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Journal of Pediatric Endocrinology and Metabolism

Editor-in-Chief: Kiess, Wieland

Ed. by Bereket, Abdullah / Darendeliler, Feyza / Dattani, Mehul / Gustafsson, Jan / Luo, Fei Hong / Mericq, Veronica / Toppari, Jorma

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Volume 32, Issue 1


Skin autofluorescence in children with and without obesity

Yvette E. Lentferink / Lisa van Teeseling / Catherijne A.J. Knibbe
  • Department of Clinical Pharmacy, St. Antonius Hospital, Nieuwegein, The Netherlands
  • LACDR, Leiden University, Leiden, The Netherlands
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Marja M.J. van der Vorst
Published Online: 2018-12-11 | DOI: https://doi.org/10.1515/jpem-2018-0237



Obesity is associated with oxidative stress, which is related to increased advanced glycation end product (AGE) formation. AGEs accumulated in skin collagen can be measured with skin autofluorescence (sAF). There are conflicting reports on the influence of obesity on sAF in adults and no data in children. Therefore, this study evaluated sAF in pediatric patients with and without obesity.


In this cross-sectional study, participants aged 4–18 years were included: patients with obesity (body mass index standard deviation score [BMI-SDS] >2.3) and lean controls (BMI-SDS >–1.1 to <1.1). sAF was measured using the AGE Reader®. Participants were stratified according to age (<10, ≥10 to <13, ≥13 to <15, ≥15 to <17 and ≥17 years) and skin type (I–VI).


In total, 143 patients and 428 controls were included. In patients, there was no influence of age on sAF (p=0.09). In controls, sAF was higher in children aged <10 years compared to ≥10 to <13 and ≥13 to <15 years (p=0.02; p=0.04). Stratified by age, sAF was higher in patients compared to controls in all age categories, except <10 years of age (p<0.01), while this was not observed when stratified by skin type (p>0.05). Skin type and BMI were significant covariates for sAF.


BMI was a covariate for sAF; however, no difference in sAF was observed between children with and without obesity, stratified by skin type. Duration of obesity as well as accuracy of the AGE Reader® might explain this difference. Further research is warranted, in which patients should be matched for age and skin type.

This article offers supplementary material which is provided at the end of the article.

Keywords: advanced glycation end products; children; obesity; skin autofluorescence


  • 1.

    Lobstein T, Jackson-Leach R. Planning for the worst: estimates of obesity and comorbidities in school-age children in 2025. Pediatr Obes 2016;11:321–5.CrossrefWeb of SciencePubMedGoogle Scholar

  • 2.

    Kelly AS, Barlow SE, Rao G, Inge TH, Hayman LL, et al. Severe obesity in children and adolescents: identification, associated health risks, and treatment approaches: a scientific statement from the American Heart Association. Circulation 2013;128:1689–712.CrossrefWeb of SciencePubMedGoogle Scholar

  • 3.

    Lutgers HL, Graaff R, Links TP, Ubink-Veltmaat LJ, Bilo HJ, et al. Skin autofluorescence as a noninvasive marker of vascular damage in patients with type 2 diabetes. Diabetes Care 2006;29:2654–9.CrossrefPubMedGoogle Scholar

  • 4.

    den Engelsen C, van den Donk M, Gorter KJ, Salome PL, Rutten GE. Advanced glycation end products measured by skin autofluorescence in a population with central obesity. Dermatoendocrinol 2012;4:33–8.CrossrefGoogle Scholar

  • 5.

    Stirban A, Pop A, Fischer A, Heckermann S, Tschoepe D. Variability of skin autofluorescence measurement over 6 and 12 weeks and the influence of benfotiamine treatment. Diabetes Technol Ther 2013;15:733–7.PubMedCrossrefWeb of ScienceGoogle Scholar

  • 6.

    Goldberg T, Cai W, Peppa M, Dardaine V, Baliga BS, et al. Advanced glycoxidation end products in commonly consumed foods. J Am Diet Assoc 2004;104:1287–91.CrossrefPubMedGoogle Scholar

  • 7.

    Gupta A, Uribarri J. Dietary advanced glycation end products and their potential role in cardiometabolic disease in children. Horm Res Paediatr 2016;85:291–300.CrossrefPubMedWeb of ScienceGoogle Scholar

  • 8.

