Abstract
Microbiological contamination changes the qualitative and quantitative profile of food, which makes it an important issue of food safety systems. Finished products with components of animal origin or combined vegetable and livestock raw materials are especially prone to microbiological contamination. This review features the most common sources of microbiological contamination and its prevention in finished products.The review covered 20 years of English and Russian scientific articles and standards indexed in Scopus, ScienceDirect, PubMed, and eLIBRARY.RU. The descriptors included microbiological contamination, food raw materials, and ready-to-eat products. The analysis involved some older publications, provided they possessed a high scientific relevance and/or a high citation index. The search criteria concentrated on the detection of microbiological contaminants in food raw materials and food products in Russia and abroad. The percentage of detections for individual groups of microorganisms was calculated as opposed to their total number.
The data obtained can be summarized as follows. Regular industrial monitoring can minimize the risk of microbiological contamination. Complex finished products have a higher risk and require heat treatment. Composite products that cannot be succumbed to additional heat treatment need new technologies that minimize microbiological contamination, e.g., intensive cooling, shock freezing, electromagnetic processing, protective food coatings, etc.
Even a small amount of animal raw materials may cause extra risk of contamination with Listeria monocytogenes, Salmonella enteritidis, etc. A mix of different raw materials changes the microbiological profile of the finished product. As a result, finished products have to be monitored throughout the entire shelf-life cycle, regardless of the percentage of animal raw material in the formulation.
Keywords
Food safety, food products, raw materials of animal origin, mixed products, semi-finished products, risk of contamination, microbiological contaminationFUNDING
The research was performed on the premises of the Russian State Center for Animal Feed and Drug Standardization and Quality (FGBU “VGNKI”).REFERENCES
- Shur PZ, Zaitseva NV. Health risk assessment when giving grounds for hygienic criteria of food products safety. Health Risk Analysis. 2018;(4):43–56. (In Russ.). https://doi.org/10.21668/health.risk/2018.4.05
- Shepelin AP, Dyatlov IA, Polosenko OV. Microbiological control of food products quality. Bacteriology. 2017;2(2):39–47. (In Russ.). https://elibrary.ru/OSZQBZ
- Beczkiewicz ATE, Kowalcyk BB. Risk factors for Salmonella contamination of whole chicken carcasses following changes in U.S. regulatory oversight. Journal of Food Protection. 2021;84(10):1713–1721. https://doi.org/10.4315/JFP-21-144
- Mbarga MJA, Desobgo SCZ, Tatsadjieu LN, Kavhiza N, Kalisa L. Antagonistic effects of raffia sap with probiotics against pathogenic microorganisms. Foods and Raw Materials. 2021;9(1):24–31. https://doi.org/10.21603/2308-4057-2021-1-24-31
- Kostenko YuG. Guidelines on microbiological sanitary and risk prevention in the production and storage of meat products. Moscow: TEKHNOSFERA; 2015. 640 p. (In Russ.).
- Fedorenko EV, Kolomiets ND, Sychik SI. Actual problems of the microbiological safety of food products. Hygiene and Sanitation. 2016;95(9):873–878. (In Russ.). https://doi.org/10.18821/0016-9900-2016-95-9-873-878
- Tulyakova TV, Kryukova EV, Paramonov GV. Problems of biological food safety. Bulletin of the Medical Institute of Continuing Education. 2022;(2):50–52. (In Russ.). https://doi.org/10.46393/27821714_2022_2_50
- Malley TJV, Butts J, Wiedmann M. Seek and destroy process: Listeria monocytogenes process controls in the ready-to-eat meat and poultry industry. Journal of Food Protection. 2015;78(2):436–445. https://doi.org/10.4315/0362-028X.JFP-13-507
- Salmonella outbreak in Sweden linked to chocolate wafers [Internet]. [cited 2023 Jan 09]. Available from: https://www.foodsafetynews.com/2021/04/salmonella-outbreak-in-sweden-linked-to-chocolate-wafers
- Fifty infected with Escherichia coli in France after eating pizza [Internet]. [cited 2023 Jan 09]. Available from: https://vetandlife.ru/sobytiya/chislo-zarazhenij-kishechnoj-palochkoj-vo-francii-posle-upotrebleniya-piccy-vyroslo-do-50
- Salmonella found in Kinder products in France [Internet]. [cited 2023 Jan 09]. Available from: https://vetandlife.ru/sobytiya/salmonellu-obnaruzhili-v-produkcii-kinder-vo-francii
- Gosmanov RG. Microbiology. St. Petersburg: Lanʹ; 2017. 496 p. (In Russ.).
