Pathogen and Spoilage Microorganisms in Meat and Dairy Analogues: Occurrence and Control Strategies
Abstract
:1. Introduction
2. Sources of Microbial Contamination of Meat and Dairy Analogues
3. Microbiology of Meat and Dairy Analogues
3.1. Pathogen Microorganisms
3.2. Spoilage Microorganisms
4. Behaviour of Pathogens and Spoilage Microorganisms in Food Analogues
4.1. pH
4.2. Water Activity
4.3. Temperature
4.4. Preservative
5. Control of Pathogens and Spoilage Microorganisms
5.1. Thermal and Non-Thermal Technologies
5.2. Biocontrol in Meat and Dairy Analogues
5.2.1. Application of LAB and Their Metabolites
- Protective Cultures: LAB have been extensively studied for their antagonistic properties against foodborne pathogens. The incorporation of LAB such as Latilactobacillus sakei, Lacticaseibacillus casei, Lactiplantibacillus plantarum, and Leuconostoc mesenteroides, among others, as protective cultures, all of them with a qualified presumption of safety (QPS) [87], have demonstrated their ability to inhibit pathogenic bacteria such as L. monocytogenes, Salmonella, and E. coli O157:H7 and spoilage microorganisms such as Pseudomonas and Enterobacteriaceae in food products [88], obtaining reductions in L. monocytogenes up to 2.2 log CFU/g in dry cured fermented sausages and up to 5 log CFU/g in ripened cheeses [89,90]. Incorporating LAB into plant-based products can inhibit undesirable microorganisms through competitive exclusion and the production of antimicrobial metabolites. Recent investigations have shown the effectiveness of LAB in extending the shelf life and enhancing the safety of meat analogues [53,91,92,93].
- Bacteriocins: These are ribosomally synthesised antimicrobial peptides produced by LAB that exhibit activity against a range of pathogens, including L. monocytogenes. For instance, bacteriocin-producing strains have been effective in reducing L. monocytogenes in RTE meat and dairy products [94]. Applying similar strategies to plant-based meats could enhance their safety profile. So, incorporating bacteriocins into plant-based meat products could significantly reduce microbial load without adversely affecting sensory attributes.
5.2.2. Bacteriophage Applications
5.2.3. Active Packaging Solutions
6. Conclusions and Future Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Gräfenhahn, M.; Beyrer, M. Plant-Based Meat Analogues in the Human Diet: What Are the Hazards? Foods 2024, 13, 1541. [Google Scholar] [CrossRef] [PubMed]
- Bonaldo, F.; Avot, B.J.P.; De Cesare, A.; Aarestrup, F.M.; Otani, S. Foodborne Pathogen Dynamics in Meat and Meat Analogues Analysed Using Traditional Microbiology and Metagenomic Sequencing. Antibiotics 2024, 13, 16. [Google Scholar] [CrossRef] [PubMed]
- Aschemann-Witzel, J.; Gantriis, R.F.; Fraga, P.; Perez-Cueto, F.J.A. Plant-Based Food and Protein Trend from a Business Perspective: Markets, Consumers, and the Challenges and Opportunities in the Future. Crit. Rev. Food Sci. Nutr. 2021, 61, 3119–3128. [Google Scholar] [CrossRef] [PubMed]
- de Boer, J.; Schösler, H.; Aiking, H. Towards a Reduced Meat Diet: Mindset and Motivation of Young Vegetarians, Low, Medium and High Meat-Eaters. Appetite 2017, 113, 387–397. [Google Scholar] [CrossRef]
- Nevalainen, E.; Niva, M.; Vainio, A. A Transition towards Plant-Based Diets on Its Way? Consumers’ Substitutions of Meat in Their Diets in Finland. Food Qual. Prefer. 2023, 104, 104754. [Google Scholar] [CrossRef]
- Martín-Miguélez, J.M.; Martín, I.; González-Mohíno, A.; Souza Olegario, L.; Peromingo, B.; Delgado, J. Ultra-Processed Plant-Based Analogs: Addressing the Challenging Journey toward Health and Safety. J. Food Sci. 2024, 89, 10344–10362. [Google Scholar] [CrossRef]
