Vet Med - Czech, 2023, 68(5):208-217 | DOI: 10.17221/105/2022-VETMED

Beta-lactam, aminoglycoside, and quinolone resistance in Escherichia coli strains isolated from shrimps and mussels in the Marmara SeaOriginal Paper

B Celik ORCID...1, B Ergul ORCID...2, AI Kekec ORCID...1, B Halac ORCID...1, B Maslak ORCID...3, B Diren Sigirci ORCID...1, B Basaran Kahraman ORCID...1, AF Bagcigil ORCID...1, K Metiner ORCID...1, S Ak1
1 Department of Microbiology, Faculty of Veterinary Medicine, Istanbul University – Cerrahpasa, Buyukcekmece/Istanbul, Turkiye
2 Ambarli Veterinary Border Control Point Directorate, Republic of Turkiye Ministry of Agriculture and Forestry, Istanbul, Turkiye
3 Institute of Graduate Studies, Istanbul University – Cerrahpasa, Avcilar/Istanbul, Turkiye

The purpose of the study was to examine the prevalence of Escherichia coli in shrimps and mussels, and to determine the distribution of β-lactam, aminoglycoside, quinolone, and multi-drug resistance phenotypically and genotypically in E. coli isolates obtained from mussels and shrimps in Istanbul. Faecal samples were collected from mussels (n = 96) and shrimps (n = 96) from the Marmara Sea coastline and fish markets in Istanbul. For the detection of antibiotic susceptibilities, seven antibiotic groups were used. β-lactamase, aminoglycoside, and quinolone genes were also determined. A total of 34 (17.7%, 15 shrimps, and 19 mussels) E. coli were isolated, and 17 (50%) were found to be resistant to one or more antimicrobials. The highest resistance was seen against aminoglycosides with 11 isolates (32.35%), followed by quinolones with 10 isolates (29.41%) and extended-spectrum β-lactamase (ESBL) with 4 isolates (11.76%). Multi-drug resistance was detected in 5 isolates (14.7%) from 3 shrimp and 2 mussel samples. The prevalence of ESBL genes was demonstrated at 3.84% in mussels and shrimp samples. There were no AmpC and carbapenemase-producing genes. These samples harbored blaCTX-M-1 (n = 3) and blaTEM (n = 4). Ten isolates were resistant to aminoglycosides genotypically. Resistance genes detected were strB in 2 isolates, aadA in 5, strB and aadA together in 3, ANT('')-Ia, aphA1 and aphA2 simultaneously in 3, aphA1 in 1, aac(3)-IIa in 1 isolate. aac(6')-Ib-cr gene was detected in only one of 10 phenotypically resistant isolates to quinolones.

Keywords: aquatic animals; E. coli; ESBL; multiple drug resistance

Received: December 6, 2022; Revised: April 27, 2023; Accepted: May 10, 2023; Published: May 29, 2023  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Celik B, Ergul B, Kekec A, Halac B, Maslak B, Diren Sigirci B, et al.. Beta-lactam, aminoglycoside, and quinolone resistance in Escherichia coli strains isolated from shrimps and mussels in the Marmara Sea. Vet Med-Czech. 2023;68(5):208-217. doi: 10.17221/105/2022-VETMED.
Download citation

