Skin autofluorescence, a novel marker for glycemic and oxidative stress-derived advanced glycation endproducts: An overview of current clinical studies, evidence, and limitations

Diabetes Technology and Therapeutics

Volumn 8, Issue 5, 2006, Pages 523-535

  Mulder, Douwe J ^a   Van De Water, Tara ^a   Lutgers, Helen L ^a   Graaff, Reindert ^a   Gans, Rijk O ^a   Zijlstra, Felix ^a   Smit, Andries J ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT;

ARTICLE; AUTOFLUORESCENCE; DIABETES MELLITUS; DIAGNOSTIC ACCURACY; DIAGNOSTIC VALUE; DISEASE COURSE; DISEASE MARKER; GLUCOSE BLOOD LEVEL; HUMAN; ISCHEMIC HEART DISEASE; KIDNEY FAILURE; MORTALITY; NON INVASIVE MEASUREMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; RELATIVE SKIN REFLECTANCE; RELIABILITY; RISK FACTOR; SKIN EXAMINATION; SKIN PIGMENTATION;

BIOLOGICAL MARKERS; DIABETIC ANGIOPATHIES; DIAGNOSTIC EQUIPMENT; EQUIPMENT DESIGN; FLUORESCENCE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; OXIDATIVE STRESS; SKIN PHYSIOLOGY; SKIN PIGMENTATION; SPECTROMETRY, FLUORESCENCE;

EID: 33845602222     PISSN: 15209156     EISSN: None     Source Type: Journal    
DOI: 10.1089/dia.2006.8.523     Document Type: Article

References (63)