- Tsukanov MF, Chernomorets AB. Technological aspects of the water activity indicator and its role in the quality of public catering products. Technico-tehnologicheskie Problemy Servisa. 2010;11(1):58–63. (In Russ.). https://elibrary.ru/MNJDPH
- Abdullaeva AM, Blinkova LP, Usha BV, Valitova RK, Hokkanen MA. Microbiological monitoring of contamination of poultry products. Russian Journal Problems of Veterinary Sanitation, Hygiene and Ecology. 2020;35(3):291–303. (In Russ.). https://doi.org/10.36871/vet.san.hyg.ecol.202003003
- Abdullaeva AM. Assessment of the level of contamination in a retrospective analysis of poultry meat and poultry products. Izvestia Orenburg State Agrarian University. 2020;86(6):232–236. (In Russ.). https://doi.org/10.37670/2073-0853-2020-86-6-232-236
- Bogomolova ES, Dʹyakova AO, Maksimenko EO, Olyushina EA. Microbiological and parasitological safety of food products: Retrospective analysis. Relevant Issues of Public Health Management: Proceedings of the V All-Russian Scientific and Practical Conference, Issue XV; 2022; Nizhny Novgorod. Nizhny Novgorod: Privolzhsky Research Medical University; 2022. p. 144–149. (In Russ.). https://elibrary.ru/TEOWEE
- Yang S, Pei X, Yang D, Zhang H, Chen Q, Chui H, et al. Microbial contamination in bulk ready-to-eat meat products of China in 2016. Food Control. 2018;91:113–122. https://doi.org/10.1016/j.foodcont.2018.03.027
- Vesta [Internet]. [cited 2023 Jan 10]. Available from: https://www.vetrf.ru/vetrf/vesta.html
- RASFF Window [Internet]. [cited 2023 Jan 10]. Available from: https://webgate.ec.europa.eu/rasff-window/screen/search?event=SearchForm&cleanSearch=1
- Import of composite products to the EU. Questions and answers [Internet]. [cited 2023 Jan 10]. Available from: https://fsvps.gov.ru/fsvps-docs/ru/importExport/eu/files/FAQ-Composite-products.pdf
- Söderqvist K, Thisted-Lambertz S, Vågsholm I, Boqvist S. Foodborne bacterial pathogens in retail prepacked ready-to-eat mixed ingredient salads. Journal of Food Protection. 2016;79(6):978–985. https://doi.org/10.4315/0362-028X.JFP-15-515
- Tseneva GYa, Solodovnikova NYu, Voskresenskaya EA. Molecular aspects of yersinia virulence. Clinical Microbiology and Antimicrobial Chemotherapy. 2002;4(3):248–266. (In Russ.).
