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Cited by 6Microbial Inactivation MethodsPlasma Applications and DiagnosticsAnimal health and immunology

The Effect of Cold Plasma on Selected Parameters of Bovine Colostrum

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Bogusławska-Wąs, Elżbieta, Dłubała, Alicja, Sawicki, Wojciech, Ożgo, Małgorzata, Lepczyński, Adam·2023·Applied Sciences
DOI 10.3390/app13095490
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Abstract

The main problem in processing bovine colostrum is preserving as many beneficial compounds as possible, most of which have low thermal stability. The present study evaluates the possibility of using cold plasma (CP) as a decontamination technology and its effect on selected biologically active fractions of freeze-dried bovine colostrum. The plasma process was carried out in air, nitrogen, and oxygen environments. The results revealed that the sterilization process using CP caused slight changes in the colour of the samples expressed by the attributes ΔC, ΔL, Δh and ΔE. The decontamination effect depended on the gas used and the type of microorganism. The highest decontamination effects were gained under oxygen conditions, where reductions were obtained for total psychrophilic bacteria (THPC) by log 1.24, mesophilic bacteria (THMC) by log 1.02, Enterobacteriaceae by log 1.16, E. coli by log 0.96, yeast (TYMC) by log 0.92. A significantly lower decontaminating effect was obtained for Gram-positive bacteria and sporophytic forms. Additionally, the application of CP, regardless of the gas used, affected the modification of protein structure and reduction of immunoglobulin concentration. as proven by proteomics analyses (1-DE, 2-DE, MALDI–TOF MS). The same applied to β-lactoglobulin in air and oxygen and BSA in nitrogen and air.

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  • The antimicrobial effects of CP, involving reactive species attacking bacterial cells, damaging cell walls, increasing membrane permeability, leading to cell membrane rupture, damage to organelles, proteins, and nucleic acids, and microbial cell death, may explain the shifts in genera.

    “The underlying mechanism for these shifts may involve the antimicrobial effects of CP: reactive species generated during CP treatment can attack bacterial cells, damaging cell walls to increase membrane permeability. This process ultimately leads to cell membrane rupture, followed by damage to organelles, proteins, and nucleic acids, culminating in microbial cell death [55,56].”

    From Effect of Atmospheric Cold Plasma Treatment on the Microorganism Growth, Diversity, and Quality of Coconut Water During Refrigerator Storage (2025) · cites this paper as [55]

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Research works printed but not linked: 58

