Public health and sanitation issues related to the bacterium Pseudomonas aeruginosa

Representatives of pseudomonads can be assigned to undesirable microorganisms frequently isolated in the food industry, including the dairy industry. Opportunistic pathogenic bacterium Pseudomonas aeruginosa is of particular importance and its role in contamination of industrial equipment and secondary contamination of finished dairy products is growing steadily. This Gram-negative bacterium is ubiquitous in the nature and is characterized by multifactor resistance to a broad spectrum of antimicrobials and the ability of quickly adapt to changing conditions of the habitat. Being quite an active biofilm former, P. aeruginosa can effectively colonize various surfaces. The ability to grow in a wide temperature range allows the bacterium to multiply directly in milk upon storage in a refrigerator. Entry of P. aeruginosa into enterprises of the food industry leads to economic losses due to food spoilage. Being a cause of a broad spectrum of acute and chronic diseases, P. aeruginosa can present a direct threat to human health when entering the food chains. The present review is devoted to the problems linked to P. aeruginosa contamination in food enterprises as well as methods of identification and control of this bacterium. The authors confirmed the topicality and necessity of the active search for and development of means to counteract P. aeruginosa, which uses multiple mechanisms of stress resistance. The system of prophylactic actions in food industry enterprises should contemplate a possibility of rapid correction of a complex of disinfection measures. To eliminate successfully such a difficult pathogen as P. aeruginosa, combinations of strategies developed with participation of specialists of different areas of expertise are desirable.

1. Atolani, O., Baker, M. T., Adeyemi, O. S., Olanrewaju, I. R., Hamid, A. A., Ameen, O. M. et al. (2020). COVID‑19: Critical discussion on the applications and implications of chemicals in sanitizers and disinfectants. EXCLI Journal, 9,785–799. https://doi.org/10.17179/excli2020-1386

2. Korotkevich, Yu. V. (2016). Antibiotic resistance analysis of Enterococcus spp. and Enterobacteriaceae spp. isolated from food. Problems of Nutrition, 85(2), 5–13. (In Russian) https://doi.org/10.24411/0042-8833-2016-00018

3. Sheveleva, S. A. (2018). Antimicrobial-resistant microorganisms in food as a hygienic problem. Hygiene and Sanitation, 97(4), 342–354. (In Russian) https://doi.org/10.47470/0016-9900-2018-97-4-342-354

4. Nezhvinskaya, O. E., Dudchik, N. V. (2015). Biofilm forming bacteria from food production. Modern Problems of Hygiene, Radiation and Ecological Medicine, 5, 188–194. (In Russian)

5. Téllez, S. (2010). Biofilms and their impact on food industry. VISAVET Outreach Journal. Retrieved from https://www.visavet.es/en/articles/biofilms-impactfood-industry.php Accessed July 11, 2024.

6. Banda, R., Nduko, J., Matofari, J. (2020). Bacterial biofilm formation in milking equipments in Lilongwe, Malawi. Journal of Food Quality and Hazards Control, 7, 142–148.

7. Quintieri, L., Fanelli, F., Caputo, L. (2019). Antibiotic resistant Pseudomonas spp. spoilers in fresh dairy products: An underestimated risk and the control strategies. Foods, 8(9), Article 372. https://doi.org/10.3390/foods8090372

8. Al-Shammary, A. H. A. (2015). The effect of heat treatment, pH and osmotic pressure on viability of Pseudomonas aeruginosa isolated from raw dairy products in Baghdad. International Journal of Advanced Research, 3(3), 675–681.

9. Langsrud, S., Sundheim, G., Borgmann-Strahsen, R. (2003). Intrinsic and acquired resistance to quaternary ammonium compounds in food-related Pseudomonas spp. Journal of Applied Microbiology, 95(4), 874–882. https://doi.org/10.1046/j.1365-2672.2003.02064.x

10. Rowbury R. J. (2005). Stress responses of foodborne pathogens, with specific reference to the switching on of such responses. Chapter in a book: Foodborne Pathogens: Microbiology and Molecular Biology. Caister Academic Press, U.K., 2005.

