Significant reduction of vancomycin resistant E. faecium in the Norwegian broiler population coincided with measures taken by the broiler industry to reduce antimicrobial resistant bacteria


Autoři: Roger Simm aff001;  Jannice Schau Slettemeås aff002;  Madelaine Norström aff002;  Katharine R. Dean aff002;  Magne Kaldhusdal aff002;  Anne Margrete Urdahl aff002
Působiště autorů: Institute of Oral Biology, University of Oslo, Oslo, Norway aff001;  Norwegian Veterinary Institute, Oslo, Norway aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226101

Souhrn

Vancomycin resistant enterococci (VRE) belong to the most common causes of nosocomial infections worldwide. It has been reported that use of the glycopeptide growth promoter avoparcin selected for a significant livestock-reservoir of VRE in many European countries, including Norway. However, although avoparcin was banned as a feed-additive in 1995, VRE have for unknown reasons consistently been reported in samples from Norwegian broilers. When avoparcin was banned, broiler-feed was supplemented with the polyether ionophore narasin in order to control the diseases coccidiosis and the frequent sequela necrotic enteritis. A potential link between transferrable vancomycin resistance and reduced susceptibility to narasin was recently reported. The use of narasin as a feed additive was abolished by the Norwegian broiler industry in 2016 and since then, broilers have been reared without in-feed antibacterial supplements. In this study, we demonstrate that all VRE isolates from Norwegian broilers collected in 2006–2014 displayed reduced susceptibility to narasin. Surveillance data collected two years after the narasin abolishment show a significant reduction in VRE, below the detection limit of the surveillance method, and a concurrent marked reduction in Enterococcus faecium with reduced susceptibility to narasin. The significant decline of E. faecium with reduced susceptibility to these antimicrobial compounds also coincided with an increased focus on cleaning and disinfection between broiler flocks. Furthermore, data from a controlled in vivo experiment using Ross 308 broilers indicate that the proportion of E. faecium with reduced susceptibility to narasin was heavily reduced in broilers fed a narasin-free diet compared to a diet supplemented with narasin. Our results are consistent with that the abolishment of this feed additive, possibly in combination with the increased focus on cleaning and disinfection, has had a substantial impact on the occurrence of VRE in the Norwegian broiler population.

Klíčová slova:

Antimicrobial resistance – Diet – Enterococcus infections – Livestock – Norwegian people – Poultry – Vancomycin – Vancomycin resistance


Zdroje

1. Faron ML, Ledeboer NA, Buchan BW. Resistance Mechanisms, Epidemiology, and Approaches to Screening for Vancomycin-Resistant Enterococcus in the Health Care Setting. J Clin Microbiol. 2016;54(10):2436–47. Epub 2016/05/06. doi: 10.1128/JCM.00211-16 27147728.

2. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015;28(3):603–61. Epub 2015/05/29. doi: 10.1128/CMR.00134-14 26016486.

3. Gouliouris T, Raven KE, Ludden C, Blane B, Corander J, Horner CS, et al. Genomic Surveillance of Enterococcus faecium Reveals Limited Sharing of Strains and Resistance Genes between Livestock and Humans in the United Kingdom. MBio. 2018;9(6). Epub 2018/11/08. doi: 10.1128/mBio.01780-18 30401778.

4. Willems RJ, Top J, van Schaik W, Leavis H, Bonten M, Siren J, et al. Restricted gene flow among hospital subpopulations of Enterococcus faecium. MBio. 2012;3(4):e00151–12. Epub 2012/07/19. doi: 10.1128/mBio.00151-12 22807567.

5. Simonsen GS, Haaheim H, Dahl KH, Kruse H, Lovseth A, Olsvik O, et al. Transmission of VanA-type vancomycin-resistant enterococci and vanA resistance elements between chicken and humans at avoparcin-exposed farms. Microb Drug Resist. 1998;4(4):313–8. Epub 1999/02/13. doi: 10.1089/mdr.1998.4.313 9988050.

6. Sorensen TL, Blom M, Monnet DL, Frimodt-Moller N, Poulsen RL, Espersen F. Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. N Engl J Med. 2001;345(16):1161–6. Epub 2001/10/20. doi: 10.1056/NEJMoa010692 11642232.