- Foddai, A.C.G.; Grant, I.R. Methods for Detection of Viable Foodborne Pathogens: Current State-of-Art and Future Prospects. Appl. Microbiol. Biotechnol. 2020, 104, 4281–4288. [Google Scholar] [CrossRef]
- Abebe, G. Cronobacter Sakazakii in Infant Food Contamination and Its Survival Strategies in Hostile Conditions. Int. J. Pediatr. Res. 2020, 6, e067. [Google Scholar] [CrossRef]
- Tóth, A.J.; Dunay, A.; Battay, M.; Illés, C.B.; Bittsánszky, A.; Süth, M. Microbial Spoilage of Plant-Based Meat Analogues. Appl. Sci. 2021, 11, 8309. [Google Scholar] [CrossRef]
- Hai, D.; Guo, B.; Qiao, M.; Jiang, H.; Song, L.; Meng, Z.; Huang, X. Evaluating the Potential Safety Risk of Plant-Based Meat Analogues by Analyzing Microbial Community Composition. Foods 2024, 13, 117. [Google Scholar] [CrossRef]
- Kyrylenko, A.; Eijlander, R.T.; Alliney, G.; van de Bos, E.L.; Wells-Bennik, M.H.J. Levels and Types of Microbial Contaminants in Different Plant-Based Ingredients Used in Dairy Alternatives. Int. J. Food Microbiol. 2023, 407, 110392. [Google Scholar] [CrossRef] [PubMed]
- Cottenet, G.; Blancpain, C. A Real-Time PCR Method to Assess the Presence of Vertebrate Material in Plant-Based Products. Food Control 2021, 125, 108001. [Google Scholar] [CrossRef]
- Cheng, C.-Y.; Shi, Y.-C.; Lin, S.-R.; Chou, C.-C.; Huang, C.-C. Use of Real-Time PCR to Detect Surimi Adulteration in Vegetarian Foods. J. Mar. Sci. Technol. 2012, 20, 570–574. [Google Scholar]
- Leclercq, A.; Tourdjman, M.; Mattheus, W.; Friesema, I.; Van Sorge, N.M.; Halbedel, S.; Wilking, H.; Lecuit, M. Outbreak of Listeriosis Associated with Consumption of Vegan Cheese. N. Engl. J. Med. 2024, 390, 1439–1440. [Google Scholar] [CrossRef]
- Louvau, H.S.; Wang, H.; Shaposhnikov, M.M.; Harris, L.J. Behavior of Salmonella during Preparation of a Fermented Cashew Cheese Analog. J. Food Prot. 2024, 87, 100311. [Google Scholar] [CrossRef]
- Schmitt, N.; Yu, G.; Greve, R.; McIntyre, L. Outbreak of S. Weltevreden Linked to Fermented Cashew Nut Cheese in Victoria, BC. Environ. Health Rev. 2018, 61, 74–81. [Google Scholar] [CrossRef]
- Kyriakopoulou, K.; Dekkers, B.; van der Goot, A.J. Plant-Based Meat Analogues. In Sustainable Meat Production and Processing; Academic Press: Cambridge, MA, USA, 2019; pp. 103–126. [Google Scholar] [CrossRef]
- Sleator, R.D.; Hill, C. Food Reformulations for Improved Health: A Potential Risk for Microbial Food Safety? Med. Hypotheses 2007, 69, 1323–1324. [Google Scholar] [CrossRef]
- Lima, J.R.; Mellinger, C.G. Pulses-Derived Proteins for the Plant-Based Market: Opportunities to Reduce Postharvest Loss and Waste. Curr. Opin. Biotechnol. 2022, 78, 102820. [Google Scholar] [CrossRef]
- Canadian Food Inspection Agency Bacterial Pathogens in Seed Powder and Plant-Based Protein Powder—1 April 2016 to 31 March 2018. Available online: https://inspection.canada.ca/en/food-safety-industry/food-chemistry-and-microbiology/food-safety-testing-reports-and-journal-articles/bacterial-pathogens-seed-powder-and-plant-based (accessed on 2 May 2025).
- Gruzdev, N.; Pinto, R.; Sela (Saldinger), S. Persistence of Salmonella enterica during Dehydration and Subsequent Cold Storage. Food Microbiol. 2012, 32, 415–422. [Google Scholar] [CrossRef]
- Fay, M.L.; Salazar, J.K.; Ren, Y.; Wu, Z.; Mate, M.; Khouja, B.A.; Lingareddygari, P.; Liggans, G. Growth Kinetics of Listeria monocytogenes and Salmonella enterica on Dehydrated Vegetables during Rehydration and Subsequent Storage. Foods 2023, 12, 2561. [Google Scholar] [CrossRef]
- European Commission High Quality Meat-like Products—From Niche Markets to Widely Accepted Meat Alternatives|LIKEMEAT|Project|Fact Sheet|FP7|CORDIS|European Commission. Available online: https://cordis.europa.eu/project/id/262560 (accessed on 27 March 2025).
