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Factors influencingmicrobial transmission in a meat processing plant

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The review paper examines the main risk factors for microbial contamination of meat at different stages of its processing. Particular emphasis has been placed on primary animal processing being the most hazardous in terms of microbial contamination of meat. Carcass cross-contamination most frequently occurs during skinning and evisceration since hides and the digestive tract are the primary sources of microbial pathogens. It is necessary to observe stringent sanitary and hygienic rules when performing these operations. Continuous cold chain management along all following stages of meat processing and control of the sanitary status of cold chambers during meat storage are of extreme importance. An increase in the microbial counts due to the high number of manual operations was observed during meat cutting, boning, and trimming. Subsequent stages of meat processing, including mincing, curing, the addition of spices, also promote significant microbial growth. Strict control regarding detection of dangerous pathogens, especially L. monocytogenes, is needed at this stage. In general, to minimize problems linked with meat and meat product safety, it is necessary to take timely measures on sanitary treatment of meat processing facilities, including the prevention of biofilm formation.

About the Authors

B. Velebit
Institute of Meat Hygiene and Technology

Branko Velebit —  M. Sc. DVM, Principal Research Fellow, Head of Department of Microbiology and Molecular Biology

Kaćanskog 13, 11040 Belgrade

Tel.: +381–11–2650–722

B. Lakicevic
Institute of Meat Hygiene and Technology

Brankica Z. Lakicevic —  Research Associate

Kaćanskog 13, 11000, Belgrade

Tel.: +381–11–2650–722

A. A. Semenova
V. M. Gorbatov Federal Research Center for Food Systems of Russian Academy of Sciences
Russian Federation

Anastasia A. Semenova —  Doctor of technical sciences, Professor, Deputy Director

Talalikhina, 26, 109316, Moscow

Tel: +7–903–016–76–70

N. M. Revutskaya
V. M. Gorbatov Federal Research Center for Food Systems of Russian Academy of Sciences
Russian Federation

Nataliya M. Revutskaya —   Candidate of technical sciences, Research Associate, Department of Applied Scientific and Technological Development

Talalikhina 26, 109316, Moscow
Tel: +7–495–676–95–11(305)

Yu. K. Yushina
V. M. Gorbatov Federal Research Center for Food Systems of Russian Academy of Sciences
Russian Federation

Yulia K. Yushina —  Candidate of technical sciences, Docent, Deputy head of laboratory «Center for food and feed testing»

Talalikhina 26, 109316, Moscow


V. V. Nasonova
V. M. Gorbatov Federal Research Center for Food Systems of Russian Academy of Sciences
Russian Federation

Victoriya V. Nasonova —   Candidate of technical sciences, Head of Department of Applied Scientific and Technological Development

Talalikhina 26, 109316, Moscow,

Tel: +7–495–676–95–11(307)


1. Bintsis, T. (2018). Microbial pollution and food safety. AIMS Microbiology, 4(3), 377–396.

2. Bintsis, T. (2017). Foodborne pathogens. AIMS Microbiology, 3(3), 529–563.

3. Hameed, S., Xie, L., Ying, Y. (2018). Conventional and emerging detection techniques for pathogenic bacteria in food science: a review. Trends in Food Science and Technology, 81, 61–73.

4. Møretrø, T., Langsrud, S. (2017). Residential bacteria on surfaces in the food industry and their implications for food safety and quality. Comprehensive Reviews in Food Science and Food Safety, 16(5), 1022–1041.–4337.12283

5. Sosnowski, M., Osek, J. (2021). Microbiological safety of food of animal origin from organic farms. Journal of Veterinary Research, 65(1), 87–92.–0015.

6. Doulgeraki, A.I., Ercolini, D., Villani, F., Nychas, G. J. E. (2012). Spoilage microbiota associated to the storage of raw meat in different conditions. International Journal of Food Microbiology, 157(2), 130–141.

7. Alvseike, O., Røssvoll, E., Røtterud, O.-J., Nesbakken, T., Skjerve, E., Prieto, M. et al. (2019). Slaughter hygiene in European cattle and sheep abattoirs assessed by microbiological testing and hygiene performance rating. Food Control, 101, 233–240.