References

  1. Akkan T, Ozsavli A, Dincer S. Balik ciftliklerinin ekolojik tahribatina bir ornek: Bakterilerdeki antibiyotik direncliligine etkileri, Iskenderun Korfezi [An example of ecological destruction of fish farms: Effects on antibiotic resistance in bacteria, Iskenderun Bay]. Anatolian Journal of Natural Sciences. 2015;6(1):20-7. Turkish.
  2. Alouache S, Kada M, Messai Y, Estepa V, Torres C, Bakour R. Antibiotic resistance and extended-spectrum β-lactamases in isolated bacteria from seawater of Algiers beaches (Algeria). Microbes Environ. 2012;27(1):80-6. Go to original source... Go to PubMed...
  3. Arlet G, Brami G, Decre D, Flippo A, Gaillot O, Lagrange PH, Philippon A. Molecular characterisation by PCR-restriction fragment length polymorphism of TEM beta-lactamases. FEMS Microbiol Lett. 1995 Dec 15;134(2-3):203-8. Go to original source... Go to PubMed...
  4. Bauernfeind A, Stemplinger I, Jungwirth R, Mangold P, Amann S, Akalin E, Ang O, Bal C, Casellas JM. Characterization of beta-lactamase gene blaPER-2, which encodes an extended-spectrum class A beta-lactamase. Antimicrob Agents Chemother. 1996 Mar;40(3):616-20. Go to original source... Go to PubMed...
  5. Boss R, Overesch G, Baumgartner A. Antimicrobial resistance of Escherichia coli, Enterococci, Pseudomonas aeruginosa, and Staphylococcus aureus from raw fish and seafood imported into Switzerland. J Food Prot. 2016 Jul;79(7):1240-6. Go to original source... Go to PubMed...
  6. Brahmi S, Touati A, Dunyach-Remy C, Sotto A, Pantel A, Lavigne JP. High prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in wild fish from the Mediterranean Sea in Algeria. Microb Drug Resist. 2018 Apr;24(3):290-8. Go to original source... Go to PubMed...
  7. Chanawong A, M'Zali FH, Heritage J, Lulitanond A, Hawkey PM. Characterisation of extended-spectrum beta-lactamases of the SHV family using a combination of PCR-single strand conformational polymorphism (PCR-SSCP) and PCR-restriction fragment length polymorphism (PCR-RFLP). FEMS Microbiol Lett. 2000 Mar 1;184(1):85-9. Go to original source... Go to PubMed...
  8. Ciesielczuk H, Hornsey M, Choi V, Woodford N, Wareham DW. Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J Med Microbiol. 2013 Dec;62(Pt 12):1823-7. Go to original source... Go to PubMed...
  9. CLSI - Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 26th ed. Wayne, Pennsylvania: Clinical and Laboratory Standard Institute; 2018. p. 52-60.
  10. Devane ML, Moriarty E, Weaver L, Cookson A, Gilpin B. Fecal indicator bacteria from environmental sources; strategies for identification to improve water quality monitoring. Water Res. 2020 Oct 15;185:116204. Go to original source... Go to PubMed...
  11. Dib AL, Agabou A, Chahed A, Kurekci C, Moreno E, Espigares M, Espigares E. Isolation, molecular characterisation and antimicrobial resistance of Enterobacteriaceae isolated from fish and seafood. Food Control. 2018 Jun;88:54-60. Go to original source...
  12. Divya PS, Thajudeen J, Yousuf J, Madavan A, Abdulla MH. Genetic relatedness, phylogenetic groups, antibiotic resistance, and virulence genes associated with ExPEC in Escherichia coli isolates from finfish and shellfish. J Food Process Preserv. 2020 Jul;44(11):e14837. Go to original source...
  13. EUCAST - European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 8.0 [Internet]. 2018 [cited 2023 Mar 20]. Available from: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_13.0_Breakpoint_Tables.pdf
  14. Foti M, Giacopello C, Bottari T, Fisichella V, Rinaldo D, Mammina C. Antibiotic resistance of gram negatives isolates from loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea. Mar Pollut Bull. 2009 Sep;58(9):1363-6. Go to original source... Go to PubMed...
  15. Gerzova L, Videnska P, Faldynova M, Sedlar K, Provaznik I, Cizek A, Rychlik I. Characterization of microbiota composition and presence of selected antibiotic resistance genes in carriage water of ornamental fish. PLoS One. 2014 Aug 1;9(8):e103865. Go to original source... Go to PubMed...
  16. Gumus B, Celik B, Kahraman BB, Diren Sigirci B, Ak S. Determination of extended-spectrum beta-lactamase (ESBL) and AmpC beta-lactamase-producing Escherichia coli prevalence in faecal samples of healthy dogs and cats. Revue Med Vet. 2017;168(1-3):46-52.
