Food Science of Animal Resources (한국축산식품학회지)

Korean Society for Food Science of Animal Resources (한국축산식품학회)
권호 표지
DOI QR코드

DOI QR Code

Detection of Antibiotic Resistance and Resistance Genes in Enterococci Isolated from Sucuk, a Traditional Turkish Dry-Fermented Sausage

  • Demirgul, Furkan (Suleyman Demirel University, Faculty of Engineering, Department of Food Engineering) ;
  • Tuncer, Yasin (Suleyman Demirel University, Faculty of Engineering, Department of Food Engineering)
  • Received : 2017.03.08
  • Accepted : 2017.08.23
  • Published : 2017.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

The aim of this study was to isolate enterococci in Sucuk, a traditional Turkish dry-fermented sausage and to analyze isolates for their biodiversity, antibiotic resistance patterns and the presence of some antibiotic resistance genes. A total of 60 enterococci strains were isolated from 20 sucuk samples manufactured without using a starter culture and they were identified as E. faecium (73.3%), E. faecalis (11.7%), E. hirae (8.3%), E. durans (3.3%), E. mundtii (1.7%) and E. thailandicus (1.7%). Most of the strains were found resistant to rifampin (51.67%) followed by ciprofloxacin (38.33%), nitrofurantoin (33.33%) and erythromycin (21.67%). All strains were found susceptible to ampicillin. Only E. faecium FYE4 and FYE60 strains displayed susceptibility to all antibiotics. Other strains showed different resistance patterns to antibiotics. E. faecalis was found more resistant to antibiotics than other species. Most of the strains (61.7%) displayed resistance from between two and eight antibiotics. The ermB, ermC, gyrA, tetM, tetL and vanA genes were detected in some strains. A lack of correlation between genotypic and phenotypic analysis for some strains was detected. The results of this study indicated that Sucuk manufactured without using a starter culture is a reservoir of multiple antibiotic resistant enterococci. Consequently, Sucuk is a potential reservoir for the transmission of antibiotic resistance genes from animals to humans.