7. Dahl KH, Mater DD, Flores MJ, Johnsen PJ, Midtvedt T, Corthier G, et al. Transfer of plasmid and chromosomal glycopeptide resistance determinants occurs more readily in the digestive tract of mice than in vitro and exconjugants can persist stably in vivo in the absence of glycopeptide selection. J Antimicrob Chemother. 2007;59(3):478–86. Epub 2007/02/07. doi: 10.1093/jac/dkl530 17283034.

8. Lester CH, Frimodt-Moller N, Sorensen TL, Monnet DL, Hammerum AM. In vivo transfer of the vanA resistance gene from an Enterococcus faecium isolate of animal origin to an E. faecium isolate of human origin in the intestines of human volunteers. Antimicrob Agents Chemother. 2006;50(2):596–9. Epub 2006/01/27. doi: 10.1128/AAC.50.2.596-599.2006 16436715.

9. Nilsson O, Greko C, Bengtsson B, Englund S. Genetic diversity among VRE isolates from Swedish broilers with the coincidental finding of transferrable decreased susceptibility to narasin. J Appl Microbiol. 2012;112(4):716–22. Epub 2012/02/14. doi: 10.1111/j.1365-2672.2012.05254.x 22324455.

10. de Niederhausern S, Bondi M, Messi P, Iseppi R, Sabia C, Manicardi G, et al. Vancomycin-resistance transferability from VanA enterococci to Staphylococcus aureus. Curr Microbiol. 2011;62(5):1363–7. Epub 2011/01/15. doi: 10.1007/s00284-011-9868-6 21234755.

11. Aarestrup FM. Occurrence of glycopeptide resistance among Enterococcus faecium isolates from conventional and ecological poultry farms. Microb Drug Resist. 1995;1(3):255–7. Epub 1995/10/01. doi: 10.1089/mdr.1995.1.255 9158784.

12. Bates J, Jordens Z, Selkon JB. Evidence for an animal origin of vancomycin-resistant enterococci. Lancet. 1993;342(8869):490–1. Epub 1993/08/21. doi: 10.1016/0140-6736(93)91613-q 8102440.

13. Devriese LA, Ieven M, Goossens H, Vandamme P, Pot B, Hommez J, et al. Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrob Agents Chemother. 1996;40(10):2285–7. Epub 1996/10/01. 8891131.

14. Klare I, Heier H, Claus H, Reissbrodt R, Witte W. vanA-mediated high-level glycopeptide resistance in Enterococcus faecium from animal husbandry. FEMS Microbiol Lett. 1995;125(2–3):165–71. Epub 1995/01/15. doi: 10.1111/j.1574-6968.1995.tb07353.x 7875564.

15. Aarestrup FM, Seyfarth AM, Emborg HD, Pedersen K, Hendriksen RS, Bager F. Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother. 2001;45(7):2054–9. Epub 2001/06/16. doi: 10.1128/AAC.45.7.2054-2059.2001 11408222.

16. Bager F, Aarestrup FM, Madsen M, Wegener HC. Glycopeptide resistance in Enterococcus faecium from broilers and pigs following discontinued use of avoparcin. Microb Drug Resist. 1999;5(1):53–6. Epub 1999/05/20. doi: 10.1089/mdr.1999.5.53 10332722.

17. Klare I, Badstubner D, Konstabel C, Bohme G, Claus H, Witte W. Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microb Drug Resist. 1999;5(1):45–52. Epub 1999/05/20. doi: 10.1089/mdr.1999.5.45 10332721.

18. Heuer OE, Pedersen K, Jensen LB, Madsen M, Olsen JE. Persistence of vancomycin-resistant enterococci (VRE) in broiler houses after the avoparcin ban. Microb Drug Resist. 2002;8(4):355–61. Epub 2003/01/14. doi: 10.1089/10766290260469624 12523633.

19. NORM/NORM-VET 2012. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2013 ISSN:1502-2307 (print) / 1890–9965 (electronic).

20. NORM/NORM-VET 2010. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2011 ISSN:1502-2307 (print) / 1890–9965 (electronic).

21. NORM/NORM-VET 2009. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2010 ISSN:1502-2307 (print) / 1890–9965 (electronic).

22. NORM/NORM-VET 2006. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2007 ISSN:1502-2307 (print) / 1890–9965 (electronic).

