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Occurrence of virulence factors and antimicrobial susceptibility of Citrobacter freundii isolated from diseased ornamental fish in Poland Cover

Occurrence of virulence factors and antimicrobial susceptibility of Citrobacter freundii isolated from diseased ornamental fish in Poland

Open Access
|Mar 2025

References

  1. Austin B., Stobie M., Robertson P.A.W.: <em>Citrobacter freundii</em>: the cause of gastro-enteritis leading to progressive low level mortalities in farmed rainbow trout, <em>Oncorhynchus mykiss</em> Walbaum, in Scotland. Bull Eur Assoc Fish Pathol 1992, 12, 166–167.
  2. Barton B.A., Iwama G.K.: Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1991, 1, 3–26, doi: <a href="https://doi.org/10.1016/0959-8030(91)90019-G." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/0959-8030(91)90019-G.</a>
  3. Bauer A.W., Kirby W.M., Sherris J.C., Turck M.: Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966, 45, 493–496, doi: <a href="https://doi.org/10.1093/ajcp/45.4_ts.493." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1093/ajcp/45.4_ts.493.</a>
  4. Behera B.K., Paria P., Das A., Das B.K.: Molecular identification and pathogenicity study of virulent <em>Citrobacter freundii</em> associated with mortality of farmed <em>Labeo rohita</em> (Hamilton 1822), in India. Aquac 2022, 547, 737437, doi: <a href="https://doi.org/10.1016/j.aquaculture.2021.737437." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/j.aquaculture.2021.737437.</a>
  5. Beveridge T.J.: Use of the Gram stain in microbiology. Biotech Histochem 2000, 76, 111–118, doi: <a href="https://doi.org/10.1080/bih.76.3.111.118." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1080/bih.76.3.111.118.</a>
  6. Bunyan I.A.: Molecular study of some virulence factors and antimicrobial susceptibility pattern of <em>Citrobacter freundii</em> isolated from human diarrhea. Sys Rev Pharm 2020, 11, 195–201, doi: <a href="https://doi.org/10.5530/srp.2019.2.04." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.5530/srp.2019.2.04.</a>
  7. Chen B., Yang X., Lu L., Long X., Cao H.: <em>Citrobacter freundii</em>: a causative agent for tail rot disease in freshwater cultured Japanese eel <em>Anguilla japonica</em>. Isr J Aquac - Bamidgeh 2016, 68, doi: <a href="https://doi.org/10.46989/001c.20822." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.46989/001c.20822.</a>
  8. Clinical and Laboratory Standards Institute: M100 Performance Standards for Antimicrobial Susceptibility Testing, 30<sup>th</sup> Edition, CLSI, Wayne, PA, USA, 2020.
  9. Dincturk E., Kumas K., Tanrikul T.T.: First report of <em>Citrobacter freundii</em> infection in Exotic <em>Tropheus</em> spp. Bull Eur Assoc Fish Pathol 2024, 44, 2, doi: <a href="https://doi.org/10.48045/001c.122390." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.48045/001c.122390.</a>
  10. Duman M., Saticioglu I.B., Buyukekiz A.G., Balta F., Altun S.: Molecular characterization and antimicrobial resistance profile of atypical <em>Citrobacter gillenii</em> and <em>Citrobacter</em> sp. isolated from diseased rainbow trout (<em>Oncorhynchus mykiss</em>). J Glob Antimicrob Resist 2017, 10, 136–142, doi: <a href="https://doi.org/10.1016/j.jgar.2017.05.014." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/j.jgar.2017.05.014.</a>
  11. Frederiksen W.: Citrobacter. In: <em>Bergey’s Manual of Systematics of Archaea and Bacteria</em>, edited by M.E. Trujillo, S. Dedysh, P. DeVos, D. Hedlund, P Kämpfer, F.A. Rainey, W.B. Whitman, John Wiley &amp; Sons in association with Bergey’s Manual Trust, Hoboken, NJ, USA, 2015, doi: <a href="https://doi.org/10.1002/9781118960608." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1002/9781118960608.</a>