- Chau ML, Aung KT, Hapuarachchi HC, Lee PSV, Lim PY, Lin JS, et al. Microbial survey of ready-to-eat salad ingredients sold at retail reveals the occurrence and the persistence of Listeria monocytogenes Sequence Types 2 and 87 in pre-packed smoked salmon. BMC Microbiology. 2017;17. https://doi.org/10.1186/s12866-017-0956-z
- Söderqvist K. Is your lunch salad safe to eat? Occurrence of bacterial pathogens and potential for pathogen growth in pre-packed ready-to-eat mixed-ingredient salads. Infection Ecology and Epidemiology. 2017;7(1). https://doi.org/10.1080/20008686.2017.1407216
- Møretrø T, Langsrud S. Listeria monocytogenes: Biofilm formation and persistence in food-processing environments. Biofilms. 2004;1(2):107–121. https://doi.org/10.1017/S1479050504001322
- Mataragas M, Skandamis PN, Drosinos EH. Risk profiles of pork and poultry meat and risk ratings of various pathogen/product combinations. International Journal of Food Microbiology. 2008;126(1–2):1–12. https://doi.org/10.1016/j.ijfoodmicro.2008.05.014
- Meyer C, Fredriksson-Ahomaa M, Kleta S, Ellerbroek L, Thiel S, Märtlbauer E. Occurrence of L. monocytogenes in ready-to-eat poultry products available on the German market. Food Research International. 2012;48(2):944–947. https://doi.org/10.1016/j.foodres.2012.02.022
- Smith AM, Tau NP, Smouse SL, Allam M, Ismail A, Ramalwa NR, et al. Outbreak of Listeria monocytogenes in South Africa, 2017–2018: Laboratory activities and experiences associated with whole-genome sequencing analysis of isolates. Foodborne Pathogens and Disease. 2019;16(7):524–530. https://doi.org/10.1089/fpd.2018.2586
- Henriques AR, Cristino JM, Fraqueza MJ. Genetic characterization of Listeria monocytogenes isolates from industrial and retail ready-to-eat meat-based foods and their relationship with clinical strains from human listeriosis in Portugal. Journal of Food Protection. 2017;80(4):551–560. https://doi.org/10.4315/0362-028X.JFP-16-310
- Maćkiw E, Korsak D, Kowalska J, Felix B, Stasiak M, Kucharek K, et al. Genetic diversity of Listeria monocytogenes isolated from ready-to-eat food products in retail in Poland. International Journal of Food Microbiology. 2021;358. https://doi.org/10.1016/j.ijfoodmicro.2021.109397
- Park M-S, Wang J, Park J-H, Forghani F, Moon J-S, Deog-Hwan O. Analysis of microbiological contamination in mixed pressed ham and cooked sausage in Korea. Journal of Food Protection. 2014;77(3):412–418. https://doi.org/10.4315/0362-028X.JFP-13-322
- Caggiano G, Dambrosio A, Ioanna F, Balbino S, Barbuti G, De Giglio O, et al. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates in food industry workers. Annali di Igiene: Medicina Preventiva e di Comunita. 2016;28:8–14. https://doi.org/10.7416/ai.2016.2080
- Balbutskaya AA, Dmitrenko OA, Skvortsov VN. The modern characteristics of species identification of coagulase-positive bacteria of genus. Clinical Laboratory Diagnostics. 2017;62(8):497–502. (In Russ.). https://elibrary.ru/ZFMCYL
- Fijałkowski K, Peitler D, Karakulska J. Staphylococci isolated from ready-to-eat meat – Identification, antibiotic resistance and toxin gene profile. International Journal of Food Microbiology. 2016;238:113–120. https://doi.org/10.1016/j.ijfoodmicro.2016.09.001
- Gelbíčová T, Brodíková K, Karpíšková R. Livestock-associated methicillin-resistant Staphylococcus aureus in Czech retailed ready-to-eat meat products. International Journal of Food Microbiology. 2022;374. https://doi.org/10.1016/j.ijfoodmicro.2022.109727
- Ethelberg S, Smith B, Torpdahl M, Lisby M, Boel J, Jensen T, et al. An outbreak of verocytotoxin-producing Escherichia coli O26:H11 caused by beef sausage, Denmark 2007. Eurosurveillance. 2007;12(22). https://doi.org/10.2807/esw.12.22.03208-en
- Dewey-Mattia D, Manikonda K, Hall AJ, Wise ME, Crowe SJ. Surveillance for foodborne disease outbreaks – United States, 2009–2015. Morbidity and Mortality Weekly Report. Surveillance Summaries. 2018;67(10):1–11. https://doi.org/10.15585/mmwr.ss6710a1
- Risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs. EFSA Journal. 2016;14(7). https://doi.org/10.2903/j.efsa.2016.4524
- Webb MD, Barker GC, Goodburn KE, Peck MW. Risk presented to minimally processed chilled foods by psychrotrophic Bacillus cereus. Trends in Food Science and Technology. 2019;93:94–105. https://doi.org/10.1016/j.tifs.2019.08.024
- Berthold-Pluta A, Pluta A, Garbowska M, Stefańska I. Prevalence and toxicity characterization of Bacillus cereus in food products from Poland. Foods. 2019;8(7). https://doi.org/10.3390/foods8070269
- Caggiano G, Diella G, Trerotoli P, Lopuzzo M, Triggiano F, Ricci M, et al. A pilot survey on hygienic-sanitary characteristics of ready-to-eat sauces and pesto. International Journal of Environmental Research and Public Health. 2020;17(14). https://doi.org/10.3390/ijerph17145005
- Orsi RH, Wiedmann M. Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Applied Microbiology and Biotechnology. 2016;100:5273–5287. https://doi.org/10.1007/s00253-016-7552-2
- Dailey RC, Welch LJ, Hitchins AD, Smiley RD. Effect of Listeria seeligeri or Listeria welshimeri on Listeria monocytogenes detection in and recovery from buffered Listeria enrichment broth. Food Microbiology. 2015;46:528–534. https://doi.org/10.1016/j.fm.2014.09.008
- Caggiano G, De Giglio O, Lovero G, Rutigliano S, Diella G, Balbino S, et al. Detection of Listeria monocytogenes in ready-to-eat foods sampled from a catering service in Apulia, Italy. Annali di Igiene: Medicina Preventiva e di Comunità. 2015;27:590–594. https://doi.org/10.7416/ai.2015.2050
- Perrin M, Bemer M, Delamare C. Fatal case of Listeria innocua bacteremia. Journal of Clinical Microbiology. 2003;41(11):5308–5309. https://doi.org/10.1128/JCM.41.11.5308-5309.2003
- Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs [Internet]. [cited 2023 Jan 12]. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A02005R2073-20200308
- Keerthirathne TP, Ross K, Fallowfield H, Whiley H. The combined effect of pH and temperature on the survival of Salmonella enterica serovar Typhimurium and implications for the preparation of raw egg mayonnaise. Pathogens. 2019;8(4). https://doi.org/10.3390/pathogens8040218
- Louis MES, Morse DL, Potter ME, DeMelfi TM, Guzewich JJ, Tauxe RV, et al. The emergence of grade a eggs as a major source of Salmonella enteritidis infections: New implications for the control of salmonellosis. JAMA. 1988;259(14):2103–2107. https://doi.org/10.1001/jama.1988.03720140023028
- Chousalkar KK, Sexton M, McWhorter A, Hewson K, Martin G, Shadbolt C, et al. Salmonella typhimurium in the Australian egg industry: Multidisciplinary approach to addressing the public health challenge and future directions. Critical Reviews in Food Science and Nutrition. 2017;57(12):2706–2711. https://doi.org/10.1080/10408398.2015.1113928
- Patrick ME, Adcock PM, Gomez TM, Altekruse SF, Holland BH, Tauxe RV, et al. Salmonella enteritidis infections, United States, 1985–1999. Emerging Infectious Diseases. 2004;10(1):1–7. https://doi.org/10.3201/eid1001.020572
- Kenny B, Miller MJ, McEvoy V, Centofanti A, Stevens CP, Housen T. A protracted outbreak of Salmonella Hessarek infection associated with one brand of eggs – South Australia, March 2017–July 2018. Communicable Diseases Intelligence. 2019;43. https://doi.org/10.33321/cdi.2019.43.22
- Hennessy TW, Hedberg CW, Slutsker L, White KE, Besser-Wiek JM, Moen ME, et al. A national outbreak of Salmonella enteritidis infections from ice cream. The New England Journal of Medicine. 1996;334(20):1281–1286. https://doi.org/10.1056/NEJM199605163342001
- Vought KJ, Tatini SR. Salmonella enteritidis contamination of ice cream associated with a 1994 multistate outbreak. Journal of Food Protection. 1998;61(1):5–10. https://doi.org/10.4315/0362-028X-61.1.5
