Prevalence of chlorquinolone- and cephalosporin-resistant Escherichia coli in fish and fish products in Ukraine
Abstract
The article is related to food safety within the framework of the One Health concept. The research results presented in the article were aimed at showing the level of prevalence of fluoroquinolone-resistant Escherichia coli strains and strains with acquired resistance to beta-lactams and carbapenems in fish and fish products of fish processing enterprises in Ukraine. 45 strains of E. coli strains were isolated from samples of common perch ( Perca fluviatilis ), mackerel ( Scomber) , silver carp ( Hypophthalmicht hy s molitrix ), marble trout ( Salmo marmora t us ), gilthead bream ( Sparus aurata ) , crucian carp ( Cara s sius cara s sius ), common carp ( Cyprinus carpio ), herring ( Clupea sp. ), Atlantic horse mackerel ( Trachurus trachurus ) and fish products – samples of caviar, including salmon, blue mussel ( Mytilus edulis ) in brine, sauce, oil, smoked Caspian trout ( Salmo caspius ) spines. The resistance to the representatives of clinically important fluoroquin o lones of the second (ofloxacin, norfloxacin ), third ( levofloxacin) and fourth (moxifloxacin) generations was studied by the phenotypic method. Resistance to fluoroquinolones was inherent in 14 (31.1% of identified) E. coli strains. The probable production of carbapenemase (OXA-48 and OXA-48-like enzymes) by E. coli strains was determined using discs with meropenem (10 μg) and was suspected in 6 (13.3%) of the tested E. coli . The production of ESBL-enzymes was co n firmed by two phenotypic methods of combined and double discs in 5 (11.1%) E. coli strains. The production of AmpC-enzymes was confirmed by the phenotypic method for resistance to cefotaxime (30 μg) in 6 (13.3%) E. coli strains. The results of the study provide a justification for inclusion in the state monitoring to detect contamination of raw materials and products of fish processing enterprises in Ukraine with bacterial contaminants. Such monitoring will help to strengthen quality control and bio-safety of fishery raw materials and products as one of the links in the food chain in the One Health system.References
Banerjee, R., & Johnson, J. R. (2014). A new clone sweeps clean: The enigmatic emergence of Escherichia coli sequence type 131. Antimicrobial Agents and Chemotherapy, 58(9), 4997–5004.
Baroud, M., Dandache, I., Araj, G. F., Wakim, R., Kanj, S., Kanafani, Z., Khairallah, M., Sabra, A., Shehab, M., Dbaibo, G., & Matar, G. M. (2013). Underlying mechanisms of carbapenem resistance in extended-spectrum β-lactamase-producing Klebsiella pneumoniae and Escherichia coli isolates at a tertiary care centre in Lebanon: Role of OXA-48 and NDM-1 carbapenemases. International Journal of Antimicrobial Agents, 41(1), 75–79.
Barrios, H., Garza-Ramos, U., Mejia-Miranda, I., Reyna-Flores, F., Sánchez-Pérez, A., Mosqueda-García, D., & Silva-Sanchez, J. (2017). ESBL-producing Escherichia coli and Klebsiella pneumoniae: The most prevalent clinical isolates obtained between 2005 and 2012 in Mexico. Journal of Global Antimicrobial Resistance, 10, 243–246.
Bryk, M. M. (2018). Current state and prospects of development of livestock industry in Ukraine. Economic Analysis, 28(4), 331–337.
Bush, K., & Bradford, P. A. (2020). Epidemiology of β-lactamase-producing pathogens. Clinical Microbiology Revievs, 33(2), 19.
Carpenter, K. E. (2015). Merluccius bilinearis. The IUCN Red List of Threatened Species, 2015, e.T16466393A16509787.
Coba-Males, M. A., Lavecchia, M. J., Alcívar-León, C. D., & Santamaría-Aguirre, J. (2023). Novel fluoroquinolones with possible antibacterial activity in gram-negative resistant pathogens: In silico drug discovery. Molecules, 28(19), 6929.
Collette, B. B., & Nauen, C. E. (1983). FAO species 1983, catalogue. Vol. 2. Scombrids of the world. An annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date. FAO Fisheries Synopsis, 125, 137.
Dirar, M. H., Bilal, N. E., Ibrahim, M. E., & Hamid, M. E. (2020). Prevalence of extended-spectrum β-lactamase (ESBL) and molecular detection of blaTEM, blaSHV and blaCTX-M genotypes among Enterobacteriaceae isolates from patients in Khartoum, Sudan. PanAfrican Medical Journal, 37, 24988.