Keywords

References

  1. Aarestrup, F. M., Agerso, Y., Gerner-Smidt, P., Madsen, M., and Jensen, L. B. (2000) Comparison of antimicrobial resist- ance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn. Microbiol. Infect. Dis. 37, 127-137. https://doi.org/10.1016/S0732-8893(00)00130-9
  2. Baylan, O., Nazik, H., Bektore, B., Citil, B. E., Turan, D., Ongen, B., Ozyurt, M., Acikel, C. H., and Haznedaroglu, T. (2011) The relationship between antibiotic resistance and virulence factors in urinary Enterococcus isolates (in Turkish). Mikrobiyol Bul. 45, 430-445.
  3. Beceiro, A., Tomas, M., and Bou, G. (2013) Antimicrobial resistance and virulence: A successful or deleterious association in the bacterial world? Clin. Microbial. Rew. 26, 185-230. https://doi.org/10.1128/CMR.00059-12
  4. Cancilla, M. R., Powell, L.B., Hillier, A. J., and Davidson, B. E. (1992) Rapid genomic fingerprinting of Lactococcus lastis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl. Environ. Microbiol. 58, 1772-1775.
  5. Cariolato, D., Andrighetto, C., and Lombardi, A. (2008) Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control 19, 886-892. https://doi.org/10.1016/j.foodcont.2007.08.019
  6. Cauwerts, K., Decostere, A., De Graef, E. M., Haesebrouck, F., and Pasmans, F. (2007) High prevalence of tetracycline resistance in Enterococcus isolates from broilers carrying the erm (B) gene. Avian Pathol. 36, 395-399. https://doi.org/10.1080/03079450701589167
  7. Chajecka-Wierzchowska, W., Zadernowska, A., Nalepa, B., and Laniewska-Trokenheim, L. (2012) Occurrence and antibiotic resistance of enterococci in ready-to-eat food of animal origin. Afr. J. Microbiol. Res. 6, 6773-6780. https://doi.org/10.5897/AJMR12.322
  8. CLSI. (2012) Performance Standards for Antimicrobial Susceptibility Testing; 22th Informational Supplement M100-S-22 NCCLS. Pennsylvania: Wayne, United States of America.
  9. Ding, Z. F., Zhang, H., Tang, W., Tong, C. Y., Li, R. T., Chen, L. X., Pu, L. J., Zhu, Z. B., and Cui, Y. D. (2012) Methylase genes-mediated erythromycin resistance in Staphylococcus aureus from bovine mastitis in China. Isr. J. Vet. Med. 67, 170-179.
  10. Dutka-Malen, S., Evers, S., and Courvalin, P. (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 33, 24-27.
  11. Edwards, U., Rogall, T., Blocker, H., Emde, M., and Bottger, E. C. (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17, 7843-7853. https://doi.org/10.1093/nar/17.19.7843
  12. Ercoskun, H. and Ozkal, S. G. (2011) Kinetics of traditional Turkish sausage quality aspects during fermentation. Food Control 22, 165-172. https://doi.org/10.1016/j.foodcont.2010.06.015
  13. Garrido, A. M., Galvez, A., and Pulido, R. P. (2014) Antimicrobial resistance in enterococci. J. Infect. Dis. Ther. 2, 1-7.
  14. Huddleston, J. R. (2014) Horizontal gene transfer in the human gastrointestinal tract: Potential spread of antibiotic resistance genes. Infect. Drug Resist. 7, 167-176.
  15. Hummel, A., Holzapfel, W. H., and Franz, C. M. A. P. (2008) Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst. Appl. Microbiol. 30, 1-7.
  16. Jahan, M., Krause, D. O., and Holley, R. A. (2013) Antimicrobial resistance of Enterococcus species from meat and fermented meat products isolated by a PCR-based rapid screening method. Int. J. Food Microbiol. 163, 89-95. https://doi.org/10.1016/j.ijfoodmicro.2013.02.017
  17. Kaban, G. (2013) Sucuk and pastirma: microbiological changes and formation of volatile compounds. Meat Sci. 95, 912-918. https://doi.org/10.1016/j.meatsci.2013.03.021
  18. Kim, T. J., Na, Y. R., and Lee, J. I. (2005) Investigation into the basis of chloramphenicol and tetracycline resistance in Staphylococcus intermedius isolated from cases of pyoderma in dogs. J. Vet. Med. B 52, 119-124. https://doi.org/10.1111/j.1439-0450.2005.00836.x
  19. Landeta, G., Curiel, J. A., Carrascosa, A. V., Munoz, R., and de las Rivas, B. (2013) Technological and safety properties of lactic acid bacteria isolated from Spanish dry-cured sausages. Meat Sci. 95, 272-280. https://doi.org/10.1016/j.meatsci.2013.05.019
  20. Morandi, S., Brasca, M., Andrighetto, C., Lombardi, A., and Lodi, R. (2006) Technological and molecular characterisation of enterococci isolated from North-West Italian dairy products. Int. Dairy J. 16, 867-875. https://doi.org/10.1016/j.idairyj.2005.09.005
  21. Ogier, J. C. and Serror, P. (2008) Safety assessment of dairy microorganisms: the Enterococcus genus. Int. J. Food Microbiol. 126, 291-301. https://doi.org/10.1016/j.ijfoodmicro.2007.08.017
  22. Ojha, K. S., Kerry, J. P., Duffy, G., Beresford, T., and Tiwari, B. K. (2015) Technological advances for enhancing quality and safety of fermented meat products. Trends Food Sci. Tech. 44, 105-116. https://doi.org/10.1016/j.tifs.2015.03.010
  23. Ouoba, L. I. I., Lei, V., and Jensen, L. B. (2008) Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: Determination and transferability of the resistance genes to other bacteria. Int. J. Food Microbiol. 121, 217-224. https://doi.org/10.1016/j.ijfoodmicro.2007.11.018
  24. Peters, J., Mac, K., Wichmann-Schauer, H., Klein, G., and Ellerbroek, L. (2003) Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. Int. J. Food Microbiol. 88, 311-314. https://doi.org/10.1016/S0168-1605(03)00193-4
  25. Petersen, A. and Jensen, L. B. (2004) Analysis of gyrA and parC mutations in enterococci from environmental samples with reduced susceptibility to ciprofloxacin. FEMS Microbiol. Lett. 231, 73-76. https://doi.org/10.1016/S0378-1097(03)00929-7
  26. Reviriego, C., Eaton, T., Martin, R., Jimenez, E., Fernandez, L., Gasson, M. J., and Rodriguez, J. M. (2005) Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. J. Hum. Lac. 21, 131-137. https://doi.org/10.1177/0890334405275394
  27. Szakacs, T. A., Kalan, L., McConnell Eshaghi, A., Shahinas, D., McGeer, A., Wright, G. D., Low D. E., and Patel, S. N. (2014) Outbreak of vancomycin-susceptible Enterococcus faecium containing the wild type vanA gene. J. Clin. Microbiol. 52, 1682-1686. https://doi.org/10.1128/JCM.03563-13
  28. Talon, R. and Leroy, S. (2011) Diversity and safety hazards of bacteria involved in meat fermentations. Meat Sci. 89, 303-309. https://doi.org/10.1016/j.meatsci.2011.04.029
  29. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599. https://doi.org/10.1093/molbev/msm092
  30. Valenzuela, A. S., Omar, N., Abriouel, H., Lopez, R. L., Veljovic, K., Canamero, M. M., Topisirovic, M. K. L., and Galvez, A. (2009) Virulence factors, antibiotic resistance and bacteriocins in enterococci from artisan food of animal origin. Food Control 20, 381-385. https://doi.org/10.1016/j.foodcont.2008.06.004
  31. Yogurtcu, N. N and Tuncer, Y. (2013) Antibiotic susceptibility patterns of Enterococcus strains isolated from Turkish Tulum cheese. Int. J. Dairy Technol. 66, 236-242. https://doi.org/10.1111/1471-0307.12014
  32. Yuceer, O. and Ozden Tuncer, B. (2015) Determination of antibiotic resistance and biogenic amine production of lactic acid bacteria isolated from fermented Turkish sausage (sucuk). J. Food Safety 35, 276-285. https://doi.org/10.1111/jfs.12177

Cited by

  1. Bacteriocinogenic properties and safety evaluation of Enterococcus faecium YT52 isolated from boza, a traditional cereal based fermented beverage pp.1661-5867, 2019, https://doi.org/10.1007/s00003-019-01213-9
  2. Comparative analysis of Enterococcus faecalis and Enterococcus faecium strains isolated from clinical samples and traditional cheese types in the Northwest of Iran: antimicrobial susceptibility and vi vol.202, pp.4, 2017, https://doi.org/10.1007/s00203-019-01792-z
  3. Antibiotic resistance in vancomycin‐resistant lactic acid bacteria (VRLAB) isolated from foods of animal origin vol.44, pp.6, 2017, https://doi.org/10.1111/jfpp.14468
  4. Assessment of safety aspect and probiotic potential of autochthonous Enterococcus faecium strains isolated from spontaneous fermented sausage vol.42, pp.8, 2020, https://doi.org/10.1007/s10529-020-02874-5
  5. Modern View on Enterococcus faecalis and Enterococcus faecium Resistance Mechanisms to Antibiotics vol.65, pp.11, 2021, https://doi.org/10.37489/0235-2990-2020-65-11-12-38-48