Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Translating the advanced glycation end products (AGEs) knowledge into real-world nutrition strategies

European Journal of Clinical Nutrition volume 76, pages 922–928 (2022)Cite this article

Subjects

Abstract

Advanced glycation end products (AGEs) are glycated proteins or lipids derived from complex metabolic pathways involved in the pathophysiology of various diseases, especially diabetes and diabetes-related complications. These compounds are omnipresent in human life, with both endogenous and exogenous sources. Despite the well-elucidated disease mechanisms, little is known about the AGEs/nutrition nexus in the circles of clinical practice recommendations. This review seeks to translate the accumulated knowledge about the biochemistry and pathophysiology of AGEs into a nutritional intervention based on real-world prescriptions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: It is normal to have some formation of AGEs via the aldose reductase pathway, but this pathway is ten times increased in poorly controlled diabetes and linked to a raised generation of ROS during the conversion of sorbitol to fructose [20].
Fig. 2

Similar content being viewed by others

References

  1. Castro JP, El-Atat FA, McFarlane SI, Aneja A, Sowers JR. Cardiometabolic syndrome: pathophysiology and treatment. Curr Hypertens Rep. 2003;5:393–401. https://doi.org/10.1007/s11906-003-0085-y

    Article  PubMed  Google Scholar 

  2. Kirk EP, Klein S. Pathogenesis and pathophysiology of the cardiometabolic syndrome. J Clin Hypertens. 2009;11:761–5. https://doi.org/10.1111/j.1559-4572.2009.00054.x

    Article  CAS  Google Scholar 

  3. Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiological Rev. 2013;93:137–88. https://doi.org/10.1152/physrev.00045.2011

    Article  CAS  Google Scholar 

  4. Jha JC, Banal C, Chow BS, Cooper ME, Jandeleit-Dahm K. Diabetes and kidney disease: role of oxidative stress. Antioxid Redox Signal. 2016;25:657–84. https://doi.org/10.1089/ars.2016.6664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation. 2006;114:597–605. https://doi.org/10.1161/CIRCULATIONAHA.106.621854

    Article  CAS  PubMed  Google Scholar 

  6. Vlassara H, Striker GE. AGE restriction in diabetes mellitus: a paradigm shift. Nat Rev Endocrinol. 2011;7:526–39. https://doi.org/10.1038/nrendo.2011.74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ostry A, Young ML, Hughes M. The quality of nutritional information available on popular websites: a content analysis. Health Educ Res. 2008;23:648–55. https://doi.org/10.1093/her/cym050

    Article  CAS  PubMed  Google Scholar 

  8. Storey KE, Forbes LE, Fraser SN, Spence JC, Plotnikoff RC, Raine KD, et al. Diet quality, nutrition and physical activity among adolescents: the Web-SPAN (Web-Survey of Physical Activity and Nutrition) project. Public Health Nutr. 2009;12:2009–17. https://doi.org/10.1017/S1368980009990292

    Article  PubMed  Google Scholar 

  9. Aragno M, Mastrocola R. Dietary sugars and endogenous formation of advanced glycation endproducts: emerging mechanisms of disease. Nutrients. 2017;9. https://doi.org/10.3390/nu9040385

  10. Perrone A, Giovino A, Benny J, Martinelli F. Advanced glycation end products (AGEs): biochemistry, signaling, analytical methods, and epigenetic effects. Oxid Med Cell Longev. 2020;2020:3818196 https://doi.org/10.1155/2020/3818196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gautieri A, Passini FS, Silvan U, Guizar-Sicairos M, Carimati G, Volpi P, et al. Advanced glycation end-products: mechanics of aged collagen from molecule to tissue. Matrix Biol. 2017;59:95–108. https://doi.org/10.1016/j.matbio.2016.09.001

    Article  CAS  PubMed  Google Scholar 

  12. Gkogkolou P, Bohm M. Advanced glycation end products: key players in skin aging? Derm-Endocrinol. 2012;4:259–70. https://doi.org/10.4161/derm.22028

