Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples

Bahar Onaran; Muammer Göncüoğlu; Fatma Seda Bilir Ormancı

doi:10.33988/auvfd.451328

Research Article

Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples

Year 2019, Volume: 66 Issue: 4, 331 - 336, 09.09.2019

Bahar Onaran , Muammer Göncüoğlu Fatma Seda Bilir Ormancı

https://doi.org/10.33988/auvfd.451328

Cited By: 6

Abstract

Antibiotic resistance is one of the serious threats to
global public health and food
safety today. Acquired antibiotic resistance in microorganisms arises from
prevalent use of antibiotics for human and animal medicine. Owing to the fact that Vancomycin Resistant Enteroccocci (VRE) is a vital
problem for public health, determination of the antibiotic resistance profiles
of Enterococcus spp. isolates have crucial importance as a part of the
farm to fork food safety. In the study, 120 retail chicken meat samples were
analyzed, and 36 (30%) of the samples were detected as Enterococcus spp.
positive. According to the results, the most prevalent species was E.
faecalis with a rate of 44.4% (16/36), followed by 27.8% (10/36) E.
faecium, 11.1% (4/36) E. durans, 2.8% (1/36) E. gallinarum
and 2.8% (1/36) E. casseliflavus. Antibiotic resistance profiles of the
verified Enterococcus spp. isolates were determined with disc diffusion
method in terms of eight different antibiotics. Among the Enterococcus
spp. isolates, 20 (55.5%) isolates were phenotypically resistant to vancomycin,
6 isolates (16.7%) were detected as vanA positive, 3 isolates (8.3%) were
detected as vanB positive, and one isolate (5%) showed high resistance
to vancomycin (MIC >256 µg/ml). Even though the observed percentages are
low, the observed resistance patterns are still of concern for public health.

Keywords

Chicken meat, E.faecalis, E.faecium, vanA, VanB

References

1. Aarestrup FM, Agerso Y, Gerner-Smidt P, et al (2000): Comparison of antimicrobial resistance 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.
2. Ahmed MO, Baptiste KE (2018): Vancomycin-resistant enterococci: A review of antimicrobial resistance mechanisms and perspectives of human and animal health. Microb Drug Resist, 25, 590-606.
3. Anonymous (2002): General Directorate of Food and Control. Turkish Food Codex Legislation No: 2002/66. Yem Katkı ve Premikslerin Üretimi, İthalatı, İhracatı, Satışı ve Kullanımı Hakkında Tebliğ. faolex.fao.org/docs/texts/tur36029.doc. (02 July 2018).
4. Centers for Disease Control and Prevention (2013): Antibiotic Resistance Threats in the United States, 2013. http://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf. (01 July 2018).
5. Clinical and Laboratory Standards Institute (2015): M100-S25 Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement. www.facm.ucl.ac.be/intranet/CLSI/CLSI-2015-M100-S25-original.pdf. (02 July 2018).
6. De Jong A, Bywater R, Butty P, et al (2009): A pan-European survey of antimicrobial susceptibility towards human-use antimicrobial drugs among zoonotic and commensal enteric bacteria isolated from healthy foodproducing animals. J Antimicrob Chemother, 63, 733-744.
7. Dutka Malen S, Evers S, 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.
8. Fracalanzza SAP, Scheidegger EMD, dos Santos PF, et al (2007): Antimicrobial resistance profiles of enterococci isolated from poultry meat and pasteurized milk in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz, 102, 853-859.
9. French GL (2010). The continuing crisis in antibiotic resistance. Int J Antimicrob Agents, 36, 3-7.
10. Gómez-Gil R, Romero-Gómez MP, García-Arias A, et al (2009): Nosocomial outbreak of linezolid-resistant Enterococcus faecalis infection in a tertiary care hospital. Diagn Microbiol Infect Dis, 65, 175-179.
11. Goncuoglu M, Bilir Ormanci FS, Uludag M, et al (2016): Prevalence and antibiotic resistance of salmonella spp. and Salmonella Typhimurium in broiler carcasses wings and liver. J Food Saf, 36, 524-531.
12. Gousia P, Economou V, Bozidis P, et al (2015): Vancomycin-resistance phenotypes, vancomycin-resistance genes, and resistance to antibiotics of enterococci isolated from food of animal origin. Foodborne Pathog Dis, 12, 214-220.
13. Hayes JR, English LL, Carter PJ, et al (2003): Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Appl Environ Microbiol, 69, 7153-7160.
14. Jackson CR, Fedorka-Cray PJ, Barrett JB (2004): Use of a genus- and species-specific multiplex PCR for identification of Enterococci. J Clin Microbiol, 42, 3558-3565.
15. Kariyama R, Mitsuhata R, Chow JW, et al (2000): Simple and reliable multiplex PCR assay for surveillance isolates of vancomycin-resistant Enterococci. J Clin Microbiol, 38, 3092-3095.
16. Kasimoglu Dogru A, Gencay YE, Ayaz ND (2010): Prevalence and antibiotic resistance profiles of Enterococcus species in chicken at slaughter level; absence of vanA and vanB genes in E. faecalis and E. faecium. Res Vet Sci, 89, 153-158.
17. Ke D, Picard FJ, Martineau F, et al (1999): Development of a PCR assay for rapid detection of Enterococci. J Clin Microbiol, 37, 3497-3503.
18. Kilonzo-Nthenge A, Brown A, Nahashon SN, et al (2015): Occurrence and antimicrobial resistance of enterococci isolated from organic and conventional retail chicken. J Food Prot, 78, 760-766.
19. Klibi N, Said LB, Jouini A, et al (2013): Species distribution, antibiotic resistance and virulence traits in enterococci from meat in Tunisia. Meat Sci, 93, 675-680.
20. López M, Sáenz Y, Rojo-Bezares B, et al (2009): Detection of vanA and vanB2-containing enterococci from food samples in Spain, including Enterococcus faecium strains of CC17 and the new singleton ST425. Int J Food Microbiol, 133, 172-178.
21. Manero A, Blanch AR (1999): Identification of Enterococcus spp. with a biochemical key. Appl Environ Microbiol, 65, 4425–4430.
22. Messi P, Guerrieri E, de Niederhäusern S, et al (2006): Vancomycin-resistant enterococci (VRE) in meat and environmental samples. Int J Food Microbiol, 107, 218-222.
23. Pesavento G, Calonico C, Ducci B, et al (2014): Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Control, 41, 1-7.
24. Trivedi K, Cupakova S, Karpiskova R (2011): Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Vet Med Czech, 56, 352-357.
25. Tyson GH, Nyirabahizi E, Crarey E, et al (2018): Prevalence and antimicrobial resistance of enterococci isolated from retail meats in the United States, 2002 to 2014. Appl Environ Microbiol, 84, e01902-17.
26. Yilmaz ES, Aslantaş O, Onen SP, et al (2016): Prevalence, antimicrobial resistance and virulence traits in enterococci from food of animal origin in Turkey. LWT-Food Sci Technol, 66, 20-26.

