Abstract
Traditional thermal processing often denatures protein, causing loss of active ingredients and nutrients in dairy products, even the formation of 5-hydroxymethylfurfural (5-HMF) and advanced glycation end products (AGEs). In this study, the high hydrostatic pressure (HHP) combined with moderate heat (50 °C) pre-incubation (MHHP) was utilized to explore the alternative processing to reduce the levels of 5-HMF and AGEs in milk. The mandatory microbial indicators including total viable count, coliform, Staphylococcus aureus, and Salmonella were assessed concurrently to ensure microbiological safety. Single-factor experiments of HHP (200–600 MPa, 3–20 min) suggested that HHP intensity was negatively correlated with the levels of 5-HMF and AGEs, while positively correlated with microbial inactivation of mandatory microbial indicators. Through orthogonal experiments, 50 °C pre-incubation for 20 min followed by 600 MPa for 15 min was ascertained as the optimal processing. Compared with commercially thermal processed milk, the levels of 5-HMF and AGEs in MHHP milk were significantly reduced (p < 0.05), but no significant difference in turbidity and pH. The MHHP treatment commendably preserved the protein content of milk compared to ultrahigh-temperature treatment. There were significant differences in the color and turbidity of milk due to different processing (p < 0.05). These results can provide the basic data to establish the novel processing for producing the high-quality milk in dairy industry.
Graphical Abstract
Similar content being viewed by others
References
D’Incecco P, Limbo S, Hogenboom JA, Pellegrino L (2021) Novel technologies for extending the shelf life of drinking milk: Concepts, research trends and current applications. LWT 148:111746
Zhang Y, Yi S, Lu J, Pang X, Xu X, Lv J, Zhang S (2021) Effect of different heat treatments on the Maillard reaction products, volatile compounds and glycation level of milk. Int Dairy J 123:105182
Li Y, Wu Y, Quan W, Jia X, He Z, Wang Z, Adhikari B, Chen J, Zeng M (2021) Quantitation of furosine, furfurals, and advanced glycation end products in milk treated with pasteurization and sterilization methods applicable in China. Food Res Int 140:110088
Schmidt VS, Kaufmann V, Kulozik U, Scherer S, Wenning M (2012) Microbial biodiversity, quality, and shelf life of microfiltered and pasteurized extended shelf life (ESL) milk from Germany, Austria and Switzerland. Int J Food Microbiol 154:1–9
Henle T (2005) Protein-bound advanced glycation end products (AGEs) as bioactive amino acid derivatives in foods. Amino Acids 29:313–322
Milkovska-Stamenova S, Hoffmann R (2019) Diversity of advanced glycation end products in the bovine milk proteome. Amino Acids 51:891–901
National Toxicology Program. (1993). Toxicology and carcinogenesis studies of furan (CAS No. 110-00-9) in F344/N Rats and B6C3Fl Mice (Gavage Studies), NTP Technical Report No. 402. Research Triangle Park, NC: Public Health Service, National Institutes of Health
Gill S, Kavanagh M, Barker M, Weld M, Vavasour E, Hou Y, Cooke GM (2011) Subchronic oral toxicity study of furan in B6C3F1 mice. Toxicol Pathol 39(5):787–794
Altuner EM, Alpas H (2018) Predictive modeling for 5-hydroxymethylfurfural formation by some application conditions of high hydrostatic pressure, namely glucose concentration and application temperature, in high glucose containing model beverages. J Food Process Eng 41:e12852
Abraham K, Gürtler R, Berg K, Heinemeyer G, Lampen A, Appel KE (2011) Toxicology and risk assessment of 5-Hydroxymethylfurfural in food. Mol Nutr Food Res 55(5):667–678
Wang C, Liu Z, Hu T, Li Y, Liu R, Zhang J, He H (2020) Potential neurotoxicity of 5-hydroxymethylfurfural and its oligomers: widespread substances in carbohydrate-containing foods. Food Funct 11:4216–4223
Akhter F, Chen D, Akhter A, Sosunov AA, Chen A, McKhann GM, Yan SF, Yan SS (2020) High dietary advanced glycation end products impair mitochondrial and cognitive function. J Alzheimers Dis 76:165–178
Wang X, Liu J, Yang Y, Zhang X (2020) An update on the potential role of advanced glycation end products in glycolipid metabolism. Life Sci 245:117344
Balasubramaniam VM (2021) Process development of high pressure-based technologies for food: research advances and future perspectives. Curr Opin Food Sci 42:270–277
Mathys A, Reineke K, Heinz V, Knorr D (2009) High pressure thermal sterilization—development and application of temperature controlled spore inactivation studies. High Pressure Res 29:3–7