  1. Brian, A.M.; Patric, F.F.; Paul, S.; Alan, K. Composition and properties of bovine colostrum: A review. Dairy Sci. Technol. 2016, 96, 133-158.
  2. Pakkanen, R.; Aalto, J. Growth factors and antimicrobial factors of bovine colostrum. Int. Dairy J. 1997, 7, 258-297. [CrossRef] · DOI
  3. Shen, R.L.; Thymann, T.; Østergaard, M.V.; Støy, A.C.; Krych, Ł.; Nielsen, D.S.; Lauridsen, C.; Hartmann, B.; Holst, J.J.; Burrin, D.G.; et al. Early gradual feeding with bovine colostrum improves gut function and NEC resistance relative to infant formula in preterm pigs. Am. J. Physiol. Gastrointest. Liver. Physiol 2015, 309, 310-320. [CrossRef] · DOI
  4. Playford, R.J.; Weiser, M.J. Bovine Colostrum: Its Constituents and Uses. Nutrients 2021, 13, 265. [CrossRef] · DOI
  5. Płusa, T. Immunomodulatory proteins in colostrum. Pol. Merkur. Lekarski. 2009, 26, 8-10.
  6. Chen, D.; Peng, P.; Zhou, N.; Cheng, Y.; Min, M.; Ma, Y.; Mao, Q.; Chen, P.; Chen, C.; Ruan, R. Evaluation of Cronobacter sakazakii inactivation and physicochemical property changes of non-fat dry milk powder by cold atmospheric plasma. Food Chem. 2019, 290, 270-276. [CrossRef] · DOI
  7. Chiang, S.H.; Chang, C.Y. Antioxidant properties of caseins and whey proteins from colostrums. J. Food Drug. Anal. 2005, 13, 57-63. [CrossRef] · DOI
  8. Wieczorek-D ąbrowska, M.; Wójcik, P.; Malinowski, E. Importance of cow colostrum and factors determining its quality. Balice Przegl ąd Hod. 2013, 81, 9-10.
  9. Kim, J.S.; Lee, E.J.; Choi, E.H.; Kim, Y.J. Inactivation of Staphylococcus aureus on the beef jerky by radio-frequency atmospheric pressure plasma discharge treatment. Innov. Food Sci. Emerg. Technol. 2014, 22, 124-130. [CrossRef] · DOI
  10. Toepfl, S.; Mathys, A.; Heinz, V.; Knorr, D. Review: Potential of High Hydrostatic Pressure and Pulsed Electric Fields for Energy Efficient and Environmentally Friendly Food Processing. Food Rev. Int. 2006, 22, 405-423. [CrossRef] · DOI
  11. van Boekel, M.; Fogliano, V.; Pellegrini, N.; Stanton, C.; Scholz, G.; Lalljie, S.; Somoza, V.; Knorr, D.; Jasti, P.R.; Eisenbrand, G. A review on the beneficial aspects of food processing. Mol. Nutr. Food Res. 2010, 54, 1215-1247. [CrossRef] · DOI
  12. Fecteau, G.; Baillargeon, P.; Higgins, R.; Paré, J.; Fortin, M. Bacterial contamination of colostrum fed to newborn calves in Québec dairy herds. Can. Vet. J. 2002, 43, 523-527.
  13. Nwabor, O.F.; Onyeaka, H.; Miri, T.; Obileke, K.; Anumudu, C.; Hart, A. A Cold Plasma Technology for Ensuring the Microbiolog- ical Safety and Quality of Foods. Food Eng. Rev. 2022, 14, 535-554. [CrossRef] · DOI
  14. Reineke, K.; Langer, K.; Hertwig, C.; Ehlbeck, J.; Schlüter, O. The impact of different process gas compositions on the inactivation effect of an atmospheric pressure plasma jet on Bacillus spores. Innov. Food Sci. Emerg. Technol. 2015, 30, 112-118. [CrossRef] · DOI
  15. Kim, H.-J.; Yong, H.I.; Park, S.; Choe, W.; Jo, C. Effects of dielectric barrier discharge plasma on pathogen inactivation and the physicochemical and sensory characteristics of pork loin. Curr. Appl. Phys. 2013, 13, 1420-1425. [CrossRef] · DOI
  16. Lee, H.J.; Jung, S.; Jung, H.; Park, S.; Choe, W.; Ham, J.S.; Jo, C. Evalution of dielectric barier discharge plasma system for inactivatating pathogens on cheese slices. J. Anim. Sci. Technol. 2012, 54, 191-198. [CrossRef] · DOI
  17. Moreau, M.; Orange, N.; Feuilloley, M.G.J. Non-thermal plasma technologies: New tools for bio-decontamination. Biotechnol. Adv. 2008, 26, 610-617. [CrossRef] · DOI
  18. Dmytrów, I.; Szymczak, M.; Szkolnicka, K.; Kami ński, P. Development of Functional Acid Curd Cheese (Tvarog) with Antioxidant Activity Containing Astaxanthin from Shrimp Shells Preliminary Experiment. Foods 2021, 10, 895. [CrossRef] · DOI
  19. Pankaj, S.K.; Bueno-Ferrer, C.; Misra, N.N.; O'Neill, L.; Tiwari, B.K.; Bourke, P.; Cullen, P.J. Physicochemical characterization of plasma-treated sodium caseinate film. Food Res. Int. 2014, 66, 438-444. [CrossRef] · DOI
  20. Drake, M.A.; Karagul-Yuceer, Y.; Cadwallader, K.R.; Civtlle, G.V.; Tong, P.S. Determination of the sensory attributes of dried milk powders and dairy ingredients. J. Sens. Stud. 2003, 18, 199-2016. [CrossRef] · DOI
