Preview

Theory and practice of meat processing

Advanced search

Testing of methods for detecting Salmonella in the air of poultry processing plants.

https://doi.org/10.21323/2414-438X-2025-10-4-385-392

Abstract

The aim of the study is to compare the effectiveness of microbiological and PCR methods for detecting Salmonella in the air at various technological sites in four poultry processing plants and in one poultry farming enterprise. The objects of the study were air samples collected on two nutrient agars: non-selective PCA agar and selective XLD agar. Microbiological and PCR methods were used. Air samples collected on PCA agar were cultured in the BPW (enrichment stage). The culture liquid obtained in this way was used in the isolation of Salmonella by the microbiological and PCR methods. The identification of colonies typical of Salmonella isolated by the microbiological method was carried out by mass spectroscopy. The conducted study demonstrated the indisputable advantages of the PCR method (after enriching air samples in BPW) over the classic microbiological method without enrichment for monitoring Salmonella in the air of poultry processing plants. The PCR method has a higher sensitivity and detection speed, allowing the pathogen to be detected even at low concentrations in a sample. This is especially important for monitoring areas with a potentially low microbial load, such as the final washing of broiler chicken carcasses. The microbiological method without the enrichment stage showed low detection of Salmonella in the study of 66.6 % of air samples (false negative results were obtained) of poultry processing plants and 80 % of air samples taken at the poultry farming enterprise. Increasing its sensitivity to a level comparable to the PCR method is possible only with the introduction of an additional enrichment step in a liquid non-selective nutrient medium, for example, in buffered peptone water. Thus, for prompt and reliable control of Salmonella contamination in the air, it is advisable to use the PCR method as the most rapid and sensitive tool, ensuring high reliability of results even with minimal bacterial contamination, and the microbiological method with sample enrichment as a relatively slow but reliable “golden” standard method.

About the Authors

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

Yulia K. Yushina, Doctor of Technical Sciences, Head of Department of Hygiene of Production and Microbiology



D. S. Bataeva
V. M. Gorbatov Federal Research Center for Food Systems
Russian Federation

Dagmara S. Bataeva, Candidate of Technical Sciences, Leading Research Fellow, Department of Hygiene of Production and Microbiology



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

Anastasia A. Semenova, Doctor of Technical Sciences, Professor, Deputy Director



M. A. Grudistova
V. M. Gorbatov Federal Research Center for Food Systems
Russian Federation

Maria A. Grudistova, Candidate of Technical Sciences, Researcher, Department of Hygiene of Production and Microbiology



E. V. Zaiko
V. M. Gorbatov Federal Research Center for Food Systems
Russian Federation

Elena V. Zaiko, Candidate of Technical Sciences, Department of Hygiene of Production and Microbiology



A. A. Makhova
V. M. Gorbatov Federal Research Center for Food Systems
Russian Federation

Anzhelica A. Makhova, Researcher, Department of Hygiene of Production and Microbiology



References

1. Miskiewicz, A., Kowalczyk, P., Oraibi, S. M., Cybulska, K., Misiewicz, A. (2018). Bird feathers as potential sources of pathogenic microorganisms: A new look at old diseases. Antonie van Leeuwenhoek, 111(9), 1493–1507. https://doi.org/10.1007/s10482-018-1048-2

2. Lou, C., Bai, Y., Chai, T., Yu, H., Lin, T., Hu, G. et al. (2022). Research progress on distribution and exposure risk of microbial aerosols in animal houses. Frontiers in Veterinary Science, 9, Article 1015238. https://doi.org/10.3389/fvets.2022.1015238

3. Lou, C., Chen, Z., Bai, Y., Chai, T., Guan, Y., Wu, B. (2023). Exploring the microbial community structure in the chicken house environment by metagenomic analysis. Animals, 14(1), Article 55. https://doi.org/10.3390/ani14010055

4. 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 Microbi ology, 21(5), 589–596. https://doi.org/10.1016/j.fm.2003.11.002

5. Buncic, S., Sofos, J. (2012). Interventions to control Salmonella contamination during poultry, cattle and pig slaughter. Food Research International, 45(2), 641–655. https://doi.org/10.1016/j.foodres.2011.10.018

6. Lelieveld, H. L. M., Holah, J. T. Hazards, sources and vectors of contamination. Chapter in a book: Hygiene in food processing. Woodhead Publishing, 2014. https://doi.org/10.1533/9780857098634.1.21

7. Urban-Chmiel, R., Osek, J., Wieczorek, K. (2025). Methods of controlling microbial contamination of food. Pathogens, 14(5), Article 492. https://doi.org/10.3390/pathogens14050492

8. Maldonade, I. R., Ginani, V. C., Riquette, R. F. R., Gurgel Gonçalves, R., Mendes, V. S., Machado, E. R. (2019). Good manufacturing practices of minimally processed vegetables reduce contamination with pathogenic microorganisms. Re vista do Instituto de Medicina Tropical de São Paulo, 61, Article e14. https://doi.org/10.1590/S1678-9946201961014