  12. Gallani S.U., Sebastiao F.D.A., Valladao G.M., Boaratti A.Z., Pilarski F.: Pathogenesis of mixed infection by <em>Spironucleus</em> sp. and <em>Citrobacter freundii</em> in freshwater angelfish <em>Pterophyllum scalare</em>. Microb Pathog 2016, 100, 119–123, doi: <a href="https://doi.org/10.1016/j.micpath.2016.09.002." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/j.micpath.2016.09.002.</a>
  13. Guidi L.R., Santos F.A., Ribeiro A.C.S., Fernandes C., Silva L.H., Gloria M.B.A.: Quinolones and tetracyclines in aquaculture fish by a simple and rapid LC-MS/MS method. Food Chem 2018, 245, 1232–1238, doi: <a href="https://doi.org/10.1016/j.foodchem.2017.11.094." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/j.foodchem.2017.11.094.</a>
  14. Hashim M.H., AlKhafaji M.H.: Isolation and identification of <em>Citrobacter freundii</em> from chicken meat samples using cultural and molecular techniques. Iraqi J Sci 2018, 59, 1216–1224, doi: <a href="https://doi.org/10.24996/ijs.2018.59.3A.9." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.24996/ijs.2018.59.3A.9.</a>
  15. Heuer O.E., Kruse H., Grave K., Collignon P., Karunasagar I., Angulo F.J.: Human health consequences of use of antimicrobial agents in aquaculture. Clin Infect Dis 2009, 49, 1248–1253, doi: <a href="https://doi.org/10.1086/605667." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1086/605667.</a>
  16. Huotari J., Tsitko I., Honkapää K., Alakomi H.L.: Characterization of microbiological quality of whole and gutted Baltic herring. Foods 2022, 11, 492, doi: <a href="https://doi.org/10.3390/foods11040492." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.3390/foods11040492.</a>
  17. Jacob J.H., Irshaid F.I.: Biochemical and molecular taxonomy of a mild halophilic strain of <em>Citrobacter</em> isolated from hypersaline environment. Res J Microbiol 2012, 7, 219–226, doi: <a href="https://doi.org/10.3923/jm.2012.219.226." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.3923/jm.2012.219.226.</a>
  18. Jeremić S., Jakić-Dimić D., Veljović L.J.: <em>Citrobacter freundii</em> as a cause of disease in fish. Acta Vet 2003, 53, 399–410, doi: <a href="https://doi.org/10.2298/AVB0306399J." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.2298/AVB0306399J.</a>
  19. Kerényi M., Allison H.E., Bátai I., Sonnevend A., Emödy L., Plaveczky N., Pál T.: Occurrence of <em>hlyA</em> and <em>sheA</em> genes in extraintestinal <em>Escherichia coli</em> strains. J Clin Microbiol 2005, 43, 2965–2968, doi: <a href="https://doi.org/10.1128/JCM.43.6.2965-2968.2005." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/JCM.43.6.2965-2968.2005.</a>
  20. Kolínská R., Španělová P., Dřevínek M., Hrabák J., Žemličková H.: Species identification of strains belonging to genus <em>Citrobacter</em> using the biochemical method and MALDI-TOF mass spectrometry. Folia Microbiol 2015, 60, 53–59, doi: <a href="https://doi.org/10.1007/s12223-014-0340-4." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1007/s12223-014-0340-4.</a>
  21. Krumperman P.H.: Multiple antibiotic resistance indexing <em>Escherichia coli</em> to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 1983, 46, 165–170, doi: <a href="https://doi.org/10.1128/aem.46.1.165-170.1983." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/aem.46.1.165-170.1983.</a>
  22. Lin C.L., Chiu C.H., Chu C., Huang Y.C., Lin T.Y., Ou J.T.: A multiplex polymerase chain reaction method for rapid identification of <em>Citrobacter freundii</em> and <em>Salmonella</em> species, including <em>Salmonella</em> Typhi. J Microbiol Immunol Infect 2007, 40, 222–226.