1. Smit A, Lutgers H: The clinical relevance of advanced glycation endproducts (AGE) and recent developments in pharmaceutics to reduce AGE accumulation. Curr Med Chem 2004;11:2767-2784.
2. Baynes JW, Thorpe SR: Glycoxidation and lipoxidation in atherogenesis. Free Radic Biol Med 2000;28:1708-1716.
3. Miyata T, Ypersele, De Strihou C, Kurokawa K, Baynes JW: Alterations in nonenzymatic biochemistry in uremia: origin and significance of 'carbonyl stress' in long-term uremic complications. Kidney Int 1999;55:389-399.
4. Fu MX, Requena JR, Jenkins AJ, Lyons TJ, Baynes JW, Thorpe SR: The advanced glycation end product, Nepsilon-(carboxymethyl)lysine, is a product of both lipid peroxidation and glycoxidation reactions. J Biol Chem 1996;271:9982-9986.
5. Monnier VM, Cerami A: Nonenzymatic browning in vivo: possible process for aging of long-lived proteins. Science 1981;211:491-493.
6. Monnier VM, Vishwanath V, Frank KE: Relation between complications of Type I diabetes mellitus and collagen-linked fluorescence. N Engl J Med 1986;314:403-408.
7. Sell DR, Lapolla A, Odetti P, Fogarty J, Monnier VM: Pentosidine formation in skin correlates with severity of complications in individuals with long-standing IDDM. Diabetes 1992;41:1286-1292.
8. McCance DR, Dyer DG, Dunn JA, Bailie KE, Thorpe SR, Baynes JW, Lyons TJ: Maillard reaction products and their relation to complications in insulin-dependent diabetes mellitus. J Clin Invest 1993;91:2470-2478.
9. Dyer DG, Dunn JA, Thorpe SR, Bailie KE, Lyons TJ, McCance DR, Baynes JW: Accumulation of Maillard reaction products in skin collagen in diabetes and aging. J Clin Invest 1993;91:2463-2469.
10. Lee WK, Akyol M, Shaw S, Dominiczak MH, Briggs JD: Kidney transplantation decreases the tissue level of advanced glycosylation end-products. Nephrol Dial Transplant 1995;10:103-107.
11. 1C as markers of diabetic complications. DCCT Skin Collagen Ancillary Study Group. Diabetes Control and Complications Trial. Diabetes 1999;48:870-880.
12. Genuth S, Sun W, Cleary P, Sell DR, Dahms W, Malone J, Sivitz W, Monnier VM; DCCT Skin Collagen Ancillary Study Group: Glycation and carboxy-methyllysine levels in skin collagen predict the risk of future 10-year progression of diabetic retinopathy and nephropathy in the Diabetes Control and Complications Trial and Epidemiology of Diabetes Interventions and Complications participants with Type 1 diabetes. Diabetes 2005;54:3103-3111.
13. Vlassara H, Uribarri J: Glycoxidation and diabetic complications: modern lessons and a warning? Rev Endocr Metab Disord 2004;5:181-188.
14. Kalousova M, Zima T, Tesar V, Stipek S, Sulkova S: Advanced glycation end products in clinical nephrology. Kidney Blood Press Res 2004;27:18-28.
15. Kanauchi M, Nishioka H, Dohi K: Serum levels of advanced glycosylation end products in diabetic nephropathy. Nephron 2001;89:228-230.
16. Dorrian CA, Cathcart S, Clausen J, Shapiro D, Dominiczak MH: Factors in human serum interfere with the measurement of advanced glycation endproducts. Cell Mol Biol 1998;44:1069-1079.
17. Hricik DE, Wu YC, Friedlander MA, Schulak JA: Disparate changes in plasma and tissue pentosidine levels after kidney and kidney-pancreas transplantation. Clin Transplant 1996;10:568-573.
18. Schwedler SB, Metzger T, Schinzel R, Wanner C: Advanced glycation end products and mortality in hemodialysis patients. Kidney Int 2002;62:301-310.
19. Stein G, Busch M, Miller A, Muller A, Wendt T, Franke C, Niwa T, Franke S: Are advanced glycation end products cardiovascular risk factors in patients with CRF? Am J Kidney Dis 2003;41(3 Suppl 1):S52-S56.
20. Stitt AW: Advanced glycation: an important pathological event in diabetic and age related ocular disease. Br J Ophthalmol 2001;85:746-753.
21. Sasaki N, Fukatsu R, Tsuzuki K, Hayashi Y, Yoshida T, Fujii N, Koike T, Wakayama I, Yanagihara R, Garruto R, Amano N, Makita Z: Advanced glycation end products in Alzheimer's disease and other neurodegenerative diseases. Am J Pathol 1998;153:1149-1155.
22. Verzijl N, Bank RA, TeKoppele JM, DeGroot J: AGEing and osteoarthritis: a different perspective. Curr Opin Rheumatol 2003;15:616-622.
23. Stitt AW, He C, Friedman S, Scher L, Rossi P, Ong L, Founds H, Li YM, Bucala R, Vlassara H: Elevated AGE-modified ApoB in sera of euglycemic, normolipidemic patients with atherosclerosis: relationship to tissue AGEs. Mol Med 1997;3:617-627.
