Skin autofluorescence predicts cardio-renal outcome in type 1 diabetes: A longitudinal study

Cardiovascular Diabetology

Volumn 15, Issue 1, 2016, Pages

  Vélayoudom Céphise, Fritz Line ^a,b,c   Rajaobelina, Kalina ^a,d   Helmer, Catherine ^d   Nov, Sovanndany ^d   Pupier, Emilie ^a   Blanco, Laurence ^a   Hugo, Marie ^a   Farges, Blandine ^a   Astrugue, Cyril ^d   Gin, Henri ^a   Rigalleau, Vincent ^a,d  

^a HAUT LÉVÊQUE HOSPITAL   (France)

^b UNIVERSITÉ DES ANTILLES   (France)

^c University Hospital of Pointe à Pitre   (France)

^d INSERM   (France)

Author keywords

Albumin excretion rate; Estimated glomerular filtration rate; Macrovascular events; Skin autofluorescence; Type 1 diabetes

Indexed keywords

HEMOGLOBIN A1C; ADVANCED GLYCATION END PRODUCT; BIOLOGICAL MARKER;

ADULT; AGE DISTRIBUTION; ARTICLE; AUTOFLUORESCENCE; BODY MASS; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; DISEASE DURATION; DISEASE MARKER; ESTIMATED GLOMERULAR FILTRATION RATE; HUMAN; HYPERTENSION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY FAILURE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; MICROALBUMINURIA; PREDICTIVE VALUE; SKIN AUTOFLUORESCENCE; SMOKING; URINARY EXCRETION; AGED; ALBUMINURIA; COMPLICATION; DIABETES MELLITUS, TYPE 1; DIABETIC ANGIOPATHIES; DIABETIC NEPHROPATHIES; FEMALE; GLOMERULUS FILTRATION RATE; KIDNEY; LUMINESCENCE; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; ODDS RATIO; PATHOPHYSIOLOGY; PROGNOSIS; RISK ASSESSMENT; RISK FACTOR; SKIN; STATISTICAL MODEL; TIME FACTOR;

ADULT; AGED; ALBUMINURIA; BIOMARKERS; DIABETES MELLITUS, TYPE 1; DIABETIC ANGIOPATHIES; DIABETIC NEPHROPATHIES; FEMALE; GLOMERULAR FILTRATION RATE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; KIDNEY; LOGISTIC MODELS; LONGITUDINAL STUDIES; LUMINESCENT MEASUREMENTS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; ODDS RATIO; PREDICTIVE VALUE OF TESTS; PROGNOSIS; RISK ASSESSMENT; RISK FACTORS; SKIN; TIME FACTORS;

EID: 84984829210     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-016-0448-8     Document Type: Article

References (36)