23. NORM/NORM-VET 2004. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2005 ISSN:1502-2307 (print) / 1890–9965 (electronic).

24. NORM/NORM-VET 2002. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2003 ISSN:1502-2307 (print) / 1890–9965 (electronic).

25. NORM/NORM-VET 2000. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2001 ISSN:1502-2307 (print) / 1890–9965 (electronic).

26. Kaldhusdal M, Benestad SL, Lovland A. Epidemiologic aspects of necrotic enteritis in broiler chickens—disease occurrence and production performance. Avian Pathol. 2016;45(3):271–4. Epub 2016/03/10. doi: 10.1080/03079457.2016.1163521 26956946.

27. Berg DH, Hamill RL. The isolation and characterization of narasin, a new polyether antibiotic. J Antibiot (Tokyo). 1978;31(1):1–6. Epub 1978/01/01. doi: 10.7164/antibiotics.31.1 627518.

28. Grave K, Kaldhusdal MC, Kruse H, Harr LM, Flatlandsmo K. What has happened in norway after the ban of avoparcin? Consumption of antimicrobials by poultry. Prev Vet Med. 2004;62(1):59–72. Epub 2004/05/25. doi: 10.1016/j.prevetmed.2003.08.009 15154685.

29. Nilsson O, Myrenas M, Agren J. Transferable genes putatively conferring elevated minimum inhibitory concentrations of narasin in Enterococcus faecium from Swedish broilers. Vet Microbiol. 2016;184:80–3. Epub 2016/02/09. doi: 10.1016/j.vetmic.2016.01.012 26854348.

30. NORM/NORM-VET 2001. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2002 ISSN:1502-2307 (print) / 1890–9965 (electronic).

31. NORM/NORM-VET 2003. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2004 ISSN:1502-2307 (print) / 1890–9965 (electronic).

32. NORM/NORM-VET 2005. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2006 ISSN:1502-2307 (print) / 1890–9965 (electronic).

33. NORM/NORM-VET 2007. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2008 ISSN:1502-2307 (print) / 1890–9965 (electronic).

34. NORM/NORM-VET 2008. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2009 ISSN:1502-2307 (print) / 1890–9965 (electronic).

35. NORM/NORM-VET 2011. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2012 ISSN:1502-2307 (print) / 1890–9965 (electronic).

36. NORM/NORM-VET 2013. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2014 ISSN:1502-2307 (print) / 1890–9965 (electronic).

37. NORM/NORM-VET 2014. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2015 ISSN:1502-2307 (print) / 1890–9965 (electronic).

38. NORM/NORM-VET 2015. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2016 ISSN:1502-2307 (print) / 1890–9965 (electronic).

39. NORM/NORM-VET 2016. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2017 ISSN:1502-2307 (print) / 1890–9965 (electronic).

40. NORM/NORM-VET 2017. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2018 ISSN:1502-2307 (print) / 1890–9965 (electronic).

41. NORM/NORM-VET 2018. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo: 2019 ISSN:1502-2307 (print) / 1890–9965 (electronic).

42. 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(5):1434. Epub 1995/05/01. 7615777.

43. Clark NC, Cooksey RC, Hill BC, Swenson JM, Tenover FC. Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob Agents Chemother. 1993;37(11):2311–7. Epub 1993/11/01. doi: 10.1128/aac.37.11.2311 8285611.

44. Kruse H, Johansen BK, Rorvik LM, Schaller G. The use of avoparcin as a growth promoter and the occurrence of vancomycin-resistant Enterococcus species in Norwegian poultry and swine production. Microb Drug Resist. 1999;5(2):135–9. Epub 1999/08/04. doi: 10.1089/mdr.1999.5.135 10432274.

45. Borgen K, Simonsen GS, Sundsfjord A, Wasteson Y, Olsvik O, Kruse H. Continuing high prevalence of VanA-type vancomycin-resistant enterococci on Norwegian poultry farms three years after avoparcin was banned. J Appl Microbiol. 2000;89(3):478–85. Epub 2000/10/06. doi: 10.1046/j.1365-2672.2000.01137.x 11021580.

