Antibacterial resistance of Enterococcus spp. isolated from commercial poultry of the Russian Federation farms in 2013–2016, and identification of vancomycin resistance genes

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Abstract

Rationale: Enterococci are the leading cause of a number of nosocomial and community-acquired human diseases. In the last decade, these pathogens are becoming resistant to antibacterials, including vancomycin. Multidrug-resistant enterococci have been also isolated from agricultural animals in many countries worldwide, which raises concern of scientists because of possible horizontal transfer of resistance genes. Aim: To assess antibacterial sensitivity of Enterococcus spp. isolates collected from the poultry in the Russian Federation from 2013 to 2016, and to identify vancomycin-resistance genes in their genomes. Materials and methods: Eighty-seven enterococci isolates belonging to E.  faecalis (n = 47, 54%), E.  faecium (n = 25, 28.7%) and other species (n = 15, 17.2%) were collected from clinical samples of 297 heads of poultry (liver, lungs, heart, spleen, contents of the nasal and sinus cavities) from 17  poultry farms of the Northwest, Central, Volga, Ural and Southern Federal districts of the Russian Federation. Sensitivity of enterococci to antibacterials was determined by disk-diffusion and broth microdilution methods. Vancomycin resistance genes van was detected by polymerase chain reaction with specific primers. Results: Most enterococci isolates were resistant to erythromycin (74/87, 85.1%), gentamicin (70/87, 80.5%), ceftriaxone (61/87, 70.1%), ciprofloxacin (56/87, 64.4%), tetracycline (57/87, 65.5%), and rifampicin (48/87, 55.2%), fewer ones to trimethoprim (38/87, 43.7%), ampicillin (28/87, 32.2%), linezolid (15/87, 17.2%) and chloramphenicol (5/87, 5.7%). The vanC type genes (vanC1 and vanC2/3) were identified in 10  isolates. Vancomycin minimal inhibitory concentrations for these isolates were 2 to 8  mg/L. E. faecium with vanC1 gene was isolated from poultry probably for the first time ever. Conclusion: Commercial poultry in the Russian poultry farms is an important reservoir and source of antibiotic-resistant enterococci populations, including enterococci carrying vanC1 and vanC2/3 vancomycin resistance genes. 

About the authors

E. A. Svetoch

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Author for correspondence.
Email: fake@neicon.ru

Svetoch Eduard A. – VD, PhD, Professor, Chief Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


 

Russian Federation

M. G. Teymurazov

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Teymurazov Marat G. – PhD (in Biology), Senior Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

O. I. Tazina

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Tazina Ol'ga I. – Assistant Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

A. A. Abaimova

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Abaimova Alena A. – Trainee Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

A. I. Lev

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Lev Anastasiya I. – Junior Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

E. I. Astashkin

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Astashkin Evgeniy I. – MD, PhD, Leading Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

E. S. Leonova

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Leonova Ekaterina S. – Trainee Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

N. N. Kartsev

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Kartsev Nikolay N. – Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279


Russian Federation

K. V. Detushev

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Detushev Konstantin V. – Researcher, Collection Cultures Department 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279

 

Russian Federation

B. V. Eruslanov

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Eruslanov Boris V. – Leading Researcher, Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279

 

Russian Federation

I. A. Dyatlov

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fake@neicon.ru

Dyatlov Ivan A. – MD, PhD, Professor, Member of Russian Academy of Sciences, Director 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279

 

Russian Federation

N. K. Fursova

State Research Center for Applied Microbiology and Biotechnology, Rospotrebnadzor

