Microstructural changes in acid milk gels due to temperature-controlled high-intensity ultrasound treatment: Quantification by analysis of super-resolution microscopy images
Zachary James Glover
Department of Physics, Chemistry and Pharmacy, University of Southern Denmark, Campusvej 55, Odense M, 5230 Denmark
Contribution: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - original draft
Search for more papers by this authorCorresponding Author
Sandra Beyer Gregersen
Department of Food Science, Aarhus University, Agro Food Park 48, Aarhus N, 8200 Denmark
Author for correspondence. E-mail: [email protected]
Contribution: Conceptualization, Data curation, Formal analysis, Writing - review & editing
Search for more papers by this authorLars Wiking
Department of Food Science, Aarhus University, Agro Food Park 48, Aarhus N, 8200 Denmark
Contribution: Conceptualization, Funding acquisition, Supervision, Writing - review & editing
Search for more papers by this authorMariannne Hammershøj
Department of Food Science, Aarhus University, Agro Food Park 48, Aarhus N, 8200 Denmark
Contribution: Conceptualization, Funding acquisition, Project administration, Supervision, Writing - review & editing
Search for more papers by this authorAdam Cohen Simonsen
Department of Physics, Chemistry and Pharmacy, University of Southern Denmark, Campusvej 55, Odense M, 5230 Denmark
Contribution: Conceptualization, Funding acquisition, Methodology, Resources, Supervision, Validation, Writing - review & editing
Search for more papers by this authorZachary James Glover
Department of Physics, Chemistry and Pharmacy, University of Southern Denmark, Campusvej 55, Odense M, 5230 Denmark
Contribution: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - original draft
Search for more papers by this authorCorresponding Author
Sandra Beyer Gregersen
Department of Food Science, Aarhus University, Agro Food Park 48, Aarhus N, 8200 Denmark
Author for correspondence. E-mail: [email protected]
Contribution: Conceptualization, Data curation, Formal analysis, Writing - review & editing
Search for more papers by this authorLars Wiking
Department of Food Science, Aarhus University, Agro Food Park 48, Aarhus N, 8200 Denmark
Contribution: Conceptualization, Funding acquisition, Supervision, Writing - review & editing
Search for more papers by this authorMariannne Hammershøj
Department of Food Science, Aarhus University, Agro Food Park 48, Aarhus N, 8200 Denmark
Contribution: Conceptualization, Funding acquisition, Project administration, Supervision, Writing - review & editing
Search for more papers by this authorAdam Cohen Simonsen
Department of Physics, Chemistry and Pharmacy, University of Southern Denmark, Campusvej 55, Odense M, 5230 Denmark
Contribution: Conceptualization, Funding acquisition, Methodology, Resources, Supervision, Validation, Writing - review & editing
Search for more papers by this authorAbstract
High-intensity ultrasound (HIU) can be applied to food materials to create novel structures and textures, and as a method of processing. HIU treatment of milk modifies the gelation behaviour, but the microstructural impact is poorly understood. Milk samples were treated with HIU at three temperatures: 27°C, 50°C, and 70°C. Acid milk gels were formed from the milk and imaged using super-resolution stimulated emission depletion and confocal microscopy. Quantitative image analysis was applied and demonstrated that HIU treatment leads to measurable changes in both protein network morphology and degree of association of the fat droplets with the protein network.
CONFLICT OF INTERESTS
The authors have no competing interests.
Open Research
DATA AVAILABILITY STATEMENT
The research data are not shared.
References
- Aguilera J M, Stanley D W and Baker K W (2000) New dimensions in microstructure of food products. Trends in Food Science & Technology 11 3–9.
- Ainis W N, Ersch C, Farinet C, Yang Q, Glover Z J and Ipsen R (2019) Rheological and water holding alterations in mixed gels prepared from whey proteins and rapeseed proteins. Food Hydrocolloids 87 723–733.
- Ako K, Durand D, Nicolai T and Becu L (2009) Quantitative analysis of confocal laser scanning microscopy images of heat-set globular protein gels. Food Hydrocolloids 23 1111–1119.
- Anema S G and Li Y (2000) Further studies on the heat-induced pH-dependent dissociation of casein from the micelles in reconstituted skim milk LWT. Food Science and Technology 33 335–343.
- Anema S G and Li Y (2003) Association of denatured whey proteins with casein micelles in heated reconstituted skim milk and its effect on casein micelle size. Journal of Dairy Research 70 73–83.
- Araiza-Calahorra A, Glover Z J, Akhtar M and Sarkar A (2020) Conjugate microgel-stabilized Pickering emulsions: Role in delaying gastric digestion. Food Hydrocolloids 105 1–13.
