Research progress in the formation mechanism, analysis and control strategies of Maillard reaction harmful products in dairy products

Abstract

Abstract: Maillard reactions endow appealing aromas, colors, or textures in foods such as bread and coffee, however, in milk and dairy products, the Maillard reactions decrease nutritional value and generate various harmful compounds, including furosine, furfural, and advanced glycation end-products (AGEs), which are associated with chronic diseases in humans. Understanding the mechanisms of formation and establishing control methods for these compounds in dairy products is crucial for improving their quality. In this review, the biohazardous nature of harmful Maillard reactions in dairy products is comprehensively discussed. The formation of furosine, 5-hydroxymethylfurfural, and AGEs are systematically introduced. Furthermore, the advantages, deficiencies, and recent advances for methods of detecting Maillard reaction harmful products are reviewed. Current strategies for controlling the Maillard reaction harmful products in dairy products are highlighted. The aim of this paper is to provide essential scientific guidance for monitoring and controlling Maillard reaction harmful products in dairy products.

Key words: Dairy product, Maillard reaction, Furosine, Furfurals, Advanced glycation end products

CLC Number:

TS252.7

Yi-Jia Xie Bing Li. Research progress in the formation mechanism, analysis and control strategies of Maillard reaction harmful products in dairy products[J]. FOOD SCIENCE, 2025, 46(3): 0-0.

References

[1]RAZA N, KIM K.Quantification techniques for important environmental contaminants in milk and dairy products[J].TRAC-Trends in Analytical Chemistry, 2018, 98:79-84 [2]MARQUES-VIDAL P, GON?ALVES A, DIAS C M.Milk intake is inversely related to obesity in men and in young women: data from the Portuguese health interview survey 1998–1999[J].International Journal of Obesity, 2006, 30(1):88-93 [3]CRICHTON G E, ALKERWI A A.Dairy food intake is positively associated with cardiovascular health: findings from observation of cardiovascular risk factors in Luxembourg study[J].Nutrition Research, 2014, 34(12):1036-1044 [4]ELWOOD P C, PICKERING J E, GIVENS D I, et al.The consumption of milk and dairy foods and the incidence of vascular disease and diabetes: An Overview of the Evidence[J].Lipids, 2010, 45(10):925-939 [5]COUNCIL T N D.Part of a balanced diet[EB/OL]. (2024) [2024-05-31]. https://ndc.ie/nutrition/food-pyramid-and-dairy-guidelines/. [6]WEBB D, DONOVAN S M, MEYDANI S N.The role of Yogurt in improving the quality of the American diet and meeting dietary guidelines[J].Nutrition Reviews, 2014, 72(3):180-189 [7]中国疾病预防控制中心.中国居民饮食指南[EB/OL]. (2022-06-16) [2024-05-31]. https://en.chinacdc.cn/health_topics/nutrition_health/202206/t20220616_259702.html. [8]WEI J, WANG J.Chinese residents’ knowledge about and behavior towards dairy products: a cross-sectional study[J].BMC Public Health, 2023, 23(1):374- [9]MEHTA B M, DEETH H C.Blocked lysine in dairy products: formation,occurrence,analysis,and nutritional implications[J].Comprehensive Reviews in Food Science and Food Safety, 2016, 15(1):206-218 [10]HODGE J E.Dehydrated foods,chemistry of browning reactions in model systems[J].Journal of Agricultural and Food Chemistry, 1953, 1(15):928-943 [11]贾晓迪.全脂液态乳及乳粉中美拉德反应有害产物生成影响因素研究[D]. 江南大学, 2019: 2-3. [12]杨晋辉, 李松励, 郑楠, 等.