1. Lind M, Svensson AM, Kosiborod M, Gudbjörnsdottir S, Pivodic A, Wedel H, Dahlqvist S, Clements M, Rosengren A. Glycemic control and excess mortality in type 1 diabetes. N Engl J Med. 2014;371:1972-82.
2. Groop PH, Thomas MC, Moran JL, Wadèn J, Thorn LM, Mäkinen VP, Rosengård-Bärlund M, Saraheimo M, Hietala K, Heikkilä O, Forsblom C, FinnDiane Study Group. The presence and severity of chronic kidney disease predicts all-cause mortality in type 1 diabetes. Diabetes. 2009;58:1651-8.
3. Chuyen NV. Toxicity of the AGEs generated from the Maillard reaction: on the relationship of food-AGEs and biological-AGEs. Mol Nutr Food Res. 2006;50:1140-9.
4. Huebschmann AG, Regensteiner JG, Vlassara H, Reusch JE. Diabetes and advanced glycoxidation end products. Diabetes Care. 2006;29:1420-32.
5. Daroux M, Prevost G, Maillard-Lefebvre H, Gaxatte C, D'Agati VD, Schmidt AM, Boulanger E. Advanced glycation end-products: implications for diabetic and non-diabetic nephropathies. Diabetes Metab. 2010;36:1-10.
6. Nin JW, Jorsal A, Ferreira I, Schalkwijk CG, Prins MH, Parving HH, Tarnow L, Rossing P, Stehouwer CD. Higher plasma levels of advanced glycation end products are associated with incident cardiovascular disease and all-cause mortality in type 1 diabetes: a 12 year follow-up study. Diabetes Care. 2011;34:442-7.
7. Genuth S, Sun W, Cleary P, Sell DR, Dahms W, Malone J, Sivitz W, Monnier VM, DCCT Skin Collagen Ancillary Study Group. Glycation and carboxymethyllysine 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;54:3103-11.
8. Monnier VM, Sun W, Gao X, Sell DR, Cleary PA, Lachin JM, Genuth S, DCCT/EDIC Research Group. Skin collagen advanced glycation endproducts (AGEs) and the long-term progression of sub-clinical cardiovascular disease in type 1 diabetes. Cardiovasc Diabetol. 2015;14:118.
9. 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;16:3687-93.
10. Gerrits EG, Lutgers HL, Kleefstra N, Graaff R, Groenier KH, Smit AJ, Gans RO, Bilo HJ. Skin autofluorescence: a tool to identify type 2 diabetic patients at risk for developing microvascular complications. Diabetes Care. 2008;31:517-21.
11. Lutgers HL, Gerrits EG, Graaff R, Links TP, Sluiter WJ, Gans RO, Bilo HJ, Smit AJ. 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. 2009;52:789-97.
12. Genevieve M, Vivot A, Gonzalez C, Raffaitin C, Barberger-Gateau, PGin H, Rigalleau V. Skin autofluorescence is associated with past glycaemic control and complications in type 1 diabetes mellitus. Diabetes Metab. 2013;39:349-54.
13. Krolewski AS, Niewczas MA, Skupien J, Gohda T, Smiles A, Eckfeldt JH, Doria A, Warram JH. Early progressive renal decline precedes the onset of microalbuminuria and its progression to macroalbuminuria. Diabetes Care. 2014;37:226-34.
14. Araszkiewicz A, Naskret D, Zozulinska-Ziolkiewicz D, Pilacinski S, Uruska A, Grzelka A, Wegner M, Wierusz-Wysocka B. Skin autofluorescence is associated with carotid intima-media thickness, diabetic microangiopathy, and long-lasting metabolic control in type 1 diabetic patients. Results from Poznan Prospective Study. Microvasc Res. 2015;98:62-7.
15. Llauradó G, Ceperuelo-Mallafré V, Vilardell C, Simó R, Gil P, Cano A, Vendrell J, González-Clemente JM. Advanced glycation end products are associated with arterial stiffness in type 1 diabetes. J Endocrinol. 2014;221:405-13.
16. Januszewski AS, Sachithanandan N, Karschimkus C, O'Neal DN, Yeung CK, Alkatib N, Jenkins AJ. Non-invasive measures of tissue autofluorescence are increased in Type 1 diabetes complications and correlate with a non-invasive measure of vascular dysfunction. Diabet Med. 2012;29:726-33.
17. Conway B, Edmundowicz D, Matter N, Maynard J, Orchard T. Skin fluorescence correlates strongly with coronary artery calcification severity in type 1 diabetes. Diabetes Technol Ther. 2010;12:339-45.
18. Sell DR, Sun W, Gao X, Strauch C, Lachin JM, Cleary PA, Genuth S, DCCT/EDIC Research Group. Monnier VM. Skin collagen fluorophore LW-1 versus skin fluorescence as markers for the long-term progression of subclinical macrovascular disease in type 1 diabetes. Cardiovasc Diabetol. 2016;15:30. doi: 10.1186/s12933-016-0343-3.