- El-Hajjaji S, Gérard A, de Laubier J, Di Tanna S, Lainé A, Patz V, et al. Assessment of growth and survival of Listeria monocytogenes in raw milk butter by durability tests. International Journal of Food Microbiology. 2020;321. https://doi.org/10.1016/j.ijfoodmicro.2020.108541
- Efimochkina NR, Sheveleva SA, Nityaga IM, Stankevich AA, Romanenko OS. The most significant species of microorganisms in separate groups of foodstuff. Russian Journal Problems of Veterinary Sanitation, Hygiene and Ecology. 2019;32(4):417–427. (In Russ.). https://doi.org/10.25725/vet.san.hyg.ecol.201904013
- Tatarnikova NA, Maul OG. Pathogenic microflora of meat and meat products. Izvestia Orenburg State Agrarian University. 2015;51(1):87–89. (In Russ.). https://elibrary.ru/TKKXUH
- Bataeva DS, Yushina YuK, Zaiko EV. Identification of the microbiological risks of contamination of cattle and pig carcasses with pathogens at slaughter and processing. Theory and Practice of Meat Processing. 2016;1(2):34–41. (In Russ.). https://doi.org/10.21323/2414-438X-2016-1-2-34-41
- Boeva SV. Microbial contamination of cattle carcasses at various slaughter stages. Students’ Contribution to Science and Practice of the Agro-Industrial Complex: Proceedings of 107th International Scientific and Practical Conference of Bachelors and Masters. In 2 parts; 2022; Vitebsk. Vitebsk: Vitebsk State Akademy or Veterinary Medicine; 2022. p. 29–30. (In Russ.). https://elibrary.ru/YLIQWC
- Shcherbinin AV, Mezentsev SV, Spirkina OS. Listeriae in the products of meat-processing companies. Bulletin of Altai State Agricultural University. 2014;118(8):101–104. (In Russ.). https://elibrary.ru/SMSYTN
- Makarov VA, Frolov VP, Shuklin NF. Veterinary and sanitary expertise: basic technology and standardization of livestock products. Moscow: Agropromizdat; 1991. 463 p. (In Russ.).
- Seryogin IG, Nikitchenko DV, Abdullayeva AM. Morphological composition of carcasses and muscle development of eland antelope. RUDN Journal of Agronomy and Animal Industries. 2017;12(2):201–209. (In Russ.). https://doi.org/10.22363/2312-797X-2017-12-2-201-209
- Abdullaeva AM, Seryogin IG, Nikitchenko VE. Microbiological monitoring of commercial poultry meat semi-finished products. RUDN Journal of Agronomy and Animal Industries. 2017;12(4):350–358. (In Russ.). https://doi.org/10.22363/2312-797X-2017-12-4-350-358
- Filatova VI. Microbiological control of food products of animal origin. International Bulletin of Veterinary Medicine. 2022;(1):104–109. (In Russ.). https://doi.org/10.52419/issn2072-2419.2022.1.104
- Sabanchieva LK, Karashaev MF. Scientific concept of maintaining microbiological safety of poultry production. Sustainable development: problems, concepts, and models: Proceedings of the All-Russian Conference with international participation; 2017; Nalchik. Nalchik: Kabardino-Balkar Scientific Center of the RAS; 2017. p. 306–308. (In Russ.). https://elibrary.ru/ZFEYHJ
- Lazhentseva LYu, Shulʹgin YuP. Microbiological risks of raw materials and products from the Far Eastern salmon. Bulletin of the Pacific State Economic University. 2007;41(1):68–74. (In Russ.). https://elibrary.ru/JXQRBX
- Sych AG, Anokhina ON. Microflora development in semi-finished fish products during storage. Innovative Technologies in the Food Industry: science, education, and production: Proceedings of the Extra-Mural International Scientific and Technical Conference; 2013; Voronezh. Voronezh: Voronezh State Technological Academy; 2013. p. 159–163. (In Russ.). https://elibrary.ru/TDCYZB
- Smirnov AM, Kartashova VM. Features of the microbial contamination of refrigerated milk and its effect on the milk products quality. Russian Journal Problems of Veterinary Sanitation, Hygiene and Ecology. 2012;7(1):42–46. (In Russ.). https://elibrary.ru/PCQLXR
- Sviridenko GM, Zakharova MB, Ivanova NV. Evaluation of microbiological risks in cream as a raw material for buttermaking. Food Systems. 2021;4(4):259–268. (In Russ.). https://doi.org/10.21323/2618-9771-2021-4-4-259-268
