Food systems

Advanced search

Glycation end products and technological aspects of reducing immunogenicity of specialized food products for nutrition of athletes

Full Text:


Food allergy, which affects about 8% of children and 5% of adults in the world, is one of the major global health problems, and allergen control is an important aspect of food safety. According to the FALCPA (Food Allergen Labeling and Consumer Protection Act of 2004 FDA), more than 160 foods can cause allergic reactions, with eight of them responsible for 90% of all food allergies in the United States, including milk, eggs, wheat, peanuts, soybeans, tree nuts, crustaceans and fish, also known as the Big 8. Most foods that are sources of obligate allergens are heat treated before consumption, which can trigger the Maillard reaction, which produces glycation end products. Symptoms of food sensitization are known to significantly affect the quality of life, gut microbial diversity and adaptation potential. In particular, in athletes, this can be expressed in a decrease in the effectiveness of the training process, which leads to poor endurance and athletic performance. In this regard, it seems relevant to study the effect of the Maillard reaction and AGEs on the immunogenicity of proteins and the possible relationship between these compounds and food allergy, as well as to develop measures to prevent the adverse effect of allergens on the body of a professional athlete and any other consumer.

About the Authors

I. V. Kobelkova
Federal Research Center for Nutrition, Biotechnology and Food Safety; Academy of Postgraduate Education
Russian Federation

Irina V. Kobelkova, Candidate of Medical Sciences, Leading Researcher, Laboratory of Sports Anthropology and Nutritionology; Docent

Ustinsky pr., 2/14с1, 109240, Moscow
Volokolamsk Highway, 91, 125371, Moscow
Tel.: + 7–910–406–40–31

M. M. Korosteleva
Federal Research Center for Nutrition, Biotechnology and Food Safety; Peoples’ Friendship University of Russia
Russian Federation

Margarita M. Korosteleva, Candidate of Medical Sciences, Senior Researcher, Laboratory of Sports Anthropology and Nutritionology; Docent, Department of Nursing Management, Medical Institute

Ustinsky pr., 2/14с1, 109240, Moscow
Miklukho-Maclay str., 6, 117198, Moscow
Tel.: +7–985–567–78–22

D. B. Nikityuk
Federal Research Center for Nutrition, Biotechnology and Food Safety; I.M. Sechenov First Moscow State Medical University
Russian Federation

Dmitry B. Nikityuk, Doctor of Medical Sciences, Professor, Corresponding Member of the Russian Academy of Sciences, Director; Professor, Department of Operative Surgery and Topographic Anatomy

Ustinsky pr., 2/14с1, 109240, Moscow
Rossolimo str., 15/13(1), 119992, Moscow
Tel.: +7–495–695–53–60

M. S. Kobelkova
“Polyclinic No. 2” of the Administrative Department of the President of the Russian Federation
Russian Federation

Maria S. Kobelkova, Doctor

2nd Frunzenskaya street, 4, 119146, Moscow
Tel. +7–915–410–78–74


1. Somoza, V., Wenzel, E., Weiß, C., Clawin-Rädecker, I., Grübel, N., Erbersdobler, H. F. (2006). Dose-dependent utilisation of casein-linked lysinoalanine, N(epsilon)-fructoselysine and N(epsilon)-carboxymethyllysine in rats. Molecular Nutrition and Food Research, 50(9), 833–841.

2. Hellwig, M., Henle, T. (2014). Baking, ageing, diabetes: A short history of the maillard reaction. Angewandte Chemie — International Edition, 53(39), 10316–10329.

3. de Oliveira, F. C., Coimbra, J. S. D. R., de Oliveira, E. B., Zuñiga, A. D. G., Rojas, E. E. G. (2016). Food protein-polysaccharide conjugates obtained via the Maillard reaction: A review. Critical Reviews in Food Science and Nutrition, 56(7), 1108–1125.

4. Teodorowicz, M., Van Neerven, J., Savelkoul, H. (2017). Food processing: The influence of the Maillard reaction on immunogenicity and allergenicity of food proteins. Nutrients, 9(8), Article 835.

