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Skin color independent assessment of aging using skin autofluorescenceM. Koetsier, Erfan Nur, Han Chunmao, Helen L. Lutgers, Thera P. Links, Andries J. Smit, Gerhard Rakhorst, and Reindert Graaff »View Author Affiliations
Marten Koetsier,1
Erfan Nur,2
Han Chunmao,3
Helen L. Lutgers,4
Thera P. Links,4
Andries J. Smit,5
Gerhard Rakhorst,1
and Reindert Graaff1,4,*
1Department of BioMedical Engineering 5Department of Medicine, University Medical Center Groningen and University of Groningen, Groningen, The Netherlands 2Deptartment of Internal Medicine / Haematology, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands 3Second Affiliated Hospital Zhejiang University College of Medicine, Hangzhou, 310009, China 4Department of Endocrinology and UMCG, BioMedical Engineering, PO-Box 196, 9700 AD Groningen, The Netherlands; phone +31 50 3637427; fax +31 50 3633159 *r.graaff@med.umcg.nl |
Optics Express, Vol. 18, Issue 14, pp. 14416-14429 (2010)
http://dx.doi.org/10.1364/OE.18.014416
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Abstract
Skin autofluorescence (AF) for the non-invasive assessment of the amount of accumulated tissue Advanced Glycation Endproducts (AGEs) increases with aging. In subjects with darker skin colors, measurements typically result in lower AF values than in subjects with fair skin colors, e.g. due to selective absorption by skin compounds. Our aim was to provide a new method for calculating skin AF, yielding values that are independent of skin color. The deviation of skin AF of healthy subjects with various darker skin types (N = 99) compared to reference values from Caucasians showed to be a function of various parameters that were derived from reflectance and emission spectra in the UV and visible range (adjusted R2 = 80%). Validation of the new algorithm, based on these findings, in a separate dataset (N = 141) showed that results of skin AF can now be obtained to assess skin AGEs independently of skin color.
© 2010 Optical Society of America
OCIS Codes
(120.3890) Instrumentation, measurement, and metrology : Medical optics instrumentation
(170.1610) Medical optics and biotechnology : Clinical applications
(170.4580) Medical optics and biotechnology : Optical diagnostics for medicine
(170.6510) Medical optics and biotechnology : Spectroscopy, tissue diagnostics
(300.6280) Spectroscopy : Spectroscopy, fluorescence and luminescence
ToC Category:
Medical Optics and Biotechnology
History
Original Manuscript: April 23, 2010
Revised Manuscript: June 7, 2010
Manuscript Accepted: June 7, 2010
Published: June 22, 2010
Virtual Issues
Vol. 5, Iss. 11 Virtual Journal for Biomedical Optics
Citation
M. Koetsier, Erfan Nur, Han Chunmao, Helen L. Lutgers, Thera P. Links, Andries J. Smit, Gerhard Rakhorst, and Reindert Graaff, "Skin color independent assessment of
aging using skin autofluorescence," Opt. Express 18, 14416-14429 (2010)
http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-18-14-14416
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References
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- I. Nishidate, Y. Aizu, and H. Mishina, “Estimation of melanin and hemoglobin in skin tissue using multiple regression analysis aided by Monte Carlo simulation,” J. Biomed. Opt. 9, 700–710 (2004). [CrossRef] [PubMed]
- S. Alaluf, D. Atkins, K. Barrett, M. Blount, N. Carter, and A. Heath, “Ethnic variation in melanin content and composition in photoexposed and photoprotected human skin,” Pigment Cell Res. 15, 112–118 (2002). [CrossRef] [PubMed]