Facchin, A., Ratti, G., Filipe, J., Penati, M., Gazzonis, A. L., Masiero, G., Dall’Ara, P., Alborali, G. L., & Lauzi, S. (2024). Fecal carriage and risk factors associated with extended-spectrum β-lactamase-/AmpC-/carbapenemase-producing Escherichia coli in dogs from Italy. Animals, 14(23), 3359.
Freyhof, J., & Kottelat, M. (2008). Perca fluviatilis. The IUCN Red List of Threatened Species 2008, e.T16580A6135168.
Garkavenko, T. О., & Malimon, Z. V. (2018). Analysis of non-conformity to microbiological criteria detected in frozen fish and fish products imported to Ukraine. Veterinary Biotechnology, 2, 85–91.
Ghotaslou, R., Sadeghi, M. R., Akhi, M. T., Hasani, A., & Asgharzadeh, M. (2018). Prevalence and antimicrobial susceptibility patterns of ESBL, AmpC and carbapenemase-producing Enterobactericeae isolated from hospitalized patients in Azerbaijan, Iran. Iran Journal Pharmaceutical Research, 17(S), 79–88.
Goncharova, O. V., & Kutishchev, P. S. (2023). Aspects of potential formation and development of Ukrainian aquaculture against the background of European integration of innovative solutions. Aquatic Bioresources and Aquaculture, 13, 73–82.
Harkavenko, T. O., Horbatyuk, O. I., Kozytska, T G., Andriyashchuk, V. O., Harkavenko, V. M., Musiets, I. V., Ordynska, D. O., & Shchur, N. V. (2021). Isolation and identification of Еnterobacteria producing ESBL-, AmpC-beta-lactamase and carbapenamases (including OXA-48 and OXA-48-like enzymes). Srildvse, Kyiv.
Harkavenko, T. O., Horbatyuk, O. I., Kozytska, T. G., & Andriyashchuk, V. A. (2021). Guidelines on the procedure for surveillance (active monitoring) of antimicrobial resistance of zoonotic and commensal bacteria in veterinary medicine. Srildvse, Kyiv.
Iakovlieva, L. V., Romanenko, I. M., Hrubnyk, I. M., & Yudina, Y. V. (2022). Analysis of antibacterials for systemic use recommended for the treatment of patients with community-acquired pneumonia in Ukraine according to the modern approach to preventing the development of antimicrobial resistance. Infusion and Chemotherapy, 4, 35–45.
John, B., & MacGregor, S. (1966). Synopsis of the biology of the Jack mackerel (Trachurus symmetricus). United States Fish and Wildlife Service Special Scientific Report-Fisheries, 526.
Kessler, K. F. (1877). The Aralo-Caspian expedition. IV. Fishes of the Aralo-Caspio-Pontine ichthyological region. Fishes of the Aralo-Caspio-Pontine ichthyological region. Saint Petersburg.
Kotelevych, V., Huralska, S., & Hоncharenko, V. (2023). Veterinary and sanitary assessment of fish and seafood by quality and safety indicators. Scientific Progress and Innovations, 26(3), 103–112.
Linnaeus, C. (1758). Systema Naturae, Ed. X. (Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata.) Holmiae. Vol. 1.
Livermore, D. M., Day, M., Cleary, P., Hopkins, K. L., Toleman, M. A., Wareham, D. W., Wiuff, C., Doumith, M., & Woodford, N. (2019). OXA-1 β-lactamase and non-susceptibility to penicillin/β-lactamase inhibitor combinations among ESBL-producing Escherichia coli. Journal Antimicrobial Chemotherapy, 74(2), 326–333.
Lungu, I.-A., Moldovan, O.-L., Biriș, V., & Rusu, A. (2022). Fluoroquinolones hybrid molecules as promising antibacterial agents in the fight against antibacterial resistance. Pharmaceutics, 14(8), 1749.
Mathiesen, S. S., Thyrring, J., Hemmer-Hansen, J., Berge, J., Sukhotin, A., Leopold, P., Bekaert, M., Sejr, M. K., & Nielsen, E. E. (2016). Genetic diversity and connectivity within Mytilus spp. in the subarctic and Arctic. Evolutionary Applications, 10(1), 39–55.
Melnychenko, S. G., & Bogadyorova, L. M. (2023). Fisheries of Ukraine: development trends, problems and solutions. Taurian Scientific Bulletin, 133, 362–367.
Musiіets, I., Rublenko, I., Chechet, O., Horbatiuk, O., Pishchanskyi, O., Rublenko, S., Ruda, M., Balanchuk, L., Mekh, N., & Zhovnir, O. (2024). Species composition of microorganisms and their quantitative indicators in microbiological tests of fish and fish products. Scientific Journal of Veterinary Medicine, 2, 56–68.