- Wells-Bennik, M.H.J.; Eijlander, R.T.; Den Besten, H.M.W.; Berendsen, E.M.; Warda, A.K.; Krawczyk, A.O.; Nierop Groot, M.N.; Xiao, Y.; Zwietering, M.H.; Kuipers, O.P.; et al. Bacterial Spores in Food: Survival, Emergence, and Outgrowth. Annu. Rev. Food Sci. Technol. 2016, 7, 457–482. [Google Scholar] [CrossRef] [PubMed]
- Khan, N.; Martínez-Hidalgo, P.; Ice, T.A.; Maymon, M.; Humm, E.A.; Nejat, N.; Sanders, E.R.; Kaplan, D.; Hirsch, A.M. Antifungal Activity of Bacillus Species against Fusarium and Analysis of the Potential Mechanisms Used in Biocontrol. Front. Microbiol. 2018, 9, 401553. [Google Scholar] [CrossRef]
- Saxena, A.K.; Kumar, M.; Chakdar, H.; Anuroopa, N.; Bagyaraj, D.J. Bacillus Species in Soil as a Natural Resource for Plant Health and Nutrition. J. Appl. Microbiol. 2020, 128, 1583–1594. [Google Scholar] [CrossRef]
- Tirloni, E.; Stella, S.; Celandroni, F.; Mazzantini, D.; Bernardi, C.; Ghelardi, E. Bacillus Cereus in Dairy Products and Production Plants. Foods 2022, 11, 2572. [Google Scholar] [CrossRef]
- Hadi, J.; Brightwell, G. Safety of Alternative Proteins: Technological, Environmental and Regulatory Aspects of Cultured Meat, Plant-Based Meat, Insect Protein and Single-Cell Protein. Foods 2021, 10, 1226. [Google Scholar] [CrossRef]
- Liu, Z.; Shaposhnikov, M.; Zhuang, S.; Tu, T.; Wang, H.; Wang, L. Growth and Survival of Common Spoilage and Pathogenic Bacteria in Ground Beef and Plant-Based Meat Analogues. Food Res. Int. 2023, 164, 112408. [Google Scholar] [CrossRef]
- Luchansky, J.B.; Shoyer, B.A.; Jung, Y.; Shane, L.E.; Osoria, M.; Porto-Fett, A.C.S. Viability of Shiga Toxin–Producing Escherichia Coli, Salmonella, and Listeria monocytogenes within Plant versus Beef Burgers during Cold Storage and Following Pan Frying. J. Food Prot. 2020, 83, 434–442. [Google Scholar] [CrossRef]
- Kabisch, J.; Joswig, G.; Böhnlein, C.; Fiedler, G.; Franz, C.M.A.P. Microbiological Status of Vegan Ground Meat Products from German Retail. J. Fur Verbraucherschutz Lebensmittelsicherheit 2024, 19, 33–40. [Google Scholar] [CrossRef]
- Geeraerts, W.; De Vuyst, L.; Leroy, F. Ready-to-Eat Meat Alternatives, a Study of Their Associated Bacterial Communities. Food Biosci. 2020, 37, 100681. [Google Scholar] [CrossRef]
- Mazaheri, T.; Cervantes-Huamán, B.R.H.; Bermúdez-Capdevila, M.; Ripolles-Avila, C.; Rodríguez-Jerez, J.J. Listeria monocytogenes Biofilms in the Food Industry: Is the Current Hygiene Program Sufficient to Combat the Persistence of the Pathogen? Microorganisms 2021, 9, 181. [Google Scholar] [CrossRef]
- Rani, Z.T.; Mhlongo, L.C.; Hugo, A. Microbial Profiles of Meat at Different Stages of the Distribution Chain from the Abattoir to Retail Outlets. Int. J. Environ. Res. Public. Health 2023, 20, 1986. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Díaz, J.M.; Calahorrano-Moreno, M.B.; Ordoñez-Bailon, J.J.; Baquerizo-Crespo, R.J.; Dueñas-Rivadeneira, A.A.; Maria, M.C. Contaminants in the Cow’s Milk We Consume? Pasteurization and Other Technologies in the Elimination of Contaminants. F1000Res 2022, 11, 91. [Google Scholar] [CrossRef]
- Mladenović, K.G.; Grujović, M.; Kiš, M.; Furmeg, S.; Tkalec, V.J.; Stefanović, O.D.; Kocić-Tanackov, S.D. Enterobacteriaceae in Food Safety with an Emphasis on Raw Milk and Meat. Appl. Microbiol. Biotechnol. 2021, 105, 8615–8627. [Google Scholar] [CrossRef]
- Nielsen, B.; Colle, M.J.; Ünlü, G. Meat Safety and Quality: A Biological Approach. Int. J. Food Sci. Technol. 2020, 56, 39–51. [Google Scholar] [CrossRef]