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- R. R. Anderson and J. A. Parrish, “The optics of human skin,” J. Invest. Dermatol. 77, 13–19 (1981). [CrossRef] [PubMed]
- S. Alaluf, D. Atkins, K. Barrett, M. Blount, N. Carter, and A. Heath, “Ethnic variation in melanin content and composition in photoexposed and photoprotected human skin,” Pigment Cell Res. 15, 112–118 (2002). [CrossRef] [PubMed]
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- L. Bachmann, D. M. Zezell, A. da Costa Ribeiro, L. Gomes, and A. S. Ito, “Fluorescence spectroscopy of biological tissues—A review,” Appl. Spectrosc. Rev. 41, 575–590 (2006). [CrossRef]
- N. Kollias and A. Baqer, “Spectroscopic characteristics of human melanin in vivo,” J. Invest. Dermatol. 85, 38–42 (1985). [CrossRef] [PubMed]
- N. Kollias and A. H. Baqer, “Absorption mechanisms of human melanin in the visible, 400–720 nm,” J. Invest. Dermatol. 89, 384–388 (1987). [CrossRef] [PubMed]
- J. B. Dawson, D. J. Barker, D. J. Ellis, E. Grassam, J. A. Cotterill, G. W. Fisher, and J. W. Feather, “A theoretical and experimental study of light absorption and scattering by in vivo skin,” Phys. Med. Biol. 25, 695–709 (1980). [CrossRef] [PubMed]
- S. Alaluf, D. Atkins, K. Barrett, M. Blount, N. Carter, and A. Heath, “Ethnic variation in melanin content and composition in photoexposed and photoprotected human skin,” Pigment Cell Res. 15, 112–118 (2002). [CrossRef] [PubMed]
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- G. Zonios, A. Dimou, I. Bassukas, D. Galaris, A. Tsolakidis, and E. Kaxiras, “Melanin absorption spectroscopy: new method for noninvasive skin investigation and melanoma detection,” J. Biomed. Opt. 13, 14017 (2008). [CrossRef]
- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
- R. Meerwaldt, J. W. L. Hartog, R. Graaff, R. J. Huisman, T. P. Links, N. C. den Hollander, S. R. Thorpe, J. W. Baynes, G. Navis, R. O. B. Gans, and A. J. Smit, “Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients,” J. Am. Soc. Nephrol. 16, 3687–3693 (2005). [CrossRef] [PubMed]
- R. Meerwaldt, R. Graaff, P. H. N. Oomen, T. P. Links, J. J. Jager, N. L. Alderson, S. R. Thorpe, J. W. Baynes, R. O. B. Gans, and A. J. Smit, “Simple non-invasive assessment of advanced glycation endproduct accumulation,” Diabetologia 47, 1324–1330 (2004). [CrossRef] [PubMed]
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- H. L. Lutgers, E. G. Gerrits, R. Graaff, T. P. Links, W. J. Sluiter, R. O. Gans, H. J. Bilo, and A. J. Smit, “Skin autofluorescence provides additional information to the UK Prospective Diabetes Study (UKPDS) risk score for the estimation of cardiovascular prognosis in type 2 diabetes mellitus,” Diabetologia 52, 789–797 (2009). [CrossRef] [PubMed]
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- S. Alaluf, D. Atkins, K. Barrett, M. Blount, N. Carter, and A. Heath, “Ethnic variation in melanin content and composition in photoexposed and photoprotected human skin,” Pigment Cell Res. 15, 112–118 (2002). [CrossRef] [PubMed]
- J. M. Coremans, C. Ince, H. A. Bruining, and G. J. Puppels, “(Semi-)quantitative analysis of reduced nicotinamide adenine dinucleotide fluorescence images of blood-perfused rat heart,” Biophys. J. 72, 1849–1860 (1997). [CrossRef] [PubMed]
- S. Alaluf, D. Atkins, K. Barrett, M. Blount, N. Carter, and A. Heath, “Ethnic variation in melanin content and composition in photoexposed and photoprotected human skin,” Pigment Cell Res. 15, 112–118 (2002). [CrossRef] [PubMed]