    Article  CAS  Google Scholar 

  13. Yamagishi S, Nakamura K, Imaizumi T. Advanced glycation end products (AGEs) and diabetic vascular complications. Curr Diabetes Rev. 2005;1:93–106. https://doi.org/10.2174/1573399052952631

    Article  CAS  PubMed  Google Scholar 

  14. Hamada Y, Araki N, Koh N, Nakamura J, Horiuchi S, Hotta N. Rapid formation of advanced glycation end products by intermediate metabolites of glycolytic pathway and polyol pathway. Biochem Biophys Res Commun. 1996;228:539–43. https://doi.org/10.1006/bbrc.1996.1695

    Article  CAS  PubMed  Google Scholar 

  15. Bonora M, Patergnani S, Rimessi A, De Marchi E, Suski JM, Bononi A, et al. ATP synthesis and storage. Purinergic Signal. 2012;8:343–57. https://doi.org/10.1007/s11302-012-9305-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. McCommis KS, Finck BN. Mitochondrial pyruvate transport: a historical perspective and future research directions. Biochem J. 2015;466:443–54. https://doi.org/10.1042/BJ20141171

    Article  CAS  PubMed  Google Scholar 

  17. Wetzels S, Wouters K, Schalkwijk CG, Vanmierlo T, Hendriks JJ. Methylglyoxal-derived advanced glycation endproducts in multiple sclerosis. Int J Mol Sci. 2017;18. https://doi.org/10.3390/ijms18020421

  18. Yan LJ. Redox imbalance stress in diabetes mellitus: Role of the polyol pathway. Anim models Exp Med. 2018;1:7–13. https://doi.org/10.1002/ame2.12001

    Article  Google Scholar 

  19. Lorenzi M. The polyol pathway as a mechanism for diabetic retinopathy: attractive, elusive, and resilient. Exp Diabetes Res. 2007;2007:61038 https://doi.org/10.1155/2007/61038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ramasamy R, Goldberg IJ. Aldose reductase and cardiovascular diseases, creating human-like diabetic complications in an experimental model. Circulation Res. 2010;106:1449–58. https://doi.org/10.1161/CIRCRESAHA.109.213447

    Article  CAS  PubMed  Google Scholar 

  21. Ramasamy R, Yan SF, Herold K, Clynes R, Schmidt AM. Receptor for advanced glycation end products: fundamental roles in the inflammatory response: winding the way to the pathogenesis of endothelial dysfunction and atherosclerosis. Ann N Y Acad Sci. 2008;1126:7–13. https://doi.org/10.1196/annals.1433.056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Luevano-Contreras C, Chapman-Novakofski K. Dietary advanced glycation end products and aging. Nutrients. 2010;2:1247–65. https://doi.org/10.3390/nu2121247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schmidt AM, Hasu M, Popov D, Zhang JH, Chen J, Yan SD, et al. Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc Natl Acad Sci USA. 1994;91:8807–11. https://doi.org/10.1073/pnas.91.19.8807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Horiuchi S, Higashi T, Ikeda K, Saishoji T, Jinnouchi Y, Sano H, et al. Advanced glycation end products and their recognition by macrophage and macrophage-derived cells. Diabetes. 1996;45:S73–76. https://doi.org/10.2337/diab.45.3.s73

    Article  CAS  PubMed  Google Scholar 

  25. Downs CA, Dang VD, Johnson NM, Denslow ND, Alli AA. Hydrogen peroxide stimulates exosomal cathepsin B regulation of the receptor for advanced glycation end-products (RAGE). J Cell Biochem. 2018;119:599–606. https://doi.org/10.1002/jcb.26219

    Article  CAS  PubMed  Google Scholar 

  26. Turk N, Mornar A, Mrzljak V, Turk Z. Urinary excretion of advanced glycation endproducts in patients with type 2 diabetes and various stages of proteinuria. Diabetes Metab. 2004;30:187–92. https://doi.org/10.1016/S1262-3636(07)70106-4

