Skip to content
1887

Journal of Medical Microbiology logo Journal of Medical Microbiology

Volume 74, Issue 3

Surveillance of and antimicrobial resistance in industrial poultry enterprises: biofilm-forming strains and critical control points Open Access

Abstract

contamination in the poultry industry poses substantial health risks, especially due to biofilm-forming strains that resist disinfection and antibiotic treatment. Biofilm-forming strains are particularly challenging to control, as they adhere to surfaces in production environments, leading to persistent contamination. This study assesses the prevalence of , examines antibiotic resistance patterns and evaluates biosecurity effectiveness at poultry farms in Kazakhstan.

There is limited data on the prevalence and antibiotic resistance of biofilm-forming strains in Kazakhstan’s poultry industry, highlighting a need to characterize these strains to inform effective control measures.

The purpose of this study was to systematically identify and characterize strains, including biofilm-forming types, within industrial poultry enterprises in Kazakhstan.

A total of 660 samples were collected from various poultry production sites, including feed, water sources, cloacal flushes and shoe covers. detection followed standardized protocols, and antibiotic sensitivity of identified strains was analysed to evaluate resistance patterns.

was detected in 11.5% (95% CI) of the 660 samples, with the highest contamination observed in shoe covers, cloacal flushes, feed and water. This prevalence rate indicates a significant presence of the pathogen in the country’s poultry production chain, falling between the higher rates seen in countries like China (22.2%) and Egypt (29.1%) and the lower rates observed in countries like Brazil (3.4%). The most prevalent strain was (61.8%), followed by (18.4%) and (14.5%). Antibiotic sensitivity analysis revealed that was largely susceptible to common antibiotics, while displayed considerable resistance, emphasizing the need for alternative treatments.

The findings underscore the importance of strict sanitary and hygiene standards throughout poultry production, with a particular focus on managing biofilm-forming strains. Implementing comprehensive Hazard Analysis and Critical Control Points protocols is essential to address contamination hotspots effectively. Future studies should investigate genetic mechanisms underlying biofilm formation and resistance in strains to inform targeted interventions, ultimately improving food safety and public health outcomes.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): food safety , infection , pathogenicity , poultry farm and systematic observation
© 2025 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001993
2025-03-25
2025-12-17

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/jmm/74/3/jmm001993.html?itemId=/content/journal/jmm/10.1099/jmm.0.001993&mimeType=html&fmt=ahah