  21. Abdalla, A.K.; Smith, J.K.; Lucey, K. Physical Properties of Nonfat Dry Milk and Skim Milk Powder. Int. J. Dairy Sci. 2017, 12, 149-154. [CrossRef] · DOI
  22. Lepczy ński, A.; O żgo, M.; Dratwa-Chałupnik, A.; Robak, P.; Pyć, A.; Zaborski, D.; Herosimczyk, A. An update on medium-and low-abundant blood plasma proteome of horse. Animal 2018, 12, 76-87. [CrossRef] · DOI
  23. Lepczy ński, A.; O żgo, M.; Michałek, K.; Dratwa-Chałupnik, A.; Grabowska, M.; Herosimczyk, A.; Liput, K.P.; Poławska, E.; Kram, A.; Pierzchała, M. Effects of three-month feeding high fat diets with different fatty acid composition on myocardial proteome in mice. Nutrients 2021, 13, 330. [CrossRef] · DOI
  24. Ozgo, M.; Lepczynski, A.; Herosimczyk, A. Two-dimensional gel-based serum protein profile of growing piglets. Turk. J. Biol. 2015, 39, 320-327. [CrossRef] · DOI
  25. Godden, S.M.; Lombard, J.E.; Woolums, A.R. Colostrum Management for Dairy Calves. Vet. Clin. North. Am. Food. Anim. Pract. 2019, 35, 535-556. [CrossRef] · DOI
  26. Lorenz, I.; Mee, J.F.; Earley, B.; More, S.J. Calf health from birth to weaning. General aspects of disease prevention. Ir. Vet. J. 2011, 16, 3-8. [CrossRef] · DOI
  27. Bourke, P.; Ziuzina, D.; Han, L.; Cullen, P.J.; Gilmore, B.F. Microbiological interactions with cold plasma. J. Appl. Microbiol. 2017, 123, 308-324. [CrossRef] · DOI
  28. Stoffels, E.; Sakiyama, Y.; Graves, D.B. Cold atmospheric plasma: Charged species and their interactions with cells and tissues. IEEE Trans. Plasma Sci. 2008, 36, 1441-1457. [CrossRef] · DOI
  29. Fröhling, A.; Baier, M.; Ehlbeck, J.; Knorr, D.; Schlüter, O. Atmospheric pressure plasma treatment of Listeria innocua and Escherichia coli at polysaccharide surfaces: Inactivation kinetics and flow cytometric characterization. Innov. Food Sci. Emerg. Technol. 2012, 13, 142-150. [CrossRef] · DOI
  30. Hertwig, C.; Reineke, K.; Ehlbeck, J.; Erdo gdu, B.; Rauh, C.; Schlüter, O. Impact of remote plasma treatment on natural microbial load and quality parameters of selected herbs and spices. J. Food Eng. 2015, 167, 12-17. [CrossRef] · DOI
  31. Cummins, C.; Lorenz, I.; Kennedy, E. Short communication: The effect of storage conditions over time on bovine colostral immunoglobulin G concentration, bacteria, and pH. J. Dairy Sci. 2016, 99, 4857-4863. [CrossRef] [PubMed] · DOI
  32. Fasse, S.; Jarmo, A.; Björn, F.; Gun, W. Bovine Colostrum for Human Consumption-Improving Microbial Quality and Maintaining Bioactive Characteristics through Processing. Dairy 2021, 2, 556-575. [CrossRef] · DOI
  33. Moisan, M.; Barbeau, J.; Moreau, S.; Pelletier, J.; Tabrizian, M.; Yahia, L.H. Low-temperature sterilization using gas plasmas: A review of the experiments and an analysis of the inactivation mechanisms. Int. J. Pharm. 2001, 226, 1-21. [CrossRef] · DOI
  34. Schlüter, O.; Fröhling, A. Non-Thermal Processing Cold Plasma for Bioefficient Food Processing, Reference Module in Food Science Encyclopedia of Food Microbiology, 2nd ed.; Elsevier: New York, NY, USA, 2014; pp. 948-953.
  35. Li, J.; Sakai, N.; Watanabe, M.; Hotta, E.; Wachi, M. Study on plasma agent effect of a direct-current atmospheric pressure oxygen-plasma jet on inactivation of E. coli using bacterial mutants. IEEE Trans. Plasma Sci. 2013, 41, 935-941. [CrossRef] · DOI
  36. Joshi, S.G.; Cooper, M.; Yost, A.; Paff, M.; Ercan, U.K.; Fridman, G.; Friedman, G.; Fridman, A.; Brooks, A.D. Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob. Agents. Chemother. 2011, 55, 1053-1062. [CrossRef] · DOI
  37. Hertwig, C.; Meneses, N.; Mathys, A. Cold atmospheric pressure plasma and low energy electron beam as alternative nonthermal decontamination technologies for dry food surfaces: A review. Trends Food Sci. Technol. 2018, 77, 131-142. [CrossRef] · DOI
  38. Deng, X.; Shi, J.; Kong, M.G. Physical mechanisms of inactivation of Bacillus subtilis spores using cold atmospheric plasmas. IEEE Trans. Plasma Sci. 2006, 34, 1310-1316. [CrossRef] · DOI
  39. Tseng, S.; Abramzon, N.; Jackson, J.O.; Lin, W.J. Gas discharge plasmas are effective in inactivating Bacillus and Clostridium spores. Appl. Microbiol. Biotechnol. 2012, 93, 2563-2570. [CrossRef] · DOI