- R. Chen, Z. Huang, H. Lui, I. Hamzavi, D. I. McLean, S. Xie, and H. Zeng, “Monte Carlo simulation of cutaneous reflectance and fluorescence measurements – The effect of melanin contents and localization,” J. Photochem. Photobiol. B. 86, 219–226 (2007). [CrossRef]
- J. M. Coremans, C. Ince, H. A. Bruining, and G. J. Puppels, “(Semi-)quantitative analysis of reduced nicotinamide adenine dinucleotide fluorescence images of blood-perfused rat heart,” Biophys. J. 72, 1849–1860 (1997). [CrossRef] [PubMed]
- J. B. Dawson, D. J. Barker, D. J. Ellis, E. Grassam, J. A. Cotterill, G. W. Fisher, and J. W. Feather, “A theoretical and experimental study of light absorption and scattering by in vivo skin,” Phys. Med. Biol. 25, 695–709 (1980). [CrossRef] [PubMed]
- L. Bachmann, D. M. Zezell, A. da Costa Ribeiro, L. Gomes, and A. S. Ito, “Fluorescence spectroscopy of biological tissues—A review,” Appl. Spectrosc. Rev. 41, 575–590 (2006). [CrossRef]
- J. W. Feather, M. Hajizadeh-Saffar, G. Leslie, and J. B. Dawson, “A portable scanning reflectance spectrophotometer using visible wavelengths for the rapid measurement of skin pigments,” Phys. Med. Biol. 34, 807–820 (1989). [CrossRef] [PubMed]
- J. B. Dawson, D. J. Barker, D. J. Ellis, E. Grassam, J. A. Cotterill, G. W. Fisher, and J. W. Feather, “A theoretical and experimental study of light absorption and scattering by in vivo skin,” Phys. Med. Biol. 25, 695–709 (1980). [CrossRef] [PubMed]
- M. Koetsier, H. L. Lutgers, C. de Jonge, T. P. Links, A. J. Smit, and R. Graaff, “Reference values of skin autofluorescence,” Diabetes Technol. Ther. 12, 399–403 (2010). [CrossRef] [PubMed]
- D. J. Mulder, P. L. van Haelst, S. Gross, K. de Leeuw, J. Bijzet, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products,” Atherosclerosis 197, 217–223 (2008). [CrossRef]
- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
- R. Meerwaldt, J. W. L. Hartog, R. Graaff, R. J. Huisman, T. P. Links, N. C. den Hollander, S. R. Thorpe, J. W. Baynes, G. Navis, R. O. B. Gans, and A. J. Smit, “Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients,” J. Am. Soc. Nephrol. 16, 3687–3693 (2005). [CrossRef] [PubMed]
- G. Zonios, A. Dimou, I. Bassukas, D. Galaris, A. Tsolakidis, and E. Kaxiras, “Melanin absorption spectroscopy: new method for noninvasive skin investigation and melanoma detection,” J. Biomed. Opt. 13, 14017 (2008). [CrossRef]
- G. Zonios and A. Dimou, “Melanin optical properties provide evidence for chemical and structural disorder in vivo,” Opt. Express 16, 8263–8268 (2008). [CrossRef] [PubMed]
- G. Zonios and A. Dimou, “Modeling diffuse reflectance from semi-infinite turbid media: application to the study of skin optical properties,” Opt. Express 14, 8661–8674 (2006). [CrossRef] [PubMed]
- C. Magnain, M. Elias, and J.-M. Frigerio, “Skin color modeling using the radiative transfer equation solved by the auxiliary function method,” J. Opt. Soc. Am. A. 24, 2196–2205 (2007). [CrossRef]
- J. B. Dawson, D. J. Barker, D. J. Ellis, E. Grassam, J. A. Cotterill, G. W. Fisher, and J. W. Feather, “A theoretical and experimental study of light absorption and scattering by in vivo skin,” Phys. Med. Biol. 25, 695–709 (1980). [CrossRef] [PubMed]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- T. Matsumoto, T. Tsurumoto, H. Baba, M. Osaki, H. Enomoto, A. Yonekura, H. Shindo, and T. Miyata, “Measurement of advanced glycation endproducts in skin of patients with rheumatoid arthritis, osteoarthritis, and dialysisrelated spondyloarthropathy using non-invasive methods,” Rheumatol. Int. 28, 157–160 (2007). [CrossRef] [PubMed]