Email: fursova@obolensk.org

Fursova Nadezhda K. – PhD (in Biology), Head of Antimicrobial Agents Laboratory 

Obolensk, Serpukhovskiy rayon, Moskovskaya oblast', 142279

Russian Federation

References

  1. Murray BE. The life and times of the Enterococcus. Clin Microbiol Rev. 1990;3(1):46–65. doi: 10.1128/CMR.3.1.46.
  2. Poulsen LL, Bisgaard M, Son NT, Trung NV, An HM, Dalsgaard A. Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam. Emerg Infect Dis. 2012;18(7):1096–100. doi: 10.3201/eid1807.111754.
  3. Velkers FC, van de Graaf-Bloois L, Wagenaar JA, Westendorp ST, van Bergen MA, Dwars RM, Landman WJ. Enterococcus hirae-associated endocarditis outbreaks in broiler flocks: clinical and pathological characteristics and molecular epidemiology. Vet Q. 2011;31(1):3–17. doi: 10.1080/01652176.2011.570107.
  4. Nowakiewicz A, Ziółkowska G, Trościańczyk A, Zięba P, Gnat S. Determination of resistance and virulence genes in Enterococcus faecalis and E. faecium strains isolated from poultry and their genotypic characterization by ADSRRS-fingerprinting. Poult Sci. 2016. pii: pew365. doi: 10.3382/ps/pew365.
  5. Getachew Y, Hassan L, Zakaria Z, Abdul Aziz S. Genetic variability of vancomycin-resistant Enterococcus faecium and Enterococcus faecalis isolates from humans, chickens, and pigs in Malaysia. Appl Environ Microbiol. 2013;79(15): 4528–33. doi: 10.1128/AEM.00650-13.
  6. Ali SA, Hasan KA, Bin Asif H, Abbasi A. Environmental enterococci: I. Prevalence of virulence, antibiotic resistance and species distribution in poultry and its related environment in Karachi, Pakistan. Lett Appl Microbiol. 2013;58(5): 423–32. doi: 10.1111/lam.12208.
  7. Diarra MS, Rempel H, Champagne J, Masson L, Pritchard J, Topp E. Distribution of antimicrobial resistance and virulence genes in Enterococcus spp. and characterization of isolates from broiler chickens. Appl Environ Microbiol. 2010;76(24):8033–43. doi: 10.1128/AEM.01545-10.
  8. Ellerbroek L, Mac KN, Peters J, Hultquist L. Hazard potential from antibiotic-resistant commensals like Enterococci. J Vet Med B Infect Dis Vet Public Health. 2004;51(8–9):393–9. doi: 10.1111/j.1439-0450.2004.00782.x.
  9. Giridhara Upadhyaya PM, Ravikumar KL, Umapathy BL. Review of virulence factors of Enterococcus: an emerging nosocomial pathogen. Indian J Med Microbiol. 2009;27(4):301–5. doi: 10.4103/0255-0857.55437.
  10. van Schaik W, Willems RJ. Genome-based insights into the evolution of enterococci. Clin Microbiol Infect. 2010;16(6):527–32. doi: 10.1111/j.1469-0691.2010.03201.x.
  11. Leclercq R, Derlot E, Duval J, Courvalin P. Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N Engl J Med. 1988;319(3):157–61. doi: 10.1056/NEJM198807213190307.
  12. Uttley AH, Collins CH, Naidoo J, George RC. Vancomycin-resistant enterococci. Lancet. 1988;1(8575–6):57–8. doi: http://dx.doi.org/10.1016/S0140-6736(88)92993-5.
  13. Arias CA, Contreras GA, Murray BE. Management of multidrug-resistant enterococcal infections. Clin Microbiol Infect. 2010;16(6):555– 62. doi: 10.1111/j.1469-0691.2010.03214.x.
  14. Napolitano LM. Emerging issues in the diagnosis and management of infections caused by multi-drug-resistant, gram-positive cocci. Surg Infect (Larchmt). 2005;6 Suppl 2:S-5–22. doi: 10.1089/sur.2005.6.s2-5.
  15. Богомолова НС, Большаков ЛВ, Кузнецова СМ, Орешкина ТД. Динамика устойчивости к антибиотикам и частота выделения стафилококков и энтерококков у больных отделений реконструктивной хирургии. Антибиотики и химиотерапия. 2011;56(5–6):37–45.
  16. Patel R. Clinical impact of vancomycin-resistant enterococci. J Antimicrob Chemother. 2003;51 Suppl 3:iii13–21. doi: 10.1093/jac/dkg272.
  17. Capita R, Alonso-Calleja C. Antibiotic-resistant bacteria: a challenge for the food industry. Crit Rev Food Sci Nutr. 2013;53(1):11–48. doi: 10.1080/10408398.2010.519837.
  18. Xu HT, Tian R, Chen DK, Xiao F, Nie ZY, Hu YJ, Zhang XZ, Li JM. Nosocomial spread of hospital-adapted CC17 vancomycin-resistant Enterococcus faecium in a tertiary-care hospital of Beijing, China. Chin Med J (Engl). 2011;124(4):498–503.