  40. Wang, S.; Doona, C.J.; Setlow, P.; Li, Y.Q. Use of Raman Spectroscopy and Phase-Contrast Microscopy to Characterize Cold Atmospheric Plasma Inactivation of Individual Bacterial Spores. Appl. Environ. Microbiol. 2016, 82, 5775-5784. [CrossRef] · DOI
  41. Segat, A.; Misra, N.N.; Cullen, P.J.; Innocente, N. Effect of atmospheric pressure cold plasma (ACP) on activity and structure of alkaline phosphatase. Food Bioprod. Process. 2016, 98, 181-188. [CrossRef] · DOI
  42. Manoharan, D.; Stephen, J.; Radhakrishnan, M. Study on low-pressure plasma system for continuous decontamination of milk and its quality evaluation. J. Food Process. Preserv. 2020, 45, 234-245. [CrossRef] · DOI
  43. Wan, Z.; Misra, N.N.; Li, G.; Keener, K.M. High voltage atmospheric cold plasma treatment of Listeria innocua and Escherichia coli K-12 on Queso Fresco (fresh cheese). LWT 2021, 146, 111406. [CrossRef] · DOI
  44. Oehmigen, K.; Hahnel, M.; Brandenburg, R.; Wilke, C.; Weltmann, K.D.; von Woedtke, T. The Role of Acidification for Antimicro- bial Activity of Atmospheric Pressure Plasma in Liquids. Plasma Process. Polym. 2010, 7, 250-257. [CrossRef] · DOI
  45. Traylor, M.J.; Pavlovich, M.J.; Karim, S.; Hait, P.; Sakiyama, Y.; Clark, D.S.; Graves, D.B. Long-term antibacterial efficacy of air plasma-activated water. J. Phys. Appl. Phys. 2011, 44, 134-145. [CrossRef] · DOI
  46. Gross, J.J.; Kessler, E.C.; Bruckmaier, R.M. Colour measurement of colostrum for estimation of colostral IgG and colostrum composition in dairy cows. J. Dairy. Res. 2014, 81, 440-444. [CrossRef] [PubMed] · DOI
  47. Gurol, C.; Ekinci, F.Y.; Aslan, N.; Korachi, M. Low Temperature Plasma for decontamination of E. coli in milk. Int. J. Food. Microbiol. 2012, 157, 1-5. [CrossRef] · DOI
  48. Yong, H.I.; Kim, H.-J.; Park, S.; Kim, K.; Choe, W.; Yoo, S.J.; Jo, C. Pathogen inactivation and quality changes in sliced cheddar cheese treated using flexible thin-layer dielectric barrier discharge plasma. Food Res. Int. 2015, 69, 57-63. [CrossRef] · DOI
  49. Nikmaram, N.; Keener, K.M. The effects of cold plasma technology on physical, nutritional, and sensory properties of milk and milk products. LWT 2022, 154, 112729. [CrossRef] · DOI
  50. Segat, A.; Misra, N.N.; Cullen, P.J.; Innocente, N. Atmospheric pressure cold plasma (ACP) treatment of whey protein isolate model solution. Innov. Food Sci. Emerg. Technol. 2015, 29, 247-254. [CrossRef] · DOI
  51. Wu, X.; Luo, Y.; Zhao, F.; Murad, M.S.; Mu, G. Influence of dielectric barrier discharge cold plasma on physicochemical property of milk for sterilization. Plasma Process. Polym. 2021, 18, 245-256. [CrossRef] · DOI
  52. Singh, P.K.; Huppertz, T. Chapter 8-Effect of Nonthermal Processing on Milk Protein Interactions and Functionality. In Milk Proteins; Boland, M., Singh, H., Eds.; Academic Press: Toronto, ON, Canada, 2020; pp. 293-324.
  53. Ng, S.W.; Lu, P.; Rulikowska, A.; Boehm, D.; O'Neill, G.; Bourke, P. The effect of atmospheric cold plasma treatment on the antigenic properties of bovine milk casein and whey proteins. Food Chem. 2021, 342, 128283. [CrossRef] [PubMed] · DOI
  54. Ramazzina, I.; Tappi, S.; Rocculi, P.; Sacchetti, G.; Berardinelli, A.; Marseglia, A.; Rizzi, F. Effect of Cold Plasma Treatment on the Functional Properties of Fresh-Cut Apples. J. Agric. Food. Chem. 2016, 64, 8010-8018. [CrossRef] [PubMed] · DOI
  55. Zhou, R.; Zhuang, J.; Zong, Z.; Zhang, X.; Liu, D.; Bazaka, K.; Ostrikov, K. Interaction of Atmospheric-Pressure Air Microplasmas with Amino Acids as Fundamental Processes in Aqueous Solution. PLoS ONE 2016, 11, 134-148. [CrossRef] · DOI
  56. Held, S.; Tyl, C.E.; Annor, G.A. Effect of radio frequency cold plasma treatment on intermediate wheatgrass (Thinopyrum intermedium) flour and dough properties in comparison to hard and soft wheat (Triticum aestivum L.). J. Food. Qual. 2019, 34, 156-176. [CrossRef] · DOI
  57. Ji, H.; Dong, S.; Han, F.; Li, Y.; Chen, G.; Li, L.; Chen, Y. Effects of Dielectric Barrier Discharge (DBD) Cold Plasma Treatment on Physicochemical and Functional Properties of Peanut Protein. Food Bioprocess Technol. 2018, 11, 344-354. [CrossRef] · DOI
  58. Zhang, W.; Xiao, S.; Ahn, D.U. Protein oxidation: Basic principles and implications for meat quality. Crit. Rev. Food. Sci. Nutr. 2013, 53, 1191-1201. [CrossRef · DOI