    Meerwaldt R, Graaff R, Oomen PH, Links TP, Jager JJ, et al. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 2004;47:1324–30.CrossrefPubMedGoogle Scholar

  • 9.

    Koetsier M, Nur E, Chunmao H, Lutgers HL, Links TP, et al. Skin color independent assessment of aging using skin autofluorescence. Opt Express 2010;18:14416–29.Web of SciencePubMedCrossrefGoogle Scholar

  • 10.

    Da Moura Semedo C, Webb M, Waller H, Khunti K, Davies M. Skin autofluorescence, a non-invasive marker of advanced glycation end products: clinical relevance and limitations. Postgrad Med J 2017;93:289–94.CrossrefWeb of SciencePubMedGoogle Scholar

  • 11.

    Koetsier M, Lutgers HL, de Jonge C, Links TP, Smit AJ, et al. Reference values of skin autofluorescence. Diabetes Technol Ther 2010;12:399–403.CrossrefWeb of SciencePubMedGoogle Scholar

  • 12.

    van Waateringe RP, Slagter SN, van Beek AP, van der Klauw MM, van Vliet-Ostaptchouk JV, et al. Skin autofluorescence, a non-invasive biomarker for advanced glycation end products, is associated with the metabolic syndrome and its individual components. Diabetol Metab Syndr 2017;9:42,017-0241-1. eCollection 2017.CrossrefPubMedWeb of ScienceGoogle Scholar

  • 13.

    Vlassara H, Uribarri J. Glycoxidation and diabetic complications: modern lessons and a warning? Rev Endocr Metab Disord 2004;5:181–8.CrossrefGoogle Scholar

  • 14.

    Genuth S, Sun W, Cleary P, Sell DR, Dahms W, et al. 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.PubMedGoogle Scholar

  • 15.

    Stitt AW, He C, Friedman S, Scher L, Rossi P, et al. Elevated AGE-modified ApoB in sera of euglycemic, normolipidemic patients with atherosclerosis: relationship to tissue AGEs. Mol Med 1997;3:617–27.PubMedCrossrefGoogle Scholar

  • 16.

    Kilhovd BK, Juutilainen A, Lehto S, Ronnemaa T, Torjesen PA, et al. 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;25:815–20.CrossrefGoogle Scholar

  • 17.

    Kanauchi M, Tsujimoto N, Hashimoto T. Advanced glycation end products in nondiabetic patients with coronary artery disease. Diabetes Care 2001;24:1620–3.CrossrefPubMedGoogle Scholar

  • 18.

    Manna P, Jain SK. Obesity, oxidative stress, adipose tissue dysfunction, and the associated health risks: causes and therapeutic strategies. Metab Syndr Relat Disord 2015;13:423–44.Web of ScienceCrossrefPubMedGoogle Scholar

  • 19.

    Ahmad MS, Damanhouri ZA, Kimhofer T, Mosli HH, Holmes E. A new gender-specific model for skin autofluorescence risk stratification. Sci Rep 2015;5:10198.CrossrefWeb of SciencePubMedGoogle Scholar

  • 20.

    Sanchez E, Baena-Fustegueras JA, de la Fuente MC, Gutierrez L, Bueno M, et al. Advanced glycation end-products in morbid obesity and after bariatric surgery: When glycemic memory starts to fail. Endocrinol Diabetes Nutr 2017;64:4–10.PubMedWeb of ScienceGoogle Scholar

  • 21.

    Sebekova K, Somoza V, Jarcuskova M, Heidland A, Podracka L. Plasma advanced glycation end products are decreased in obese children compared with lean controls. Int J Pediatr Obes 2009;4:112–8.PubMedCrossrefWeb of ScienceGoogle Scholar

  • 22.

    Accacha S, Rosenfeld W, Jacobson A, Michel L, Schnurr FJ, et al. Plasma advanced glycation end products (AGEs), receptors for AGEs and their correlation with inflammatory markers in middle school-age children. Horm Res Paediatr 2013;80:318–27.PubMedCrossrefWeb of ScienceGoogle Scholar

  • 23.

    Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes 2012;7:284–94.Web of ScienceCrossrefPubMedGoogle Scholar

  • 24.