  17. Jiang HX, Tang D, Liu YH, Zhang XH, Zeng ZL, Xu L, Hawkey PM. Prevalence and characteristics of β-lactamase and plasmid-mediated quinolone resistance genes in Escherichia coli isolated from farmed fish in China. J Antimicrob Chemother. 2012 Oct;67(10):2350-3. Go to original source... Go to PubMed...
  18. Kahraman BB, Sigirci BD, Celik B, Gumus B, Metiner K, Adiguzel MC, Bagcigil AF, Ikiz S, Ozgur NY, Ak S. Detection of extended-spectrum β-lactamase and AmpC β-lactamase producing Escherichia coli isolates from chickens. Kafkar Univ Vet Fak Derg. 2016 Mar;22(4):591-6.
  19. Kumar HS, Parvathi A, Karunasagar I, Karunasagar I. Prevalence and antibiotic resistance of Escherichia coli in tropical seafood. World J Microbiol Biotechnol. 2005;21(5):619-23. Go to original source...
  20. Kummerer K. Antibiotics in the aquatic environment - A review - Part I. Chemosphere. 2009 Apr;75(4):417-34. Go to original source... Go to PubMed...
  21. Kurekci C, Aydin M, Yipel M, Katouli M, Gundogdu A. Characterization of extended spectrum β-lactamase (ESBL)-producing Escherichia coli in Asi (Orontes) River in Turkey. J Water Health. 2017 Oct;15(5):788-98. Go to original source... Go to PubMed...
  22. Lim CS, Lee YS, Kahng HY, Ahn S, Jung JS. Resistance genes in high-level streptomycin-resistant Escherichia coli isolated from shellfish. Korean J Microbiol. 2018;54(3):228-36.
  23. Matyar F, Eraslan B, Akkan T, Kaya A, Dincer S. Iskenderun Korfezi baliklarindan izole edilen bakterilerde antibiyotik ve agir metal direncliliklerinin arastirilmasi [Antibiotic and heavy metal resistance of bacteria isolated from fish of Iskenderun Bay]. Biyoloji Bilimleri Araºtirma Dergisi. 2009;1(3):69-73. Turkish.
  24. Ng C, Chen H, Goh SG, Haller L, Wu Z, Charles FR, Trottet A, Gin K. Microbial water quality and the detection of multidrug resistant E. coli and antibiotic resistance genes in aquaculture sites of Singapore. Mar Pollut Bull. 2018 Oct;135:475-80. Go to original source... Go to PubMed...
  25. Noor Uddin GM, Larsen MH, Guardabassi L, Dalsgaard A. Bacterial flora and antimicrobial resistance in raw frozen cultured seafood imported to Denmark. J Food Prot. 2013 Mar;76(3):490-9. Go to original source... Go to PubMed...
  26. Obeid A, Maliha P, Abdallah S, Akl E, Deeb M, El Moussawi H, Salem-Sokhn E, Matar G, Daoud Z. ESBL-producing Escherichia coli and Klebsiella pneumoniae in two major Lebanese hospitals: Molecular epidemiology and correlation with consumption. J Infect Dev Ctries. 2018 Feb 22;12(2.1):16S. Go to original source... Go to PubMed...
  27. Oliveira AMS, Barauna RA, Marcon DJ, Lago LAB, Silva A, Lusio J, Tavares RDS, Tacao M, Henriques I, Schneider MPC. Occurrence, antibiotic-resistance and virulence of E. coli strains isolated from mangrove oysters (Cras-sostrea gasar) farmed in estuaries of Amazonia. Mar Pollut Bull. 2020 Aug;157:111302. Go to original source... Go to PubMed...
  28. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K, Huijsdens X, Kluytmans J. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis. 2011 Jul;17(7):1216-22. Go to original source... Go to PubMed...
  29. Ozcan G, Balik S. Species composition of the fish species in Kemer Reservoir and Akcay Stream, Aydin, Turkey. J Cent Eur Agric. 2008;9(4):683-8.
  30. Ozgumus OB, Sandalli C, Sevim A, Celik-Sevim E, Sivri N. Class 1 and class 2 integrons and plasmid-mediated antibiotic resistance in coliforms isolated from ten rivers in northern Turkey. J Microbiol. 2009 Feb;47(1):19-27. Go to original source... Go to PubMed...
  31. Palma E, Tilocca B, Roncada P. Antimicrobial resistance in veterinary medicine: An overview. Int J Mol Sci. 2020 Mar 11;21(6):1914. Go to original source... Go to PubMed...
  32. Pehlivanoglu F. Gram negatif bakterilerin beta-laktamaz enzim cesitliligi ve Turkiye'deki hayvan orjinli bakterilerdeki durum [Diversity in beta-lactamase enzymes of gram negative bacteria and situation in bacteria of animal origin in Turkey]. Sağlik Bilimleri Veteriner Dergisi, Firat Üniversitesi. 2019;33(2):113-22. Turkish.
  33. Pendergraph DP, Ranieri J, Ermatinger L, Baumann A, Metcalf AL, DeLuca TH, Church MJ. Differentiating sources of fecal contamination to wilderness waters using droplet digital PCR and fecal indicator bacteria methods. Wilderness Environ Med. 2021 Sep;32(3):332-9. Go to original source... Go to PubMed...
  34. Perez-Perez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol. 2002 Jun;40(6):2153-62. Go to original source... Go to PubMed...