热处理对牛乳成分的影响以及热敏感指标的变化研究进展[J].食品科学, 2017, 38(07):302-308 [13]LI Y, JIA X, WANG Z, et al.Characterizing changes in Maillard reaction indicators in whole milk powder and reconstituted low-temperature pasteurized milk under different preheating conditions[J].Journal of Food Science, 2022, 87(1):193-205 [14]GENG Y, MOU Y, XIE Y, et al.Dietary advanced glycation end products: an emerging concern for processed foods[J].Food reviews international, 2024, 40(1):417-433 [15]FARAG M R, Alagawany M, Bin-Jumah M, et al.The toxicological aspects of the heat-borne toxicant 5-Hydroxymethylfurfural in Animals: A Review[J].Molecules, 2020, 25(8):1941- [16]NARANJO G B, MALEC L S, Vigo M.Reducing sugars effect on available lysine loss of casein by moderate heat treatment[J].Food Chemistry, 1998, 62(3):309-313 [17]XIE Y, VAN DER FELS-KLERX H J, VAN LEEUWEN S P J, et al.Dietary advanced glycation end-products,2-monochloropropane-1,3-diol esters and 3-monochloropropane-1,2-diol esters and glycidyl esters in infant formulas: Occurrence,formulation and processing effects,mitigation strategies[J].Comprehensive Reviews in Food Science and Food Safety, 2021, 20(6):5489-5515 [18]LI M, SHEN M, LU J, et al.Maillard reaction harmful products in dairy products: formation, occurrence, analysis, and mitigation strategies[J].Food Research International, 2022, 151:110839- [19]LI Y, JIA X, WANG Z, et al.Changes in harmful Maillard reaction products in low-temperature long-time pasteurization-treated milks reconstituted from whole-milk powders after different storage times[J].Journal of Food Composition and Analysis, 2022, 106:104280- [20]MONNIER V M, SUN W, SELL D R, et al.Glucosepane: a poorly understood advanced glycation end product of growing importance for diabetes and its complications[J].Clinical Chemistry and Laboratory Medicine, 2014, 52(1):21-32 [21]SAEED Y, WANG J Q, ZHENG N.Furosine induces DNA damage and cell death in selected human cell lines: a strong toxicant to kidney Hek-293 cells[J].Food Science and Biotechnology, 2017, 26(4):1093-1101 [22]赵男.采用小鼠模型评价糠氨酸的毒性作用[D]. 安徽农业大学, 2018: 16-36. [23]LI H, YANG H, LI P, et al.Maillard reaction products with furan ring, like furosine, cause kidney injury through triggering ferroptosis pathway[J].Food Chemistry, 2020, 319:126368- [24]LEE C, CHEN K, LIN J, et al.Recent advances in processing technology to reduce 5-hydroxymethylfurfural in foods[J].Trends in Food Science & Technology, 2019, 93:271-280 [25]BARZEGAR F, KAMANKESH M, MOHAMMADI A.Recent development in formation,toxic effects,human health and analytical techniques of food contaminants[J].Food Reviews International, 2023, 39(2):1157-1183 [26]FRADE R F M, COELHO J A S, SIMEONOV S P, et al.An emerging platform from renewable resources: selection guidelines for human exposure of furfural-related compounds[J].Toxicology Research, 2014, 3(5):311-314 [27]ABRAHAM K, GüRTLER R, BERG K, et al.Toxicology and risk assessment of 5-Hydroxymethylfurfural in food[J].Molecular Nutrition & Food Research, 2011, 55(5):667-678 [28]PASTORIZA De La Cueva S, áLVAREZ J, VéGVáRI á, et al.Relationship between HMF intake and SMF formation in vivo: An animal and human study[J].Molecular Nutrition & Food Research, 2017, 61(3):1600773- [29]BROWNLEE M, VLASSARA H, CERAMI A.Nonenzymatic glycosylation and the pathogenesis of diabetic complications[J].Annals of Internal Medicine, 1984, 101(4):527-537 [30]沈正超.