5. Xiang, J., Liu, F., Wang, B., Chen, L., Liu, W., Tan, S. (2021). A literature review on Maillard reaction based on milk proteins and carbohydrates in food and pharmaceutical products: Advantages, disadvantages, and avoidance strategies. Foods, 10(9), Article 1998.

6. Newton, A. E., Fairbanks, A. J., Golding, M., Andrewes, P., Gerrard, J. A. (2012). The role of the Maillard reaction in the formation of flavour compounds in dairy products — not only a deleterious reaction but also a rich source of flavour compounds. Food and Function, 3(12), 1231–1241.

7. Nooshkam, M., Varidi, M., Bashash, M. (2019). The Maillard reaction products as food-born antioxidant and antibrowning agents in model and real food systems. Food Chemistry, 275, 644–660.

8. Oliver, C. M., Melton, L. D., Stanley, R. A. (2006). Creating proteins with novel functionality via the maillard reaction: A review. Critical Reviews in Food Science and Nutrition, 46(4), 337–350.

9. Abd El-Salam, M. H., El-Shibiny, S. (2018). Glycation of whey proteins: Technological and nutritional implications. International Journal of Biological Macromolecules, 112, 83–92.

10. Sedaghat Doost, A., Nikbakht Nasrabadi, M., Wu, J., A’yun, Q., Van der Meeren, P. (2019). Maillard conjugation as an approach to improve whey proteins functionality: A review of conventional and novel preparation techniques. Trends in Food Science and Technology, 91, 1–11.

11. Seo, C. W., Yoo, B. (2021). Preparation of milk protein isolate/κcarrageenan conjugates by Maillard reaction in wet-heating system and their application to stabilization of oil-in-water emulsions. LWT, 139, Article 110542.

12. Meydani, B., Vahedifar, A., Askari, G., Madadlou, A. (2019). Influence of the Maillard reaction on the properties of cold-set whey protein and maltodextrin binary gels. International Dairy Journal, 90, 79–87.

13. Andrade, M. A., Ribeiro-Santos, R., Guerra, M., Sanches-Silva, A. (2019). Evaluation of the oxidative status of salami packaged with an active whey protein film. Foods, 8(9), Article 387.

14. Spanneberg, R., Salzwedel, G., Glomb, M. A. (2012). Formation of early and advanced Maillard reaction products correlates to the ripening of cheese. Journal of Agricultural and Food Chemistry, 60(2), 600–607.

15. Erbersdobler, H. F., Somoza, V. (2007). Forty years of furosine — forty years of using Maillard reaction products as indicators of the nutritional quality of foods. Molecular Nutrition and Food Research, 51(4), 423–430.

16. García, M. M., Seiquer, I., Delgado-Andrade, C., Galdó, G., Navarro, M. P. (2009). Intake of Maillard reaction products reduces iron bioavailability in male adolescents. Molecular Nutrition and Food Research, 53(12), 1551–1560.

17. ALjahdali, N., Carbonero, F. (2019). Impact of Maillard reaction products on nutrition and health: Current knowledge and need to understand their fate in the human digestive system. Critical Reviews in Food Science and Nutrition, 59(3), 474–487.

18. Wang, Z., Jiang, Y., Liu, N., Ren, L., Zhu, Y., An, Y. et al. (2012). Advanced glycation end-product N e{open}- carboxymethyl-lysine accelerates progression of atherosclerotic calcification in diabetes. Atherosclerosis, 221(2), 387–396.

19. Li, J., Liu, D., Sun, L., Lu, Y., Zhang, Z. (2012). Advanced glycation end products and neurodegenerative diseases: Mechanisms and perspective. Journal of the Neurological Sciences, 317(1–2), 1–5.

20. Rao, Q., Jiang, X., Li, Y., Samiwala, M., Labuza, T. P. (2018). Can glycation reduce food allergenicity? Journal of Agricultural and Food Chemistry, 66(17), 4295–4299.