- Awad T S, Moharram H A, Shaltout O E, Asker D Y M M and Youssef M M (2012) Applications of ultrasound in analysis processing and quality control of food: a review. Food Research International 48 410–427.
- Bui A T H, Cozzolino D, Zisu B and Chandrapala J (2021) Infrared analysis of ultrasound treated milk systems with different levels of caseins whey proteins and fat. International Dairy Journal 117 1–11.
- Carrillo-Lopez L M, Garcia-Galicia I A, Tirado-Gallegos J M, Sanchez-Vega R, Huerta-Jimenez M, Ashokkumar M and Alarcon-Rojo A D (2021) Recent advances in the application of ultrasound in dairy products: effect on functional physical chemical microbiological and sensory properties. Ultrasonics Sonochemistry 73 1–35.
- Chatterton D E, Smithers G, Roupas P and Brodkorb A (2006) Bioactivity of β-lactoglobulin and α-lactalbumin—technological implications for processing. International Dairy Journal 16 1229–1240.
- Cho Y H, Lucey J A and Singh H (1999) Rheological properties of acid milk gels as affected by the nature of the fat globule surface material and heat treatment of milk. International Dairy Journal 9 537–545.
- De Kruif C G, Huppertz T, Urban V S and Petukhov A V (2012) Casein micelles and their internal structure. Advances in Colloid and Interface Science 171 36–52.
- Ersch C, Meinders M B, Bouwman W G, Nieuwland M, van der Linden E, Venema P and Martin A H (2016) Microstructure and rheology of globular protein gels in the presence of gelatin. Food Hydrocolloids 55 34–46.
- Gao X, Yongsawatdigul J, Wu R, You J, Xiong S, Du H and Liu R (2021) Effect of ultrasound pre-treatment modes on gelation properties of silver carp surimi. LWT 150 111945.
- Glover Z J, Bisgaard A H, Andersen U, Povey M J, Brewer J R and Simonsen A C (2019b) Cross-correlation analysis to quantify relative spatial distributions of fat and protein in super-resolution microscopy images of dairy gels. Food Hydrocolloids 97 105225.
- Glover Z J, Ersch C, Andersen U, Holmes M J, Povey M J, Brewer J R and Simonsen A C (2019a) Super-resolution microscopy and empirically validated autocorrelation image analysis discriminates microstructures of dairy derived gels. Food Hydrocolloids 90 62–71.
- Glover Z J, Francis M J, Bisgaard A H, Andersen U, Johansen L B, Povey M J, Holmes M J, Brewer J R and Simonsen A C (2020) Dynamic moisture loss explored through quantitative super-resolution microscopy spatial micro-viscosity and macroscopic analyses in acid milk gels. Food Hydrocolloids 101 105501.
- Glover Z J and Holmes M J (2020) Physics in the rehydration and structure formation of recombined dairy products. In Physics in Food Manufacturing: Case Studies in Fundamental and Applied Research, pp 9-1–9-21. M J Povey, eds. Bristol, UK: IOP Publishing.
10.1088/978-0-7503-2596-7ch9 Google Scholar
- Gregersen S B, Glover Z J, Wiking L, Simonsen A C, Bertelsen K, Pedersen B, Poulsen K R, Andersen U and Hammershøj M (2021) Microstructure and rheology of acid milk gels and stirred yoghurts–quantification of process-induced changes by auto-and cross correlation image analysis. Food Hydrocolloids 111 106269.
- Gregersen S B, Wiking L and Hammershøj M (2019) Acceleration of acid gel formation by high intensity ultrasound is linked to whey protein denaturation and formation of functional milk fat globule-protein complexes. Journal of Food Engineering 254 17–24.
- Hansen S F, Nielsen S D, Rasmusen J T, Larsen L B and Wiking L (2020) Disulfide bond formation is not crucial for the heat-induced interaction between β-lactoglobulin and milk fat globule membrane proteins. Journal of Dairy Science 103 5874–5881.
- Hell S W (2007) Far-field optical nanoscopy. Science 316 1153–1158.
- Hell S W and Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Optics Letters 19 780–782.
- Huppertz T and Kelly A L (2006) Physical chemistry of milk fat globules. In Advanced Dairy Chemistry Volume 2 Lipids, pp. 173–212. P. F. Fox & P. L. H. McSweeney eds, Boston, MA: Springer.
10.1007/0-387-28813-9_5 Google Scholar
- Jenness R and Koops J (1962) Preparation and properties of a salt solution which simulates milk ultrafiltrate. Netherlands Milk and Dairy Journal 16 153–164.
- Kentish S and Feng H (2014) Applications of power ultrasound in food processing. Annual Review of Food Science and Technology 5 263–284.