    Article  CAS  PubMed  Google Scholar 

  27. Coughlan MT, Patel SK, Jerums G, Penfold SA, Nguyen TV, Sourris KC, et al. Advanced glycation urinary protein-bound biomarkers and severity of diabetic nephropathy in man. Am J Nephrol. 2011;34:347–55. https://doi.org/10.1159/000331064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lapolla A, Piarulli F, Sartore G, Ceriello A, Ragazzi E, Reitano R, et al. Advanced glycation end products and antioxidant status in type 2 diabetic patients with and without peripheral artery disease. Diabetes Care. 2007;30:670–6. https://doi.org/10.2337/dc06-1508

    Article  CAS  PubMed  Google Scholar 

  29. Tang WH, Martin KA, Hwa J. Aldose reductase, oxidative stress, and diabetic mellitus. Front Pharmacol. 2012;3:87 https://doi.org/10.3389/fphar.2012.00087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cecilia OM, Jose Alberto CG, Jose NP, Ernesto German CM, Ana Karen LC, Luis Miguel RP, et al. Oxidative stress as the main target in diabetic retinopathy pathophysiology. J Diabetes Res. 2019;2019:8562408 https://doi.org/10.1155/2019/8562408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Vankoningsloo S, Piens M, Lecocq C, Gilson A, De Pauw A, Renard P, et al. Mitochondrial dysfunction induces triglyceride accumulation in 3T3-L1 cells: role of fatty acid beta-oxidation and glucose. J Lipid Res. 2005;46:1133–49. https://doi.org/10.1194/jlr.M400464-JLR200

    Article  CAS  PubMed  Google Scholar 

  32. Vlassara H, Uribarri J. Advanced glycation end products (AGE) and diabetes: cause, effect, or both? Curr Diabetes Rep. 2014;14:453 https://doi.org/10.1007/s11892-013-0453-1

    Article  CAS  Google Scholar 

  33. Deshpande AD, Harris-Hayes M, Schootman M. Epidemiology of diabetes and diabetes-related complications. Phys Ther. 2008;88:1254–64. https://doi.org/10.2522/ptj.20080020

    Article  PubMed  PubMed Central  Google Scholar 

  34. Abudawood M. Diabetes and cancer: a comprehensive review. J Res Med Sci. 2019;24:94 https://doi.org/10.4103/jrms.JRMS_242_19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Nagai R, Shirakawa J, Fujiwara Y, Ohno R, Moroishi N, Sakata N, et al. Detection of AGEs as markers for carbohydrate metabolism and protein denaturation. J Clin Biochem Nutr. 2014;55:1–6. https://doi.org/10.3164/jcbn.13-112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sanguineti R, Puddu A, Mach F, Montecucco F, Viviani GL. Advanced glycation end products play adverse proinflammatory activities in osteoporosis. Mediators Inflamm. 2014;2014:975872 https://doi.org/10.1155/2014/975872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tahara N, Imaizumi T, Takeuchi M, Yamagishi S. Insulin resistance is an independent correlate of high serum levels of advanced glycation end products (AGEs) and low testosterone in non-diabetic men. Oxid Med Cell Longev. 2010;3:262–5. https://doi.org/10.4161/oxim.3.4.12734

    Article  PubMed  PubMed Central  Google Scholar 

  38. Rivas AM, Mulkey Z, Lado-Abeal J, Yarbrough S. Diagnosing and managing low serum testosterone. Proceedings. 2014;27:321–4. https://doi.org/10.1080/08998280.2014.11929145

    Article  Google Scholar 

  39. Del Turco S, Basta G. An update on advanced glycation endproducts and atherosclerosis. BioFactors. 2012;38:266–74. https://doi.org/10.1002/biof.1018

    Article  CAS  PubMed  Google Scholar 

  40. McNulty M, Mahmud A, Feely J. Advanced glycation end-products and arterial stiffness in hypertension. Am J Hypertens. 2007;20:242–7. https://doi.org/10.1016/j.amjhyper.2006.08.009