21. Yang, S. -Y., Kim, S. -W., Kim, Y., Lee, S. -H., Jeon, H., Lee, K. -W. (2015). Optimization of Maillard reaction with ribose for enhancing anti-allergy effect of fish protein hydrolysates using response surface methodology. Food Chemistry, 176, 420–425.

22. Liu, E. G., Yin, X., Swaminathan, A., Eisenbarth, S. C. (2021). Antigenpresenting cells in food tolerance and allergy. Frontiers in Immunology, 11, Article 616020.

23. Bøgh, K. L., Madsen, C. B. (2016). Food allergens: Is there a correlation between stability to digestion and allergenicity? Critical Reviews in Food Science and Nutrition, 56(9), 1545–1567.

24. Teodorowicz, M., Hendriks, W. H., Wichers, H. J., Savelkoul, H. F. J. (2018). Immunomodulation by processed animal feed: The role of maillard reaction products and advanced glycation end-products (AGEs). Frontiers in Immunology, 9(SEP), Article 2088.

25. Bastos, D. H. M., Gugliucci, A. (2015). Contemporary and controversial aspects of the Maillard reaction products. Current Opinion in Food Science, 1(1), 13–20.

26. Sanz, M. L., Corzo-Martínez, M., Rastall, R. A., Olano, A., Moreno, F. J. (2007). Characterization and in vitro digestibility of bovine β-lactoglobulin glycated with galactooligosaccharides. Journal of Agricultural and Food Chemistry, 55(19), 7916–7925.

27. Zhang, Z., Li, Z., Lin, H. (2021). Reducing the allergenicity of shrimp tropomyosin and allergy desensitization based on glycation modification. Journal of Agricultural and Food Chemistry. (unpublished data)

28. Xu, L., Gong, Y., Gern, J. E., Ikeda, S., Lucey, J. A. (2018). Glycation of whey protein with dextrans of different molar mass: Effect on immunoglobulin E-binding capacity with blood sera obtained from patients with cow milk protein allergy. Journal of Dairy Science, 101(8), 6823–6834.–14338

29. Maleki, S. J., Chung, S. -Y., Champagne, E. T., Raufman, J. -P. (2000). The effects of roasting on the allergenic properties of peanut proteins. Journal of Allergy and Clinical Immunology, 106(4), 763–768.

30. Liu, F., Teodorowicz, M., Van Boekel, M. A. J. S., Wichers, H. J., Hettinga, K. A. (2016). The decrease in the IgG-binding capacity of intensively dry heated whey proteins is associated with intense Maillard reaction, structural changes of the proteins and formation of RAGE-ligands. Food and Function, 7(1), 239–249.

31. De Martinis, M., Sirufo, M. M., Suppa, M., Ginaldi, L. (2020). New perspectives in food allergy. International Journal of Molecular Sciences, 21(4), Article 1474.

32. Gupta, R. K., Gupta, K., Sharma, A., Das, M., Ansari, I. A., Dwivedi, P. D. (2018). Maillard reaction in food allergy: Pros and cons. Critical Reviews in Food Science and Nutrition, 58(2), 208–226.

33. Liang, Z., Chen, X., Li, L., Li, B., Yang, Z. (2019). The fate of dietary advanced glycation end products in the body: From oral intake to excretion. Critical Reviews in Food Science and Nutrition, 60(20), 3475–3491.

34. Hegele, J., Buetler, T., Delatour, T. (2008). Comparative LC–MS/MS profiling of free and protein-bound early and advanced glycation-induced lysine modifications in dairy products. Analytica Chimica Acta, 617(1–2), 85–96.

35. Ling, B., Tang, J., Kong, F., Mitcham, E. J., Wang, S. (2015). Kinetics of food quality changes during thermal processing: A review. Food and Bioprocess Technology, 8(2), 343–358.–014–1398–3

36. Collin, M., Bigley, V. (2018). Human dendritic cell subsets: An update. Immunology, 154(1), 3–20

37. Jaiswal, N., Agrawal, S., Agrawal, A. (2019). High fructose-induced metabolic changes enhance inflammation in human dendritic cells. Clinical and Experimental Immunology, 197(2), 237–249.