19. Conway BN, Aroda VR, Maynard JD, Matter N, Fernandez S, Ratner RE, Orchard TJ. Skin intrinsic fluorescence is associated with coronary artery disease in individuals with long duration of type 1 diabetes. Diabetes Care. 2012;35:2331-6.
20. Nin JW, Ferreira I, Schalkwijk CG, Prins MH, Chaturvedi N, Fuller JH, Stehouwer CD, EURODIAB Prospective Complications Study Group. Levels of soluble receptor for AGE are cross-sectionally associated with cardiovascular disease in type 1 diabetes, and this association is partially mediated by endothelial and renal dysfunction and by low-grade inflammation: the EURODIAB Prospective Complications Study. Diabetologia. 2009;52:705-14.
21. Fokkens BT, Smit AJ. Skin fluorescence as a clinical tool for non-invasive assessment of advanced glycation and long-term complications of diabetes. Glycoconj J. 2016. doi: 10.1007/s10719-016-9683-1.
22. 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;47:1324-30.
23. Hofmann B, Jacobs K, Navarrete Santos A, Wienke A, Silber RE, Simm A. Relationship between cardiac tissue glycation and skin autofluorescence in patients with coronary artery disease. Diabete Metab. 2015;41:410-5.
24. Tanaka K, Nakayama M, Kanno M, Kimura H, Watanabe K, Tani Y, Kusano Y, Suzuki H, Hayashi Y, Asahi K, Sato K, Miyata T, Watanabe T. Skin autofluorescence is associated with the progression of chronic kidney disease: a prospective observational study. PLoS One. 2013;8(12):e83799.
25. Sugisawa E, Miura J, Iwamoto Y, Uchigata Y. Skin autofluorescence reflects integration of past long-term glycemic control in patients with type 1 diabetes. Diabetes Care. 2013;36:2339-45.
26. Tanaka K, Tani Y, Asai J, Nemoto F, Kusano Y, Suzuki H, Hayashi Y, Asahi K, Katoh T, Miyata T, Watanabe T. Skin autofluorescence is associated with renal function and cardiovascular diseases in pre-dialysis chronic kidney disease patients. Nephrol Dial Transplant. 2011;26:214-20.
27. Sternberg M, M'bemba J, Urios P, Borsos AM, Selam JL, Peyroux J, Slama G. Skin collagen pentosidine and fluorescence in diabetes were predictors of retinopathy progression and creatininemia increase already 6 years after punch-biopsy. Clin Biochem. 2016;49:225-31.
28. de Boer IH, Afkarian M, Rue TC, Cleary PA, Lachin JM, Molitch ME, Steffes MW, Sun W, Zinman B, Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Research Group. Renal outcomes in patients with type 1 diabetes and macroalbuminuria. J Am Soc Nephrol. 2014;25(10):2342-50.
29. Beisswenger PJ, Howell SK, Russell GB, Miller ME, Rich SS, Mauer M. Early progression of diabetic nephropathy correlates with methylglyoxal-derived advanced glycation end products. Diabetes Care. 2013;36:3234-9.
30. Rajaobelina K, Cougnard-Gregoire A, Delcourt C, Gin H, Barberger-Gateau P, Rigalleau V. Autofluorescence of skin advanced glycation end products: marker of metabolic memory in elderly population. J Gerontol A Biol Sci Med Sci. 2015;70:841-6.
31. Lind M, Odén A, Fahlén M, Eliasson B. The shape of the metabolic memory of HbA1c: re-analysing the DCCT with respect to time-dependent effects. Diabetologia. 2010;53:1093-8.
32. Banser A, Naafs JC, Hoorweg-Nijman JJ, van de Garde EM, van der Vorst MM. Advanced glycation end products, measured in skin, vs. HbA1c in children with type 1 diabetes mellitus. Pediatr Diabetes. 2016;17(6):426-32.
33. Orchard TJ, Lyons TJ, Cleary PA, Braffett BH, Maynard J, Cowie C, Gubitosi-Klug RA, Way J, Anderson K, Barnie A, Villavicencio S, DCCT/EDIC Research Group. The association of skin intrinsic fluorescence with type 1 diabetes complications in the DCCT/EDIC study. Diabetes Care. 2013;36:3146-53.
34. Cleary PA, Braffett BH, Orchard T, Lyons TJ, Maynard J, Cowie C, Gubitosi-Klug RA, Way J, Anderson K, Barnie A, Villavicencio S, DCCT/EDIC Research Group. Clinical and technical factors associated with skin intrinsic fluorescence in subjects with type 1 diabetes from the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Study. Diabetes Technol Ther. 2013;15:466-74.
35. Goh SY, Cooper ME. Clinical review: The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab. 2008;93:1143-52.
36. Borch-Johnsen K. Epidemiology of microangiopathy in type 1 diabetes mellitus. A review. Diabete Metab. 1993;19:133-7.