- G. N. Stamatas, R. B. Estanislao, M. Suero, Z. S. Rivera, J. Li, A. Khaiat, and N. Kollias, “Facial skin fluorescence as a marker of the skin’s response to chronic environmental insults and its dependence on age,” Br. J. Dermatol. 154, 125–132 (2006). [CrossRef] [PubMed]
- J. W. Feather, M. Hajizadeh-Saffar, G. Leslie, and J. B. Dawson, “A portable scanning reflectance spectrophotometer using visible wavelengths for the rapid measurement of skin pigments,” Phys. Med. Biol. 34, 807–820 (1989). [CrossRef] [PubMed]
- J. B. Dawson, D. J. Barker, D. J. Ellis, E. Grassam, J. A. Cotterill, G. W. Fisher, and J. W. Feather, “A theoretical and experimental study of light absorption and scattering by in vivo skin,” Phys. Med. Biol. 25, 695–709 (1980). [CrossRef] [PubMed]
- J. B. Dawson, D. J. Barker, D. J. Ellis, E. Grassam, J. A. Cotterill, G. W. Fisher, and J. W. Feather, “A theoretical and experimental study of light absorption and scattering by in vivo skin,” Phys. Med. Biol. 25, 695–709 (1980). [CrossRef] [PubMed]
- C. Magnain, M. Elias, and J.-M. Frigerio, “Skin color modeling using the radiative transfer equation solved by the auxiliary function method,” J. Opt. Soc. Am. A. 24, 2196–2205 (2007). [CrossRef]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- G. Zonios, A. Dimou, I. Bassukas, D. Galaris, A. Tsolakidis, and E. Kaxiras, “Melanin absorption spectroscopy: new method for noninvasive skin investigation and melanoma detection,” J. Biomed. Opt. 13, 14017 (2008). [CrossRef]
- H. L. Lutgers, E. G. Gerrits, R. Graaff, T. P. Links, W. J. Sluiter, R. O. Gans, H. J. Bilo, and A. J. Smit, “Skin autofluorescence provides additional information to the UK Prospective Diabetes Study (UKPDS) risk score for the estimation of cardiovascular prognosis in type 2 diabetes mellitus,” Diabetologia 52, 789–797 (2009). [CrossRef] [PubMed]
- D. J. Mulder, P. L. van Haelst, S. Gross, K. de Leeuw, J. Bijzet, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products,” Atherosclerosis 197, 217–223 (2008). [CrossRef]
- D. J. Mulder, T. van deWater, H. L. Lutgers, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations,” Diabetes Technol. Ther. 8, 523–535 (2006). [CrossRef] [PubMed]
- M. Koetsier, H. L. Lutgers, A. J. Smit, T. P. Links, R. de Vries, R. O. B. Gans, G. Rakhorst, and R. Graaff, “Skin autofluorescence for the risk assessment of chronic complications in diabetes: a broad excitation range is sufficient,” Opt. Express 17, 509–519 (2009). [CrossRef] [PubMed]
- R. Meerwaldt, J. W. L. Hartog, R. Graaff, R. J. Huisman, T. P. Links, N. C. den Hollander, S. R. Thorpe, J. W. Baynes, G. Navis, R. O. B. Gans, and A. J. Smit, “Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients,” J. Am. Soc. Nephrol. 16, 3687–3693 (2005). [CrossRef] [PubMed]
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- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
- D. J. Mulder, T. van deWater, H. L. Lutgers, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations,” Diabetes Technol. Ther. 8, 523–535 (2006). [CrossRef] [PubMed]
- R. Meerwaldt, J. W. L. Hartog, R. Graaff, R. J. Huisman, T. P. Links, N. C. den Hollander, S. R. Thorpe, J. W. Baynes, G. Navis, R. O. B. Gans, and A. J. Smit, “Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients,” J. Am. Soc. Nephrol. 16, 3687–3693 (2005). [CrossRef] [PubMed]
- R. Meerwaldt, R. Graaff, P. H. N. Oomen, T. P. Links, J. J. Jager, N. L. Alderson, S. R. Thorpe, J. W. Baynes, R. O. B. Gans, and A. J. Smit, “Simple non-invasive assessment of advanced glycation endproduct accumulation,” Diabetologia 47, 1324–1330 (2004). [CrossRef] [PubMed]
- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- G. N. Stamatas, R. B. Estanislao, M. Suero, Z. S. Rivera, J. Li, A. Khaiat, and N. Kollias, “Facial skin fluorescence as a marker of the skin’s response to chronic environmental insults and its dependence on age,” Br. J. Dermatol. 154, 125–132 (2006). [CrossRef] [PubMed]
- N. Kollias, G. Zonios, and G. N. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002). [CrossRef]
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- R. Na, I.-M. Stender, M. Henriksen, and H. C. Wulf, “Autofluorescence of human skin is age-related after correction for skin pigmentation and redness,” J. Invest. Dermatol. 116, 536–540 (2001). [CrossRef] [PubMed]
- G. N. Stamatas, R. B. Estanislao, M. Suero, Z. S. Rivera, J. Li, A. Khaiat, and N. Kollias, “Facial skin fluorescence as a marker of the skin’s response to chronic environmental insults and its dependence on age,” Br. J. Dermatol. 154, 125–132 (2006). [CrossRef] [PubMed]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
- R. Meerwaldt, J. W. L. Hartog, R. Graaff, R. J. Huisman, T. P. Links, N. C. den Hollander, S. R. Thorpe, J. W. Baynes, G. Navis, R. O. B. Gans, and A. J. Smit, “Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients,” J. Am. Soc. Nephrol. 16, 3687–3693 (2005). [CrossRef] [PubMed]
- R. Meerwaldt, R. Graaff, P. H. N. Oomen, T. P. Links, J. J. Jager, N. L. Alderson, S. R. Thorpe, J. W. Baynes, R. O. B. Gans, and A. J. Smit, “Simple non-invasive assessment of advanced glycation endproduct accumulation,” Diabetologia 47, 1324–1330 (2004). [CrossRef] [PubMed]
- G. Zonios, A. Dimou, I. Bassukas, D. Galaris, A. Tsolakidis, and E. Kaxiras, “Melanin absorption spectroscopy: new method for noninvasive skin investigation and melanoma detection,” J. Biomed. Opt. 13, 14017 (2008). [CrossRef]
- T. Matsumoto, T. Tsurumoto, H. Baba, M. Osaki, H. Enomoto, A. Yonekura, H. Shindo, and T. Miyata, “Measurement of advanced glycation endproducts in skin of patients with rheumatoid arthritis, osteoarthritis, and dialysisrelated spondyloarthropathy using non-invasive methods,” Rheumatol. Int. 28, 157–160 (2007). [CrossRef] [PubMed]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- D. J. Mulder, T. van deWater, H. L. Lutgers, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations,” Diabetes Technol. Ther. 8, 523–535 (2006). [CrossRef] [PubMed]
- D. J. Mulder, P. L. van Haelst, S. Gross, K. de Leeuw, J. Bijzet, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products,” Atherosclerosis 197, 217–223 (2008). [CrossRef]
- J. Sandby-Møller, T. Poulsen, and H. C. Wulf, “Influence of epidermal thickness, pigmentation and redness on skin autofluorescence,” Photochem. Photobiol. 77, 616–620 (2003). [CrossRef] [PubMed]
- R. Na, I.-M. Stender, M. Henriksen, and H. C. Wulf, “Autofluorescence of human skin is age-related after correction for skin pigmentation and redness,” J. Invest. Dermatol. 116, 536–540 (2001). [CrossRef] [PubMed]
- R. Chen, Z. Huang, H. Lui, I. Hamzavi, D. I. McLean, S. Xie, and H. Zeng, “Monte Carlo simulation of cutaneous reflectance and fluorescence measurements – The effect of melanin contents and localization,” J. Photochem. Photobiol. B. 86, 219–226 (2007). [CrossRef]
- T. Matsumoto, T. Tsurumoto, H. Baba, M. Osaki, H. Enomoto, A. Yonekura, H. Shindo, and T. Miyata, “Measurement of advanced glycation endproducts in skin of patients with rheumatoid arthritis, osteoarthritis, and dialysisrelated spondyloarthropathy using non-invasive methods,” Rheumatol. Int. 28, 157–160 (2007). [CrossRef] [PubMed]
