View More View Less
  • 1 Department of Pharmaceutical Microbiology, Gülhane Faculty of Pharmacy, University of Health Sciences, Ankara, Turkey
  • 2 Institute of Health Sciences, Kırıkkale University, Kırıkkale, Turkey
  • 3 Department of Molecular Biology and Genetic Microbiology, Uşak University, Uşak, Turkey
  • 4 Vocational School of Health Services, Hacettepe University, Ankara, Turkey
  • 5 Medical Genetic Department, Medical Faculty, Selçuk University, Konya, Turkey
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $836.00

Abstract

Vancomycin-resistant enterococcus (VRE) is a global threat to public health. Knowledge about the occurrence of vanA-carrying enterococci in broiler and environmental samples is important as antibiotic resistance can be transferred to human bacteria. The aim of this study was to investigate the presence of VRE in broiler cloacal and environmental (house) samples and to genotype the isolates. In this study, 350 swabs were collected from broiler farms. All samples were plated onto enterococcus selective agar containing 6 mg/L vancomycin and 64 mg/L ceftazidime. Minimum inhibitory concentration (MIC) values were determined for vancomycin and teicoplanin. Vancomycin-resistant Enterococcus faecium (VREfm) was isolated from 6 out of 300 (2%) broiler cloacal samples and 13 out of 50 (26%) house samples. All E. faecium isolates had vanA genes. All VREfm isolates (19 isolates) were confirmed to be 95% similar to each other. In conclusion, although 20 years have passed since the ban on avoparcin in Turkey, the present study shows that VREfm isolates are still present in broiler production and especially in broiler houses, and most importantly, a major VREfm clone was isolated from broiler cloacal and house samples.

  • Al-Subaihi, A. (2003): Sample size determination: influencing factors and calculation strategies for survey research. Neurosciences 8, 7986.

    • Search Google Scholar
    • Export Citation
  • Aslantaş, Ö. (2019): Molecular and phenotypic characterization of enterococci isolated from broiler flocks in Turkey. Trop. Anim. Health Prod. 51, 10731082.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bager, F., Madsen, M., Christensen, J. and Aarestrup, F. M. (1997): Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Prev. Vet. Med. 31, 95112.

    • Search Google Scholar
    • Export Citation
  • Bender, J. K., Cattoir, V., Hegstad, K., Sadowy, E., Coque, T. M., Westh, H., Hammerum, A. M., Schaffer, K., Burns, K., Murchan, S., Novais, C., Freitas, A. R., Peixe, L., Grosso, M. D., Pantosti, A. and Werner, G. (2018): Update on prevalence and mechanisms of resistance to linezolid, tigecycline and daptomycin in enterococci in Europe: towards a common nomenclature. Drug Resist. Updat. 40, 2539.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bortolaia, V., Mander, M., Jensen, L. B., Olsen, J. E. and Guardabassi, L. (2015): Persistence of vancomycin resistance in multiple clones of Enterococcus faecium isolated from Danish broilers 15 years after the ban of avoparcin. Antimicrob. Agents Chemother. 59, 29262929.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cattoir, V. and Leclercq, R. (2013): Twenty-five years of shared life with vancomycin-resistant enterococci: is it time to divorce? J. Antimicrob. Chemother. 68, 731742.