  19. Ozawa Y, Tanimoto K, Nomura T, Yoshinaga M, Arakawa Y, Ike Y. Vancomycin-resistant enterococci in humans and imported chickens in Japan. Appl Environ Microbiol. 2002;68(12):6457– 61. doi: 10.1128/AEM.68.12.6457-6461.2002.
  20. Freitas AR, Coque TM, Novais C, Hammerum AM, Lester CH, Zervos MJ, Donabedian S, Jensen LB, Francia MV, Baquero F, Peixe L. Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J Clin Microbiol. 2011;49(3):925–31.doi: 10.1128/JCM.01750-10.
  21. Hammerum AM, Fussing V, Aarestrup FM, Wegener HC. Characterization of vancomycin-resistant and vancomycin-susceptible Enterococcus faecium isolates from humans, chickens and pigs by RiboPrinting and pulsedfield gel electrophoresis. J Antimicrob Chemother. 2000;45(5):677–80.
  22. Kühn I, Iversen A, Finn M, Greko C, Burman LG, Blanch AR, Vilanova X, Manero A, Taylor H, Caplin J, Domínguez L, Herrero IA, Moreno MA, Möllby R. Occurrence and relatedness of vancomycin-resistant enterococci in animals, humans, and the environment in different European regions. Appl Environ Microbiol. 2005;71(9):5383–90. doi: 10.1128/AEM.71.9.5383-5390.2005.
  23. Dutka-Malen S, Evers S, Courvalin P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol. 1995;33(1):24–7.
  24. Poeta P, Costa D, Klibi N, Rodrigues J, Torres C. Phenotypic and genotypic study of gelatinase and beta-haemolysis activities in faecal enterococci of poultry in Portugal. J Vet Med B Infect Dis Vet Public Health. 2006;53(5):203–8. doi: 10.1111/j.1439-0450.2006.00941.x.
  25. Champagne J, Diarra MS, Rempel H. Development of a DNA microarray for enterococcal species, virulence, and antibiotic resistance gene determinations among isolates from poultry. Appl Environ Microbiol. 2011;77(8): 2625–33. doi: 10.1128/AEM.00263-11.
  26. Страчунский ЛС, Козлов СН. Современная антимикробная химиотерапия. Руководство для врачей. М.: Боргес; 2002. 432 с.
  27. Kaszanyitzky EJ, Tenk M, Ghidán A, Fehérvári GY, Papp M. Antimicrobial susceptibility of enterococci strains isolated from slaughter animals on the data of Hungarian resistance monitoring system from 2001 to 2004. Int J Food Microbiol. 2007;115(1):119–23. doi: 10.1016/j.ijfoodmicro.2006.10.004.
  28. Reynolds PE, Courvalin P. Vancomycin resistance in enterococci due to synthesis of precursors terminating in D-alanyl-D-serine. Antimicrob Agents Chemother. 2005;49(1):21–5. doi: 10.1128/AAC.49.1.21-25.2005.
  29. Ramotar K, Woods W, Larocque L, Toye B. Comparison of phenotypic methods to identify enterococci intrinsically resistant to vancomycin (VanC VRE). Diagn Microbiol Infect Dis. 2000;36(2):119–24. doi: http://dx.doi.org/10.1016/S0732-8893(99)00126-1.
  30. Schwaiger K, Bauer J, Hörmansdorfer S, Mölle G, Preikschat P, Kämpf P, Bauer-Unkauf I, Bischoff M, Hölzel C. Presence of the resistance genes vanC1 and pbp5 in phenotypically vancomycin and ampicillin susceptible Enterococcus faecalis. Microb Drug Resist. 2012;18(4): 434–9. doi: 10.1089/mdr.2011.0227.
  31. Moura TM, Cassenego AP, Campos FS, Ribeiro AM, Franco AC, d'Azevedo PA, Frazzon J, Frazzon AP. Detection of vanC1 gene transcription in vancomycin-susceptible Enterococcus faecalis. Mem Inst Oswaldo Cruz. 2013;108(4):453–6. doi: 10.1590/S0074-0276108042013009.
  32. de Garnica ML, Valdezate S, Gonzalo C, Saez-Nieto JA. Presence of the vanC1 gene in a vancomycin-resistant Enterococcus faecalis strain isolated from ewe bulk tank milk. J Med Microbiol. 2013;62(Pt 3):494–5. doi: 10.1099/jmm.0.052274-0.
  33. Sun M, Wang Y, Chen Z, Zhu X, Tian L, Sun Z. The first report of the vanC₁ gene in Enterococcus faecium isolated from a human clinical specimen. Mem Inst Oswaldo Cruz. 2014;109(6): 712–5. doi: http://dx.doi.org/10.1590/0074-0276140019.

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Copyright (c) 2017 Svetoch E.A., Teymurazov M.G., Tazina O.I., Abaimova A.A., Lev A.I., Astashkin E.I., Leonova E.S., Kartsev N.N., Detushev K.V., Eruslanov B.V., Dyatlov I.A., Fursova N.K.

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