    Article  CAS  PubMed  Google Scholar 

  41. Ren X, Ren L, Wei Q, Shao H, Chen L, Liu N. Advanced glycation end-products decreases expression of endothelial nitric oxide synthase through oxidative stress in human coronary artery endothelial cells. Cardiovasc Diabetol. 2017;16:52 https://doi.org/10.1186/s12933-017-0531-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Di Marco E, Gray SP, Jandeleit-Dahm K. Diabetes alters activation and repression of pro- and anti-inflammatory signaling pathways in the vasculature. Front Endocrinol. 2013;4:68 https://doi.org/10.3389/fendo.2013.00068

    Article  Google Scholar 

  43. Gu L, Hagiwara S, Fan Q, Tanimoto M, Kobata M, Yamashita M, et al. Role of receptor for advanced glycation end-products and signalling events in advanced glycation end-product-induced monocyte chemoattractant protein-1 expression in differentiated mouse podocytes. Nephrol Dial Transplant. 2006;21:299–313. https://doi.org/10.1093/ndt/gfi210

    Article  CAS  PubMed  Google Scholar 

  44. Festa A, Schmolzer B, Schernthaner G, Menzel EJ. Differential expression of receptors for advanced glycation end products on monocytes in patients with IDDM. Diabetologia. 1998;41:674–80. https://doi.org/10.1007/s001250050967

    Article  CAS  PubMed  Google Scholar 

  45. Akirav EM, Henegariu O, Preston-Hurlburt P, Schmidt AM, Clynes R, Herold KC. The receptor for advanced glycation end products (RAGE) affects T cell differentiation in OVA induced asthma. PLoS ONE. 2014;9:e95678 https://doi.org/10.1371/journal.pone.0095678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Reed JC, Preston-Hurlburt P, Philbrick W, Betancur G, Korah M, Lucas C, et al. The receptor for advanced glycation endproducts (RAGE) modulates T cell signaling. PLoS ONE. 2020;15:e0236921 https://doi.org/10.1371/journal.pone.0236921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Milutinovic A, Suput D, Zorc-Pleskovic R. Pathogenesis of atherosclerosis in the tunica intima, media, and adventitia of coronary arteries: an updated review. Bosn J Basic Med Sci. 2020;20:21–30. https://doi.org/10.17305/bjbms.2019.4320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Onat D, Brillon D, Colombo PC, Schmidt AM. Human vascular endothelial cells: a model system for studying vascular inflammation in diabetes and atherosclerosis. Curr Diabetes Rep. 2011;11:193–202. https://doi.org/10.1007/s11892-011-0182-2

    Article  CAS  Google Scholar 

  49. Das A. Diabetic retinopathy: battling the global epidemic. Investig Ophthalmol Vis Sci. 2016;57:6669–82. https://doi.org/10.1167/iovs.16-21031

    Article  CAS  Google Scholar 

  50. Turner DP. Advanced glycation end-products: a biological consequence of lifestyle contributing to cancer disparity. Cancer Res. 2015;75:1925–9. https://doi.org/10.1158/0008-5472.CAN-15-0169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ott C, Jacobs K, Haucke E, Navarrete Santos A, Grune T, Simm A. Role of advanced glycation end products in cellular signaling. Redox Biol. 2014;2:411–29. https://doi.org/10.1016/j.redox.2013.12.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Zhang Q, Ames JM, Smith RD, Baynes JW, Metz TO. A perspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: probing the pathogenesis of chronic disease. J Proteome Res. 2009;8:754–69. https://doi.org/10.1021/pr800858h

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lederer MO, Klaiber RG. Cross-linking of proteins by Maillard processes: characterization and detection of lysine-arginine cross-links derived from glyoxal and methylglyoxal. Bioorg Med Chem. 1999;7:2499–507. https://doi.org/10.1016/s0968-0896(99)00212-6

    Article  CAS  PubMed  Google Scholar 

  54. Ansari NA, Dash D. Amadori glycated proteins: role in production of autoantibodies in diabetes mellitus and effect of inhibitors on non-enzymatic glycation. Aging Dis. 2013;4:50–6.