8. Bataeva, D.S., Yushina, Yu.K., Zaiko, E.V. (2016). Identification of the microbiological risks of contamination of cattle and pig carcasses with pathogens at slaughter and processing. Theory and Practice of Meat Processing, 1(2), 34–41.–438X-2016–1–2–34–41 (In Russian)

9. Wang, H., Zhang, X., Zhang, Q., Ye, K., Xu, X., Zhou, G. (2015). Comparison of microbial transfer rates from Salmonella spp. biofilm growth on stainless steel to selected processed and raw meat. Food Control, 50, 574–580.

10. Mertz, A.W., Koo, O.K., O’Bryan, C.A., Morawicki, R., Sirsat, S.A., Neal, J.A. et al. (2014). Microbial ecology of meat slicers as determined by denaturing gradient gel electrophoresis. Food Control, 42, 242–247.

11. Bakhtiary, F., Sayevand, H.R., Remely, M., Hippe, B., Hosseini, H., Haslberger, A.G. (2016). Evaluation of bacterial contamination sources in meat production line. Journal of food quality, 39(6), 750–756.

12. Serraino, A., Bardasi, L., Riu, R., Pizzamiglio, V., Liuzzo, G. et al. (2012). Visual evaluation of cattle cleanliness and correlation to carcass microbial contamination during slaughtering.Meat Science, 90(2), 502–506.

13. Antic, D., Blagojevic, B., Ducic, M., Nastasijevic, I., Mitrovic, R. et al. (2010). Distribution of microflora on cattle hides and its transmission to meat via direct contact. Food Control, 21(7), 1025–1029.

14. Zweifel, C., Capek, M., Stephan, R. (2014). Microbiological contamination of cattle carcasses at different stages of slaughter in two abattoirs. Meat Science, 98(2), 198–202.

15. Nastasijevic, I., Mitrovic, R., Buncic, S. (2008). Occurrence of Escherichia coli O157on hides of slaughtered cattle.Letters in Applied Microbiology,46, 126–131–765x.2007.02270.x

16. Adakova, N.V., Krasnova, O.A., Hardina, E.V. (2012). Meat microorganisms contamination in the treatment of primary slaughtered animals. The Bulletin of Izhevsk State Agricultural Academy, 2(31), 32–34. (In Russian)

17. Bolton, D.J., Pearce, R.A., Sheridan, J.J., Blair, I.S., McDowell, D.A., Harrington, D. (2002). Washing and chilling as critical control points in pork slaughter hazard analysis and critical control point (HACCP) systems. Journal of Applied Microbiology, 92(5), 893–902.–2672.2002.01599.x

18. Zdolec, N., Dobranić, V., Filipović, I. (2014). Prevalence of Salmonella spp. and Yersinia enterocolitica in/on tonsils and mandibular lymph nodes of slaughtered pigs. Folia Microbiologica, 60(2), 131–135.–014–0356–9

19. Wheatley, P., Giotis, E. S., McKevitt, A. I. (2014). Effects of slaughtering operations on carcass contamination in an Irish pork production plant. Irish Veterinary Journal, 67(1), 1.–0481–67–1

20. De Busser, E. V., De Zutter, L., Dewulf, J., Houf, K., Maes, D. (2013). Salmonella control in live pigs and at slaughter.The Veterinary Journal, 196(1), 20–27.

21. Delhalle, L., De Sadeleer, L., Bollaerts, K., Farnir, F., Saegerman, C. et al. (2008). Risk factors for Salmonellaand hygiene indicators in the 10 largest Belgian pig slaughterhouses. Journal of Food Protection, 71(7): 1320–1329.–028X-71.7.1320

22. Paliy, A.P., Rodionova, K.O., Braginec, M.V., Nalivayko, L.I. (2018). Sanitary-hygienic evaluation of objects of meat processing enterprises and means of their sanation. Ukrainian Journal of Ecology, 8(2), 81–88.

23. Buncic, S., Nychas, G.-J., Lee, M. R. F., Koutsoumanis, K., Hébraud, M. et al. (2014). Microbial pathogen control in the beef chain: Recent research advances. Meat Science, 97(3), 288–297.

24. Peruzy, M.F., Houf, K., Joossens, M., Yu, Z., Proroga, Y. T.R., Murru, N. (2021). Evaluation of microbial contamination of different pork carcass areas through culture-dependent and independent methods in small-scale slaughterhouses. International Journal of Food Microbiology,336, Article 108902.