- Lyu, F.; Zhang, T.; Gui, M.; Wang, Y.; Zhao, L.; Wu, X.; Rao, L.; Liao, X. The Underlying Mechanism of Bacterial Spore Germination: An Update Review. Compr. Rev. Food Sci. Food Saf. 2023, 22, 2728–2746. [Google Scholar] [CrossRef]
- Li, X.; Wang, H.; Guo, C.; Wang, L. Profiling of Microbial Populations Present in Ground Beef and Plant-Based Meat Analogues. LWT 2024, 196, 115845. [Google Scholar] [CrossRef]
- Ismail, I.; Hwang, Y.H.; Joo, S.T. Meat Analog as Future Food: A Review. J. Anim. Sci. Technol. 2020, 62, 111. [Google Scholar] [CrossRef]
- Webb, D.; Dogan, H.; Li, Y.; Alavi, S. Physico-Chemical Properties and Texturization of Pea, Wheat and Soy Proteins Using Extrusion and Their Application in Plant-Based Meat. Foods 2023, 12, 1586. [Google Scholar] [CrossRef]
- Dušková, M.; Dorotíková, K.; Bartáková, K.; Králová, M.; Šedo, O.; Kameník, J. The Microbial Contaminants of Plant-Based Meat Analogues from the Retail Market. Int. J. Food Microbiol. 2024, 425, 110869. [Google Scholar] [CrossRef]
- Yadav, D.; Bansal, S.; Jaiswal, A.; Singh, R. Plant Based Dairy Analogues: An Emerging Food. Agric. Res. Technol. 2017, 10, 1–4. [Google Scholar] [CrossRef]
- Campbell, J.; Marshall, R. Dairy Production and Processing: The Science of Milk and Milk Products; Waveland Press, Inc.: Long Grove, IL, USA, 2016; ISBN 1-4786-1120-0. [Google Scholar]
- De Angelis, D.; van der Goot, A.J.; Pasqualone, A.; Summo, C. Advancements in Texturization Processes for the Development of Plant-Based Meat Analogs: A Review. Curr. Opin. Food Sci. 2024, 58, 101192. [Google Scholar] [CrossRef]
- Mehany, T.; Siddiqui, S.A.; Olawoye, B.; Olabisi Popoola, O.; Hassoun, A.; Manzoor, M.F.; Punia Bangar, S. Recent Innovations and Emerging Technological Advances Used to Improve Quality and Process of Plant-Based Milk Analogs. Crit. Rev. Food Sci. Nutr. 2024, 64, 7237–7267. [Google Scholar] [CrossRef]
- Lomas, M.N.; Paradell, N.G.; Garralda, V.C.; Sanz, L.A.; Calderón, J.; Sabaté, S. Plant-Based Meat Analogues Marketed in Catalonia: Analysis of Contaminants, Essential Elements, Microbiological and Physicochemical Status, Dietary Intake Estimation and Health Risk Assessment. Food Risk Assess. Eur. 2024, 2, 0040E. [Google Scholar] [CrossRef]
- Roch, F.F.; Dzieciol, M.; Quijada, N.M.; Alteio, L.V.; Mester, P.J.; Selberherr, E. Microbial Community Structure of Plant-Based Meat Alternatives. NPJ Sci. Food 2024, 8, 1–15. [Google Scholar] [CrossRef]
- Jaeger, I.; Köhn, C.R.; Evans, J.D.; Frazzon, J.; Renault, P.; Kothe, C.I. Nutritional and Microbial Profiles of Ripened Plant-Based Cheese Analogs Collected from the European Market. Food Res. Int. 2024, 191, 114724. [Google Scholar] [CrossRef]
- de Souza, E.L.; de Oliveira, K.Á.; de Oliveira, M.E. Influence of Lactic Acid Bacteria Metabolites on Physical and Chemical Food Properties. Curr. Opin. Food Sci. 2023, 49, 100981. [Google Scholar] [CrossRef]
- Harper, A.R.; Dobson, R.C.J.; Morris, V.K.; Moggré, G.J. Fermentation of Plant-Based Dairy Alternatives by Lactic Acid Bacteria. Microb. Biotechnol. 2022, 15, 1404–1421. [Google Scholar] [CrossRef]
- Ou, M.; Lou, J.; Lao, L.; Guo, Y.; Pan, D.; Yang, H.; Wu, Z. Plant-Based Meat Analogue of Soy Proteins by the Multi-Strain Solid-State Mixing Fermentation. Food Chem. 2023, 414, 135671. [Google Scholar] [CrossRef]
- Elhalis, H.; See, X.Y.; Osen, R.; Chin, X.H.; Chow, Y. Significance of Fermentation in Plant-Based Meat Analogs: A Critical Review of Nutrition, and Safety-Related Aspects. Foods 2023, 12, 3222. [Google Scholar] [CrossRef]
- Zapaśnik, A.; Sokołowska, B.; Bryła, M. Role of Lactic Acid Bacteria in Food Preservation and Safety. Foods 2022, 11, 1283. [Google Scholar] [CrossRef]