11. Stintzi, A. (2003). Gene expression profile of Campylobacter jejuni in response to growth temperature variation. Journal of Bacteriology, 185(6), 2009–2016. https://doi.org/10.1128/jb.185.6.2009-2016.2003

12. Efimochkina, N. R. (2013). Microbiology of food products and modern methods of pathogen detection. Moscow. Russian Academy of Medical Sciences, 2013. (In Russian)

13. Oliver, J. D. (2005). The viable but nonculturable state in bacteria. Journal of Microbiology, 43(Spec), 93–100.

14. Schauer, B., Wald, R., Urbantke, V., Loncaric, I., Baumgartner, M. (2021). Tracing mastitis pathogens — epidemiological investigations of a Pseudomonas aeruginosa mastitis outbreak in an Austrian dairy herd. Animals, 11(2), Article 279. https://doi.org/10.3390/ani11020279

15. Mahmoud, S. F., Fayez, M., Swelum, A. A., Alswat, A. S., Alkafafy, M., Alzahrani, O. M. et al. (2022). Genetic Diversity, Biofilm formation, and antibiotic resistance of Pseudomonas aeruginosa isolated from cow, camel, and mare with clinical endometritis. Veterinary Sciences, 9(5), Article 239. https://doi.org/10.3390/vetsci9050239

16. Badawy, B., Moustafa, S., Shata, R., Sayed-Ahmed, M. Z., Alqahtani, S. S., Ali, M. S. et al. (2023). Prevalence of multidrug-resistant Pseudomonas aeruginosa isolated from dairy cattle, milk, environment, and workers’ hands. Microorganisms, 11(11), Article 2775. https://doi.org/10.3390/microorganisms11112775

17. Eneroth, Å., Ahrné, S., Molin, G. (2000). Contamination of milk with Gramnegative spoilage bacteria during filling of retail containers. International Journal of Food Microbiology, 57(1–2), 99–106. https://doi.org/10.1016/S0168-1605(00)00239-7

18. Meesilp, N., Mesil, N. (2019). Effect of microbial sanitizers for reducing biofilm formation of Staphylococcus aureus and Pseudomonas aeruginosa on stainless steel by cultivation with UHT milk. Food Science and Biotechnology, 28(1), 289–296. https://doi.org/10.1007/s10068-018-0448-4

19. Marchand, S., De Block, J., De Jonghe, V., Coorevits, A., Heyndrickx, M., Herman, L. (2012). Biofilm formation in milk production and processing environments; influence on milk quality and safety. Comprehensive Reviews in Food Science and Food Safety, 11(2), 133–147. https://doi.org/10.1111/j.1541-4337.2011.00183.x

20. Beena, A. K., Ranjini, A. R., Riya, T. G. (2011). Isolation of psychrotrophic multiple drug resistant Pseudomonas from pasteurised milk. Veterinary World, 4(8), 349–352. https://doi.org/10.5455/vetworld.2011.349-352

21. Martin, N. H., Boor, K. J., Wiedmann, M. (2018). Symposium review: Effect of post-pasteurization contamination on fluid milk quality. Journal of Dairy Science, 101(1), 861–870. https://doi.org/10.3168/jds.2017-13339

22. Trmčić, A., Martin, N. H., Boor, K. J., Wiedmann, M. (2015). A standard bacterial isolate set for research on contemporary dairy spoilage. Journal of Dairy Science, 98(8), 5806–5817. https://doi.org/10.3168/jds.2015-9490

23. Brown, A. G., Luke, R. K. J. (2010). Siderophore production and utilization by milk spoilage Pseudomonas species. Journal of Dairy Science, 93(4), 1355–1363. https://doi.org/10.3168/jds.2009-2395

24. Lazareva, A.V., Chebotar, I. V., Kryzhanovskaya, O. A., Chebotar, V. I., Mayansky, N. A. (2015). Pseudomonas aeruginosa: Pathogenicity, pathogenesis and diseases. Clinical Microbiology and Antimicrobial Chemotherapy, 17(3), 170–186. (In Russian)