Cited by

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Authors
Bogusławska-Wąs, E., Dłubała, A., Sawicki, W., Ożgo, M., & Lepczyński, A.
Affiliations
  • Department of Applied Microbiology and Human Nutrition Physiology, Faculty of Food Sciences and Fisheries, West Pomeranian University of Technology Szczecin, Papieża Pawła VI 3, 71-459 Szczecin, Poland
  • West Pomeranian University of Technology in Szczecin (PL)
  • Department of Physiology, Cytobiology and Proteomics, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology Szczecin, Klemensa Janickiego 29, 71-270 Szczecin, Poland
ORCID
Venue
Applied Sciences
Publisher
MDPI AG
Published
2023-04-28
Volume
13
Issue
9
Pages
5490
ISSN
2076-3417 (ISSN-L)
DOI
10.3390/app13095490
OpenAlex
W4367314262
Cited by
6
References
1
Citations by year
2026: 2 · 2025: 4
FWCI
0.78
Type
journal article
Language
en
Open access
Licence
Locations
  • Applied Sciences (publishedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Intelligent Development Operational Program (POIR 02.03.02–30–0065-20-00)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Inactivation Methods
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Plasma Applications and Diagnostics
  • Health Sciences › Veterinary › Small Animals › Animal health and immunology
Keywords
non-thermal plasma, bovine colostrum, decontamination, psychrophilic bacteria, mesophilic bacteria, Enterobacteriaceae, Escherichia coli, yeast, protein structure modification, immunoglobulins, β-lactoglobulin, bovine serum albumin, proteomics, color change

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