- Yang, X.; Hong, J.; Wang, L.; Cai, C.; Mo, H.; Wang, J.; Fang, X.; Liao, Z. Effect of Lactic Acid Bacteria Fermentation on Plant-Based Products. Fermentation 2024, 10, 48. [Google Scholar] [CrossRef]
- Ballester, E.; Ribes, S.; Barat, J.M.; Fuentes, A. Spoilage Yeasts in Fermented Vegetables: Conventional and Novel Control Strategies. Eur. Food Res. Technol. 2022, 248, 315–328. [Google Scholar] [CrossRef]
- Riesute, R.; Salomskiene, J.; Moreno, D.S.; Gustiene, S. Effect of Yeasts on Food Quality and Safety and Possibilities of Their Inhibition. Trends Food Sci. Technol. 2021, 108, 1–10. [Google Scholar] [CrossRef]
- Bartula, K.; Begley, M.; Latour, N.; Callanan, M. Growth of Food-Borne Pathogens Listeria and Salmonella and Spore-Forming Paenibacillus and Bacillus in Commercial Plant-Based Milk Alternatives. Food Microbiol. 2023, 109, 104143. [Google Scholar] [CrossRef]
- Bartula, K.; Biagui, S.; Begley, M.; Callanan, M. Investigation of the Growth of Listeria in Plant-Based Beverages. Food Microbiol. 2024, 121, 104530. [Google Scholar] [CrossRef]
- Präger, L.; Christoph Simon, J.; Treudler, R.; med Lea-Isabell Präger, C. Food Allergy—New Risks through Vegan Diet? Overview of New Allergen Sources and Current Data on the Potential Risk of Anaphylaxis. JDDG J. Der Dtsch. Dermatol. Gesellschaft 2023, 21, 1308–1313. [Google Scholar] [CrossRef]
- Abu Risha, M.; Rick, E.M.; Plum, M.; Jappe, U. Legume Allergens Pea, Chickpea, Lentil, Lupine and Beyond. Curr. Allergy Asthma Rep. 2024, 24, 527–548. [Google Scholar] [CrossRef]
- Martín, I.; Córdoba, J.J.; Rodríguez, A. Effect of Acidic Conditions on the Growth and Expression of Two Virulence Genes of Listeria monocytogenes Serotype 4b. Res. Microbiol. 2023, 174, 104042. [Google Scholar] [CrossRef]
- Thierry, A.; Valence, F.; Deutsch, S.M.; Even, S.; Falentin, H.; Le Loir, Y.; Jan, G.; Gagnaire, V. Strain-to-Strain Differences within Lactic and Propionic Acid Bacteria Species Strongly Impact the Properties of Cheese—A Review. Dairy. Sci. Technol. 2015, 95, 895–918. [Google Scholar] [CrossRef]
- Marlapati, L.; Basha, R.F.S.; Navarre, A.; Kinchla, A.J.; Nolden, A.A. Comparison of Physical and Compositional Attributes between Commercial Plant-Based and Dairy Yogurts. Foods 2024, 13, 984. [Google Scholar] [CrossRef]
- Grasso, N.; Roos, Y.H.; Crowley, S.V.; Arendt, E.K.; O’Mahony, J.A. Composition and Physicochemical Properties of Commercial Plant-Based Block-Style Products as Alternatives to Cheese. Future Foods 2021, 4, 100048. [Google Scholar] [CrossRef]
- Harvey, H.J.; Hendry, A.C.; Archer, D.B.; Avery, S.V. Evaluating the Potential of Natural Product Combinations with Sorbic Acid for Improving Preservative Action against Food-Spoilage Yeasts. Fungal Biol. 2023, 127, 1218–1223. [Google Scholar] [CrossRef]
- Seo, Y.; Sung, M.; Hwang, J.; Yoon, Y. Minimum Inhibitory Concentration (MIC) of Propionic Acid, Sorbic Acid, and Benzoic Acid against Food Spoilage Microorganisms in Animal Products to Use MIC as Threshold for Natural Preservative Production. Food Sci. Anim. Resour. 2023, 43, 319–330. [Google Scholar] [CrossRef]
- Szűcs, V.; Szabó, E.; Guerrero, L.; Tarcea, M.; Bánáti, D. Modelling of Avoidance of Food Additives: A Cross Country Study. Int. J. Food Sci. Nutr. 2019, 70, 1020–1032. [Google Scholar] [CrossRef]
- Zhong, Y.; Wu, L.; Chen, X.; Huang, Z.; Hu, W. Effects of Food-Additive-Information on Consumers’ Willingness to Accept Food with Additives. Int. J. Environ. Res. Public. Health 2018, 15, 2394. [Google Scholar] [CrossRef]