25. Pang, Z., Raudonis, R., Glick, B. R., Lin, T.-J., Cheng, Z. (2019). Antibiotic resistance in Pseudomonas aeruginosa: Mechanisms and alternative therapeutic strategies. Biotechnology Advances, 37(1), 177–192. https://doi.org/10.1016/j.biotechadv.2018.11.013

26. Shepelin, A. P., Sergeeva, A. B., Polosenko, O. V. (2017). Determination of nutrient medium specific activity for Pseudomonas aeruginosa. Bacteriology, 2(1), 54–60. (In Russian)

27. Egorova, O. N., Brusina, E. B., Grigoriev, E. V. (2014). Epidemiology and prevention of Pseudomonas aeruginosa infection. Federal clinical recommendations. National Association of Specialists for the Control of Healthcare-Associated Infections. Moscow, 2014 (In Russian)

28. Visca, P., Imperi, F., Lamont, I. L. (2007). Pyoverdine siderophores: From biogenesis to biosignificance. Trends in Microbiology, 15(1), 22–30. https://doi.org/10.1016/j.tim.2006.11.004

29. Chebotar, I. V., Bocharova, Yu. A., Mayansky, N. A. (2017). Mechanisms and regulation of antimicrobial resistance in Pseudomonas aeruginosa. Clinical Microbiology and Antimicrobial Chemotherapy, 19(4), 308–319. (In Russian)

30. Pyzh, A. E., Nikandrov, V. N. (2011). Contribution of blue-green pigments to hemolytic activity of Pseudomonas aeruginosa cultural fluid. Journal of Microbiology, Epidemiology and Immunobiology, 1, 19–25. (In Russian)

31. Rossi, C., Serio, A., Chaves-López, C., Anniballi, F., Auricchio, B., Goffredo, E. et al. (2018). Biofilm formation, pigment production and motility in Pseudomonas spp. isolated from the dairy industry. Food Control, 86, 241–248. https:/doi.org/10.1016/j.foodcont.2017.11.018

32. Shestakov, A. G. (2010). Improving methods for isolation, identification and indication of bacteria Pseudomonas aeruginosa. Author’s abstract of the dissertation for the scientific degree of Candidate of Biological Sciences. Saratov State Agrarian University named after N. I. Vavilov. Saratov, 2010. (In Russian)

33. Quintieri, L., Zühlke, D., Fanelli, F., Caputo, L., Liuzzi, V. C., Logrieco, A. F. et al. (2019). Proteomic analysis of the food spoiler Pseudomonas fluorescens ITEM 17298 reveals the antibiofilm activity of the pepsin-digested bovine lactoferrin. Food Microbiology, 82, 177–193. https://doi.org/10.1016/j.fm.2019.02.003

34. Cornelis, P., Dingemans, J., Baysse, C. (2023). Pseudomonas aeruginosa Soluble Pyocins as Antibacterial Weapons. Chapter in a book: Pseudomonas aeruginosa. Methods in Molecular Biology Humana, New York, NY, 2023. https://doi.org/10.1007/978-1-0716-3473-8_9

35. Michel-Briand, Y., Baysse, C. (2002). The pyocins of Pseudomonas aeruginosa. Biochimie, 84(5–6), 499–510. https://doi.org/10.1016/S0300-9084(02)01422-0

36. MacDonald, I. A., Kuehn, M. J. (2013). Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. Journal of Bacteriology, 195(13), 2971–2981. https://doi.org/10.1128/jb.02267-12

37. Fominykh, S. G. (2011). Wound infections: A role of microbiological monitoring for the hospital antimicrobial policy. Clinical Microbiology and Antimicrobial Chemotherapy, 13(4), 368–375. (In Russian)

38. Andreeva, S. V., Bachareva, L. I., Nochrin, D. Yu. (2013). Species composition of microflora of burn wounds of the patients of the Chelyabinsk regional burn center. Bulletin of Chelyabinsk State University, 7(298), 58–59. (In Russian)

39. Mansoor, T., Musani, M. A., Khalid, G., Kamal, M. (2009). Pseudomonas aeruginosa in chronic suppurative otitis media: Sensitivity spectrum against various antibiotics in Karachi. Journal of Ayub Medical College, Abbottabad, 21(2), 120–123.