    Hirasing RA, Fredriks AM, van Buuren S, Verloove-Vanhorick SP, Wit JM. Increased prevalence of overweight and obesity in Dutch children, and the detection of overweight and obesity using international criteria and new reference diagrams. Ned Tijdschr Geneeskd 2001;145:1303–8.PubMedGoogle Scholar

  • 25.

    Fitzpatrick TB. The validity and practicality of sun-reactive skin types I through VI. Arch Dermatol 1988;124:869–71.CrossrefPubMedGoogle Scholar

  • 26.

    De TNO groeicalculator voor professionals - op basis van de vijfde landelijke groeistudie. Available at: https://www.tno.nl/nl/aandachtsgebieden/gezond-leven/prevention-work-health/gezond-en-veilig-opgroeien/groeicalculator-voor-professionals/.

  • 27.

    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412–9.PubMedCrossrefGoogle Scholar

  • 28.

    van der Aa MP, Farsani FS, Kromwijk LA, de Boer A, Knibbe CA, et al. How to screen obese children at risk for type 2 diabetes mellitus? Clin Pediatr (Phila) 2014;53:337–42.PubMedCrossrefGoogle Scholar

  • 29.

    Mulder DJ, Water TV, Lutgers HL, Graaff R, Gans RO, et al. 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 2006;8:523–35.CrossrefPubMedGoogle Scholar

  • 30.

    Felipe DL, Hempe JM, Liu S, Matter N, Maynard J, et al. Skin intrinsic fluorescence is associated with hemoglobin A(1c) and hemoglobin glycation index but not mean blood glucose in children with type 1 diabetes. Diabetes Care 2011;34:1816–20.PubMedWeb of ScienceCrossrefGoogle Scholar

  • 31.

    Klenovics SK, Kollarova R, Hodosy J, Celec P, Sebekova K. Reference values of skin autofluorescence as an estimation of tissue accumulation of advanced glycation end products in a general Slovak population. Diabet Med 2014;31:581–5.CrossrefGoogle Scholar

  • 32.

    Yue X, Hu H, Koetsier M, Graaff R, Han C. Reference values for the Chinese population of skin autofluorescence as a marker of advanced glycation end products accumulated in tissue. Diabet Med 2011;28:818–23.CrossrefPubMedGoogle Scholar

  • 33.

    Mook-Kanamori MJ, Selim MM, Takiddin AH, Al-Homsi H, Al-Mahmoud KA, et al. Ethnic and gender differences in advanced glycation end products measured by skin auto-fluorescence. Dermatoendocrinol 2013;5:325–30.CrossrefPubMedGoogle Scholar

  • 34.

    de Ranitz-Greven WL, Kaasenbrood L, Poucki WK, Hamerling J, Bos DC, et al. Advanced glycation end products, measured as skin autofluorescence, during normal pregnancy and pregnancy complicated by diabetes mellitus. Diabetes Technol Ther 2012;14:1134–9.PubMedCrossrefWeb of ScienceGoogle Scholar

  • 35.

    Results of the fifth national growth study. Available at: https://www.tno.nl/media/1996/20100608-factsheet-resultaten-vijfde-landelijke-groeistudie1.pdf.

About the article

Corresponding author: Marja M.J. van der Vorst, MD, PhD, Department of Pediatrics, St. Antonius Hospital, Koekoekslaan 1, 3435 CM, P.O. Box 2500 3430 EM, Nieuwegein, The Netherlands, Phone: +31 (0)88 320 6325, Fax: +31 (0)30 6092602

Received: 2018-05-29

Accepted: 2018-11-14

Published Online: 2018-12-11

Published in Print: 2019-01-28

Author contributions: YL recruited participants, collected study data, analyzed the data and wrote the manuscript. LVT recruited participants and critically reviewed and revised the manuscript. MVDV contributed to the conception and design of the study, supervised data collection and critically reviewed and revised the manuscript. CK contributed to the conception and design of the study, critically reviewed and revised the manuscript. MVDV is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

Research funding: None declared.

Employment or leadership: None declared.

Honorarium: None declared.

Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

Citation Information: Journal of Pediatric Endocrinology and Metabolism, Volume 32, Issue 1, Pages 41–47, ISSN (Online) 2191-0251, ISSN (Print) 0334-018X, DOI: https://doi.org/10.1515/jpem-2018-0237.

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