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Yushina Yu.K., Makhova A.A., Zaiko E.V., Semenova A.A., Bataeva D.S., Nekrasov R.V. Seasonal patterns and antibiotic resistance of pathogenic microorganisms at a poultry processing plant. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2025, Vol. 60, № 4, p. 739-755.
(how to cite this article)

doi: 10.15389/agrobiology.2025.4.739eng

UDC: 619:614.36:579.63

 

SEASONAL PATTERNS AND ANTIBIOTIC RESISTANCE OF PATHOGENIC MICROORGANISMS AT A POULTRY PROCESSING PLANT

Yu.K. Yushina^{1 ✉}, A.A. Makhova¹, E.V. Zaiko¹,
A.A. Semenova¹, D.S. Bataeva¹, R.V. Nekrasov²

¹V.M. Gorbatov Federal Center for Food Systems RAS, 26, ul. Talalikhina, Moscow,109316 Russia, e-mail a.semenova@fncps.ru, labsens@mail.ru, v.pchelkina@fncps.ru, v.nasonova@fncps.ru, spbsl21@gmail.com;
²Ernst Federal Research Center for Animal Husbandry, 60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail nek_roman@mail.ru (✉ corresponding author), 652202@mail.ru

ORCID:
Yushina Yu.K. orcid.org/0000-0001-9265-5511
Semenova A.A. orcid.org/0000-0002-4372-6448
Makhova A.A. orcid.org/0000-0002-2508-2888
Bataeva D.S. orcid.org/0000-0002-1374-2746
Zaiko E.V. orcid.org/0000-0002-5048-9321
Nekrasov R.V. orcid.org/0000-0003-4242-2239

Final revision received December 04, 2024
Accepted April 04, 2025

Due to the steady growth of the Russian poultry industry, the problem of microbiological safety of products is of exceptional importance Special control is required for the pathogens Salmonella spp., Campylobacter spp. and Listeria monocytogenes, which can cause food poisoning, while cross-contamination from poultry processing facilities is a key risk for the release of dangerous products. The danger is increased by the transmission of antibiotic-resistant pathogens in the production environment. This study is the first to establish the seasonal and zonal specificity of pathogenic microorganism contamination on abiotic surfaces within a poultry processing facility. It detected the highest probability of detecting Campylobacter spp., Salmonella spp., and Listeria monocytogenes in both the dirty and clean zones of the plant during the summer and shoulder seasons, the dominance of Campylobacter jejuni among the pathogens (83 % of cases). Their localization was identified on equipment in the slaughter and cooling zones. A statistically significant reduction total number of mesophilic aerobic and facultative anaerobic microorganisms (Total Viable Count, TVC) was demonstrated only in the clean zone compared to the dirty and intermediate zones. A seasonal imbalance was shown: maximum TVC values were recorded during the shoulder season, while the peak detection of pathogens occurred in summer. The aim of the work was to study the total number of mesophilic aerobic and facultative anaerobic microorganisms on abiotic objects in the production environment depending on the season and to identify pathogenic microorganisms sensitive to antibiotics. Samples at the poultry processing plant (Moscow Province) were collected at different times of the year: summer (end of August 2021), winter (end of February 2021), and the shoulder season, autumn (end of September 2020). The research methodology involved collecting 72 swabs in the middle of the work shift from 12 abiotic surfaces not in contact with the product, located in the dirty, intermediate, and clean zones. Pathogen detection was carried out using loop-mediated isothermal amplification (LAMP) on a 3M MDS device (3M, USA) followed by microbiological confirmation of positive results in accordance with GOST. The sensitivity of the isolated isolates to antimicrobial drugs was determined by the disk diffusion method according to CLSI and EUCAST recommendations. Quantitative accounting of TVC/APC was performed by plating on PCA agar with incubation at 30 °C for 72 hours. Given the non-normal distribution of the obtained data (d = 0.47 > d* = 0.20, Smirnov-Kolmogorov test), statistical analysis was performed using non-parametric methods: two-factor rank analysis of variance and Duncan's test for multiple comparisons at a significance level of a = 0.1. As a result of the study, the seasonally-dependent and zone-specific nature of contamination was established for the first time. The probability of detecting at least one pathogen was 33 %, distributed as 42 % (dirty zone), 17 % (intermediate zone), and 42 % (clean zone) along the production process, and depending on seasonality — 50 % (summer), 42 % (shoulder season), and 8 % (winter). The probability of detecting at least one pathogen was 33%, while during the production process it was distributed as 42 % (dirty zone), 17 % (intermediate zone) and 42 % (clean zone), and depending on the seasonality — 50 % (summer), 42 % (off-season) and 8 % (winter). The ranking of pathogens by probability of detection showed the dominance of Campylobacter spp. (17 %), followed by Listeria monocytogenes (14 %) and Salmonella spp. (11 %). Campylobacter jejuni was mainly detected in the slaughter and primary treatment area. Salmonella spp. were found in all zones, including the clean one, and Listeria monocytogenes was concentrated in the finishing and packaging zone. All Salmonella spp. strains exhibited resistance to nalidixic acid; a number of strains also showed resistance to co-trimoxazole, moxifloxacin, sulfamethoxazole, and tetracycline. An atypical resistance profile was identified in the Salmonella strain S_1 which showed selective resistance to moxifloxacin while remaining susceptible to other fluoroquinolones, which may be associated with accumulated mutations in genes or plasmids. Analysis of the antibiotic susceptibility of Listeria monocytogenes revealed limited resistance, manifested mainly to ceftazidime and tetracycline. One of the five strains was susceptible to all antimicrobials, and multidrug-resistant phenotypes were not detected. Strains of the genus Campylobacterexhibited resistance to ciprofloxacin, erythromycin, and tetracycline. Some of the studied isolates were identified as multidrug-resistant. When evaluating the TVC, a statistically significant decrease was shown only in the clean zone — (4.16±2.27)×10⁴ CFU/cm² vs dirty (5.23±1.95)×10⁶ CFU/cm² and intermediate (8.88±5.74)×10⁵ CFU/cm² zones (p < 0.05), while contamination of dirty and intermediate the zones did not differ significantly. The maximum TVC values (1.07±0.47)×10⁶ CFU/cm² were recorded during the shoulder season. Thus, the results obtained comprehensively characterize the abiotic surfaces of poultry processing plants as hidden reservoirs of pathogens and antibiotic-resistant strains demonstrating complex seasonal and zonal dynamics. The identified high probability of clean zone contamination, the circulation of multidrug-resistant isolates and seasonal risk peaks indicate the need to revise existing approaches to sanitary and microbiological control, develop preventive strategies based on regular monitoring of pathogens directly during production, and tighten measures to limit the use of antibiotics in poultry farming to ensure the biosafety of poultry production.

Keywords: swabs, Salmonella spp., Campylobacter spp., Listeria monocytogenes, total aerobic microbial count, TAMC, antibiotic resistance.

 

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