    PubMed  Google Scholar 

  55. Kerr D, Partridge H, Knott J, Thomas PW. HbA1c 3 months after diagnosis predicts premature mortality in patients with new onset type 2 diabetes. Diabet Med. 2011;28:1520–4. https://doi.org/10.1111/j.1464-5491.2011.03443.x

    Article  CAS  PubMed  Google Scholar 

  56. Burke LM, Cox GR, Culmmings NK, Desbrow B. Guidelines for daily carbohydrate intake: do athletes achieve them? Sports Med. 2001;31:267–99. https://doi.org/10.2165/00007256-200131040-00003

    Article  CAS  PubMed  Google Scholar 

  57. Ebeling P, Bourey R, Koranyi L, Tuominen JA, Groop LC, Henriksson J, et al. Mechanism of enhanced insulin sensitivity in athletes. Increased blood flow, muscle glucose transport protein (GLUT-4) concentration, and glycogen synthase activity. J Clin Investig. 1993;92:1623–31. https://doi.org/10.1172/JCI116747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Carbonero F NAL. Impact of Maillard reaction products on nutrition and health: Current knowledge and need to understand their fate in the human digestive system. Crit Rev Food Sci Nutr. 2019;59:474–87. https://doi.org/10.1080/10408398.2017.1378865

    Article  CAS  PubMed  Google Scholar 

  59. Tamanna N, Mahmood N. Food processing and maillard reaction products: effect on human health and nutrition. Int J Food Sci. 2015;2015:526762 https://doi.org/10.1155/2015/526762

    Article  PubMed  PubMed Central  Google Scholar 

  60. DeChristopher LR. Perspective: the paradox in dietary advanced glycation end products research-the source of the serum and urinary advanced glycation end products is the intestines, not the food. Adv Nutr. 2017;8:679–83. https://doi.org/10.3945/an.117.016154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Udilova N, Jurek D, Marian B, Gille L, Schulte-Hermann R, Nohl H. Induction of lipid peroxidation in biomembranes by dietary oil components. Food Chem Toxicol. 2003;41:1481–9. https://doi.org/10.1016/s0278-6915(03)00164-9

    Article  CAS  PubMed  Google Scholar 

  62. Guasch-Ferre M, Salas-Salvado J, Ros E, Estruch R, Corella D, Fito M, et al. The PREDIMED trial, Mediterranean diet and health outcomes: how strong is the evidence? Nutr Metab Cardiovas Dis. 2017;27:624–32. https://doi.org/10.1016/j.numecd.2017.05.004

    Article  CAS  Google Scholar 

  63. Estruch R, Ros E, Salas-Salvado J, Covas MI, Corella D, Aros F, et al. Primary prevention of cardiovascular disease with a Mediterranean diet supplemented with extra-virgin olive oil or nuts. N Engl J Med. 2018;378:e34 https://doi.org/10.1056/NEJMoa1800389

    Article  CAS  PubMed  Google Scholar 

  64. Uribarri J, Woodruff S, Goodman S, Cai W, Chen X, Pyzik R, et al. Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Dietetic Assoc. 2010;110:911–6.e912. https://doi.org/10.1016/j.jada.2010.03.018

    Article  Google Scholar 

  65. Santos HO, de Moraes W, da Silva GAR, Prestes J, Schoenfeld BJ. Vinegar (acetic acid) intake on glucose metabolism: a narrative review. Clin Nutr ESPEN. 2019;32:1–7. https://doi.org/10.1016/j.clnesp.2019.05.008

    Article  PubMed  Google Scholar 

  66. Freitas D, Boue F, Benallaoua M, Airinei G, Benamouzig R, Le Feunteun S. Lemon juice, but not tea, reduces the glycemic response to bread in healthy volunteers: a randomized crossover trial. Eur J Nutr. 2020. https://doi.org/10.1007/s00394-020-02228-x

  67. Sohouli MH, Fatahi S, Sharifi-Zahabi E, Santos HO, Tripathi N, Lari A, et al. The impact of low advanced glycation end products diet on metabolic risk factors: a systematic review and meta-analysis of randomized controlled trials. Adv Nutr. 2020. https://doi.org/10.1093/advances/nmaa150