- R. Chen, Z. Huang, H. Lui, I. Hamzavi, D. I. McLean, S. Xie, and H. Zeng, “Monte Carlo simulation of cutaneous reflectance and fluorescence measurements – The effect of melanin contents and localization,” J. Photochem. Photobiol. B. 86, 219–226 (2007). [CrossRef]
- L. Bachmann, D. M. Zezell, A. da Costa Ribeiro, L. Gomes, and A. S. Ito, “Fluorescence spectroscopy of biological tissues—A review,” Appl. Spectrosc. Rev. 41, 575–590 (2006). [CrossRef]
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- D. J. Mulder, P. L. van Haelst, S. Gross, K. de Leeuw, J. Bijzet, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products,” Atherosclerosis 197, 217–223 (2008). [CrossRef]
- D. J. Mulder, T. van deWater, H. L. Lutgers, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations,” Diabetes Technol. Ther. 8, 523–535 (2006). [CrossRef] [PubMed]
- G. Zonios, A. Dimou, I. Bassukas, D. Galaris, A. Tsolakidis, and E. Kaxiras, “Melanin absorption spectroscopy: new method for noninvasive skin investigation and melanoma detection,” J. Biomed. Opt. 13, 14017 (2008). [CrossRef]
- G. Zonios and A. Dimou, “Melanin optical properties provide evidence for chemical and structural disorder in vivo,” Opt. Express 16, 8263–8268 (2008). [CrossRef] [PubMed]
- G. Zonios and A. Dimou, “Modeling diffuse reflectance from semi-infinite turbid media: application to the study of skin optical properties,” Opt. Express 14, 8661–8674 (2006). [CrossRef] [PubMed]
- N. Kollias, G. Zonios, and G. N. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002). [CrossRef]
Appl. Opt.
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Appl. Spectrosc. Rev.
- L. Bachmann, D. M. Zezell, A. da Costa Ribeiro, L. Gomes, and A. S. Ito, “Fluorescence spectroscopy of biological tissues—A review,” Appl. Spectrosc. Rev. 41, 575–590 (2006). [CrossRef]
Atherosclerosis
- D. J. Mulder, P. L. van Haelst, S. Gross, K. de Leeuw, J. Bijzet, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products,” Atherosclerosis 197, 217–223 (2008). [CrossRef]
Biophys. J.
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Br. J. Dermatol.
- G. N. Stamatas, R. B. Estanislao, M. Suero, Z. S. Rivera, J. Li, A. Khaiat, and N. Kollias, “Facial skin fluorescence as a marker of the skin’s response to chronic environmental insults and its dependence on age,” Br. J. Dermatol. 154, 125–132 (2006). [CrossRef] [PubMed]
Diabetes Res. Clin. Pract.
- M. Monami, C. Lamanna, F. Gori, F. Bartalucci, N. Marchionni, and E. Mannucci, “Skin autofluorescence in type 2 diabetes: beyond blood glucose,” Diabetes Res. Clin. Pract. 79, 56–60 (2008). [CrossRef]
Diabetes Technol. Ther.
- D. J. Mulder, T. van deWater, H. L. Lutgers, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations,” Diabetes Technol. Ther. 8, 523–535 (2006). [CrossRef] [PubMed]
- M. Koetsier, H. L. Lutgers, C. de Jonge, T. P. Links, A. J. Smit, and R. Graaff, “Reference values of skin autofluorescence,” Diabetes Technol. Ther. 12, 399–403 (2010). [CrossRef] [PubMed]
Diabetologia
- H. L. Lutgers, E. G. Gerrits, R. Graaff, T. P. Links, W. J. Sluiter, R. O. Gans, H. J. Bilo, and A. J. Smit, “Skin autofluorescence provides additional information to the UK Prospective Diabetes Study (UKPDS) risk score for the estimation of cardiovascular prognosis in type 2 diabetes mellitus,” Diabetologia 52, 789–797 (2009). [CrossRef] [PubMed]
- R. Meerwaldt, R. Graaff, P. H. N. Oomen, T. P. Links, J. J. Jager, N. L. Alderson, S. R. Thorpe, J. W. Baynes, R. O. B. Gans, and A. J. Smit, “Simple non-invasive assessment of advanced glycation endproduct accumulation,” Diabetologia 47, 1324–1330 (2004). [CrossRef] [PubMed]