25. Barco, L., Belluco, S., Roccato, A., Ricci, A. (2014). Escherichia coli and Enterobacteriaceae counts on pig and ruminant carcasses along the slaughterline, factors influencing the counts and relationship between visual faecal contamination of carcasses and counts: a review.EFSA Supporting Publications, 11(8), EN-634.

26. Barkocy-Gallagher, G. A., Arthur, T. M., Rivera-Betancourt, M., Nou, X., Shackelford, S. D. et al. (2003). Seasonal prevalence of shiga toxin–producing Escherichia coli, including O 157: H7and Non-O157Serotypes, and Salmonellain commercial beef processing plants. Journal of Food Protection, 66 (11), 1978–1986.–028X-66.11.1978

27. Petruzzelli, A., Osimani, A., Pasquini, M., Clementi, F., Vetrano, V., Paolini, F. et al. (2016). Trends in the microbial contamination of bovine, ovine and swine carcasses in three small-scale abattoirs in central Italy: A four-year monitoring.Meat Science, 111, 53–59.

28. Choi, Y. M., Park, H. J., Jang, H. I., Kim, S. A., Imm, J. Y. et al. (2013). Changes in microbial contamination levels of porcine carcasses and fresh pork in slaughterhouses, processing lines, retail outlets, and local markets by commercial distribution.Research in Veterinary Science, 94(3), 413–418.

29. Reid, R., Fanning, S., Whyte, P., Kerry, J., Lindqvist, R. et al. (2017). The microbiology of beef carcasses and primals during chilling and commercial storage. Food Microbiology, 61, 50–57.

30. Wickramasinghe, N.N., Ravensdale, J., Coorey, R., Chandry, S.P., Dykes, G.A. (2019). The predominance of psychrotrophic pseudomonads on aerobically stored chilled red meat. Comprehensive Reviews in Food Science and Food Safety, 18(5), 1622–1635.–4337.12483

31. Umiraliyeva, L.B., Chizhayeva, A.V., Velamov, M.T., Avylov, Ch.K., Potoroko, I. Yu., Ibraikhan, A.T. (2020). Impact of refrigeration equipment’s sanitary condition on shelf life of meat. Bulletin of the South Ural State University. Series: Food and Biotechnology, 8(3), 73–82. (In Russian)

32. Nastasijević, I., Lakićević, B., Petrović, Z. (2017). Cold chain management in meat storage, distribution and retail: a review. IOP Conference Series: Earth and Environmental Science, 85, 012022.–1315/85/1/012022

33. Kinsella, K.J., Sheridan, J.J., Rowe, T.A., Butler, F., Delgado, A., Quispe-Ramirez, A. et al. (2006). Impact of a novel spray-chilling system on surface microflora, water activity and weight loss during beef carcass chilling. Food Microbiology, 23(5), 483–490.

34. Voloski, F.L.S., Tonello, L., Ramires, T., Reta, G.G., Dewes, C., Iglesias, M. et al. (2016). Influence of cutting and deboning operations on the microbiological quality and shelf life of buffalo meat. Meat Science, 116, 207–212.

35. Althaus, D., Zweifel, C., Stephan, R. (2017). Analysis of a poultry slaughter process: Influence of process stages on the microbiological contamination of broiler carcasses. Italian Journal of Food Safety, 6(4), 190–194.

36. Hamby, P.L., Savell, J.W., Acuff, G.R., Vanderzant, C., Cross, H.R. (1987). Spray-chilling and carcass decontamination systems using lactic and acetic acid. Meat Science, 21(1), 1–14.–1740(87)90038–6

37. Minaev, M. Yu., Bataeva, D.S., Krasnova, M.A. (2008). Aspects of sanitary-microbiological control of long-storage cooled meat. Vsyo o myase, 6, 48–50.(In Russian)

38. Garima, U. (2016). Psychrophilic pathogens: potential risk for food borne illness. Research Journal of Recent Sciences, 5(7), 50–52.

39. Biasino, W., De Zutter, L., Mattheus, W., Bertrand, S., Uyttendaele, M. et al. (2017) Correlation between slaughter practices and the distribution of Salmonella and hygiene indicator bacteria on pig carcasses during slaughter. Food Microbiology, 70, 192–199.

