lasers,” The J. Phys. Chem. B 117, 4634–4640 (2013).
[Crossref]

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Figures (6)

Fig. 1
Fig. 1 CRS images of human stratum corneum acquired from ex vivo skin explants. (a–c) CARS and (d–f) SRS images of stratum corneum showing (a,d) lipid-weighted content; (b,e) protein-weighted content; and (c,f) water-weighted content. The NRB in the CARS data manifests itself as a homogeneous and unspecific haze distributed across the field of view.
Fig. 2
Fig. 2 Manual segmentation of SRS lipid content image to distinguish intracellular and extracellular spaces for subsequent analysis. (a) Unlabeled image. (b) Manually segmented image, showing corneocytes identified by indices 1 through 22, and extracellular space corresponding to the surrounding region identified by index number 23.
Fig. 3
Fig. 3 Corneometer measurements obtained from ex vivo human skin throughout the dehydration time course on a plastic substrate (i.e. rapid dehydration) and a gel substrate (i.e. slow dehydration). Data points correspond to the mean of the triplicate corneometer measurements with error bars indicating the standard error of the mean. Statistically significant deviations from the corresponding initial timepoint are denoted by asterisks and determined via Student’s t-test (*: p < 0.05/N ; **: p < 0.01/N ; ***: p < 0.001/N, adjusted using Bonferroni correction with N = 4 pairwise comparisons).
Fig. 4
Fig. 4 Corneometry-based assessment of ex vivo human skin hydration dynamics during rehydration under various environmental and treatment conditions. Data points correspond to the rate of change of corneometer measurements per hour, with error bars showing the 95% confidence interval. For the ambient condition without treatment (control), asterisks denote rates of change significantly different from zero; for all other conditions, they denote rates of change that are significantly different from the control (*: p < 0.05; **: p < 0.01; ***: p < 0.001, where p-values are adjusted using Holm-Bonferroni correction with N = 36 metrics).
Fig. 5
Fig. 5 Chemical content dynamics of ex vivo human skin during rehydration under various environmental and treatment conditions. Data points correspond to the rate of change of CRS imaging metrics per hour, with error bars showing the 95% confidence interval. For the ambient condition without treatment (control), asterisks denote rates of change significantly different from zero; for all other conditions, they denote rates of change that are significantly different from the control (*: p < 0.05; **: p < 0.01; ***: p < 0.001, where p-values are adjusted using Holm-Bonferroni correction with N = 36 metrics).
Fig. 6
Fig. 6 Morphological dynamics of ex vivo human corneocytes during rehydration under various environmental and treatment conditions. Data points correspond to the rate of change of each spatial metric in microns per hour with error bars showing the 95% confidence interval. Nearest neighbor distances are computed between corneocyte cell centers (NNDCenters) as well as between cell walls (NNDWalls). For the ambient condition without treatment (control), asterisks denote rates of change significantly different from zero; for all other conditions, they denote rates of change that are significantly different from the control (*: p < 0.05; **: p < 0.01; ***: p < 0.001, where p-values are adjusted using Holm-Bonferroni correction with N = 36 metrics).

Tables (2)

Tables Icon

Table 1 Stratum corneum metric dynamics measured over the time course of ex vivo human skin dehydration on two different substrates. For the plastic substrate, asterisks denote rates of change significantly different from zero; for the gel substrate, they denote rates of change that are significantly different from the plastic substrate (*: p < 0.05; **: p < 0.01; ***: p < 0.001, where p-values are adjusted using Holm-Bonferroni correction with N = 36 metrics. IER: intracellular-to-extracellular ratio; NND: nearest neighbor distance; CI: confidence interval.)

Tables Icon

Table 2 Summary of observed changes over the time course of skin explant rehydration. (N/C: no change; +++, ++, +: strong, moderate, and modest increase, respectively; – – –, – –, –: strong, moderate, and modest decrease, respectively.)

Metrics