    • Search Google Scholar
    • Export Citation
  • Cha, J. O., Jung, Y. H., Lee, H. R., Yoo, J. I. and Lee, Y. S. (2012): Comparison of genetic epidemiology of vancomycin-resistant Enterococcus faecium isolates from humans and poultry. J. Med. Microbiol. 61, 11211128.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Costa, P. M., Bica, A., Vaz-Pires, P. and Bernardo, F. (2010): Changes in antimicrobial resistance among faecal enterococci isolated from growing broilers prophylactically medicated with three commercial antimicrobials. Prev. Vet. Med. 93, 7176.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • de Jong, A., Simjee, S., El Garch, F., Moyaert, H., Rose, M., Youala, M., Dry, M. and EASSA Study Group (2018): Antimicrobial susceptibility of enterococci recovered from healthy cattle, pigs and chickens in nine EU countries (EASSA Study) to critically important antibiotics. Vet. Microbiol. 216, 168175.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • de Jong, A., Simjee, S., Rose, M., Moyaert, H., El Garch, F., Youala, M. and EASSA Study Group (2019): Antimicrobial resistance monitoring in commensal enterococci from healthy cattle, pigs and chickens across Europe during 2004–14 (EASSA Study). J. Antimicrob. Chemother. 74, 921930.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Del Grosso, M., Caprioli, A., Chinzari, P., Fontana, M. C., Pezzotti, G., Manfrin, A., Giannatale, E. D., Goffredo, E. and Pantosti, A. (2000): Detection and characterization of vancomycin-resistant enterococci in farm animals and raw meat products in Italy. Microb. Drug Resist. 6, 313318.

    • Search Google Scholar
    • Export Citation
  • Eisner, A., Feierl, G., Gorkiewicz, G., Dieber, F., Kessler, H. H., Marth, E. and Köfer, J. (2005): High prevalence of vanA-type vancomycin-resistant enterococci in Austrian poultry. Appl. Environ. Microbiol. 71, 64076409.

    • Search Google Scholar
    • Export Citation
  • EUCAST (2019): Preparation of media for determination of MIC values by EUCAST disc diffusion test and broth microdilution method. http://www.eucast.org/clinical_breakpoints/.

    • Export Citation
  • Fisher, K. and Phillips, C. (2009): The ecology, epidemiology and virulence of Enterococcus. Microbiol. 155, 17491757.

  • Getachew, Y. M., Hassan, L., Zakaria, Z., Zaid, C. Z. M., Yardi, A., Shukor, R. A., Marawin, L. T., Embong, F. and Aziz, S. A. (2012): Characterization and risk factors of vancomycin-resistant enterococci (VRE) among animal-affiliated workers in Malaysia. J. Appl. Microbiol. 113, 11841195.

    • Search Google Scholar
    • Export Citation
  • Hammerum, A. M. (2012): Enterococci of animal origin and their significance for public health. Clin. Microbiol. Infect. 18, 619625.

  • Hao, H., Sander, P., Iqbal, Z., Wang, Y., Cheng G. and Yuan, Z. (2016): The risk of some veterinary antimicrobial agents on public health associated with antimicrobial resistance and their molecular basis. Front. Microbiol. 7, 1626.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jansson, D. S., Nilsson, O., Lindblad, J., Greko, C. and Bengtsson, B. (2012): Inter-batch contamination and potential sources of vancomycin-resistant Enterococcus faecium on broiler farms. Br. Poult. Sci. 53, 790799.

    • Search Google Scholar
    • Export Citation
  • Kolonen, A., Sinisalo, M., Huttunen, R., Syrjanen, J., Aittoniemi, J., Huhtala, H., Sankelo, M., Rintala, H., Raty, R., Jantunen, E., Nousiainen, T., Saily, M., Kauppila, M., Itala, R. M., Ollikainen, H., Rauhala, A., Koistinen, P., Elonen, E. and Finnish, L. G. (2017): Bloodstream infections in acute myeloid leukemia patients treated according to the Finnish leukemia group AML-2003 protocol – a prospective nationwide study. Infect. Dis. (Lond.) 49, 799808.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Leclercq, R., Derlot, E., Duval, J. and Courvalin, P. (1988): Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N. Engl. J. Med. 319, 157161.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Leinweber, H., Alotaibi, S. M., Overballe-Petersen, S., Hansen, F., Hasman, H., Bortolaia, V. and Ingmer, H. (2018): Vancomycin resistance in Enterococcus faecium isolated from Danish chicken meat is located on a pVEF4-like plasmid persisting in poultry for 18 years. Int. J. Antimicrob. Agents 52, 283286.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Maasjost, J., Mühldorfer, K., Cortez De Jäckel S. and Hafez, H. M. (2009): Antimicrobial susceptibility patterns of Enterococcus faecalis and Enterococcus faecium isolated from poultry flocks in Germany. Avian Dis. 59, 143148.