- Pereira, R.N.; Vicente, A.A. Environmental Impact of Novel Thermal and Non-Thermal Technologies in Food Processing. Food Res. Int. 2010, 43, 1936–1943. [Google Scholar] [CrossRef]
- Zaaboul, F.; Raza, H.; Cao, C.; Yuanfa, L. The Impact of Roasting, High Pressure Homogenization and Sterilization on Peanut Milk and Its Oil Bodies. Food Chem. 2019, 280, 270–277. [Google Scholar] [CrossRef]
- Andressa, I.; Kelly Silva do Nascimento, G.; Monteiro dos Santos, T.; da Silva Rodrigues, R.; de Oliveira Teotônio, D.; Paucar-Menacho, L.M.; Machado Benassi, V.; Schmiele, M. Technological and Health Properties and Main Challenges in the Production of Vegetable Beverages and Dairy Analogs. Food Funct. 2024, 15, 460–480. [Google Scholar] [CrossRef]
- Leong, S.Y.; Oey, I. Application of Novel Thermal Technology in Foods Processing. Foods 2022, 11, 125. [Google Scholar] [CrossRef]
- Toro-Funes, N.; Bosch-Fusté, J.; Latorre-Moratalla, M.L.; Veciana-Nogués, M.T.; Vidal-Carou, M.C. Isoflavone Profile and Protein Quality during Storage of Sterilised Soymilk Treated by Ultra High Pressure Homogenisation. Food Chem. 2015, 167, 78–83. [Google Scholar] [CrossRef]
- Xia, Q.; Liu, Q.; Denoya, G.I.; Yang, C.; Barba, F.J.; Yu, H.; Chen, X. High Hydrostatic Pressure-Based Combination Strategies for Microbial Inactivation of Food Products: The Cases of Emerging Combination Patterns. Front. Nutr. 2022, 9, 878904. [Google Scholar] [CrossRef]
- Li, Y.Q.; Tian, W.L.; Mo, H.Z.; Zhang, Y.L.; Zhao, X.Z. Effects of Pulsed Electric Field Processing on Quality Characteristics and Microbial Inactivation of Soymilk. Food Bioproc Tech. 2013, 6, 1907–1916. [Google Scholar] [CrossRef]
- Iorio, M.C.; Bevilacqua, A.; Corbo, M.R.; Campaniello, D.; Sinigaglia, M.; Altieri, C. A Case Study on the Use of Ultrasound for the Inhibition of Escherichia coli O157:H7 and Listeria monocytogenes in Almond Milk. Ultrason. Sonochem. 2019, 52, 477–483. [Google Scholar] [CrossRef]
- Lucas, J.R.; Cárcel, J.A.; Velasco, R.; Benedito, J.; Cabeza, M.C. Modelling of the Electron Range for Use of E-Beam Treatment for Boned Dry-Cured Hams Sanitation. Innov. Food Sci. Emerg. Technol. 2023, 84, 103296. [Google Scholar] [CrossRef]
- Lung, H.M.; Cheng, Y.C.; Chang, Y.H.; Huang, H.W.; Yang, B.B.; Wang, C.Y. Microbial Decontamination of Food by Electron Beam Irradiation. Trends Food Sci. Technol. 2015, 44, 66–78. [Google Scholar] [CrossRef]
- Singh, H.; Bhardwaj, S.K.; Khatri, M.; Kim, K.H.; Bhardwaj, N. UVC Radiation for Food Safety: An Emerging Technology for the Microbial Disinfection of Food Products. Chem. Eng. J. 2021, 417, 128084. [Google Scholar] [CrossRef]
- Yemmireddy, V.; Adhikari, A.; Moreira, J. Effect of Ultraviolet Light Treatment on Microbiological Safety and Quality of Fresh Produce: An Overview. Front. Nutr. 2022, 9, 871243. [Google Scholar] [CrossRef]
- Tamang, J.P.; Watanabe, K.; Holzapfel, W.H. Review: Diversity of Microorganisms in Global Fermented Foods and Beverages. Front. Microbiol. 2016, 7, 377. [Google Scholar] [CrossRef]
- Lin, X.; Duan, N.; Wu, J.; Lv, Z.; Wang, Z.; Wu, S. Potential Food Safety Risk Factors in Plant-Based Foods: Source, Occurrence, and Detection Methods. Trends Food Sci. Technol. 2023, 138, 511–522. [Google Scholar] [CrossRef]
- Chauhan, K.; Rao, A. Clean-Label Alternatives for Food Preservation: An Emerging Trend. Heliyon 2024, 10, e35815. [Google Scholar] [CrossRef]
- Udayakumar, S.; Rasika, D.M.D.; Priyashantha, H.; Vidanarachchi, J.K.; Ranadheera, C.S. Probiotics and Beneficial Microorganisms in Biopreservation of Plant-Based Foods and Beverages. Appl. Sci. 2022, 12, 11737. [Google Scholar] [CrossRef]