Stratakos AC, Inguglia ES, Linton M, Tollerton J, Murphy L, Corcionivoschi N, Koidis A, Tiwari BK (2019) Effect of high pressure processing on the safety, shelf life and quality of raw milk. Innov Food Sci Emerg Tech 52:325–333
Anwar SH, Hifdha RW, Hasan H, Rohaya S, Martunis (2020) Optimizing the sterilization process of canned yellowfin tuna through time and temperature combination. IOP Conf Ser: Earth Environ Sci 425:012031
Gupta R, Mikhaylenko G, Balasubramaniam VM, Tang J (2011) Combined pressure–temperature effects on the chemical marker (4-hydroxy-5-methyl- 3(2H)-furanone) formation in whey protein gels. LWT 44:2141–2146
Gratz M, Sevenich R, Hoppe T, Schottroff F, Vlaskovic N, Belkova B, Chytilova L, Filatova M, Stupak M, Hajslova J, Rauh C, Jaeger H (2021) Gentle sterilization of carrot-based purees by high-pressure thermal sterilization and ohmic heating and influence on food processing contaminants and quality attributes. Front Nutr 8:643837
Valdez-Fragoso A, Mújica-Paz H, Welti-Chanes J, Torres JA (2011) Reaction kinetics at high pressure and temperature: effects on milk flavor volatiles and on chemical compounds with nutritional and safety importance in several foods. Food Bioprocess Tech 4:986–995
Wang Y, Ismail M, Farid M (2017) Processing of baby food using pressure-assisted thermal sterilization (PATS) and comparison with thermal treatment. High Pressure Res 37:579–593
Bravo KS, Ramirez R, Durst R, Escobedo-Avellaneda ZJ, Welti-Chanes J, Sanz PD, Torres JA (2012) Formation risk of toxic and other unwanted compounds in pressure-assisted thermally processed foods. J Food Sci 77:1–10
Dhakal S, Balasubramaniam VM, Cocuron JC, Alonso AP, Agcam E, Kamat S (2017) Pressure-thermal kinetics of furan formation in selected fruit and vegetable juices. Food Bioprocess Tech 10:1959–1969
Evelyn F, Silva VM (2015) High pressure processing of milk: modeling the inactivation of psychrotrophic Bacillus cereus spores at 38–70°C. J Food Eng 165:141–148
Fekraoui F, Ferret É, Paniel N, Auvy O, Chamontin C, André S, Simonin H, Perrier-Cornet JM (2021) Cycling versus continuous high pressure treatments at moderate temperatures: effect on bacterial spores? Innov Food Sci Emerg Tech 74:102828
Raso J, Barbosa-Cánovas GV (2003) Nonthermal preservation of foods using combined processing techniques. Crit Rev Food Sci 43:265–285
Gervilla R, Ferragut V, Guamis B (2001) High hydrostatic pressure effects on color and milk-fat globule of ewe’s milk. J Food Sci 66:880–885
Moreno FJ, Molina E, Olano A, López-Fandiño R (2003) High-pressure effects on Maillard reaction between glucose and lysine. J Agri Food Chem 51:394–400
Buckow R, Wendorff J, Hemar Y (2011) Conjugation of bovine serum albumin and glucose under combined high pressure and heat. J Agric Food Chem 59:3915–3923
Ma XJ, Gao JY, Tong P, Li X, Chen HB (2017) Tracking the behavior of Maillard browning in lysine/arginine–sugar model systems under high hydrostatic pressure. J Sci Food Agri 97:5168–5175
Schwarzenbolz U, Förster A, Henle T (2017) Influence of high hydrostatic pressure on the reaction between glyoxal and lysine residues. Eur Food Res Tech 243(8):1355–1361
Ministry of Agriculture of the People’s Republic of China. Agricultural industry standards of the People’s Republic of China-Identification of reconstituted milk in pasteurized and UHT milk: NY/T 939–2016
Huang Y, Li C, Hu H, Wang Y, Shen M, Nie S, Chen J, Zeng M, Xie M (2019) Simultaneous determination of acrylamide and 5-hydroxymethylfurfural in heat-processed foods employing enhanced matrix removal—lipid as a new dispersive solid-phase extraction sorbent followed by liquid chromatography–tandem mass spectrometry. J Agric Food Chem 67:5017–5025
Han Z, Gao J, Li J, Zhang Y, Yang Y, Wang S (2019) Mitigation of 3-deoxyglucosone and 5-hydroxymethylfurfural in brown fermented milk via an alternative browning process based on the hydrolysis of endogenous lactose. Food Funct 10:2022–2029
Li M, Lu J, Huang Y, Wang W, Xie J, Xie M, Shen M (2022) Quantitative assessment of furosine, furfurals, and advanced glycation end products in different types of commercially available cheeses. Food Control 136:108866
Ministry of Health of the People’s Republic of China. National standard for food safety: Determination of aerobic plate count in Food. GB/T 4789.2-2016