  23. Liu L., Hao S., Lan R., Wang G., Xiao D., Sun H., Xu J.: The type VI secretion system modulates flagellar gene expression and secretion in <em>Citrobacter freundii</em> and contributes to adhesion and cytotoxicity to host cells. Infect Immun 2015, 83, 2596–2604, doi: <a href="https://doi.org/10.1128/IAI.03071-14." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/IAI.03071-14.</a>
  24. Liu L., Lan R., Liu L., Wang Y., Zhang Y., Wang Y., Xu J.: Antimicrobial resistance and cytotoxicity of <em>Citrobacter</em> spp. in Maanshan Anhui Province, China. Front Microbiol 2017, 8, 1357, doi: <a href="https://doi.org/10.3389/fmicb.2017.01357." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.3389/fmicb.2017.01357.</a>
  25. Nair G.B., Takeda Y.: The heat-stable enterotoxins. Microb Pathog 1998, 24, 123–131, doi: <a href="https://doi.org/10.1006/mpat.1997.0177." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1006/mpat.1997.0177.</a>
  26. Nawaz M., Khan A.A., Khan S., Sung K., Steele R.: Isolation and characterization of tetracycline-resistant <em>Citrobacter</em> spp. from catfish. Food Microbiol 2008, 25, 85–91, doi: <a href="https://doi.org/10.1016/j.fm.2007.07.008." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/j.fm.2007.07.008.</a>
  27. Neill R.J., Twiddy E.M., Holmes R.K.: Synthesis of plasmid-coded heat-labile enterotoxin in wild-type and hypertoxinogenic strains of <em>Escherichia coli</em> and in other genera of <em>Enterobacteriaceae</em>. Infect Immun 1983, 41, 1056–1061, doi: <a href="https://doi.org/10.1128/iai.41.3.1056-1061.1983." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/iai.41.3.1056-1061.1983.</a>
  28. Nhu N.T.K., Phan M.D., Forde B.M., Murthy A.M., Peters K.M., Day C.J., Poole J., Kidd T.J., Welch R.A., Jennings M.P., Ulett G.C., Sweet M.J., Beatson S.A., Schembri M.A.: Complex multilevel control of hemolysin production by uropathogenic <em>Escherichia coli</em>. MBio 2019, 10, e02248–19, doi: <a href="https://doi.org/10.1128/mbio.02248-19." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/mbio.02248-19.</a>
  29. Özavci V., Dolgun H.T.Y., Kirkan S.: Identification of <em>Citrobacter freundii</em> from skin wounds in goldfish (<em>Carassius auratus</em>) and determination of antibacterial susceptibility. C R Acad Bulg Sci 2023, 76, 911–918, doi: <a href="https://doi.org/10.7546/CRABS.2023.06.11." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.7546/CRABS.2023.06.11.</a>
  30. Pádua S.D., Marques D.P., Sebastião F.A., Pilarski F., Martins M.L., Ishikawa M.M.: Isolation, characterization and pathology of <em>Citrobacter freundii</em> infection in native Brazilian catfish <em>Pseudoplatystoma</em>. Braz J Vet Pathol 2014, 7, 151–157.
  31. Pardia S.N., Verma I.C., Deb M., Bhujwala R.A.: An outbreak of diarrhea due to <em>Citrobacter freundii</em> in a neonatal special care nursery. Indian J Pediatr 1980, 47, 81–84, doi: <a href="https://doi.org/10.1007/bf02900180." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1007/bf02900180.</a>
  32. Pastuszka A., Guz L., Michalak K., Pietras-Ożga D., Puk K.: <em>Vibrio</em> infection in freshwater fish in Poland. Pol J Vet Sci 2024, 27, 117–125, doi: <a href="https://doi.org/10.24425/pjvs.2024.149341." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.24425/pjvs.2024.149341.</a>
  33. Popa L.I., Barbu I.C., Chifiriuc M.C.: Mobile genetic elements involved in the horizontal transfer of antibiotic resistance genes. Rom Arch Microbiol Immunol 2018, 77, 263–276.