- Kethireddipalli P, Hill A R and Dalgleish D G (2011) Interaction between casein micelles and whey protein/κ-casein complexes during renneting of heat-treated reconstituted skim milk powder and casein micelle/serum mixtures. Journal of Agricultural and Food Chemistry 59 1442–1448.
- Liang F, Zhu Y, Ye T, Jiang S, Lin L and Lu J (2020) Effect of ultrasound assisted treatment and microwave combined with water bath heating on gel properties of surimi-crabmeat mixed gels. LWT 133 110098.
- Liu Y, Boeren S, Zhang L, Zhou P and Hettinga K (2021) Ultrasonication retains more milk fat globule membrane proteins compared to equivalent shear-homogenization. Innovative Food Science & Emerging Technologies 70 102703.
- Lopez C, Camier B and Gassi J Y (2007) Development of the milk fat microstructure during the manufacture and ripening of Emmental cheese observed by confocal laser scanning microscopy. International Dairy Journal 17 235–247.
- Lucey J A, Munro P A and Singh H (1999) Effects of heat treatment and whey protein addition on the rheological properties and structure of acid skim milk gels. International Dairy Journal 9 275–279.
- Nguyen N H and Anema S G (2010) Effect of ultrasonication on the properties of skim milk used in the formation of acid gels. Innovative Food Science & Emerging Technologies 11 616–622.
- Nguyen N H and Anema S G (2017) Ultrasonication of reconstituted whole milk and its effect on acid gelation. Food Chemistry 217 593–601.
- Povey M J (2017) Applications of ultrasonics in food science-novel control of fat crystallization and structuring. Current Opinion in Colloid & Interface Science 28 1–6.
- Qayum A, Hussai M, Li M, Li J, Shi R, Li T, Anwar A, Ahmed Z, Hou J and Jiang Z (2021) Gelling, microstructure and water-holding properties of alpha-lactalbumin emulsion gel: Impact of combined ultrasound pretreatment and laccase cross-linking. Food Hydrocolloids 110 106122.
- Ragab E S, Zhang S, Pang X, Lu J, Nassar K S, Yang B, Obaroakpo U J and Lv J (2020) Ultrasound improves the rheological properties and microstructure of rennet-induced gel from goat milk. International Dairy Journal 104 104642.
- Riener J, Noci F, Cronin D A, Morgan D J and Lyng J G (2009) The effect of thermosonication of milk on selected physicochemical and microstructural properties of yoghurt gels during fermentation. Food Chemistry 114 905–911.
- Shanmugam A, Chandrapala J and Ashokkumar M (2012) The effect of ultrasound on the physical and functional properties of skim milk. Innovative Food Science & Emerging Technologies 16 251–258.
- Steffl A, Schreiber R, Hafenmair M and Kessler H G (1999) Effect of denatured whey proteins on the rennet-induced aggregation of casein micelles. International Dairy Journal 9 401–402.
- Sun Y, Ma L, Fu Y, Dai H and Zhang Y (2021) The improvement of gel and physicochemical properties of porcine myosin under low salt concentrations by pulsed ultrasound treatment and its mechanism. Food Research International 141 1–9.
- Urbonaite V, De Jongh H H J, Van Der Linden E and Pouvreau L (2015) Water holding of soy protein gels is set by coarseness modulated by calcium binding rather than gel stiffness. Food Hydrocolloids 46 103–111.
- Urbonaite V, Van der Kaaij S, De Jongh H H J, Scholten E, Ako K, Van der Linden E and Pouvreau L (2016) Relation between gel stiffness and water holding for coarse and fine-stranded protein gels. Food Hydrocolloids 56 334–343.
- Van Vliet T (1988) Rheological properties of filled gels Influence of filler matrix interaction. Colloid and Polymer Science 266 518–524.
- Villamiel M and de Jong P (2000) Influence of high-intensity ultrasound and heat treatment in continuous flow on fat proteins and native enzymes of milk. Journal of Agricultural and Food Chemistry 48 472–478.
- Watson N J, Johal R K, Glover Z, Reinwald Y, White L J, Ghaemmaghami A M, Morgan S P, Rose F R A J, Povey M J W and Parker N G (2013) Post-processing of polymer foam tissue scaffolds with high power ultrasound: a route to increased pore interconnectivity pore size and fluid transport. Materials Science and Engineering: C 33 4825–4832.
- Yadav J S S, Yan S, Pilli S, Kumar L, Tyagi R D and Surampalli R Y (2015) Cheese whey: A potential resource to transform into bioprotein functional/nutritional proteins and bioactive peptides. Biotechnology Advances 33 756–774.
- Zhao C, Chu Z, Miao Z, Liu J, Liu J, Xu X, Wu Y, Qi B and Yan J (2021) Ultrasound heat treatment effects on structure and acid-induced cold set gel properties of soybean protein isolate. Food Bioscience 39 1–9.