- Bohrer, B.M. An Investigation of the Formulation and Nutritional Composition of Modern Meat Analogue Products. Food Sci. Hum. Wellness 2019, 8, 320–329. [Google Scholar] [CrossRef]
- Allende, A.; Alvarez-Ordóñez, A.; Bortolaia, V.; Bover-Cid, S.; De Cesare, A.; Dohmen, W.; Guillier, L.; Jacxsens, L.; Nauta, M.; Mughini-Gras, L.; et al. Update of the List of Qualified Presumption of Safety (QPS) Recommended Microbiological Agents Intentionally Added to Food or Feed as Notified to EFSA 21: Suitability of Taxonomic Units Notified to EFSA until September 2024. EFSA J. 2025, 23, e9169. [Google Scholar] [CrossRef]
- Barcenilla, C.; Ducic, M.; López, M.; Prieto, M.; Álvarez-Ordóñez, A. Application of Lactic Acid Bacteria for the Biopreservation of Meat Products: A Systematic Review. Meat Sci. 2022, 183, 108661. [Google Scholar] [CrossRef]
- Martín, I.; Rodríguez, A.; Sánchez-Montero, L.; Padilla, P.; Córdoba, J.J. Effect of the Dry-Cured Fermented Sausage “Salchichón” Processing with a Selected Lactobacillus sakei in Listeria monocytogenes and Microbial Population. Foods 2021, 10, 856. [Google Scholar] [CrossRef]
- Martín, I.; Rodríguez, A.; Córdoba, J.J. Application of Selected Lactic-Acid Bacteria to Control Listeria monocytogenes in Soft-Ripened “Torta Del Casar” Cheese. LWT 2022, 168, 113873. [Google Scholar] [CrossRef]
- Gungor, G.; Akpinar, A.; Yerlikaya, O. Production of Plant-Based Fermented Beverages Using Probiotic Starter Cultures and Propionibacterium spp. Food Biosci. 2024, 59, 103840. [Google Scholar] [CrossRef]
- Erem, E.; Kilic-Akyilmaz, M. The Role of Fermentation with Lactic Acid Bacteria in Quality and Health Effects of Plant-based Dairy Analogues. Compr. Rev. Food Sci. Food Saf. 2024, 23, e13402. [Google Scholar] [CrossRef]
- Martín-Miguélez, J.M.; Castaño, C.; Delgado, J.; Olegario, L.S.; González-Mohino, A. Protective Effect of Lactic Acid Bacteria Isolated from Ripened Foods Against Listeria monocytogenes in Plant-Based Fermented Dry-Cured Sausages. Foods 2025, 14, 1491. [Google Scholar] [CrossRef]
- Martín, I.; Rodríguez, A.; Delgado, J.; Córdoba, J.J. Strategies for Biocontrol of Listeria monocytogenes Using Lactic Acid Bacteria and Their Metabolites in Ready-to-Eat Meat- and Dairy-Ripened Products. Foods 2022, 11, 542. [Google Scholar] [CrossRef]
- Imran, A.; Shehzadi, U.; Islam, F.; Afzaal, M.; Ali, R.; Ali, Y.A.; Chauhan, A.; Biswas, S.; Khurshid, S.; Usman, I.; et al. Bacteriophages and Food Safety: An Updated Overview. Food Sci. Nutr. 2023, 11, 3621–3630. [Google Scholar] [CrossRef]
- Endersen, L.; O’Mahony, J.; Hill, C.; Ross, R.P.; McAuliffe, O.; Coffey, A. Phage Therapy in the Food Industry. Annu. Rev. Food Sci. Technol. 2014, 5, 327–349. [Google Scholar] [CrossRef]
- Barache, N.; Belguesmia, Y.; Martinez, B.; Seal, B.S.; Drider, D. Bacteriocins and Bacteriophages as Dual Biological Players for Food Safety Applications. Encyclopedia 2024, 4, 79–90. [Google Scholar] [CrossRef]
- García, P.; Rodríguez, L.; Rodríguez, A.; Martínez, B. Food Biopreservation: Promising Strategies Using Bacteriocins, Bacteriophages and Endolysins. Trends Food Sci. Technol. 2010, 21, 373–382. [Google Scholar] [CrossRef]
- Rodríguez-Marca, C.; Domenech-Coca, C.; Nakamura, M.; Ortega-Olivé, N.; Puigbò, P. Use of Live Biopreservatives and Bacteriophages to Enhance the Safety of Meat Products. Life 2025, 15, 197. [Google Scholar] [CrossRef]
- Realini, C.E.; Marcos, B. Active and Intelligent Packaging Systems for a Modern Society. Meat Sci. 2014, 98, 404–419. [Google Scholar] [CrossRef]