J. Am. Soc. Nephrol.
- R. Meerwaldt, J. W. L. Hartog, R. Graaff, R. J. Huisman, T. P. Links, N. C. den Hollander, S. R. Thorpe, J. W. Baynes, G. Navis, R. O. B. Gans, and A. J. Smit, “Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients,” J. Am. Soc. Nephrol. 16, 3687–3693 (2005). [CrossRef] [PubMed]
J. Biomed. Opt.
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J. Inherit. Metab. Dis.
- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
J. Invest. Dermatol.
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J. Opt. Soc. Am. A.
- C. Magnain, M. Elias, and J.-M. Frigerio, “Skin color modeling using the radiative transfer equation solved by the auxiliary function method,” J. Opt. Soc. Am. A. 24, 2196–2205 (2007). [CrossRef]
J. Photochem. Photobiol. B.
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- R. Chen, Z. Huang, H. Lui, I. Hamzavi, D. I. McLean, S. Xie, and H. Zeng, “Monte Carlo simulation of cutaneous reflectance and fluorescence measurements – The effect of melanin contents and localization,” J. Photochem. Photobiol. B. 86, 219–226 (2007). [CrossRef]
Metabolism
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
Opt. Express
- G. Zonios and A. Dimou, “Modeling diffuse reflectance from semi-infinite turbid media: application to the study of skin optical properties,” Opt. Express 14, 8661–8674 (2006). [CrossRef] [PubMed]
- G. Zonios and A. Dimou, “Melanin optical properties provide evidence for chemical and structural disorder in vivo,” Opt. Express 16, 8263–8268 (2008). [CrossRef] [PubMed]
- M. Koetsier, H. L. Lutgers, A. J. Smit, T. P. Links, R. de Vries, R. O. B. Gans, G. Rakhorst, and R. Graaff, “Skin autofluorescence for the risk assessment of chronic complications in diabetes: a broad excitation range is sufficient,” Opt. Express 17, 509–519 (2009). [CrossRef] [PubMed]
Photochem. Photobiol.
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Phys. Med. Biol.
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Pigment Cell Res.
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PLoS Biol.
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Rheumatol. Int.
- T. Matsumoto, T. Tsurumoto, H. Baba, M. Osaki, H. Enomoto, A. Yonekura, H. Shindo, and T. Miyata, “Measurement of advanced glycation endproducts in skin of patients with rheumatoid arthritis, osteoarthritis, and dialysisrelated spondyloarthropathy using non-invasive methods,” Rheumatol. Int. 28, 157–160 (2007). [CrossRef] [PubMed]
Vib. Spectrosc.
- N. Kollias, G. Zonios, and G. N. Stamatas, “Fluorescence spectroscopy of skin,” Vib. Spectrosc. 28, 17–23 (2002). [CrossRef]
Other
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- Y. P. Sinichkin, N. Kollias, G. I. Zonios, S. R. Utz, and V. V. Tuchin, “Reflectance and fluorescence spectroscopy of human skin in vivo,” in Handbook of optical biomedical diagnostics, V. V. Tuchin, ed., (SPIE Press, Bellingham, WA, USA, 2002), chap. 13, pp. 725–785.
2010, Koetsier, Diabetes Technol. Ther.