24. Kanauchi M, Tsujimoto N, Hashimoto T: Advanced glycation end products in nondiabetic patients with coronary. Diabetes Care 2001;24:1620-1623.
25. Kilhovd BK, Juutilainen A, Lehto S, Ronnemaa T, Torjesen PA, Birkeland KI, Berg TJ, Hanssen KF, Laakso M: High serum levels of advanced glycation end products predict increased coronary heart disease mortality in nondiabetic women but not in nondiabetic men: a population-based 18-year follow-up study. Arterioscler Thromb Vasc Biol 2005;25:815-820.
26. Monnier VM: Skin collagen fluorescence predicts coronary artery calcium deposition in the Epidemiology of Diabetes Intervention and Complications (EDIC) study [abstract]. Diabetes 2004;53:A77.
27. Monnier VM, Vishwanath V, Frank KE, Elmets CA, Dauchot P, Kohn RR: Relation between complications of type I diabetes mellitus and collagen-linked fluorescence. N Engl J Med 1986;314:403-408.
28. Niwa T: Mass spectrometry in the search for uremic toxins. Mass Spectrom Rev 1997;16:307-332.
29. Miyata T, Ueda Y, Shinzato T, Iida Y, Tanaka S, Kurokawa K, van Ypersele de Strihou C, Maeda K: Accumulation of albumin-linked and free-form pentosidine in the circulation of uremic patients with endstage renal failure: renal implications in the pathophysiology of pentosidine. J Am Soc Nephrol 1996;7:1198-1206.
30. Dorrian CA, Cathcart S, Clausen J, Shapiro D, Dominiczak MH: Factors in human serum interfere with the measurement of advanced glycation endproducts. Cell Mol Biol (Noisy-le-grand) 1998;44:1069-1079.
31. Schiel R, Franke S, Appel T: Improvement of the quality of diabetes control and decrease in the concentrations of AGE-products in patients with type 1 and insulin-treated type 2 diabetes mellitus-results from a 10 year-prospective, population-based survey on the quality of diabetes care in Germany (JEVIN). Eur J Med Res 2004;9:391-399.
32. Sampathkumar R, Balasubramanyam M, Rema M, Premanand C, Mohan V: A novel advanced glycation index and its association with diabetes and microangiopathy. Metabolism 2005;54:1002-1007.
33. Rocken C, Kientsch-Engel R, Mansfeld S, Stix B, Stubenrauch K, Weigle B, Buhling F, Schwan M, Saeger W: Advanced glycation end products and receptor for advanced glycation end products in AA amyloidosis. Am J Pathol 2003;162:1213-1220.
34. Wrobel K, Wrobel K, Garay-Sevilla ME, Nava LE, Malacara JM: Novel analytical approach to monitoring advanced glycosylation end products in human serum with on-line spectrophotometric and spectrofluorometric detection in a flow system. Clin Chem 1997;43:1563-1569.
35. Falcone C, Emanuele E, D'Angelo A, Buzzi MP, Belvito C, Cuccia M, Geroldi D: Plasma levels of soluble receptor for advanced glycation end products and coronary artery disease in nondiabetic men. Arterioscler Thromb Vasc Biol 2005;25:1032-1037.
36. Geroldi D, Falcone C, Emanuele E, D'Angelo A, Calcagnino M, Buzzi MP, Scioli GA, Fogari R: Decreased plasma levels of soluble receptor for advanced glycation end-products in patients with essential hypertension. J Hypertens 2005;23:1725-1729.
37. Bierhaus A, Hofmann MA, Ziegler R, Nawroth PP: AGEs and their interaction with AGE-receptors in vascular disease and diabetes mellitus. I. The AGE concept. Cardiovasc Res 1998;37:586-600.
38. Stam F, Schalkwijk CG, van Guldener C, ter Wee PM, Stehouwer CDA: Advanced glycation end-product peptides are associated with impaired renal function, but not with biochemical markers of endothelial dysfunction and inflammation, in non-diabetic individuals. Nephrol Dial Transplant 2006;21:677-682. Epub 2005 Dec 5.
39. Deppisch R, Beck W, Ritz E, Henle T, Hergesell O, Hensch GM: Advanced glycated end-products (AGE) during haemodialysis treatment: discrepant results with different methodologies reflecting the heterogeneity of AGE compounds. Nephrol Dial Transplant 1999;14:1968-1975.
40. Meerwaldt R, Hartog JW, Graaff R, Huisman RJ, Links TP, den Hollander NC, Thorpe SR, Baynes JW, Navis G, Gans RO, Smit AJ: Skin autofluorescence, a measure of cumulative metabolic stress and advanced glycation end products, predicts mortality in hemodialysis patients. J Am Soc Nephrol 2005;16:3687-3693.
41. Jager J, Oomen PH, Sluiter WJ, Reitsma WD, Smit AJ: Improved reproducibility of the 'large-window' method of assessing transcapillary and interstitial fluorescein diffusion in the skin in healthy subjects and in subjects with insulin-dependent diabetes mellitus. Int J Microcirc Clin Exp 1997;17:150-158.