    • Search Google Scholar
    • Export Citation
  • Mendes, R. E., Hogan, P. A., Streit, J. M., Jones, R. N. and Flamm, R. K. (2014): Zyvox® annual appraisal of potency and spectrum (ZAAPS) program: report of linezolid activity over 9 years (2004–2012). J. Antimicrob. Chemother. 69, 15821588.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Morrison, D., Woodford, N., Barrett, S. P., Sisson, P. and Cookson, B. D. (1999): DNA banding pattern polymorphism in vancomycin-resistant Enterococcus faecium and criteria for defining strains. J. Clin. Microbiol. 37, 10841091.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Naas, T., Fortineau, N., Snanoudj, R., Spicq, C., Durrbach, A. and Nordmann, P. (2005): First nosocomial outbreak of vancomycin-resistant Enterococcus faecium expressing a VanD-like phenotype associated with a vanA genotype. J. Clin. Microbiol. 43, 36423649.

    • Search Google Scholar
    • Export Citation
  • Nilsson, O., Alm, E., Greko, C. and Bengtsson, B. (2019): The rise and fall of a vancomycin-resistant clone of Enterococcus faecium among broilers in Sweden. Acta Vet. Scand. 17, 233235.

    • Search Google Scholar
    • Export Citation
  • O'Dea, M., Sahibzada, S., Jordan, D., Laird, T., Lee, T., Hewson, K., Pang, S., Abraham, R., Coombs, G. W., Harris, T., Pavic, A. and Abraham, S. (2019): Genomic, antimicrobial resistance, and public health insights into Enterococcus spp. from Australian chickens. J. Clin. Microbiol. 57, 8, e00319–19.

    • Search Google Scholar
    • Export Citation
  • Oravcová, V., Peixe, L., Coquec, T. M., Novais, C., Francia, M. V., Literák, I. and Freitas, A. R. (2018): Wild corvid birds colonized with vancomycin-resistant Enterococcus faecium of human origin harbor epidemic vanA plasmids. Environ. Int. 118, 125133.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pinholt, M., Bayliss, S. C., Gumpert, H., Worning, P., Jensen, V. V. S., Pedersen, M., Feil, E. J. and Westh, H. (2019): WGS of 1058 Enterococcus faecium from Copenhagen, Denmark, reveals rapid clonal expansion of vancomycin-resistant clone ST80 combined with widespread dissemination of a vanA-containing plasmid and acquisition of a heterogeneous accessory genome. J. Antimic. Chemother. 74, 17761785.

    • Search Google Scholar
    • Export Citation
  • Savas, S., Hazırolan, G., Karagöz, A. and Parlak, M. (2019): From days to hours: can MALDI-TOF MS system replace both conventional and molecular typing methods with new cut off level for vancomycin resistant Enterococcus faecium. J. Microbiol. Methods 162, 6268.

    • Search Google Scholar
    • Export Citation
  • Tenover, F. C., Arbeit, R. D., Goering, R. V., Mickelsen, P. A., Murray, B. E., Persing, D. H. and Swaminathan, B. (1995): Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33, 22332239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ünal, N., Aşkar, Ş. and Yıldırım, M. (2017): Antibiotic resistance profile of Enterococcus faecium and Enterococcus faecalis isolated from broiler cloacal samples. Turk. J. Vet. Anim. Sci. 41, 199203.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yang, J., Yuan, Y., Tang, M., Liu, L., Yang, K. and Liu, J. (2019): Phenotypic and genetic characteristics of vancomycin-resistant Enterococcus faecium. Microb. Pathog. 128, 131135.

    • Crossref
    • Search Google Scholar
    • Export Citation