乳制品全链条热加工污染物的检测、变化规律及风险评估研究[D]. 北京化工大学, 2022: 7. [31]LIANG Z, CHEN X, LI L, et al.The fate of dietary advanced glycation end products in the body: from oral intake to excretion[J].Critical Reviews in Food Science and Nutrition, 2020, 60(20):3475-3491 [32]QU W, NIE C, ZHAO J, et al.Microbiome–metabolomics analysis of the impacts of long-term dietary advanced-glycation-end-product consumption on C57BL6 mouse fecal microbiota and metabolites[J].Journal of Agricultural and Food Chemistry, 2018, 66(33):8864-8875 [33]QU W, YUAN X, ZHAO J, et al.Dietary advanced glycation end products modify gut microbial composition and partially increase colon permeability in rats[J].Molecular Nutrition & Food Research, 2017, 61(10):1700118- [34]LIN R, CHOUDHURY R P, CAI W, et al.Dietary glycotoxins promote diabetic atherosclerosis in apolipoprotein E-deficient mice[J].Atherosclerosis, 2003, 168(2):213-220 [35]BOGDANOV S, LüLLMANN C, MARTIN P, et al.Honey quality and international regulatory standards: review by the International Honey Commission[J].Bee World, 1999, 80(2):61-69 [36]COUNCIL E U.Council directive 2001/110/EC of 20 December 2001 relating to honey[J].Official Journal of the European Communities L, 2002, 10:47-52 [37]JANSSON T, CLAUSEN M R, SUNDEKILDE U K, et al.Lactose-hydrolyzed milk is more prone to chemical changes during storage than conventional Ultra-High-Temperature (UHT) Milk[J].Journal of Agricultural and Food Chemistry, 2014, 62(31):7886-7896 [38]TOKU?O?LU ?, AKALIN A S, UNAL K.Rapid high performance liquid chromatographic detection of furosine (ε-n-2-furoylmethyl-l-lysine) in yogurt and cheese marketed in turkey*[J].Journal of Food Quality, 2006, 29(1):38-46 [39]GUO Y, LI H, ZHAO X, et al.Changes in Maillard reaction products, volatile substances and active proteins of goat milk under different heat treatments[J]. Changes in Maillard reaction products, volatile substances and active proteins of goat milk under different heat treatments[J]. International Dairy Journal, 2023, 146:105714- [40]SUNDS A V, RAUH V M, S?RENSEN J, et al.Maillard reaction progress in UHT milk during storage at different temperature levels and cycles[J].International Dairy Journal, 2018, 77:56-64 [41]FERRER E, ALEGRI?A A, COURTOIS G, et al.High-performance liquid chromatographic determination of Maillard compounds in store-brand and name-brand ultra-high-temperature-treated cows’ milk[J].Journal of Chromatography A, 2000, 881(1):599-606 [42]VAN Boekel M A J S.Effect of heating on Maillard reactions in milk[J].Food chemistry, 1998, 62(4):403-414 [43]HAN Z, GAO J, WANG X, et al.Formation and alterations of the potentially harmful Maillard reaction products during the production and storage of brown fermented milk[J].Molecules, 2019, 24(2):- [44]CUI Y, SHI X, TANG Y, et al.The effects of heat treatment and fermentation processes on the formation of furfurals in milk-based dairy products using a QuEChERS technique followed by gas chromatography coupled with triple quadrupole mass spectrometry[J].Food Chemistry, 2020, 313:125930- [45]AMEUR L A, MATHIEU O, LALANNE V, et al.Comparison of the effects of sucrose and hexose on furfural formation and browning in s baked at different temperatures[J].Food Chemistry, 2007, 101(4):1407-1416 [46]HELLWIG M, HENLE T.Baking,ageing,diabetes: a short history of the Maillard reaction[J].Angewandte Chemie International Edition, 2014, 53(39):10316-10329 [47]SHARMA C, KAUR