9. Bataeva, D. S., Yushina, Yu. K., Grudistova, M. A., Makhova А. A. (2024). Pseudomonas growth on cattle carcasses during chilling: Predictive modeling. Vsyo o Myase, 1, 32–35. https://doi.org/10.21323/2071-2499-2024-1-32-35 (In Russian)

10. Yushina, Yu. K., Bataeva, D. S., Reshchikov, M. D. Zayko, E. V. Grudistova, M.A., Makhova А. A. et al. (2025). Indicator microorganisms of meat processing plants: From air borne bioaerosols to surface contaminants. Meat Industry, 4, 32–36. (In Russian)

11. King, M. D. (2024). Monitoring airborne pathogen transmission for enhanced safety at food processing facilities. Acta Alimentaria, 53(3), 337–348. https://doi.org/10.1556/066.2024.00151

12. Mullane, N. R., Whyte, P., Wall, P. G., Quinn, T., Fanning, S. (2007). Application of pulsed-field gel electrophoresis to characterise and trace the prevalence of Enterobacter saka zakii in an infant formula processing facility. Internation al Journal of Food Microbiology, 116(1), 73–81. https://doi.org/10.1016/j.ijfoodmicro.2006.12.036

13. López-Gómez, A., Castano-Villar, A. M., Palop, A., Marín-Iniesta, F. (2013). Hygienic design and microbial control of refrigeration and air conditioning systems for food processing and packaging plants. Food Engineering Reviews, 5(1), 18–35. https://doi.org/10.1007/s12393-012-9060-1

14. Parpas, D., Amaris, C., Tassou, S. A. (2018). Investigation into air distribution systems and thermal environment control in chilled food processing facilities. International Journal of Refrigeration, 87, 47–64. https://doi.org/10.1016/j.ijrefrig.2017.10.019

15. Moracanin, S. V., Memisi, N., Djukic, D., Milijasevic, M., Borovic, B., Raseta, M. (September 22–25, 2019.). Air quality and impact on food safety. The 60th International Meat Industry Conference MEATCON2019. IOP conference series: Earth and environmental science. IOP Publishing, 2019. https://doi.org/10.1088/1755-1315/333/1/012111

16. Umiralieva, L., Chizhayeva, A., Ibraikhan, A., Avylov, C., Velyamov, M. (2021). Investigation of the sanitary state of air and refrigeration equipment of meat processing enterpris es in Kazakhstan using the method of metagenomic analysis. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 69(3), 403–416. https://doi.org/10.11118/actaun.2021.037

17. Mbareche, H., Veillette, M., Bilodeau, G. J., Duchaine, C. (2018). Bioaerosol sampler choice should consider efficiency and ability of samplers to cover microbial diversity. Appliedand Environmental Microbiology, 84(23), Article e01589–18. https://doi.org/10.1128/AEM.01589-18

18. Reponen, T., Willeke, K., Grinshpun, S., Nevalainen, A. (2011). Biological particle sampling. Chapter in a book: Aerosol measurement: Principles, techniques, and ap plications. John Wiley & Sons, Inc., 2011. https://doi.org/10.1002/9781118001684.ch24

19. Lee, K. M., Runyon, M., Herrman, T. J., Phillips, R., Hsieh, J. (2015). Review of Salmonella detection and identification methods: Aspects of rapid emergency response and food safety. Food Control, 47, 264–276. https://doi.org/10.1016/j.foodcont.2014.07.011

20. Kasturi, K. N., Drgon, T. (2017). Real-time PCR method for detection of Salmonella spp. in environmental samples. Applied and Environmental Microbiology, 83(14), Article e00644–17. https://doi.org/10.1128/AEM.00644-17

21. Oppliger, A. (2014). Advancing the science of bioaerosol ex posure assessment. Annals of Occupational Hygiene, 58(6), 661–663. https://doi.org/10.1093/annhyg/meu042

22. 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. https://doi.org/10.1016/j.foodcont.2007.08.016

23. Chauhan, A., Jindal, T. (2020). Microbiological Methods for Water, Soil and Air Analysis. Chapter in d book: Microbiological Methods for Environment, Food and Pharmaceutical Analysis. Cham: Springer International Publishing, 2020. https://doi.org/10.1007/978-3-030-52024-3_7

24. Maukonen, J. (2007). Molecular techniques and microscopy in bacterial detection and typing. (January 22–23, 2007). Microbial Contaminants and Contamination Routes in Food Industry. 1ST open seminar arranged BYSAFOODNET and food safety and hygiene networking within new member states and associated candidate countrie VTT Technical Research Centre of Finland. Espoo, Finland, 2007.