Ministry of Health of the People’s Republic of China. National standard for food safety: Determination of coliforms in Food. GB/T 4789.3-2016
Ministry of Health of the People’s Republic of China. National standard for food safety: Determination of Staphylococcus aureus in Food. GB 4789.10-2016
Ministry of Health of the People’s Republic of China. National standard for food safety: Determination of Salmonella in Food. GB/T 4789.4-2016
Li F, Cao J, Liu Q, Hu X, Liao X, Zhang Y (2020) Acceleration of the Maillard reaction and achievement of product quality by high pressure pretreatment during black garlic processing. Food Chem 318:126517
Al-Nabulsi A, Shaker R, Osaili T, Clark S, Harte F, Barbosa-Cánovas G (2012) Impact of high hydrostatic pressure and heat treatments on milk gel properties: a comparative rheological study. Int J Food Prop 15:613–627
Ministry of Health of the People’s Republic of China. National standard for food safety: Determination of Protein in Food. GB/T 5009.5-2016
Koszucka A, Nowak A (2019) Thermal processing food-related toxicants: a review. Crit Rev Food Sci 59:3579–3596
Claeys WL, Van Loey AM, Hendrickx ME (2003) Influence of seasonal variation on kinetics of time temperature integrators for thermally processed milk. J Dairy Res 70:217–225
Önür İ, Misra NN, Barba FJ, Putnik P, Lorenzo JM, Gökmen V, Alpas H (2018) Effects of ultrasound and high pressure on physicochemical properties and HMF formation in Turkish honey types. J Food Eng 219:129–136
Divine RD, Sommer D, Lopez-Hernandez A, Rankin SA (2012) Short communication: evidence for methylglyoxal-mediated browning of Parmesan cheese during low temperature storage. J Dairy Sci 95:2347–2354
Walsh Aaron M, Crispie F, Kilcawley K, O’Sullivan O, O’Sullivan Maurice G, Claesson Marcus J, Cotter Pau D (2016) Microbial succession and flavor production in the fermented dairy beverage kefir. mSystems 1:e00052-16
Schwarzenbolz U, Henle T (2010) Non-enzymatic modifications of proteins under high-pressure treatment. High Pressure Res 30:458–465
Prestes Fallavena L, Poerner Rodrigues N, Damasceno Ferreira Marczak L, Domeneghini MG (2022) Formation of advanced glycation end products by novel food processing technologies: a review. Food Chem 393:133338
Stoynev GA, Srebreva LN, Ivanov IG (2004) Histone H1 as a reporter protein to investigate glycation in bacteria. Curr Microbiol 49:423–427
Sarker MR, Akhtar S, Torres JA, Paredes-Sabja D (2015) High hydrostatic pressure-induced inactivation of bacterial spores. Crit Rev Microbiol 41:18–26
Pellegrino L, De Noni I, Resmini P (1995) Coupling of lactulose and furosine indices for quality evaluation of sterilized milk. Int Dairy J 5:647–659
Tamaoka T, Itoh N, Hayashi R (1991) High pressure effect on Maillard reaction. Agri Biol Chem 55:2071–2074
Zhang W, Poojary MM, Olsen K, Ray CA, Lund MN (2019) Formation of α-dicarbonyls from dairy related carbohydrates with and without Nα-Acetyl-l-Lysine during incubation at 40 °C and 50 °C. J Agri Food Chem 67:6350–6358
Hill VM, Ledward DA, Ames JM (1996) Influence of high hydrostatic pressure and pH on the rate of Maillard browning in a glucose−lysine system. J Agri Food Chem 44:594–598
Ministry of Health of the People’s Republic of China. National food safety standard Pasteurized milk. GB 19645—2010
Mazri C, Sánchez L, Ramos SJ et al (2012) Effect of high-pressure treatment on denaturation of bovine β-lactoglobulin and α-lactalbumin. Eur Food Res Technol 234:813–819
Altuner EM, Alpas H, Erdem YK, Bozoglu F (2006) Effect of high hydrostatic pressure on physicochemical and biochemical properties of milk. Eur Food Res Tech 222(3–4):392–396
Kiełczewska K, Jankowska A, Dąbrowska A, Wachowska M, Ziajka J (2020) The effect of high pressure treatment on the dispersion of fat globules and the fatty acid profile of caprine milk. Int Dairy J 102:104607
Funding
This work was supported by the grants from National Key R&D Program of China (No. 2018YFC1604203).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Compliance with Ethics Requirements
This article does not contain any studies with human or animal subjects.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wu, Y., Wu, S., Sun, M. et al. Reduction of the levels of 5-hydroxymethylfurfural and advanced glycation end products in milk by the combination of high pressure and moderate heat pre-incubation. Eur Food Res Technol 249, 923–937 (2023). https://doi.org/10.1007/s00217-022-04184-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00217-022-04184-8