40. Mittal, R., Aggarwal, S., Sharma, S., Chhibber, S., Harjai, K. (2009). Urinary tract infections caused by Pseudomonas aeruginosa: A minireview. Journal of Infection and Public Health, 2(3), 101–111. https://doi.org/10.1016/j.jiph.2009.08.003

41. Yu, Y., Cheng, A. S., Wang, L., Dunne, W. M., Bayliss, S. J. (2007). Hot tub folliculitis or hot hand–foot syndrome caused by Pseudomonas aeruginosa. Journal of the American Academy of Dermatology, 57(4), 596–600. https://doi.org/10.1016/j.jaad.2007.04.004

42. Calhoun, J. H., Murray, C. K., Manring, M. M. (2008). Multidrug-resistant organisms in military wounds from Iraq and Afghanistan. Clinical Orthopaedics and Related Research, 466(6), 1356–1362. https://doi.org/10.1007/s11999-008-0212-9

43. Sato, H., Frank, D. W. (2004). ExoU is a potent intracellular phospholipase. Molecular Microbiology, 53(5), 1279–1290. https://doi.org/10.1111/j.1365-2958.2004.04194.x

44. Morlon-Guyot, J., Méré, J., Bonhoure, A., Beaumelle, B. (2009). Processing of Pseudomonas aeruginosa exotoxin A is dispensable for cell intoxication. Infection and Immunity, 77(7), 3090–3099. https://doi.org/10.1128/IAI.01390-08

45. Tacconelli, E. (2017). Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development, Infection Control Africa Network. South Africa. Retrieved from https://coilink.org/20.500.12592/khnnff Accessed July 15, 2024.

46. Pirnay, J. P., Matthijs, S., Colak, H., Chablain, P., Bilocq, F., Van Eldere, J. et al (2005). Global Pseudomonas aeruginosa biodiversity as reflected in a Belgian river. Environmental Microbiology, 7(7), 969–980. https://doi.org/10.1111/j.1462-2920.2005.00776.x

47. Crone, S., Vives-Flórez, M., Kvich, L., Saunders, A. M., Malone, M., Nicolaisen, M. H. et al. (2020). The environmental occurrence of Pseudomonas aeruginosa. APMIS, 128(3), 220–231. https://doi.org/10.1111/apm.13010

48. Custovic, A., Smajlovic, J., Hadzic, S., Ahmetagic, S., Tihic, N., Hadzagic, H. (2014). Epidemiological surveillance of bacterial nosocomial infections in the surgical intensive care unit. Materia Socio Medica, 26(1), 7–11. https://doi.org/10.5455/msm.2014.26.7-11

49. Breidenstein, E. B. M., de la Fuente-Núñez, C., Hancock, R. E. W. (2011). Pseudomonas aeruginosa: All roads lead to resistance. Trends in Microbiology, 19(8), 419–426. https://doi.org/10.1016/j.tim.2011.04.005

50. Nemchenko, U. M., Sitnikova, K. O., Belkova, N. L., Grigorova, E. V., Voropaeva, N. M., Sukhoreva, M. V. et al. (2022) Effects of аntimicrobials on Pseudomonas aeruginosabiofilm formation. Vavilov Journal of Genetics and Breeding, 26(5), 495–501. (In Russian) https://doi.org/10.18699/VJGB‑22–60

51. Edelstein, M. V., Shek, E. A., Sukhorukova, M. V., Skleenova, E. Yu., Ivanchik, N. V., Shajdullina, E. R. et al. (2019). Antimicrobial resistance, carbapenemase production, and genotypes of nosocomial Pseudomonas aeruginosa isolates in Russia: Results of multicenter epidemiological study “Marathon 2015–2016”. Clinical Microbiology and Antimicrobial Chemotherapy, 21(2), 160–170. (In Russian)