42. Utzinger U, Richards-Kortum RR: Fiber optic probes for biomedical optical spectroscopy. J Biomed Opt 2003;8:121-147.
43. Koefoed Theil P, Larsen M, Lund-Andersen H, Hansen T, Pedersen O: Lens autofluorescence is increased in newly diagnosed patients with NIDDM. Diabetologia 1996;39:1524-1527.
44. Mota MC, Pereira P, Burrows H, Morgado AM, Matos A: Evaluation of a non-invasive fluorescence technique as a marker for diabetic lenses in vivo. Graefes Arch Clin Exp Ophthalmol 1999;237:187-192.
45. Sato E, Mori F, Igarashi S, Abiko T, Takeda M, Ishiko S, Yoshida A: Corneal advanced glycation end products increase in patients with proliferative diabetic retinopathy. Diabetes Care 2001;24:479-482.
46. Coremans JM, Ince C, Bruining HA, Puppels GJ: (Semi-)quantitative analysis of reduced nicotinamide adenine dinucleotide fluorescence images of blood-perfused rat heart. Biophys J 1997;72:1849-1860.
47. Na R, Stender IM, Henriksen M, Wulf HC: Autofluorescence of human skin is age-related after correction for skin pigmentation and redness. J Invest Dermatol 2001;116:536-540.
48. Meerwaldt R, Links T, Graaff R, Thorpe SR, Baynes JW, Hartog J, Gans R, Smit A: Simple noninvasive measurement of skin autofluorescence. Ann NY Acad Sci 2005;1043:290-298.
49. Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, Alderson NL, Thorpe SR, Baynes JW, Gans RO, Smit AJ: Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 2004;47:1324-1330.
50. Ahmed MU, Brinkmann FE, Degenhardt TP, Thorpe SR, Baynes JW: N-epsilon-(Carboxyethyl) lysine, a product of the chemical modification of proteins by methylglyoxal, increases with age in human lens proteins. Biochem J 1997;324:565-570.
51. Maekawa T, Rathinasamy TK, Altman KI, Forbes WF: Changes in collagen with age. I. The extraction of acid soluble collagens from the skin of mice. Exp Gerontol 1970;5:177-186.
52. Meerwaldt R, Links TP, Graaff R, Hoogenberg K, Lefrandt JD, Baynes JW, Gans RO, Smit AJ: Increased accumulation of skin advanced glycation end-products precedes and correlates with clinical manifestation of diabetic neuropathy. Diabetologia 2005;48:1637-1644.
53. Lutgers HL, Links TP, Graaff R, Bilo HJG, Gans ROB, Smit AJ: Skin AGE-levels are increased in type 2 diabetes mellitus with complications [abstract]. Diabetologia 2005;48:A419.
54. Hartog J, de Vries A, Lutgers H, Meerwaldt R, Huisman RM, van Son WJ, de Jong PE, Smit AJ: Accumulation of advanced glycation end products, measured as skin autofluorescence, in renal disease. Ann NY Acad Sci 2005;1043:299-307.
55. Mulder DJ, van Haelst PL, Graaff R, Smit AJ, Gans ROB, Zijlstra F: Skin autofluorescence is an independent marker for acute myocardial infarction. Circulation 2005;112:II-371.
56. Kollias N, Zonios G, Stamatas GN: Fluorescence spectroscopy of skin. Vibrational Spectrosc 2002;28:17-23.
57. Evans ND, Gnudi L, Rolinski OJ, Birch DJ, Pickup JC: Non-invasive glucose monitoring by NAD(P)H autofluorescence spectroscopy in fibroblasts and adipocytes: a model for skin glucose sensing. Diabetes Technol Ther 2003;5:807-816.
58. Evans ND, Gnudi L, Rolinski OJ, Birch DJ, Pickup JC: Glucose-dependent changes in NAD(P)H-related fluorescence lifetime of adipocytes and fibroblasts in vitro: potential for non-invasive glucose sensing in diabetes mellitus. J Photochem Photobiol B 2005;80:122-129.
59. Kollias N, Gillies R, Moran M, Kochevar IE, Anderson RR: Endogenous skin fluorescence includes bands that may serve as quantitative markers of aging and photoaging. J Invest Dermatol 1998;111:776-780.
60. Sandby-Moller J, Poulsen T, Wulf HC: Influence of epidermal thickness, pigmentation and redness on skin autofluorescence. Photochem Photobiol 2003;77:616-620.
61. Fitzpatrick TB: The validity and practicality of sun-reactive skin types I through VI. Arch Dermatol 1988;124:869-871.
62. Hull E, Ediger M, Unione A, Deemer E, Stroman M, Baynes J: Noninvasive, optical detection of diabetes: model studies with porcine skin. Optics Express 2004;12:4496-4510.
63. Graaf R, Meerwaldt R, Lutgers HL, Baptist R, de Jong ED, Zijp JR, Links TP, Smit AJ, Rakhorst G: Instrumentation for the measurement of autofluorescence on the human skin. Proc SPIE 2005;5692:111-118.