A, THIND S S, et al.Advanced glycation end-products (AGEs): an emerging concern for processed food industries[J].Journal of Food Science and Technology, 2015, 52(12):7561-7576 [48]MILKOVSKA-STAMENOVA S, HOFFMANN R.Diversity of advanced glycation end products in the bovine milk proteome[J].Amino Acids, 2019, 51(6):891-901 [49]BüSER W, ERBERSDOBLER H F, LIARDON R.Identification and determination of N-ε-carboxymethyllysine by gas-liquid chromatography[J].Journal of Chromatography A, 1987, 387:515-519 [50]卞华伟, 李玉婷, 李冰, 等.国内常见食品中羧甲基赖氨酸含量分析[J].现代食品科技, 2014, 30(11):223-228 [51]LI L, ZHUANG Y, ZOU X, et al.Advanced glycation end products: a comprehensive review of their detection and occurrence in food[J].Foods, 2023, 12(11):- [52]ZHANG W, POOJARY M M, Rauh V, et al.Limitation of Maillard reactions in lactose-reduced UHT Milk via enzymatic conversion of lactose into galactooligosaccharides during production[J].Journal of Agricultural and Food Chemistry, 2020, 68(11):3568-3575 [53]ZHU R, HONG M, ZHUANG C, et al.Pectin oligosaccharides from hawthorn (Crataegus pinnatifida BungeVarmajor) inhibit the formation of advanced glycation end products in infant formula milk powder[J].Food & Function, 2019, 10(12):8081-8093 [54]LI Y, JIA X, WANG Z, et al.Characterizing changes in Maillard reaction indicators in whole milk powder and reconstituted low-temperature pasteurized milk under different preheating conditions[J].Journal of Food Science, 2022, 87(1):193-205 [55]WANG M, YUAN X, ZHENG Y, et al.Maillard reaction indicators formation, changes and possible intake in infant formula produced by different thermal treatments during domestic use[J].Food Chemistry, 2022, 395:113576- [56]SCHWIETZKE U, MALINOWSKI J, ZERGE K, et al.Quantification of Amadori products in cheese[J].European Food Research and Technology, 2011, 233(2):243-251 [57]RESMINI P, PELLEGRINO L, BATTELLI G.Accurate quantification of furosine in milk and dairy products by a direct HPLC method[J].Italian journal of food science : IJFS = Rivista italiana di scienza degli alimenti., 1990, 2(3):173-183 [58]SCHMIDT A, BOITZ L I, MAYER H K.A new UHPLC method for the quantitation of furosine as heat load indicator in commercial liquid milk[J].Journal of Food Composition and Analysis, 2017, 56:104-109 [59]BIGNARDI C, CAVAZZA A, CORRADINI C.Determination of furosine in food products by capillary zone electrophoresis-tandem mass spectrometry[J].Electrophoresis, 2012, 33(15):2382-2389 [60]TROISE A D, FIORE A, WILTAFSKY M, et al.Quantification of Nε-(2-Furoylmethyl)-l-lysine (furosine), Nε-(Carboxymethyl)-l-lysine (CML), Nε-(Carboxyethyl)-l-lysine (CEL) and total lysine through stable isotope dilution assay and tandem mass spectrometry[J].Food Chemistr, 2015, 188:357-364 [61]ASYLBEK K, éRIC D.Determination of lactulose and furosine in milk using front-face fluorescence spectroscopy[J].Lait, 2002, 82(6):725-735 [62]姚桂红, 凌云, 张雨佳, 等.高效液相色谱-四极杆飞行时间质谱法测定液态乳中糠氨酸[J].色谱, 2023, 41(11):1038-1043 [63]王峰恩, 张养东, 郑楠, 等.奶及奶制品中糠氨酸检测方法的研究进展[J].食品安全质量检测学报, 2021, 12(06):2304-2312 [64]RUTTKAT A, ERBERSDOBLER H F.Degradation of furosine during heptafluorobutyric anhydride derivatization for gas chromatographic determination[J].Journal of Chromatography A, 1994, 678(1):103-107 [65]邢倩倩.乳制品中糠醛类化合物研究进展[J].