- Ribeiro-Santos, R.; Andrade, M.; de Melo, N.R.; Sanches-Silva, A. Use of Essential Oils in Active Food Packaging: Recent Advances and Future Trends. Trends Food Sci. Technol. 2017, 61, 132–140. [Google Scholar] [CrossRef]
- Dutta, P.K.; Tripathi, S.; Mehrotra, G.K.; Dutta, J. Perspectives for Chitosan Based Antimicrobial Films in Food Applications. Food Chem. 2009, 114, 1173–1182. [Google Scholar] [CrossRef]
- Emamifar, A.; Kadivar, M.; Shahedi, M.; Soleimanian-Zad, S. Evaluation of Nanocomposite Packaging Containing Ag and ZnO on Shelf Life of Fresh Orange Juice. Innov. Food Sci. Emerg. Technol. 2010, 11, 742–748. [Google Scholar] [CrossRef]
- Singh, T.; Shukla, S.; Kumar, P.; Wahla, V.; Bajpai, V.K.; Rather, I.A. Application of Nanotechnology in Food Science: Perception and Overview. Front. Microbiol. 2017, 8, 1501. [Google Scholar] [CrossRef]
- Mousavi Khaneghah, A.; Hashemi, S.M.B.; Limbo, S. Antimicrobial Agents and Packaging Systems in Antimicrobial Active Food Packaging: An Overview of Approaches and Interactions. Food Bioprod. Process. 2018, 111, 1–19. [Google Scholar] [CrossRef]
- Sharma, S.; Barkauskaite, S.; Jaiswal, A.K.; Jaiswal, S. Essential Oils as Additives in Active Food Packaging. Food Chem. 2021, 343, 128403. [Google Scholar] [CrossRef]
- Perdones, Á.; Vargas, M.; Atarés, L.; Chiralt, A. Physical, Antioxidant and Antimicrobial Properties of Chitosan-Cinnamon Leaf Oil Films as Affected by Oleic Acid. Food Hydrocoll. 2014, 36, 256–264. [Google Scholar] [CrossRef]
Plant-Based Meat Analogue | Protein Source | Pathogenic Bacteria | Source |
---|---|---|---|
Ground meat | Soy, pea | Escherichia coli O157:H7 Salmonella spp. Listeria monocytogenes | [29] |
Burger, steak, meatball | Soy, pea, wheat | Bacillus cereus | [42] |
Ground meat | Soy, pea | Escherichia coli HEHA16 Listeria monocytogenes Salmonella enterica ser. Typhi Cronobacter sakazakii | [2] |
Fermented sausage, sausage, meatball | Pulses | Salmonella spp. Listeria monocytogenes | [47] |
Plant-Based Analogue | Protein Source | Spoilage Microorganisms | Source |
---|---|---|---|
Ground meat | Soy, pea | Pseudomonas fluorescens Brochothrix thermosphacta | [29] |
Burger, steak, meatball | Soy, pea, wheat | Lactic acid bacteria Enterobacteriaceae Yeasts | [42] |
Burger, steak, sausages | Soy, pea | Lactic acid bacteria | [48] |
Sausage | Soy | Lactic acid bacteria Thermoactinomyces spp. | [10] |
Ground meat | Soy, pea | Brochothrix spp. Lactic acid bacteria | [39] |
Soft ripened cheese | Cashew nut | Pediococcus pentosaceus Enterococcus spp. | [49] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Martín-Miguélez, J.M.; Martín, I.; Peromingo, B.; Delgado, J.; Córdoba, J.J. Pathogen and Spoilage Microorganisms in Meat and Dairy Analogues: Occurrence and Control Strategies. Foods 2025, 14, 1819. https://doi.org/10.3390/foods14101819
Martín-Miguélez JM, Martín I, Peromingo B, Delgado J, Córdoba JJ. Pathogen and Spoilage Microorganisms in Meat and Dairy Analogues: Occurrence and Control Strategies. Foods. 2025; 14(10):1819. https://doi.org/10.3390/foods14101819
Chicago/Turabian StyleMartín-Miguélez, José M., Irene Martín, Belén Peromingo, Josué Delgado, and Juan J. Córdoba. 2025. "Pathogen and Spoilage Microorganisms in Meat and Dairy Analogues: Occurrence and Control Strategies" Foods 14, no. 10: 1819. https://doi.org/10.3390/foods14101819
APA StyleMartín-Miguélez, J. M., Martín, I., Peromingo, B., Delgado, J., & Córdoba, J. J. (2025). Pathogen and Spoilage Microorganisms in Meat and Dairy Analogues: Occurrence and Control Strategies. Foods, 14(10), 1819. https://doi.org/10.3390/foods14101819