  68. Singh P, Jayaramaiah RH, Agawane SB, Vannuruswamy G, Korwar AM, Anand A, et al. Potential dual role of eugenol in inhibiting advanced glycation end products in diabetes: proteomic and mechanistic insights. Sci Rep. 2016;6:18798 https://doi.org/10.1038/srep18798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Colin-Gonzalez AL, Santana RA, Silva-Islas CA, Chanez-Cardenas ME, Santamaria A, Maldonado PD. The antioxidant mechanisms underlying the aged garlic extract- and S-allylcysteine-induced protection. Oxid Med Cell Longev. 2012;2012:907162 https://doi.org/10.1155/2012/907162

    Article  PubMed  PubMed Central  Google Scholar 

  70. Cortes-Rojas DF, de Souza CR, Oliveira WP. Clove (Syzygium aromaticum): a precious spice. Asian Pac J Trop Biomed. 2014;4:90–6. https://doi.org/10.1016/S2221-1691(14)60215-X

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hartnoll G, Moore D, Douek D. Near fatal ingestion of oil of cloves. Arch Dis Child. 1993;69:392–3. https://doi.org/10.1136/adc.69.3.392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Avula PR, Asdaq SM, Asad M. Effect of aged garlic extract and s-allyl cysteine and their interaction with atenolol during isoproterenol induced myocardial toxicity in rats. Indian J Pharmacol. 2014;46:94–9. https://doi.org/10.4103/0253-7613.125185

    Article  PubMed  PubMed Central  Google Scholar 

  73. Lawson LD, Hunsaker SM. Allicin bioavailability and bioequivalence from garlic supplements and garlic foods. Nutrients. 2018;10. https://doi.org/10.3390/nu10070812

  74. Shabani E, Sayemiri K, Mohammadpour M. The effect of garlic on lipid profile and glucose parameters in diabetic patients: a systematic review and meta-analysis. Prim Care Diabetes. 2019;13:28–42. https://doi.org/10.1016/j.pcd.2018.07.007

    Article  PubMed  Google Scholar 

  75. Wang J, Zhang X, Lan H, Wang W. Effect of garlic supplement in the management of type 2 diabetes mellitus (T2DM): a meta-analysis of randomized controlled trials. Food Nutr Res. 2017;61:1377571 https://doi.org/10.1080/16546628.2017.1377571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Ansary J, Forbes-Hernandez TY, Gil E, Cianciosi D, Zhang J, Elexpuru-Zabaleta M, et al. Potential health benefit of garlic based on human intervention studies: a brief overview. Antioxidants. 2020;9 https://doi.org/10.3390/antiox9070619

  77. Cooper ME. Importance of advanced glycation end products in diabetes-associated cardiovascular and renal disease. Am J Hypertens. 2004;17:31S–38S. https://doi.org/10.1016/j.amjhyper.2004.08.021

    Article  CAS  PubMed  Google Scholar 

  78. American Diabetes A. 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2020. Diabetes Care. 2020;43:S14–S31. https://doi.org/10.2337/dc20-S002

    Article  Google Scholar 

  79. Sacks DB, Arnold M, Bakris GL, Bruns DE, Horvath AR, Kirkman MS, et al. National Academy of Clinical B, Evidence-Based Laboratory Medicine Committee of the American Association for Clinical C. Guidelines and recommendations for laboratory analysis in the diagnosis and management of diabetes mellitus. Diabetes Care. 2011;34:e61–99. https://doi.org/10.2337/dc11-9998

  80. Macedo RCO, Santos HO, Tinsley GM, Reischak-Oliveira A. Low-carbohydrate diets: Effects on metabolism and exercise - a comprehensive literature review. Clin Nutr ESPEN. 2020;40:17–26. https://doi.org/10.1016/j.clnesp.2020.07.022

    Article  PubMed  Google Scholar 

  81. Kennedy JW, Hirshman MF, Gervino EV, Ocel JV, Forse RA, Hoenig SJ, et al. Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes. 1999;48:1192–7. https://doi.org/10.2337/diabetes.48.5.1192

    Article  CAS  PubMed  Google Scholar 

  82. Boor P, Celec P, Behuliak M, Grancic P, Kebis A, Kukan M, et al. Regular moderate exercise reduces advanced glycation and ameliorates early diabetic nephropathy in obese Zucker rats. Metab: Clin Exp. 2009;58:1669–77. https://doi.org/10.1016/j.metabol.2009.05.025