中国乳品工业, 2020, 48(4):35-39 [66]XING Q, MA Y, FU X, et al.Effects of heat treatment,homogenization pressure,and overprocessing on the content of furfural compounds in liquid milk[J].Journal of the Science of Food and Agriculture, 2020, 100(14):5276-5282 [67]G?KMEN V, ?ENYUVA H Z.Improved method for the determination of hydroxymethylfurfural in baby foods using liquid chromatography?mass spectrometry[J].Journal of Agricultural and Food Chemistry, 2006, 54(8):2845-2849 [68]BIGNARDI C, CAVAZZA A, CORRADINI C.Selected product ion monitoring for quantification of 5-hydroxymethylfurfural in food products by capillary zone electrophoresis-tandem ion trap mass spectrometry[J].Food Control, 2014, 46:41-48 [69]LI M, YAN A, HUANG Y, et al.Simultaneous quantification of four furfurals in cheeses by gas chromatography-triple quadrupole mass spectrometry[J].Journal of Food Composition and Analysis, 2023, 118:105213- [70]VELLA C, ATTARD E.Consumption of minerals,toxic metals and hydroxymethylfurfural: analysis of infant foods and formulae: Toxics[J].Toxics, 2019, 7(2):33- [71]李宇栋.羟甲基糠醛在乳制品热损伤评价中的应用[D]. 天津科技大学, 2013:23-28. [72]MADANI-TONEKABONI M, KAMANKESH M, MOHAMMADI A.Determination of furfural and hydroxymethyl furfural from baby formula using dispersive liquid–liquid microextraction coupled with high performance liquid chromatography and method optimization by response surface methodology[J].Journal of Food Composition and Analysis, 2015, 10:1-7 [73]WU Q, SHI X, REN D, et al.A rapid and sensitive method for simultaneous quantification of seven furfural compounds in milk powder based on GC-MSMS combined with QuEChERS method[J].Food Science and Technology Research, 2021, 27(4):671-679 [74]WANG Q, ZHANG J, XU Y, et al.A one-step electrochemically reduced graphene oxide based sensor for sensitive voltammetric determination of furfural in milk products[J].Analytical Methods, 2021, 13(1):56-63 [75]LI Y, HUANG L, WENG X, et al.Black Phosphorene Modified Electrochemical sensor for fast determination of 5-Hydroxymethyl-2-furfural in milk[J].Electroanalysis, 2021, 33(12):2452-2459 [76]CZERWONKA M, PIETRZAK-SAJJAD R, BOBROWSKA-KORCZAK B.Evaluation of 5-hydroxymethylfurfural content in market milk products[J].Food Addit Contam Part A Chem Anal Control Expo Risk Assess, 2020, 37(7):1135-1144 [77]PROSSER C G, CARPENTER E A, HODGKINSON A J.Nε-carboxymethyllysine in nutritional milk formulas for infants[J].Food Chemistry, 2019, 274:886-890 [78]CHARISSOU A, AIT-AMEUR L, BIRLOUEZ-ARAGON I.Evaluation of a gas chromatographymass spectrometry method for the quantification of carboxymethyllysine in food samples[J].Journal of Chromatography A, 2007, 1140(1):189-194 [79]URIBARRI J, WOODRUFF S, GOODMAN S, et al.Advanced glycation end products in foods and a practical guide to their reduction in the Diet[J].Journal of the American Dietetic Association, 2010, 110(6):911-916 [80]XIAO S, SHI L, WANG P, et al.Determination of Nε-(carboxymethyl)lysine in commercial dairy products in China with liquid chromatography tandem mass spectroscopy[J].Journal of Food Measurement and Characterization, 2022, 16(1):714-721 [81]CHEN Q, LI Y, DONG L, et al.Quantitative determination of Nε-(carboxymethyl)lysine in sterilized milk by isotope dilution UPLC-MS/MS method without derivatization and ion pair reagents[J].Food Chemistry, 2022, 385:132697- [82]YU H, ZHONG Q, GUO Y, et al.Potential of resveratrol in mitigating advanced glycation end-products formed in baked milk and baked yogurt[J]. Food Research International, 2020, 133:109191- [83]DRUSCH S, FAIST V, ERBERSDOBLER H F.Determination of N?