Park, Y. S., Adams-Haduch, J. M., Shutt, K. A., Yarabinec, D. M., Johnson, L. E., Hingwe, A., Lewis, J. S., Jorgensen, J. H., & Doi, Y. (2012). Clinical and microbiologic characteristics of cephalosporin-resistant Escherichia coli at three centers in the United States. Antimicrobial Agents and Chemotherapy, 56, 1870–1876.
Peirano, G., & Pitout, J. D. D. (2019). Extended-spectrum β-lactamase-producing Enterobacteriaceae: Update on molecular epidemiology and treatment options. Drugs, 79, 1529–1541.
Perez, F., & Bonomo, R. A. (2019). Carbapenem-resistant Enterobacteriaceae: Global action required. The Lancet Infections Diseases, 19, 561–562.
Polishchuck, N. M., Kyryk, D. L., Yurchuk, I. Y., Filippova, O. M., Lischenko, T. M., & Yehorova, S. V. (2020). Biological properties of the major causes factors of purulently inflammatory diseases of surgical patients in Zaporizhzhia Clinical Hospital of Emergency and Critical Care Medicine. Current Issues in Pharmacy and Medicine: Science and Practice, 13(2), 271–277.
Roux, C. (1976). On the dating of the first edition of Cuvier's Règne Animal. Journal of the Society for the Bibliography of Natural History, 8(1), 31.
Prevar, A., Kryzshanovskaya, A., Radionov, V., & Mrug, V. (2018). Analysis of the monitoring study of the antibiotic-resistance of the agents of purulent-inflammatory processes of soft tissue. Reports of Vinnytsia National Medical University, 22(2), 285–288.
Pulss, S., Stolle, I., Stamm, I., Leidner, U., Heydel, C., Semmler, T., Prenger-Berninghoff, E., & Ewers, C. (2018). Multispecies and clonal dissemination of OXA-48 carbapenemase in Enterobacteriaceae from companion animals in Germany 2009–2016. Fronties in Microbiology, 9, 1265.
Salmanov, A. H., & Muzyka, V. P. (2017). Combating antibiotic resistance based on the principles of the "One Health" concept. International Journal of Antibiotics and Probiotics, 1(2), 8–29.
Samofatova, V., & Neveseliuk, V. (2020). The current state of the fishing industry of Ukraine. Food Industry Economics, 12(2), 38–45.
Shariati, A., Arshadi, M., Khosrojerdi, M. A., Abedinzadeh, M, Ganjalishahi, M, Maleki, A., Heydari, M., & Hoshnud, S. (2022). The resistance mechanisms of bacteria against ciprofloxacin and new approaches for enhancing the efficacy of this antibiotic. Front Public Health, 10, 1025633.
Tsipas, G., Tsiamis, G., Vidalis, K., & Bourtzis, K. (2008). Genetic differentiation among Greek lake populations of Carassius gibelio and Cyprinus carpio carpio. Genetica, 136, 491–500.
Trofymchuk, A. M., Hrynevych, N. E., Trofymchuk, M. I., Kunovskyi, Y. V., Bondar, O. S., Tkachenko, O. V., & Savchuk, O. V. (2021). The current state and trends in the development of fish farming in Ukraine and the world. Technology of Production and Processing of Animal Husbandry Products, 2, 123–133.
Wilson, W. R., Kline, E. G., Jones, C. E., Morder, K. T., Mettus, R. T., Doi, Y., Nguyen, M. H., Clancy, C. J., & Shields, R. K. (2019). Effects of KPC variant and porin genotype on the in vitro activity of meropenem-vaborbactam against carbapenem-resistant Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 63(3), e02048-18.
Winfield, I. J., & Nelson, J. S. (2012). Cyprinid fishes: Systematics, biology and exploitation. Springer Science and Business Media, Cham.
Yabumoto, Y., & Nazarkin, M. V. (2018). A new Miocene herring, Clupea macrocephala, from Sakaki Town, Hanishina County, Nagano, Japan. Paleontological Research, 22(4), 352–363.
Yemtsev, V., Solodovnik, N., & Yemtseva, G. (2022). Fisheries of Ukraine: Current state and prospects for restoration. Scientific Innovations and Advanced Technologies, 9(11), 314–326.
Zhang, Y.-Z., & Singh, S. (2015). Antibiotic stewardship programmes in intensive care units: Why, how, and where are they leading us. World Journal of Critical Care Medicine, 4(1), 13–28.
Zhao, H. H. (2011). Hypophthalmichthys molitrix. The IUCN Red List of Threatened Species 2011, e.T166081A6168056.
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