38. Uribarri, J., Woodruff, S., Goodman, S., Cai, W., Chen, X., Pyzik, R. et al. (2010). Advanced glycation end products in foods and a practical guide to their reduction in the diet. Journal of the American Dietetic Association, 110(6), 911–916.e12.

39. Ott, C., Jacobs, K., Haucke, E., Navarrete Santos, A., Grune, T., Simm, A. (2014). Role of advanced glycation end products in cellular signaling. Redox Biology, 2(1), 411–429.

40. Saleh, A., Smith, D. R., Tessler, L., Mateo, A. R., Martens, C., Schartner, E. et al. (2013). Receptor for advanced glycation end-products (RAGE) activates divergent signaling pathways to augment neurite outgrowth of adult sensory neurons. Experimental Neurology, 249, 149–159.

41. Cai, W., Ramdas, M., Zhu, L., Chen, X., Striker, G. E., Vlassara, H. (2012). Oral advanced glycation endproducts (AGEs) promote insulin resistance and diabetes by depleting the antioxidant defenses AGE receptor-1 and sirtuin 1. Proceedings of the National Academy of Sciencesof the United States of America, 109(39), 15888–15893.

42. Ilchmann, A., Burgdorf, S., Scheurer, S., Waibler, Z., Nagai, R., Wellner, A. et al. (2010). Glycation of a food allergen by the Maillard reaction enhances its T-cell immunogenicity: Role of macrophage scavenger receptor class A type I and II. The Journal of Allergy and Clinical Immunology, 125(1–3), 175–183.e11.

43. Maillard-Lefebvre, H., Boulanger, E., Daroux, M., Gaxatte, C., Hudson, B. I., Lambert, M. (2009). Soluble receptor for advanced glycation end products: A new biomarker in diagnosis and prognosis of chronic inflammatory diseases. Rheumatology (Oxford, England), 48(10), 1190–1196.

44. Jiménez-Saiz, R., Belloque, J., Molina, E., López-Fandiño, R. (2011). Human immunoglobulin e (IgE) binding to heated and glycated ovalbumin and ovomucoid before and after in vitro digestion. Journal of Agricultural and Food Chemistry, 59(18), 10044–10051

45. Taheri-Kafrani, A., Gaudin, J.-C., Rabesona, H., Nioi, C., Agarwal, D., Drouet, M. et al. (2009). Effects of heating and glycation of β-lactoglobulin on its recognition by ige of sera from cow milk allergy patients. Journal of Agricultural and Food Chemistry, 57(11), 4974–4982.

46. Bu, G., Lu, J., Zheng, Z., Luo, Y. (2009). Influence of maillard reaction conditions on the antigenicity of bovine α-lactalbumin using response surface methsodology. Journal of the Science of Food and Agriculture, 89(14), 2428–2434.

47. Heilmann, M., Wellner, A., Gadermaier, G., Ilchmann, A., Briza, P., Krause, M. et al. (2014). Ovalbumin modified with pyrraline, a maillard reaction product, shows enhanced T-cell immunogenicity. Journal of Biological Chemistry, 289(11), 7919–7928.

48. Cucu, T., De Meulenaer, B., Bridts, C., Devreese, B., Ebo, D. (2012). Impact of thermal processing and the maillard reaction on the basophil activation of hazelnut allergic patients. Food and Chemical Toxicology, 50(5), 1722–1728.

49. Han, X.-Y., Yang, H., Rao, S.-T., Liu, G.-Y., Hu, M.-J., Zeng, B.-C. et al. (2018). The Maillard reaction reduced the sensitization of tropomyosin and arginine kinase from Scylla paramamosain, simultaneously. Journal of Agricultural and Food Chemistry, 66(11), 2934–2943.