52. Tkacheva, T. S., Gataullina, E. F., Bibartseva, E. V. (January 26–27, 2022). Mechanisms of resistance of Pseudomonas aeruginosa to antibiotics. Proceedings of the All-Russian scientific-methodological conference: University complex as a regional center of education, science and culture. Orenburg, 2022. (In Russian)

53. Maciá, M. D., Blanquer, D., Togores, B., Sauleda, J., Pérez, J. L., Oliver, A. (2005). Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrobial Agents and Chemotherapy, 49(8), 3382–3386. https://doi.org/10.1128/aac.49.8.3382-3386.2005

54. Koza, N. M. (2013). Infections connected with rendering medical care. epidemiology and prevention (review lecture). Perm Medical Journal, 30(4), 135–143. (In Russian)

55. Tutelyan, A. V., Yushina, Yu. K., Sokolova, O. V., Bataeva, D. S., Fesyun, A. D., Datiy, A. V. (2019). Formation of biological films by microororganisms in food productions. Problems of Nutrition, 88(3), 32–43. (In Russian) https://doi.org/10.24411/0042-8833-2019-10027

56. Magiorakos, A. P., Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G. et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrugresistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18(3), 268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x

57. Bengtsson-Palme, J., Kristiansson, E., Larsson, D. G. J. (2018). Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiology Reviews, 42(1), Article fux053. https://doi.org/10.1093/femsre/fux053

58. Fernandes, P., Martens, E. (2017). Antibiotics in late clinical development. Biochemical Pharmacology, 133, 152–163. https://doi.org/10.1016/j.bcp.2016.09.025

59. Yaita, K., Sameshima, I., Takeyama, H., Matsuyama, S., Nagahara, C., Hashiguchi, R. et al (2013). Liver abscess caused by multidrug-resistant Pseudomonas aeruginosa treated with colistin; a case report and review of the literature. Internal Medicine, 52(12), 1407–1412. https://doi.org/10.2169/internalmedicine.52.9296

60. Afonyushkin, V. N., Donchenko, N. A., Kozlova, Ju. N., Davidova, N. V., Koptev, V. Yu. Cherepushkina, V. S. (2020). Questions on the role of biofilms for the adaptation of microorganisms to unfavorable environmental factors by the example of P. aeruginosa. Hygiene and Sanitation, 99(4), 379–383. (In Russian) https://doi.org/10.47470/0016-9900-2020-99-4-379-383

61. Hall, J. P., Brockhurst, M. A., Harrison, E. (2017). Sampling the mobile gene pool: Innovation via horizontal gene transfer in bacteria. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1735), Article 20160424. https://doi.org/10.1098/rstb.2016.0424

62. Heir, E., Moen, B., Åsli, A. W., Sunde, M., Langsrud, S. (2021). Antibiotic resistance and phylogeny of Pseudomonas spp. isolated over three decades from chicken meat in the Norwegian food chain. Microorganisms, 9(2), Article 207. https://doi.org/10.3390/microorganisms9020207

63. Lerma, L., Benomar, N., Casado Muñoz, M. del C., Gálvez, A., Abriouel, H. (2014). Antibiotic multiresistance analysis of mesophilic and psychrotrophic Pseudomonas spp. isolated from goat and lamb slaughterhouse surfaces throughout the meat production process. Applied and Environmental Microbiology, 80(21), 6792–6806. https://doi.org/10.1128/aem.01998-14

64. Verraes, C., Van Boxstael, S., Van Meervenne, E., Van Coillie, E., Butaye, P., Catry, B. et al. (2013). Antimicrobial resistance in the food chain: A review. International Journal of Environmental Research and Public Health, 10(7), 2643–2669. https://doi.org/10.3390/ijerph10072643

65. Frieri, M., Kumar, K., Boutin, A. (2017). Antibiotic resistance. Journal of Infection and Public Health, 10(4), 369–378. https://doi.org/10.1016/j.jiph.2016.08.007

66. Gabrielyan, N. I., Gorskaya, E. M., Romanova, N. I., Tsirulnikova, O. M. (2014). Nosocomial infection and microbial biofilms in surgery. Russian Journal of Transplantation and Artificial Organs, 14(3), 83–91. (In Russian)