40. Kim, J.H., Hur, S.J., Yim, D.G. (2018). Monitoring of microbial contaminants of beef, pork, and chicken in HACCP implemented meat processing plants of Korea. Korean Journal for Food Science of Animal Resources, 38(2), 282–290.

41. Ivanović, J., Janjić, J., Marković, R., Dokmanović, M., Bošković, M., Dimovska, N., et al. (2015) Presence of selected microorganisms on meat contact surfaces in the meat cutting facility. Journal of Hygienic Engineering and Design, 12,18–23.

42. McSharry, S., Koolman, L., Whyte, P., Bolton, D. (2021).The microbiology of beef from carcass chilling through primal storage to retail steaks. Current Research in Food Science, 4, 150–162.

43. Laban S. E., Mashaly M. M., Aly A. M., Maher N. E., Zaki M. M. (2021). Evaluation of different hygienic practices applied in slaughterhouses and its effect on beef quality. Advances in Animal and Veterinary Sciences,9 (3), 429–437.

44. Tomasevic, I., Kuzmanović, J., Anđelković, A., Saračević, M., Stojanović, M. M., Djekic, I. (2016). The effects of mandatory HACCP implementation on microbiological indicators of process hygiene in meat processing and retail establishments in Serbia.Meat Science, 114, 54–57.

45. Fagerlund, A., Møretrø, T., Heir, E., Briandet, R., Langsrud, S. (2017). Cleaning and disinfection of biofilms composed of Listeria monocytogenes and background microbiota from meat processing surfaces. Applied and Environmental Microbiology, 83(17), Article e01046–17.–17

46. Metaxopoulos, J., Kritikos, D., Drosinos, E. (2003). Examination of microbiological parameters relevant to the implementation of GHP and HACCP system in Greek meat industry in the production of cooked sausages and cooked cured meat products. Food Control, 14(5), 323–332.–7135(02)00097-x

47. Hultman, J., Rahkila, R., Ali, J., Rousu, J., Björkroth, K.J. (2015). Meat processing plant microbiome and contamination patterns of cold-tolerant bacteria causing food safety and spoilage risks in the manufacture of vacuum-packaged cooked sausages. Applied and Environmental Microbiology, 81(20), 7088–7097.–15

48. Garbowska, M., Berthold-Pluta, A., Stasiak-Różańska, L. (2015). Microbiological quality of selected spices and herbs including the presence of Cronobacter spp. Food Microbiology, 49, 1–5.

49. 9 Fogele, B., Granta, R., Valciņa, O., Bērziņš, A. (2018). Occurrence and diversity of Bacillus cereus and moulds in spices and herbs. Food Control, 83, 69–74.

50. Banach, J.L., Stratakou, I., van der Fels-Klerx, H.J., Besten, H.M.W.D., Zwietering, M.H. (2016). European alerting and monitoring data as inputs for the risk assessment of microbiological and chemical hazards in spices and herbs. Food Control, 69, 237–249.

51. Säde, E., Lassila, E., Björkroth, J. (2016). Lactic acid bacteria in dried vegetables and spices. Food Microbiology, 53, 110–114.

52. Eveleva, V.V., Cherpalova, T.M., Shipovskaya, E.A. (2019). Technological innovations for treatment of casings. Theory and Practice of Meat Processing, 4(2), 14–19.–438X-2019–4–2–14–19

53. Çağlar, A., Bor, Y., Tomar, O., Beykaya, M., Gök, V. (2018). Mechanical and microbiological properties of natural casings using in meat products. Kafkas Universitesi Veteriner Fakultesi Dergisi, 24(3), 327–334.

54. Korkeala, H. J. Björkroth, K. J. (1997). Microbiological spoilage and contamination of vacuum-packaged cooked sausages. Journal of Food Protection, 60(6), 724–731.–028X-60.6.724

55. Sofos, J. N., Geornaras, I. (2010). Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O 157: H7in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Science, 86(1), 2–14.

56. Nityaga, I.M. (2016). Listeria contamination of meat products and express their identity using methods based on PCR. Russian Journal Problems of Veterinary Sanitation, Hygiene and Ecology, 1(17), 17–22. (In Russian)

57. Gómez, D., Iguácel, L., Rota, M., Carramiñana, J., Ariño, A. et al. (2015). Occurrence of Listeria monocytogenes in ready-to-eat meat products and meat processing plants in Spain. Foods, 4(4), 271–282.