References

  1. Al-Shafee AAJ, Abdulwahid MT. Occurrence, antimicrobial resistance, and molecular characterization of Salmonella enterica from chicken products and human in Wasit Governorate of Iraq. Open Vet J 2024; 14:1117–1129 [View Article] [PubMed]
     [Google Scholar]
  2. Bureau of National Statistics of the Agency of Strategic Planning and Reforms of the Republic of Kazakhstan Statistics of agriculture, forestry, hunting and fishing economy.
  3. Zhusanbayeva A, Biyashev B, Kirkimbaeva Z, Zhylkaydar A, Valdovska A. Study of antibiotic resistance of Salmonella strains forming biofilm. Scientific Horizons 2024; 27:20–31 [View Article]
     [Google Scholar]
  4. Pyatkovskyy T. Inactivation of microorganisms by high hydrostatic pressure: a literature review. Bull Med Biol Res 2023; 5:53–61 [View Article]
     [Google Scholar]
  5. Liasota V, Bohatko N, Tkachuk S, Bukalova N, Khitska O. Effectiveness of detergents and disinfectants in the production of cow’s milk. Ukr J Vet Sci 2022; 13:25–33 [View Article]
     [Google Scholar]
  6. Abylgazinova AT, Orazov AZh, Stathopoulos C, Nugmanov KS, Zaidullina AS. Assessment of quality and safety indicators of poultry carcasses produced at the enterprises of the West Kazakhstan region. Sci Educ Anim Husb 2023; 2:17–24
     [Google Scholar]
  7. Mendybayeva AM, Aliyeva GK, Chuzhebayeva GD, Tegza AA, Rychshanova RM. Antibiotic resistance of enterobacterial pathogens isolated on the territory of the Northern Kazakhstan. Comp Immunol Microbiol Infect Dis 2022; 87:101854 [View Article] [PubMed]
     [Google Scholar]
  8. Barmak SM, Sinyavskiy YA, Berdygaliev AB, Sharmanov TS, Savitskaya IS et al. Development and evaluation of alternative methods to identify the three most common serotypes of Salmonella enterica causing clinical infections in Kazakhstan. Microorganisms 2021; 9:2319 [View Article] [PubMed]
     [Google Scholar]
  9. Mogilev К, Yeleusizova A, Aisin M, Dyusembekov S. Evaluation of the sanitary and hygienic characteristics of chicken meat and semi-finished products. Glym Zhane Bilim 2023; 1:27–34 [View Article]
     [Google Scholar]
  10. Mussayeva A, Yegorova N, Namet A, Kozhabayev M, Syrym N. Salmonella sheep abortion: distribution, diagnosis, and control measures. J Appl Anim Welfare Sci 2025; 28:29–43 [View Article]
     [Google Scholar]
  11. Interstate Standard GOST R 53665-2009 Poultry meat, edible offal, and poultry meat ready-to-cook. Method for detection of Salmonellae; 2012
  12. Interstate Standard GOST 31659-2012 Poultry meat, edible offal, and poultry meat ready-to-cook. Method for detection of Salmonellae; 2012
  13. Interstate Standard GOST 21237-75 Meat. Methods of bacteriological analysis; 2006
  14. European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes 1986 https://rm.coe.int/168007a67b
  15. Universal Declaration on Animal Welfare 2007 https://web.archive.org/web/20090219033045/http://animalsmatter.org/downloads/UDAW_Text_2005.pdf
  16. Semina NA, Sidorenko SV. Guidelines for susceptibility testing of microorganisms to antibacterial agents. Clin Microbiol Antimicrob Chemother 2004; 6:306–359
     [Google Scholar]
  17. Patel J, Sharma M. Differences in attachment of Salmonella enterica serovars to cabbage and lettuce leaves. Int J Food Microbiol 2010; 139:41–47 [View Article] [PubMed]
     [Google Scholar]
  18. Karabasanavar N, Madhavaprasad C, Gopalakrishna S, Hiremath J, Patil G et al. Prevalence of Salmonella serotypes S. enteritidis and S. typhimurium in poultry and poultry products. J Food Saf 2020; 40: [View Article]
     [Google Scholar]
  19. Ashrafudoulla M, Na KW, Byun K-H, Kim DH, Yoon JW et al. Isolation and characterization of Salmonella spp. from food and food contact surfaces in a chicken processing factory. Poult Sci 2021; 100:101234 [View Article] [PubMed]
     [Google Scholar]
  20. Siddique A, Azim S, Ali A, Andleeb S, Ahsan A et al. Antimicrobial resistance profiling of biofilm forming non typhoidal Salmonella enterica isolates from poultry and its associated food products from Pakistan. Antibiotics 2021; 10:785 [View Article] [PubMed]
     [Google Scholar]
  21. Shahbazi G, Shayegh J, Ghazaei C, Ghazani MHM, Hanifian S. Molecular detection, typing, and virulence potential of Salmonella serotypes isolated from poultry feeds. Pol J Vet Sci 2023; 26:239–247 [View Article] [PubMed]
     [Google Scholar]
  22. Melo N, Silva M, Almeida A, Medeiros A, Silva D et al. Salmonella spp. virulent and resistant multidrug recovered from chicken carcasses in Brazil. Rev Cient Multidisc Núcleo Conhecimento 2023; 1:92–114 [View Article]
     [Google Scholar]
  23. Brasão SC, Melo RT de, Prado RR, Monteiro GP, Santos FAL dos et al. Characterization and control of biofilms of Salmonella Minnesota of poultry origin. Food Biosci 2021; 39:100811 [View Article]
     [Google Scholar]