25. Terzieva, S., Donnelly, J., Ulevicius, V., Grinshpun, S. A., Willeke, K., Stelma, G. N., Brenner, K. P. (1996). Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Applied and Environmental Microbiology, 62(7), 2264–2272. https://doi.org/10.1128/aem.62.7.2264-2272.1996

26. Stetzenbach, L. D., Buttner, M. P., Cruz, P. (2004). Detection and enumeration of airborne biocontaminants. Current Opinion in Biotechnology, 15(3), 170–174. https://doi.org/10.1016/j.copbio.2004.04.009

27. Boubendir, S., Arsenault, J., Quessy, S., Thibodeau, A., Fravalo, P., Thériault, W. et al. (2020). Salmonella contamination of broiler chicken carcasses at critical steps of the slaughter process and in the environment of two slaughter plants: Prevalence, genetic profiles and association with the final carcass status. Journal of Food Protection, 82(4), 321–332. https://doi.org/10.4315/JFP-20-250

28. Mead, G. C. (1993). Problems of producing safe poultry: Discussion paper. Journal of the Royal Society of Medicine, 86(1), 39–42.

29. Rivera-Pérez, W., Barquero-Calvo, E., Zamora-Sanabria, R. (2014). Salmonella contamination risk points in broiler car casses during slaughter line processing. Journal of Food Protection, 77(12), 2031–2034. https://doi.org/10.4315/0362-028X.JFP-14-052

30. Salehi, S., Howe, K., Lawrence, M. L., Brooks, J. P., Bailey, R. H., Karsi, A. (2017). Salmonella enterica serovar Kentucky flagella are required for broiler skin adhesion and Caco-2 cell invasion. Applied and Environmental Microbiology, 83(2), Article e02115–16. https://doi.org/10.1128/AEM.02115-16

31. Ferguson, R. M. W., Garcia‐Alcega, S., Coulon, F., Dumbrell, A. J., Whitby, C., Colbeck, I. (2019). Bioaerosol biomonitoring: Sampling optimization for molecular microbial ecology. Molecular Ecology Resources, 19(3), 672–690. https://doi.org/10.1111/1755-0998.13002

32. Masotti, F., Cattaneo, S., Stuknytė, M., De Noni, I. (2019). Airborne contamination in the food industry: An update on monitoring and disinfection techniques of air. Trends in Food Science and Technology, 90, 147–156. https://doi.org/10.1016/j.tifs.2019.06.006

33. den Aantrekker, E. D., Boom, R. M., Zwietering, M. H., van Schothorst, M. (2003). Quantifying recontamination through factory environments — A review. International Journal of Food Microbiology, 80(2), 117–130. https://doi.org/10.1016/S0168-1605(02)00137-X

34. Schrank, I. S., Mores, M. A. Z., Costa, J. L. A., Frazzon, A. P. G., Soncini, R., Schrank, A. et. el. (2001). Influence of enrichment media and application of a PCR based method to detect Salmonella in poultry industry products and clinical samples. Veterinary Microbiology, 82(1), 45–53. https://doi.org/10.1016/S0378-1135(01)00350-9

35. Ahaduzzaman, M., Groves, P. J., Walkden-Brown, S. W., Gerber, P. F. (2021). A molecular based method for rapid detection of Salmonella spp. in poultry dust samples. MethodsX, 8, Article 101356. https://doi.org/10.1016/j.mex.2021.101356

36. Siceloff, A. T. (2025). High-Resolution Salmonella Surveil lance in Commercial Broiler Breeder Production. Doctoral dissertation, University of Georgia, USA.

37. Adell, E., Moset, V., Zhao, Y., Jiménez-Belenguer, A., Cerisuelo, A., Cambra-López, M. (2014). Comparative performance of three sampling techniques to detect airborne Sal monella species in poultry farms. Annals of Agricultural and Environmental Medicine, 21(1), 15–24.

38. Holt, P. S., Mitchell, B. W., Gast, R. K. (1998). Airborne horizontal transmission of Salmonella enteritidis in molted laying chickens. Avian Diseases, 42(1), 45–52. https://doi.org/10.2307/1592575

39. Fallschissel, K., Kämpfer, P., Jäckel, U. (2009). Direct detection of Salmonella cells in the air of livestock stables by real time PCR. Annals of Occupational Hygiene, 53(8), 859–868. https://doi.org/10.1093/annhyg/mep060

40. Gast, R. K., Mitchell, B. W., Holt, P. S. (2004). Evaluation of culture media for detecting airborne Salmonella Enteritidis collected with an electrostatic sampling device from the environment of experimentally infected laying hens. Poultry Science, 83(7), 1106–1111. https://doi.org/10.1093/ps/83.7.1106


Review

For citations:


Yushina Yu.K., Bataeva D.S., Semenova A.A., Grudistova M.A., Zaiko E.V., Makhova A.A. Testing of methods for detecting Salmonella in the air of poultry processing plants. Theory and practice of meat processing. 2025;10(4):385-392. https://doi.org/10.21323/2414-438X-2025-10-4-385-392

Views: 19

JATS XML


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2414-438X (Print)
ISSN 2414-441X (Online)