  35. Quinn PJ, Carter ME, Markey B, Carter GR. Clinical veterinary microbiology. London: Wolfe Publishing; 1994. p. 42-126.
  36. Rashid M, Rakib MM, Hasan B. Antimicrobial-resistant and ESBL-producing Escherichia coli in different ecological niches in Bangladesh. Infect Ecol Epidemiol. 2015 Jul 17;5:26712. Go to original source... Go to PubMed...
  37. Reverter M, Sarter S, Caruso D, Avarre JC, Combe M, Pepey E, Pouyaud L, Vega-Heredia S, de Verdal H, Gozlan RE. Aquaculture at the crossroads of global warming and antimicrobial resistance. Nat Commun. 2020 Apr;11(1):1870. Go to original source... Go to PubMed...
  38. Ryu SH, Park SG, Choi SM, Hwang YO, Ham HJ, Kim SU, Lee YK, Kim MS, Park GY, Kim KS, Chae YZ. Antimicrobial resistance and resistance genes in Escherichia coli strains isolated from commercial fish and seafood. Int J Food Microbiol. 2012 Jan 3;152(1-2):14-8. Go to original source... Go to PubMed...
  39. Sellera FP, Fernandes MR, Moura Q, Carvalho MPN, Lincopan N. Extended-spectrum-β-lactamase (CTX-M)-producing Escherichia coli in wild fishes from a polluted area in the Atlantic Coast of South America. Mar Pollut Bull. 2018 Oct;135:183-6. Go to original source... Go to PubMed...
  40. Sharma L, Nagpal R, Jackson CR, Patel D, Singh P. Antibiotic-resistant bacteria and gut microbiome communities associated with wild-caught shrimp from the United States versus imported farm-raised retail shrimp. Sci Rep. 2021 Feb 8;11(1):3356. Go to original source... Go to PubMed...
  41. Singh AS, Nayak BB, Kumar SH. High prevalence of multiple antibiotic-resistant, extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in fresh seafood sold in retail markets of Mumbai, India. Vet Sci. 2020 Apr 16;7(2):46. Go to original source... Go to PubMed...
  42. Sullam KE, Essinger SD, Lozupone CA, O'Connor MP, Rosen GL, Knight R, Kilham SS, Russell JA. Environmental and ecological factors that shape the gut bacterial communities of fish: A meta-analysis. Mol Ecol. 2012 Jul;21(13):3363-78. Go to original source... Go to PubMed...
  43. Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, McDermott PF. Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerg Infect Dis. 2012 May;18(5):741-9. Go to original source... Go to PubMed...
  44. Vahaboglu H, Ozturk R, Akbal H, Saribas S, Tansel O, Coskunkan F. Practical approach for detection and identification of OXA-10-derived ceftazidime-hydrolyzing extended-spectrum beta-lactamases. J Clin Microbiol. 1998 Mar;36(3):827-9. Go to original source... Go to PubMed...
  45. Vakulenko SB, Donabedian SM, Voskresenskiy AM, Zervos MJ, Lerner SA, Chow JW. Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob Agents Chemother. 2003 Apr;47(4):1423-6. Go to original source... Go to PubMed...
  46. Van TT, Chin J, Chapman T, Tran LT, Coloe PJ. Safety of raw meat and shellfish in Vietnam: An analysis of Escherichia coli isolations for antibiotic resistance and virulence genes. Int J Food Microbiol. 2008 Jun 10;124(3):217-23. Go to original source... Go to PubMed...
  47. Voets GM, Fluit AC, Scharringa J, Cohen Stuart J, Leverstein-van Hall MA. A set of multiplex PCRs for genotypic detection of extended-spectrum β-lactamases, carbapenemases, plasmid-mediated AmpC β-lactamases and OXA β-lactamases. Int J Antimicrob Agents. 2011 Apr;37(4):356-9. Go to original source... Go to PubMed...
  48. WHO - World Health Organization. WHO report on surveillance of antibiotic consumption: 2016-2018 early implementation. Licence: CC BY-NC-SA 3.0. Geneva, Switzerland: World Health Organization; 2018.
  49. WHO - World Health Organization. Factsheets: Antibiotic resistance [Internet]. 2021 [cited 2022 Mar 11]. Available from: www.who.int/mediacentre/factsheets/antibiotic-resistance/en/.
  50. Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, Amyes SG, Livermore DM. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents. 2006 Apr;27(4):351-3. Go to original source... Go to PubMed...
  51. Zhao JY, Dang H. Coastal seawater bacteria harbor a large reservoir of plasmid-mediated quinolone resistance determinants in Jiaozhou Bay, China. Microb Ecol. 2012 Jul;64(1):187-99. Go to original source... Go to PubMed...
  52. Zhao Y, Duan C, Zhang X, Chen H, Ren H, Yin Y, Ye L. Insights into the gut microbiota of freshwater shrimp and its associations with the surrounding microbiota and environmental factors. J Microbiol Biotechnol. 2018 Jun 28;28(6):946-56. Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.