  24. Obe T, Nannapaneni R, Schilling W, Zhang L, Kiess A. Antimicrobial tolerance, biofilm formation, and molecular characterization of Salmonella isolates from poultry processing equipment. J Appl Poult Res 2021; 30:100195 [View Article]
     [Google Scholar]
  25. Zeng H, De Reu K, Gabriël S, Mattheus W, de Zutter L et al. Salmonella prevalence and persistence in industrialized poultry slaughterhouses. Poult Sci 2021; 100:100991 [View Article] [PubMed]
     [Google Scholar]
  26. Roy PK, Ha AJ-W, Mizan MFR, Hossain MI, Ashrafudoulla M et al. Effects of environmental conditions (temperature, pH, and glucose) on biofilm formation of Salmonella enterica serotype Kentucky and virulence gene expression. Poult Sci 2021; 100:101209 [View Article] [PubMed]
     [Google Scholar]
  27. Shen X, Yin L, Zhang A, Zhao R, Yin D et al. Prevalence and characterization of Salmonella Isolated from Chickens in Anhui, China. Pathogens 2023; 12:465 [View Article] [PubMed]
     [Google Scholar]
  28. Farahani RK, Ebrahimi-Rad M, Shahrokhi N, Khaltabadi Farahani AH, Ghafouri SA et al. High prevalence of antibiotic resistance and biofilm formation in Salmonella gallinarum. Iran J Microbiol 2023; 15:631–641 [View Article]
     [Google Scholar]
  29. Tiwari A, Swamy M, Shrivastav N, Mishra P, Rajput N et al. Occurrence of multi-drug resistant avian Salmonellae in commercial poultry. Indian J Anim Res 2022 [View Article]
     [Google Scholar]
  30. Krüger GI, Pardo-Esté C, Zepeda P, Olivares-Pacheco J, Galleguillos N et al. Mobile genetic elements drive the multidrug resistance and spread of Salmonella serotypes along a poultry meat production line. Front Microbiol 2023; 14:1072793 [View Article] [PubMed]
     [Google Scholar]
  31. Chen W, Xu Z, Li C, Wang C, Wang M et al. Investigation of biofilm formation and the associated genes in multidrug-resistant Salmonella pullorum in China (2018-2022). Front Vet Sci 2023; 10:1248584 [View Article] [PubMed]
     [Google Scholar]
  32. Kamal W, Mahmoud R, Allah AE, Farghali AA, Abdelwahab A et al. Controlling multi-drug-resistant traits of Salmonella obtained from retail poultry shops using metal-organic framework (MOF) as a novel technique. Microorganisms 2023; 11:2506 [View Article] [PubMed]
     [Google Scholar]
  33. Ohashi I, Kobayashi S, Tamamura-Andoh Y, Arai N, Takamatsu D. Disinfectant resistance of Salmonella in in vitro contaminated poultry house models and investigation of efficient disinfection methods using these models. J Vet Med Sci 2022; 84:1633–1644 [View Article] [PubMed]
     [Google Scholar]
  34. Das PK, Mandal A, Rahman MdM, Sarkar SL, Jahid IK et al. Salmonella enterica serovar typhimurium and enteritidis isolated from raw shrimp in Bangladesh: an investigation based on molecular characteristics, survival, virulence, antibiotic resistance, and biofilm formation attributes. J Food Qual 2022; 2022:1–9 [View Article]
     [Google Scholar]
  35. Korzeniowski P, Śliwka P, Kuczkowski M, Mišić D, Milcarz A et al. Bacteriophage cocktail can effectively control Salmonella biofilm in poultry housing. Front Microbiol 2022; 13:901770 [View Article] [PubMed]
     [Google Scholar]
  36. Rakkith NS, Madhavaprasad CB, Bagalakote PS, Arun SJ, Udupa KG et al. Quantification of biofilm forming ability of Salmonella species at different time interval. Int J Curr Microbiol Appl Sci 2023; 12:144–148 [View Article]
     [Google Scholar]
  37. Naz F, Ahmad A, Sarwar Y, Khan MM, Schierack P et al. Characterization of Salmonella enterica biofilms and antibiofilm effect of carvacrol and 2-aminobenzimidazole. Foodborne Pathog Dis 2024; 21:52–60 [View Article] [PubMed]
     [Google Scholar]
  38. Voss-Rech D, Ziech RE, Vaz CSL, Coldebella A, Kuchiishi SS et al. Association between antimicrobial resistance and biofilm forming ability of Salmonella enterica serotypes from commercial broiler farms in Brazil. Br Poult Sci 2023; 64:224–230 [View Article] [PubMed]
     [Google Scholar]
  39. Saeed El-Naggar M, Mohammed Ibrahim H, Mohammed Salem H, Marouf S. A novel locally prepared inactivated bivalent Mycoplasma vaccine for chicken flocks in Egypt. Adv Anim Vet Sci 2021; 10:55–61 [View Article]
     [Google Scholar]
  40. Fotina T, Hunko O, Fotin A, Borkovskyi R, Morozov B. Peculiarities of rearing poultry by floor method on deep bedding. Sci Horiz 2024; 27:9–23 [View Article]
     [Google Scholar]
  41. Sakudo A. Effect of combined infection with Salmonella and influenza virus on their respective proliferation in chicken embryonated eggs. Open Vet J 2024; 14:913–918 [View Article] [PubMed]
     [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001993
Loading
Surveillance of Salmonella and antimicrobial resistance in industrial poultry enterprises: biofilm-forming strains and critical control points
J. Med. Microbiol. 74, 001993 (2025); https://doi.org/10.1099/jmm.0.001993
/content/journal/jmm/10.1099/jmm.0.001993
/content/journal/jmm/10.1099/jmm.0.001993
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error