- Polyakova SP, Voronkova NE, Khokhlova EA. Safety of confectionery in the production control. Bread Products. 2012;(9):60–63. (In Russ.). https://elibrary.ru/PCHKRD
- Ganina VI, Grinevich AI, Loiko NG, Guchok ZhL. Microbiological safety of the milk raw materials. Dairy Industry. 2015;(11):22–23. (In Russ.). https://elibrary.ru/UXVGNB
- Sviridenko GM, Kalabushkin VV, Shishkina AN, Uskova EE. Research on the possibility of extending the shelf life of cheese raw material and heat-treated cheese by their freezing for further use in HoReCa. Food Systems. 2020;3(4):39–44. https://doi.org/10.21323/2618-9771-2020-3-4-39-44
- Efimochkina NR, Bykova IB, Stetsenko VV, Minaeva LP, Pichugina TV, Markova YuM, et al. The study of the contamination and the levels of Campylobacter spp. during the processing of selected types of foods. Problems of Nutrition. 2016;85(5):52–59. (In Russ.). https://elibrary.ru/WYMSNF
- Kharitonov DV, Dobriyan EI, Il'ina AM. Study of microbiological background of herbal ingredients and dairy-vegetable compositions. Proceedings of the Voronezh State University of Engineering Technologies. 2016;69(3):159–163. (In Russ.). https://doi.org/10.20914/2310-1202-2016-3-159-163
- Sheveleva SA, Efimochkina NR, Bykova IB, Batishcheva SYu. Substantiating microbiological safety indicators for new food products. Problems of Nutrition. 2014;83(S3):162. (In Russ.). https://elibrary.ru/XCEWKD
- Lubimova LV, Kupin GA, Vlasov PA, Bugayets NA. Processing electromagnetic field of culinary products for process control microbiological damage. Scientific Works of the Kuban State Technological University. 2016;(14):204–209. (In Russ.). https://elibrary.ru/ZHJRIX
- Zakharova II. Modern methods of cooling culinary products and raw materials in the food industry. Agro Production and Econimics Journal. 2020;(1):7–13. (In Russ.). https://elibrary.ru/WKXDZM
- Baranenko DA, Zabelina NA. Meat and meat products spoilage microflora vital functions suppression by means of hurdle technology. Food Production Processes and Equipment. 2011;(1):238–245. (In Russ.). https://elibrary.ru/NDKBZR
- Gonotskiy VA, Kozak SS, Dubrovskiy NV, Dubrovskaya VI, Gonotskaya VA. Effective bacteriostatics as a guarantee of microbiological safety of semi-finished products during storage. In: Gushchin VV, editor. New Methods and Technologies of Processing Poultry and eggs: Collection of scientific papers. Rzhavki: VNIIPP; 2011. pp. 83–88. (In Russ.). https://elibrary.ru/UAWYDZ
- Kostenko YuG, Bataeva DS, Krasnova MA. Chilled pork with a long shelf life: Sanitary and microbiological production aspects. Meat Industry. 2009;(4):66–67. (In Russ.). https://elibrary.ru/KUEMNP
- Menéndez R, Rendueles E, Sanz JJ, Capita R, García-Fernández C. Behavior of Listeria monocytogenes in sliced ready-to-eat meat products packaged under vacuum or modified atmosphere conditions. Journal of Food Protection. 2015;78(10):1891–1895. https://doi.org/10.4315/0362-028X.JFP-15-103
- Horita CN, Baptista RC, Caturla MYR, Lorenzo JM, Barba FJ, Sant’Ana AS. Combining reformulation, active packaging and non-thermal post-packaging decontamination technologies to increase the microbiological quality and safety of cooked ready-to-eat meat products. Trends in Food Science and Technology. 2018;72:45–61. https://doi.org/10.1016/j.tifs.2017.12.003
- Abdullaeva AM, Blinkova LP, Pershina TA, Udavliev DI, Satyukova LP, Pakhomov YuD, et al. Testing of bacteriophages as safe means of protection of minced chicken from contamination by microorganisms. Russian Journal Problems of Veterinary Sanitation, Hygiene and Ecology. 2019;31(3):259–265. (In Russ.). https://doi.org/10.25725/vet.san.hyg.ecol.201903004
- Fomushkin VI, Blagoveshchenskaya MM, Nosenko SM, Blagoveshchenskii IG. The automated expert system for raw meat microbiological spoilage risks monitoring. Food Industry. 2015;(6):14–17. (In Russ.). https://elibrary.ru/ULRKYH