-carboxymethyllysine in milk products by a modified reversed-phase HPLC method[J].Food Chemistry, 1999, 65(4):547-553 [84]KHAN M, LIU H, WANG J, et al.Inhibitory effect of phenolic compounds and plant extracts on the formation of advance glycation end products: A comprehensive review[J].Food Research International, 2020, 130:108933- [85]章银良, 熊卫东, 白明星.美拉德反应制备新型抗氧化剂的研究[J].食品科技, 2010, 35(02):219-222 [86]LI H, ZHANG Y, JIANG Y, et al.Application of tea polyphenols as additives in brown fermented milk: Potential analysis of mitigating Maillard reaction products[J].Journal of Dairy Science, 2023, 106(10):6731-6740 [87]PRESTEL S, DE FALCO B, BLIDI S, et al.Evaluation of the effect of berry extracts on carboxymethyllysine and lysine in ultra-high temperature treated milk[J].Food Research International, 2020, 130:108923- [88]LUND M N, RAY C A.Control of Maillard Reactions in Foods: Strategies and Chemical Mechanisms[J].Journal of Agricultural and Food Chemistry, 2017, 65(23):4537-4552 [89]ZHU R, HONG M, ZHUANG C, et al.Pectin oligosaccharides from hawthorn (Crataegus pinnatifida BungeVar. major) inhibit the formation of advanced glycation end products in infant formula milk powder[J].Food & Function, 2019, 10(12):8081-8093 [90]ZHANG H, TROISE A D, ZHANG H, et al.Cocoa melanoidins reduce the formation of dietary advanced glycation end-products in dairy mimicking system[J].Food Chemistry, 2021, 345:128827- [91]TROISE A D, VITIELLO D, TSANG C, et al.Encapsulation of ascorbic acid promotes the reduction of Maillard reaction products in UHT milk[J].Food & Function, 2016, 7(6):2591-2602 [92]AALAEI K, SJ?HOLM I, RAYNER M, et al.The impact of different drying techniques and controlled storage on the development of advanced glycation end products in skim milk powders using isotope dilution ESI-LC-MSMS[J].Food and Bioprocess Technology, 2017, 10(9):1704-1714 [93]LEE H, YANG S, HAN J, et al.Optimization of spray drying parameters and food additives to reduce glycation using response surface methodology in powdered infant formulas[J].Food Science and Biotechnology, 2019, 28(3):769-777 [94]GLIGUEM H, BIRLOUEZ-ARAGON I.Effects of Sterilization,Packaging,and Storage on Vitamin C Degradation,Protein Denaturation,and Glycation in Fortified Milks[J].Journal of Dairy Science, 2005, 88(3):891-899 [95]COUTINHO N M, SILVEIRA M R, ROCHA R S, et al.Cold plasma processing of milk and dairy products[J].Trends in Food Science & Technology, 2018, 74:56-58 [96]AMARAL G V, SILVA E K, CAVALCANTI R N, et al.Dairy processing using supercritical carbon dioxide technology: Theoretical fundamentals, quality and safety aspects[J].Trends in Food Science & Technology, 2017, 64:94-101 [97]ODUEKE O B, FARAG K W, BAINES R N, et al.Irradiation applications in dairy products: a review[J].Food and Bioprocess Technology, 2016, 9(5):751-767 [98]ASHOKKUMAR M, BHASKARACHARYA R, KENTISH S, et al.The ultrasonic processing of dairy products - an overview[J].Dairy Science & Technology, 2010, 90(2):147-168 [99]PARK H, OH M, PARK Y, et al.Nε-(carboxymethyl)lysine formation from the Maillard reaction of casein and different reducing sugars[J].Food Science and Biotechnology, 2020, 29(4):487-491 [100]ZHANG W, RAY C, POOJARY M M, et al.Inhibition of Maillard reactions by replacing galactose with galacto-oligosaccharides in casein model systems[J].Journal of Agricultural and Food Chemistry, 2019, 67(3):875-886