- M. Koetsier, H. L. Lutgers, C. de Jonge, T. P. Links, A. J. Smit, and R. Graaff, “Reference values of skin autofluorescence,” Diabetes Technol. Ther. 12, 399–403 (2010). [CrossRef] [PubMed]
- H. L. Lutgers, E. G. Gerrits, R. Graaff, T. P. Links, W. J. Sluiter, R. O. Gans, H. J. Bilo, and A. J. Smit, “Skin autofluorescence provides additional information to the UK Prospective Diabetes Study (UKPDS) risk score for the estimation of cardiovascular prognosis in type 2 diabetes mellitus,” Diabetologia 52, 789–797 (2009). [CrossRef] [PubMed]
- K. P. Nielsen, L. Zhao, G. A. Ryzhikov, M. S. Biryulina, E. R. Sommersten, J. J. Stamnes, K. Stamnes, and J. Moan, “Retrieval of the physiological state of human skin from UV–Vis reflectance spectra – a feasibility study,” J. Photochem. Photobiol. B. 93, 23–31 (2008). [CrossRef] [PubMed]
- G. Zonios, A. Dimou, I. Bassukas, D. Galaris, A. Tsolakidis, and E. Kaxiras, “Melanin absorption spectroscopy: new method for noninvasive skin investigation and melanoma detection,” J. Biomed. Opt. 13, 14017 (2008). [CrossRef]
- D. J. Mulder, P. L. van Haelst, S. Gross, K. de Leeuw, J. Bijzet, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence is elevated in patients with stable coronary artery disease and is associated with serum levels of neopterin and the soluble receptor for advanced glycation end products,” Atherosclerosis 197, 217–223 (2008). [CrossRef]
- H. Ueno, H. Koyama, S. Tanaka, S. Fukumoto, K. Shinohara, T. Shoji,M. Emoto, H. Tahara, R. Kakiya, T. Tabata, T. Miyata, and Y. Nishizawa, “Skin autofluorescence, a marker for advanced glycation end product accumulation, is associated with arterial stiffness in patients with end-stage renal disease,” Metabolism 57, 1452–1457 (2008). [CrossRef] [PubMed]
- M. Monami, C. Lamanna, F. Gori, F. Bartalucci, N. Marchionni, and E. Mannucci, “Skin autofluorescence in type 2 diabetes: beyond blood glucose,” Diabetes Res. Clin. Pract. 79, 56–60 (2008). [CrossRef]
- N. C. den Hollander, D. J. Mulder, R. Graaff, S. R. Thorpe, J. W. Baynes, G. P. A. Smit, and A. J. Smit, “Advanced glycation end products and the absence of premature atherosclerosis in glycogen storage disease Ia,” J. Inherit. Metab. Dis. 30, 916–923 (2007). [CrossRef] [PubMed]
- T. Matsumoto, T. Tsurumoto, H. Baba, M. Osaki, H. Enomoto, A. Yonekura, H. Shindo, and T. Miyata, “Measurement of advanced glycation endproducts in skin of patients with rheumatoid arthritis, osteoarthritis, and dialysisrelated spondyloarthropathy using non-invasive methods,” Rheumatol. Int. 28, 157–160 (2007). [CrossRef] [PubMed]
- C. Magnain, M. Elias, and J.-M. Frigerio, “Skin color modeling using the radiative transfer equation solved by the auxiliary function method,” J. Opt. Soc. Am. A. 24, 2196–2205 (2007). [CrossRef]
- R. Chen, Z. Huang, H. Lui, I. Hamzavi, D. I. McLean, S. Xie, and H. Zeng, “Monte Carlo simulation of cutaneous reflectance and fluorescence measurements – The effect of melanin contents and localization,” J. Photochem. Photobiol. B. 86, 219–226 (2007). [CrossRef]
- G. N. Stamatas, R. B. Estanislao, M. Suero, Z. S. Rivera, J. Li, A. Khaiat, and N. Kollias, “Facial skin fluorescence as a marker of the skin’s response to chronic environmental insults and its dependence on age,” Br. J. Dermatol. 154, 125–132 (2006). [CrossRef] [PubMed]
- L. Bachmann, D. M. Zezell, A. da Costa Ribeiro, L. Gomes, and A. S. Ito, “Fluorescence spectroscopy of biological tissues—A review,” Appl. Spectrosc. Rev. 41, 575–590 (2006). [CrossRef]
- D. J. Mulder, T. van deWater, H. L. Lutgers, R. Graaff, R. O. Gans, F. Zijlstra, and A. J. Smit, “Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: an overview of current clinical studies, evidence, and limitations,” Diabetes Technol. Ther. 8, 523–535 (2006). [CrossRef] [PubMed]
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