67. Monroe, D. (2007). Looking for chinks in the armor of bacterial biofilms. PLoS Biology, 5(11), Article e307. https://doi.org/10.1128/iai.01390-08

68. Mayansky, A. N., Chebotar, I. V., Rudneva, E. I., Chistyakova, V. P. (2012). Pseudomonas aeruginosa: Characteristics of the biofilm process. Molecular Genetics, Microbiology and Virology, 27(1), 1–6. https://doi.org/10.3103/S0891416812010053

69. Ghafoor, A., Hay, I. D., Rehm, B. H. A. (2011). Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Applied and Environmental Microbiology, 77(15), 5238–5246. https://doi.org/10.1128/AEM.00637-11

70. Coughlan, L. M., Cotter, P. D., Hill, C., Alvarez-Ordóñez, A. (2016). New weapons to fight old enemies: Novel strategies for the (bio) control of bacterial biofilms in the food industry. Frontiers in Microbiology, 7, Article 1641. https://doi.org/10.3389/fmicb.2016.01641

71. Okulich, V. K., Kabanova, A. A., Plotnikov, F. V. (2017). Microbial biofilms in clinical microbiology and antibacterial therapy. Vitebsk: VSMU, 2017. (In Russian)

72. Hentzer, M., Teitzel, G. M., Balzer, G. J., Heydorn, A., Molin, S., Givskov, M. et al. (2001). Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. Journal of Bacteriology, 183(18), 5395–5401. https://doi.org/10.1128/JB.183.18.5395-5401.2001

73. Nikolaev, Y. A., Plakunov, V. K. (2007). Biofilm — “City of microbes” or an analogue of multicellular organisms? Microbiology 76, 125–138. https://doi.org/10.1134/S0026261707020014

74. Echeverz, M., García, B., Sabalza, A., Valle, J., Gabaldón, T., Solano, C. et al. (2017). Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host. PLoS Genetics, 13(5), Article e1006816. https://doi.org/10.1371/journal.pgen.1006816

75. Akinbobola, A. B., Sherry, L., Mckay, W. G., Ramage, G., Williams, C. (2017). Tolerance of Pseudomonas aeruginosa in in-vitro biofilms to high-level peracetic acid disinfection. Journal of Hospital Infection, 97(2), 162–168. https://doi.org/10.1016/j.jhin.2017.06.024

76. Billings, N., Ramirez Millan, M., Caldara, M., Rusconi, R., Tarasova, Y., Stocker, R. et al. (2013). The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathogens, 9(8), Article e1003526. https://doi.org/10.1371/journal.ppat.1003526

77. Ma, L., Conover, M., Lu, H., Parsek, M. R., Bayles, K., Wozniak, D. J. (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathogens, 5(3), Article e1000354. https://doi.org/10.1371/journal.ppat.1000354

78. Irie, Y., Borlee, B. R., O’Connor, J. R., Hill, P. J., Harwood, C. S., Wozniak, D. J. et al. (2012). Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, 109(50), 20632–20636. https://doi.org/10.1073/pnas.1217993109

79. Jennings, L. K., Storek, K. M., Ledvina, H. E., Coulon, C., Marmont, L. S., Sadovskaya, I. et al. (2015). Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proceedings of the National Academy of Sciences, 112(36), 11353–11358. https://doi.org/10.1073/pnas.1503058112

80. Bjarnsholt, T., Ciofu, O., Molin, S., Givskov, M., Høiby, N. (2013). Applying insights from biofilm biology to drug development — can a new approach be developed? Nature Reviews Drug Discovery, 12(10), 791–808. https://doi.org/10.1038/nrd4000

81. Derevenshchikova, M. I., Syromyatnikov, M. Yu., Popov, V. N. (2018). The use of molecular genetic methods for microbiological control of food products. Food Processing: Techniques and Technology, 48(4), 87–113. (In Russian) http://doi.org/10.21603/2074-9414-2018-4-87-113

82. Al-Ahmadi, G. J., Roodsari, R. Z. (2016). Fast and specific detection of Pseudomonas аeruginosa from other pseudomonas species by PCR. Annals of Burns and Fire Disasters, 29(4), 264–267.