    Article  CAS  Google Scholar 

  83. Drenth H, Zuidema SU, Krijnen WP, Bautmans I, Smit AJ, van der Schans C, et al. Advanced glycation end products are associated with physical activity and physical functioning in the older population. J Gerontol Ser A, Biol Sci Med Sci. 2018;73:1545–51. https://doi.org/10.1093/gerona/gly108

    Article  CAS  Google Scholar 

  84. van Waateringe RP, Slagter SN, van Beek AP, van der Klauw MM, van Vliet-Ostaptchouk JV, Graaff R, 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 https://doi.org/10.1186/s13098-017-0241-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Isami F, West BJ, Nakajima S, Yamagishi SI. Association of advanced glycation end products, evaluated by skin autofluorescence, with lifestyle habits in a general Japanese population. J Int Med Res. 2018;46:1043–51. https://doi.org/10.1177/0300060517736914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Willemsen S, Hartog JW, Hummel YM, van Ruijven MH, van der Horst IC, van Veldhuisen DJ, et al. Tissue advanced glycation end products are associated with diastolic function and aerobic exercise capacity in diabetic heart failure patients. Eur J Heart Fail. 2011;13:76–82. https://doi.org/10.1093/eurjhf/hfq168

    Article  CAS  PubMed  Google Scholar 

  87. Kunimoto M, Shimada K, Yokoyama M, Matsubara T, Aikawa T, Ouchi S, et al. Association between the tissue accumulation of advanced glycation end products and exercise capacity in cardiac rehabilitation patients. BMC Cardiovasc Disord. 2020;20:195 https://doi.org/10.1186/s12872-020-01484-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Rodrigues KL, Borges JP, Lopes GO, Pereira E, Mediano MFF, Farinatti P, et al. Influence of physical exercise on advanced glycation end products levels in patients living with the human immunodeficiency virus. Front Physiol. 2018;9:1641 https://doi.org/10.3389/fphys.2018.01641

    Article  PubMed  PubMed Central  Google Scholar 

  89. Macias-Cervantes MH, Rodriguez-Soto JM, Uribarri J, Diaz-Cisneros FJ, Cai W, Garay-Sevilla ME. Effect of an advanced glycation end product-restricted diet and exercise on metabolic parameters in adult overweight men. Nutrition. 2015;31:446–51. https://doi.org/10.1016/j.nut.2014.10.004

    Article  CAS  PubMed  Google Scholar 

  90. Gill JM, Cooper AR. Physical activity and prevention of type 2 diabetes mellitus. Sports Med. 2008;38:807–24. https://doi.org/10.2165/00007256-200838100-00002

    Article  PubMed  Google Scholar 

  91. Kriska A. Physical activity and the prevention of type 2 diabetes mellitus: how much for how long? Sports Med. 2000;29:147–51. https://doi.org/10.2165/00007256-200029030-00001

    Article  CAS  PubMed  Google Scholar 

  92. Aune D, Norat T, Leitzmann M, Tonstad S, Vatten LJ. Physical activity and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis. Eur J Epidemiol. 2015;30:529–42. https://doi.org/10.1007/s10654-015-0056-z

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Medicine, Uberlandia Federal University (UFU), Uberlândia, Minas Gerais, Brazil

    Heitor O. Santos

  2. Institute of Biotechnology, Federal University of Uberlândia, Uberlândia, MG, Brazil

    Nilson Penha-Silva

Authors
  1. Heitor O. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nilson Penha-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors’ responsibilities were as follows—HOS: review design, full text screening, and manuscript writing. NPS: review of the entire manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Heitor O. Santos.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos, H.O., Penha-Silva, N. Translating the advanced glycation end products (AGEs) knowledge into real-world nutrition strategies. Eur J Clin Nutr 76, 922–928 (2022). https://doi.org/10.1038/s41430-021-01028-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-021-01028-8

This article is cited by

Search

Advanced search

Quick links