50. Zhang, Z., Li, X. -M., Xiao, H., Nowak-Wegrzyn, A., Zhou, P. (2020). Insight into the allergenicity of shrimp tropomyosin glycated by functional oligosaccharides containing advanced glycation end products. Food Chemistry, 302, Article 125348.

51. Zhao, Y.-J., Cai, Q.-F., Jin, T., Zhang, L.-J., Fei, D.-X., Liu, G.-M., Cao, M.-J. (2017). Effect of Maillard reaction on the structural and immunological properties of recombinant silver carp parvalbumin. LWT — Food Science and Technology, 75, 25–33.

52. Kobelkova, M.S., Korosteleva, M.M., Kobelkova, I.V. (2021). Applied aspects of the use of Maillard reaction products in the development of specialized food products for the nutrition of athletes. Food systems, 4(3S), 137–141.–9771–2021–4–3S-137–141

53. Yang, Z. -H., Li, C., Li, Y. -Y., Wang, Z. -H. (2013). Effects of maillard reaction on allergenicity of buckwheat allergen fag t 3 during thermal processing. Journal of the Science of Food and Agriculture, 93(6), 1510–1515.

54. Warren, C.M., Jiang, J., Gupta, R.S. (2020). Epidemiology and burden of food allergy. Current Allergy and Asthma Reports, 20(2), Article 6.–020–0898–7

55. Warren, C. M., Turner, P. J., Chinthrajah, R. S., Gupta, R. S. (2021). Advancing food allergy through epidemiology: Understanding and addressing disparities in food allergy management and outcomes. Journal of Allergy and Clinical Immunology: In Practice, 9(1), 110–118.

56. Smith, P. K., Masilamani, M., Li, X. -M., Sampson, H. A. (2017). The false alarm hypothesis: Food allergy is associated with high dietary advanced glycation end-products and proglycating dietary sugars that mimic alarmins. Journal of Allergy and Clinical Immunology, 139(2), 429–437.

57. Wei, Q., Liu, T., Sun, D. -W. (2018). Advanced glycation end-products (AGEs) in foods and their detecting techniques and methods: A review. Trends in Food Science and Technology, 82, 32–45.

58. Takeuchi, M., Takino, J., Furuno, S., Shirai, H., Kawakami, M., Muramatsu, M. et al. (2015). Assessment of the concentrations of various advanced glycation end-products in beverages and foods that are commonly consumed in Japan. Plos One, 10(3), Article e0118652.

59. Hull, G. L. J., Woodside, J. V., Ames, J. M., Cuskelly, G. J. (2012). N ε (carboxymethyl) lysine content of foods commonly consumed in a Western style diet. Food Chemistry, 131(1), 170–174.

60. Pouillart, P., Mauprivez, H., Ait-Ameur, L., Cayzeele, A., Lecerf, J., Tessier, F. J. et al. (2008). Strategy for the study of the health impact of dietary Maillard products in clinical studies: The example of the ICARE clinical study on healthy adults. Annals of the New York Academy of Sciences, 1126, 173–176.

61. Zhang, Z., Li, D. (2018). Thermal processing of food reduces gut microbiota diversity of the host and triggers adaptation of the microbiota: Evidence from two vertebrates. Microbiome, 6(1), 99.–018–0471-y

62. Koliada, A., Syzenko, G., Moseiko, V., Budovska, L., Puchkov, K., Perederiy, V. et al. (2017). Association between body mass index and Firmicutes/ Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiology, 17(1), Article 120.–017–1027–1

63. Mao, Z., Ren, Y., Zhang, Q., Dong, S., Han, K., Feng, G. et al. (2019). Glycated fish protein supplementation modulated gut microbiota composition and reduced inflammation but increased accumulation of advanced glycation end products in high-fat diet fed rats. Food and Function, 10(6), 3439–3451.

64. Yacoub, R., Nugent, M., Cai, W., Nadkarni, G. N., Chaves, L. D., Abyad, S. et al. (2017). Advanced glycation end products dietary restriction effects on bacterial gut microbiota in peritoneal dialysis patients; a randomized open label controlled trial. PLoS One, 12(9), Article e0184789.