83. Kuznetsova, M. V., Pavlova, Yu. A., Karpunina, T. I., Demakov, V. A. (2013). The experience of applying techniques of molecular genetics in identification of clinical strains Pseudomonas aeruginosa. Clinical Laboratory Diagnostics, 3, 34–37. (In Russian)

84. Cherepushkina, V. S., Mironova, T. E., Afonyushkin, V. N., Lukanina, S. A., Bobikova, A. S., Kozlova, Yu. N. (2021). Development of PCR in real-time mode for detection of P. aeruginosa in biofilm. Veterinarny Vrach, 5, 64–72. (In Russian)

85. Kuznetsov, A. L., Puchkova, A. S., Knyazev E. Y., Suvorov O. A. (2023). Formation of biosafety and greening of the production environment of food production with application of anolyte. FOOD METAENGINEERING, 1(2), 11–20. (In Russian) https://doi.org/10.37442/fme.2023.2.8

86. Cappello, S., Guglielmino, S. P. P. (2006). Effects of growth temperature on polystyrene adhesion of Pseudomonas aeruginosa ATCC2785. Brazilian Journal of Microbiology, 37(3), 205–207. https://doi.org/10.1590/S1517-83822006000300001

87. Vandervoort, K. G., Brelles-Marino, G. (2014). Plasma-mediated inactivation of Pseudomonas aeruginosa biofilms grown on borosilicate surfaces under continuous culture system. PLoS One, 9(10), Article e108512. https://doi.org/10.1371/journal.pone.0108512

88. Lacivita, V., Conte, A., Lyng, J. G., Arroyo, C., Zambrini, V. A., Del Nobile, M. A. (2018). High intensity light pulses to reduce microbial load in fresh cheese. Journal of Dairy Research, 85(2), 232–237. https://doi.org/10.1017/s0022029918000134

89. Lacivita, V., Conte, A., Musavian, H. S., Krebs, N. H., Zambrini, V. A., Del Nobile, M. A. (2018). Steam-ultrasound combined treatment: A promising technology to significantly control mozzarella cheese quality. LWT, 93, 450–455. http:// doi.org/10.1016/j.lwt.2018.03.062

90. Lacivita, V., Mentana, A., Centonze, D., Chiaravalle, E., Zambrini, V. A., Conte, A. et al (2019). Study of X-Ray irradiation applied to fresh dairy cheese. LWT, 103, 186–191. https://doi.org/10.1016/J.LWT.2018.12.073

91. Brackman, G., Coenye, T. (2015). Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design, 21(1), 5–11. https://doi.org/10.2174/1381612820666140905114627

92. Donlan, R. M. (2009). Preventing biofilms of clinically relevant organisms using bacteriophage. Trends in Microbiology, 17(2), 66–72. https://doi.org/10.1016/j.tim.2008.11.002

93. Chan, B. K., Sistrom, M., Wertz, J. E., Kortright, K. E., Narayan, D., Turner, P. E. (2016). Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Scientific Reports, 6(1), Article 26717. https://doi.org/10.1038/srep26717

94. Costa, M. J., Pastrana, L. M., Teixeira, J. A., Sillankorva, S. M., Cerqueira, M. A. (2023). Bacteriophage delivery systems for food applications: Opportunities and perspectives. Viruses, 15(6), Article 1271. https://doi.org/10.3390/v15061271

95. Sukhina, M. A., Shelygin, Yu. A., Zhukhovitsky, V. G., Frolov, S. A., Kashnikov, V. N., Veselov, A. V. et al. (2018). Prospects of using antagonistic activity of lactobacilli to suppress the growth of Clostridium (Clostridioides) difficile. Experimental and Clinical Gastroenterology, 12, 19–24. (In Russian)