Year 2019, Volume: 66 Issue: 4, 331 - 336, 09.09.2019

Bahar Onaran , Muammer Göncüoğlu Fatma Seda Bilir Ormancı

https://doi.org/10.33988/auvfd.451328

Cited By: 6

Abstract

References

1. Aarestrup FM, Agerso Y, Gerner-Smidt P, et al (2000): Comparison of antimicrobial resistance 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.
2. Ahmed MO, Baptiste KE (2018): Vancomycin-resistant enterococci: A review of antimicrobial resistance mechanisms and perspectives of human and animal health. Microb Drug Resist, 25, 590-606.
3. Anonymous (2002): General Directorate of Food and Control. Turkish Food Codex Legislation No: 2002/66. Yem Katkı ve Premikslerin Üretimi, İthalatı, İhracatı, Satışı ve Kullanımı Hakkında Tebliğ. faolex.fao.org/docs/texts/tur36029.doc. (02 July 2018).
4. Centers for Disease Control and Prevention (2013): Antibiotic Resistance Threats in the United States, 2013. http://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf. (01 July 2018).
5. Clinical and Laboratory Standards Institute (2015): M100-S25 Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement. www.facm.ucl.ac.be/intranet/CLSI/CLSI-2015-M100-S25-original.pdf. (02 July 2018).
6. De Jong A, Bywater R, Butty P, et al (2009): A pan-European survey of antimicrobial susceptibility towards human-use antimicrobial drugs among zoonotic and commensal enteric bacteria isolated from healthy foodproducing animals. J Antimicrob Chemother, 63, 733-744.
7. Dutka Malen S, Evers S, 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.
8. Fracalanzza SAP, Scheidegger EMD, dos Santos PF, et al (2007): Antimicrobial resistance profiles of enterococci isolated from poultry meat and pasteurized milk in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz, 102, 853-859.
9. French GL (2010). The continuing crisis in antibiotic resistance. Int J Antimicrob Agents, 36, 3-7.
10. Gómez-Gil R, Romero-Gómez MP, García-Arias A, et al (2009): Nosocomial outbreak of linezolid-resistant Enterococcus faecalis infection in a tertiary care hospital. Diagn Microbiol Infect Dis, 65, 175-179.
11. Goncuoglu M, Bilir Ormanci FS, Uludag M, et al (2016): Prevalence and antibiotic resistance of salmonella spp. and Salmonella Typhimurium in broiler carcasses wings and liver. J Food Saf, 36, 524-531.
12. Gousia P, Economou V, Bozidis P, et al (2015): Vancomycin-resistance phenotypes, vancomycin-resistance genes, and resistance to antibiotics of enterococci isolated from food of animal origin. Foodborne Pathog Dis, 12, 214-220.
13. Hayes JR, English LL, Carter PJ, et al (2003): Prevalence and antimicrobial resistance of Enterococcus species isolated from retail meats. Appl Environ Microbiol, 69, 7153-7160.
14. Jackson CR, Fedorka-Cray PJ, Barrett JB (2004): Use of a genus- and species-specific multiplex PCR for identification of Enterococci. J Clin Microbiol, 42, 3558-3565.
15. Kariyama R, Mitsuhata R, Chow JW, et al (2000): Simple and reliable multiplex PCR assay for surveillance isolates of vancomycin-resistant Enterococci. J Clin Microbiol, 38, 3092-3095.
16. Kasimoglu Dogru A, Gencay YE, Ayaz ND (2010): Prevalence and antibiotic resistance profiles of Enterococcus species in chicken at slaughter level; absence of vanA and vanB genes in E. faecalis and E. faecium. Res Vet Sci, 89, 153-158.
17. Ke D, Picard FJ, Martineau F, et al (1999): Development of a PCR assay for rapid detection of Enterococci. J Clin Microbiol, 37, 3497-3503.
18. Kilonzo-Nthenge A, Brown A, Nahashon SN, et al (2015): Occurrence and antimicrobial resistance of enterococci isolated from organic and conventional retail chicken. J Food Prot, 78, 760-766.
19. Klibi N, Said LB, Jouini A, et al (2013): Species distribution, antibiotic resistance and virulence traits in enterococci from meat in Tunisia. Meat Sci, 93, 675-680.
20. López M, Sáenz Y, Rojo-Bezares B, et al (2009): Detection of vanA and vanB2-containing enterococci from food samples in Spain, including Enterococcus faecium strains of CC17 and the new singleton ST425. Int J Food Microbiol, 133, 172-178.
21. Manero A, Blanch AR (1999): Identification of Enterococcus spp. with a biochemical key. Appl Environ Microbiol, 65, 4425–4430.
22. Messi P, Guerrieri E, de Niederhäusern S, et al (2006): Vancomycin-resistant enterococci (VRE) in meat and environmental samples. Int J Food Microbiol, 107, 218-222.
23. Pesavento G, Calonico C, Ducci B, et al (2014): Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Control, 41, 1-7.
24. Trivedi K, Cupakova S, Karpiskova R (2011): Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Vet Med Czech, 56, 352-357.
25. Tyson GH, Nyirabahizi E, Crarey E, et al (2018): Prevalence and antimicrobial resistance of enterococci isolated from retail meats in the United States, 2002 to 2014. Appl Environ Microbiol, 84, e01902-17.
26. Yilmaz ES, Aslantaş O, Onen SP, et al (2016): Prevalence, antimicrobial resistance and virulence traits in enterococci from food of animal origin in Turkey. LWT-Food Sci Technol, 66, 20-26.