65. Seiquer, I., Rubio, L. A., Peinado, M. J., Delgado-Andrade, C., Navarro, M. P. (2014). Maillard reaction products modulate gut microbiota composition in adolescents. Molecular Nutrition and Food Research, 58(7), 1552-1560.

66. Luévano-Contreras, C., Garay-Sevilla, M. E., Wrobel, K., Malacara, J. M., Wrobel, K. (2012). Dietary advanced glycation end products restriction diminishes inflammation markers and oxidative stress in patients with type 2 diabetes mellitus. Journal of Clinical Biochemistry and Nutrition, 52(1), 12–40.–40

67. Vlassara, H., Striker, G. E. (2011). AGE restriction in diabetes mellitus: A paradigm shift. Nature Reviews Endocrinology, 7(9), 526–539.

68. Di Pino, A., Currenti, W., Urbano, F., Mantegna, C., Purrazzo, G., Piro, S. et al. (2016). Low advanced glycation end product diet improves the lipid and inflammatory profiles of prediabetic subjects. Journal of Clinical Lipidology, 10(5), 1098–1108.

69. Poulsen, M. W., Bak, M. J., Andersen, J. M., Monošík, R., Giraudi-Futin, A. C., Holst, J. J. et al. (2014). Effect of dietary advanced glycation end products on postprandial appetite, inflammation, and endothelial activation in healthy overweight individuals. European Journal of Nutrition, 53(2), 661–672.–013–0574-y

70. Macías-Cervantes, M. H., Rodríguez-Soto, J. M. D., Uribarri, J., DíazCisneros, F. J., Cai, W., Garay-Sevilla, M. E. (2015). Effect of an advanced glycation end product-restricted diet and exercise on metabolic parameters in adult overweight men. Nutrition, 31(3), 446–451.

71. Munekata, P.E.S., Domínguez, R., Budaraju, S., Roselló-Soto, E., Barba, F.J., Mallikarjunan, K. et al. (2020). Effect of innovative food processing technologies on the physicochemical and nutritional properties and quality of non-dairy plant-based beverages. Foods, 9(3), Article 288.

72. Khan, M., Liu, H., Wang, J., Sun, B. (2019). Inhibitory effect of phenolic compounds and plant extracts on the formation of advance glycation end products: A comprehensive review. Food Research International, 130, Article 108933.

73. Abdallah, H. M., El-Bassossy, H., Mohamed, G. A., El-Halawany, A. M., Alshali, K. Z., Banjar, Z. M. (2016). Phenolics from Garcinia mangostana inhibit advanced glycation endproducts formation: Effect on amadori products, cross-linked structures and protein thiols. Molecules, 21(2), Article 251.

74. Zhu, R., Wang, C., Zhang, L., Wang, Y., Chen, G., Fan, J. et al. (2019). Pectin oligosaccharides from fruit of Actinidia arguta: Structure-activity relationship of prebiotic and antiglycation potentials. Carbohydrate Polymers, 217, 90–97.

75. Sharma, C., Kaur, A., Thind, S. S., Singh, B., Raina, S. (2015). Advanced glycation end-products (AGEs): an emerging concern for processed food industries. Journal of Food Science and Technology, 52(12), 7561–7576.–015–1851-y

76. Zhang, Q., Wang, Y., Fu, L. (2020). Dietary advanced glycation end-products: Perspectives linking food processing with health implications. Comprehensive Reviews in Food Science and Food Safety, 19(5), 559–2587.–4337.12593


For citations:

Kobelkova I.V., Korosteleva M.M., Nikityuk D.B., Kobelkova M.S. Glycation end products and technological aspects of reducing immunogenicity of specialized food products for nutrition of athletes. Food systems. 2021;4(4):278-285. (In Russ.)

Views: 244

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.

ISSN 2618-9771 (Print)
ISSN 2618-7272 (Online)