96. Ait Ouali, F., Al Kassaa, I., Cudennec, B., Abdallah, M., Bendali, F., Sadoun, D. et al. (2014). Identification of lactobacilli with inhibitory effect on biofilm formation by pathogenic bacteria on stainless steel surfaces. International Journal of Food Microbiology, 191, 116–124. https://doi.org/10.1016/j.ijfoodmicro.2014.09.011

97. Fedorova, T. V., Vasina, D. V., Begunova, A. V., Rozhkova, I. V., Raskoshnaya, T. A., Gabrielyan, N. I. (2018). Antagonistic activity of lactic acid bacteria Lactobacillus spp. against clinical isolates of Klebsiella pneumoniae. Applied Biochemistry and Microbiology, 54, 277–287. https://doi.org/10.1134/S0003683818030043

98. Savinova, O. S., Glazunova, O. A., Moiseenko, K. V., Begunova, A. V., Rozhkova, I. V., Fedorova, T. V. (2021). Exoproteome analysis of antagonistic interactions between the probiotic bacteria Limosilactobacillus reuteri LR1 and Lacticaseibacillus rhamnosus F and multidrug resistant strain of Klebsiella pneumonia. International Journal of Molecular Sciences, 22(20), Article 10999. https://doi.org/10.3390/ijms222010999

99. Kishilova, S. A., Kolokolova, A. Yu., Rozhkova, I. V. (2024). Antimicrobial activity of metabolite complexes of lactobacillus against Pseudomonas aeruginosa. Biophysics, 69(2), 324–332. (In Russian) https://doi.org/10.31857/S0006302924020141

100. Lewies, A., Du Plessis, L. H., Wentzel, J. F. (2019). Antimicrobial peptides: The Achilles’ heel of antibiotic resistance? Probiotics and Antimicrobial Proteins, 11(2), 370–381. https://doi.org/10.1007/s12602-018-9465-0

101. Beaudoin, T., Stone, T. A., Glibowicka, M., Adams, C., Yau, Y., Ahmadi, S. et al. (2018). Activity of a novel antimicrobial peptide against Pseudomonas aeruginosa biofilms. Scientific Reports, 8(1), Article 14728. https://doi.org/10.1038/s41598-018-33016-7

102. Moussouni, M., Nogaret, P., Garai, P., Ize, B., Vivès, E., Blanc-Potard, A. B. (2019). Activity of a synthetic peptide targeting MgtC on Pseudomonas aeruginosa intramacrophage survival and biofilm formation. Frontiers in Cellular and Infection Microbiology, 9, Article 84. https://doi.org/10.3389/fcimb.2019.00084

103. Chapter in a book: Advances in applied microbiology Academic Press, 2018.

104. Tutelyan, A. V., Romanova, Yu. M., Manevich, B. V., Yushina, Yu. K., Fedorova, L. S., Sinitsyna, O. A. et al. (2020). Methods of combating biological films in food production. Название по данным журнала: Biofilm control methods in food production. Dairy Industry, 11, 48–53. (In Russian)

105. Kong, H., Jang, J. (2008). Synthesis and antimicrobial properties of novel silver/ polyrhodanine nanofibers. Biomacromolecules, 9(10), 2677–2681. https://doi.org/10.1021/bm800574x

106. Dima, C., Dima, S. (2015). Essential oils in foods: Extraction, stabilization, and toxicity. Current Opinion in Food Science, 5, 29–35. https://doi.org/10.1016/j.cofs.2015.07.003

107. Myszka, K., Schmidt, M. T., Majcher, M., Juzwa, W., Olkowicz, M., Czaczyk, K. (2016). Inhibition of quorum sensing-related biofilm of Pseudomonas fluorescens KM121 by Thymus vulgare essential oil and its major bioactive compounds. International Biodeterioration and Biodegradation, 114, 252–259. https://doi.org/10.1016/j.ibiod.2016.07.006

108. Bai A, J., Rai Vittal, R. (2014). Quorum sensing regulation and inhibition of exoenzyme production and biofilm formation in the food spoilage bacteria Pseudomonas psychrophila PSPF19. Food Biotechnology, 28(4), 293–308. https://doi.org/10.1080/08905436.2014.963601