There are 26 citations in total.

Details

Primary Language	English
Subjects	Veterinary Surgery
Journal Section	Articles
Authors	Bahar Onaran 0000-0002-3515-7548 Muammer Göncüoğlu 0000-0001-7245-1941 Fatma Seda Bilir Ormancı 0000-0003-3614-4666
Publication Date	September 9, 2019
Published in Issue	Year 2019Volume: 66 Issue: 4

Cite

APA	Onaran, B., Göncüoğlu, M., & Bilir Ormancı, F. S. (2019). Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 66(4), 331-336. https://doi.org/10.33988/auvfd.451328
AMA	Onaran B, Göncüoğlu M, Bilir Ormancı FS. Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Univ Vet Fak Derg. September 2019;66(4):331-336. doi:10.33988/auvfd.451328
Chicago	Onaran, Bahar, Muammer Göncüoğlu, and Fatma Seda Bilir Ormancı. “Antibiotic Resistance Profiles of Vancomycin Resistant Enterococci in Chicken Meat Samples”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66, no. 4 (September 2019): 331-36. https://doi.org/10.33988/auvfd.451328.
EndNote	Onaran B, Göncüoğlu M, Bilir Ormancı FS (September 1, 2019) Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66 4 331–336.
IEEE	B. Onaran, M. Göncüoğlu, and F. S. Bilir Ormancı, “Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples”, Ankara Univ Vet Fak Derg, vol. 66, no. 4, pp. 331–336, 2019, doi: 10.33988/auvfd.451328.
ISNAD	Onaran, Bahar et al. “Antibiotic Resistance Profiles of Vancomycin Resistant Enterococci in Chicken Meat Samples”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 66/4 (September 2019), 331-336. https://doi.org/10.33988/auvfd.451328.
JAMA	Onaran B, Göncüoğlu M, Bilir Ormancı FS. Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Univ Vet Fak Derg. 2019;66:331–336.
MLA	Onaran, Bahar et al. “Antibiotic Resistance Profiles of Vancomycin Resistant Enterococci in Chicken Meat Samples”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 66, no. 4, 2019, pp. 331-6, doi:10.33988/auvfd.451328.
Vancouver	Onaran B, Göncüoğlu M, Bilir Ormancı FS. Antibiotic resistance profiles of vancomycin resistant enterococci in chicken meat samples. Ankara Univ Vet Fak Derg. 2019;66(4):331-6.