  34. Rodkhum C., Hirono I., Crosa J.H., Aoki T.: Four novel hemolysin genes of <em>Vibrio anguillarum</em> and their virulence to rainbow trout. Microb Pathog 2005, 39, 109–119, doi: <a href="https://doi.org/10.1016/j.micpath.2005.06.004." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1016/j.micpath.2005.06.004.</a>
  35. Samonis G., Karageorgopoulos D.E., Kofteridis D.P., Matthaiou D.K., Sidiropoulou V., Maraki S., Falagas M.E.: <em>Citrobacter</em> infections in a general hospital: characteristics and outcomes. Eur J Clin Microbiol 2009, 28, 61–68, doi: <a href="https://doi.org/10.1007/s10096-008-0598-z." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1007/s10096-008-0598-z.</a>
  36. Sato N., Yamane N., Kawamura T.: Systemic <em>Citrobacter freundii</em> infection among sunfish <em>Mola mola</em> in Matsushima aquarium. Bull Jpn Soc Sci Fish 1982, 48, 1551–1557, doi: <a href="https://doi.org/10.2331/suisan.48.1551." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.2331/suisan.48.1551.</a>
  37. Sekhi R.J., Al-Samarraae I.A.A.: Isolation and characterization of <em>Citrobacter freundii</em> from sheep and detect some of their virulence gene using PCR technique. Eur Sch J 2022, 3, 105–113.
  38. Sjoling A., Wiklund G., Savarino S.J., Cohen D.I., Svennerholm A.M.: Comparative analyses of phenotypic and genotypic methods for detection of enterotoxigenic <em>Escherichia coli</em> toxins and colonization factors. J Clin Microbiol 2007, 45, 3295–3301, doi: <a href="https://doi.org/10.1128/jcm.00471-07." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/jcm.00471-07.</a>
  39. Tamara K., Stecher G., Kumar S.: MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021, 38, 3022–3027, doi: <a href="https://doi.org/10.1093/molbev/msab120." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1093/molbev/msab120.</a>
  40. Thompson J.D., Higgins D.G., Gibson T.J.: Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 1994, 22, 4673–4680, doi: <a href="https://doi.org/10.1093/nar/22.22.4673." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1093/nar/22.22.4673.</a>
  41. Toranzo A.E., Cutrin J.M., Roberson B.S., Nunez S., Abell J.M., Hetrick F.M., Baya A.M.: Comparison of the taxonomy, serology, drug resistance transfer, and virulence of <em>Citrobacter freundii</em> strains from mammals and poikilothermic hosts. Appl Environ Microbiol 1994, 60, 1789–1797, doi: <a href="https://doi.org/10.1128/aem.60.6.1789-1797.1994." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1128/aem.60.6.1789-1797.1994.</a>
  42. Walczak N., Puk K., Guz L.: Bacterial flora associated with diseased freshwater ornamental fish. J Vet Res 2017, 61, 445–449, doi: <a href="https://doi.org/10.1515/jvetres-2017-0070." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1515/jvetres-2017-0070.</a>
  43. Welch R.A.: Pore-forming cytolysins of Gram-negative bacteria. Mol Microbiol 1991, 5, 521–528, doi: <a href="https://doi.org/10.1111/j.1365-2958.1991.tb00723.x." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.1111/j.1365-2958.1991.tb00723.x.</a>
  44. Witaningrum A.M., Wibisono F.J., Permatasari D.A., Effendi M.H., Ugb E.N.: Multidrug resistance-encoding gene in <em>Citrobacter freundii</em> isolated from healthy laying chicken in Blitar District, Indonesia. Int J One Health 2022, 8, 161–166, doi: <a href="https://doi.org/10.14202/IJOH.2022.161-166." target="_blank" rel="noopener noreferrer" class="text-signal-blue hover:underline">10.14202/IJOH.2022.161-166.</a>
Language: English
Page range: 17 - 26
Submitted on: Sep 4, 2024
Accepted on: Mar 12, 2025
Published on: Mar 25, 2025
Published by: National Veterinary Research Institute in Pulawy
In partnership with: Paradigm Publishing Services
Publication frequency: 4 times per year

© 2025 Anna Pastuszka, Leszek Guz, Krzysztof Puk, Dorota Pietras-Ożga, published by National Veterinary Research Institute in Pulawy
This work is licensed under the Creative Commons Attribution 4.0 License.