58. Nastasijevic, I., Milanov, D., Velebit, B., Djordjevic, V., Swift, C. et al (2017). Tracking of Listeria monocytogenes in meat establishment using Whole Genome Sequencing as a food safety management tool: a proof of concept.International Journal of Food Microbiology, 257, 157–164.

59. Pearce, R.A., Sheridan, J.J., Bolton, D.J. (2006). Distribution of airborne microorganisms in commercial pork slaughter processes. International Journal of Food Microbiology, 107(2), 186–191.

60. Prendergast, D.M., Daly, D.J., Sheridan, J.J., McDowell, D.A., Blair, I.S. (2004). The effect of abattoir design on aerial contamination levels and the relationship between aerial and carcass contamination levels in two Irish beef abattoirs. Food Microbiology, 21(5), 589–596.

61. Byrne, B., Lyng, J., Dunne, G., Bolton, D.J. (2008). An assessment of the microbial quality of the air within a pork processing plant. Food Control, 19(9), 915–920.

62. Wang, H., He, A., Yang, X. (2018). Dynamics of microflora on conveyor belts in a beef fabrication facility during sanitation. Food Control, 85, 42–47. doi:10.1016/j.foodcont.2017.09.017

63. 63.Vargová, M., Sasáková, N., Laktičová, K. V., Zigo, F. (2021). Evaluation of the hygienic condition of the slaughterhouse. Acta Fytotechnica Et Zootechnica, 24, 37–40.–40

64. Minaev, M. Yu., Rybaltovsky, V.O., Solodovnikova, G.I. (2009). Criterion of selection of detergents and disinfectants for sanitation at meat processing plants. Vsyo o myase, 3, 44–45. (In Russian)

65. Joshi, K., Mahendran, R., Alagusundaram, K., Norton, T., Tiwari, B.K. (2013). Novel disinfectants for fresh produce. Trends in Food Science and Technology, 34(1), 54–61.

66. Langsrud, S., Sidhu, M. S., Heir, E., Holck, A. L. (2003). Bacterial disinfectant resistance — a challenge for the food industry.International Biodeterioration and Biodegradation, 51(4), 283–290. https://doi:10.1016/s0964–8305(03)00039–8

67. Møretrø, T., Langsrud, S., Heir, E. (2013). Bacteria on Meat Abattoir Process Surfaces after Sanitation: Characterisation of Survival Properties of Listeria monocytogenesand the Commensal Bacterial Flora. Advances in Microbiology, 3(3), 255–264.

68. Carrascosa, C., Raheem, D., Ramos, F., Saraiva, A., Raposo, A. (2021). Microbial biofilms in the food industry — a comprehensive review. International Journal of Environmental Research and Public Health, 18(4), 1–31.

69. Giaouris, E., Heir, E., Hébraud, M., Chorianopoulos, N., Langsrud, S. et al (2014). Attachment and biofilm formation by foodborne bacteria in meat processing environments: Causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Science, 97(3), 298–309.

70. Parussolo, G., Bernardi, A.O., Garcia, M.V., Stefanello, A., Silva, T. dos S., Copetti, M.V. (2019). Fungi in air, raw materials and surface of dry fermented sausage produced in Brazil. LWT, 108, 190–198.

71. Bernardi, A.O., Garcia, M.V., Copetti, M.V. (2019). Food industry spoilage fungi control through facility sanitization. Current Opinion in Food Science, 29, 28–34.

72. Siqueira, V.M., Lima, N. (2013). Biofilm formation by filamentous fungi recovered from a water system. Journal of Mycology, 3, 1–9.

73. Costa-Orlandi, C. B., Sardi, J. C. O., Pitangui, N. S., de Oliveira, H. C., Scorzoni, L., Galeane, M. C. et al. (2017). Fungal biofilms and polymicrobial diseases. Journal of Fungi, 3(2), Article 22.

74. Simões, M., Simões, L. C., Vieira, M. J. (2010). A review of current and emergent biofilm control strategies. LWT — Food Science and Technology, 43(4), 573–583.

For citation:

Velebit B., Lakicevic B., Semenova A.A., Revutskaya N.M., Yushina Yu.K., Nasonova V.V. Factors influencingmicrobial transmission in a meat processing plant. Theory and practice of meat processing. 2021;6(2):183-190.

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