46. Sorum M, Johnsen PJ, Aasnes B, Rosvoll T, Kruse H, Sundsfjord A, et al. Prevalence, persistence, and molecular characterization of glycopeptide-resistant enterococci in Norwegian poultry and poultry farmers 3 to 8 years after the ban on avoparcin. Appl Environ Microbiol. 2006;72(1):516–21. Epub 2006/01/05. doi: 10.1128/AEM.72.1.516-521.2006 16391086.

47. Sletvold H, Johnsen PJ, Hamre I, Simonsen GS, Sundsfjord A, Nielsen KM. Complete sequence of Enterococcus faecium pVEF3 and the detection of an omega-epsilon-zeta toxin-antitoxin module and an ABC transporter. Plasmid. 2008;60(1):75–85. Epub 2008/05/31. doi: 10.1016/j.plasmid.2008.04.002 18511120.

48. Rosvoll TC, Pedersen T, Sletvold H, Johnsen PJ, Sollid JE, Simonsen GS, et al. PCR-based plasmid typing in Enterococcus faecium strains reveals widely distributed pRE25-, pRUM-, pIP501- and pHTbeta-related replicons associated with glycopeptide resistance and stabilizing toxin-antitoxin systems. FEMS Immunol Med Microbiol. 2010;58(2):254–68. Epub 2009/12/18. doi: 10.1111/j.1574-695X.2009.00633.x 20015231.

49. Johnsen PJ, Simonsen GS, Olsvik O, Midtvedt T, Sundsfjord A. Stability, persistence, and evolution of plasmid-encoded VanA glycopeptide resistance in enterococci in the absence of antibiotic selection in vitro and in gnotobiotic mice. Microb Drug Resist. 2002;8(3):161–70. Epub 2002/10/05. doi: 10.1089/107662902760326869 12363004.

50. SVARM 2012, Swedish Veterinary Antimicrobial Resistance Monitoring. The National Veterinary Institute (SVA), Uppsala, Sweden, 2013 ISSN 1650-6332.

51. Nilsson O, Greko C, Top J, Franklin A, Bengtsson B. Spread without known selective pressure of a vancomycin-resistant clone of Enterococcus faecium among broilers. J Antimicrob Chemother. 2009;63(5):868–72. Epub 2009/02/26. doi: 10.1093/jac/dkp045 19240078.

52. SVARM 2010, Swedish Veterinary Antimicrobial Resistance Monitoring. The National Veterinary Institute (SVA), Uppsala, Sweden, 2011 ISSN 1650-6332.

53. Arthur M, Molinas C, Depardieu F, Courvalin P. Characterization of Tn1546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol. 1993;175(1):117–27. Epub 1993/01/01. doi: 10.1128/jb.175.1.117-127.1993 8380148.

54. Nilsson O, Alm E, Greko C, Bengtsson B. The rise and fall of a vancomycin-resistant clone of Enterococcus faecium among broilers in Sweden. J Glob Antimicrob Resist. 2019;17:233–5. Epub 2019/01/07. doi: 10.1016/j.jgar.2018.12.013 30611929.

55. Borgen K, Sorum M, Kruse H, Wasteson Y. Persistence of vancomycin-resistant enterococci (VRE) on Norwegian broiler farms. FEMS Microbiol Lett. 2000;191(2):255–8. Epub 2000/10/12. doi: 10.1111/j.1574-6968.2000.tb09348.x 11024272.

56. Jansson DS, Nilsson O, Lindblad J, Greko C, Bengtsson B. Inter-batch contamination and potential sources of vancomycin-resistant Enterococcus faecium on broiler farms. Br Poult Sci. 2012;53(6):790–9. Epub 2013/02/13. doi: 10.1080/00071668.2012.750715 23398424.

57. Garcia-Migura L, Pleydell E, Barnes S, Davies RH, Liebana E. Characterization of vancomycin-resistant Enterococcus faecium isolates from broiler poultry and pig farms in England and Wales. J Clin Microbiol. 2005;43(7):3283–9. Epub 2005/07/08. doi: 10.1128/JCM.43.7.3283-3289.2005 16000449.

58. Mo SS, Kristoffersen AB, Sunde M, Nodtvedt A, Norstrom M. Risk factors for occurrence of cephalosporin-resistant Escherichia coli in Norwegian broiler flocks. Prev Vet Med. 2016;130:112–8. Epub 2016/07/21. doi: 10.1016/j.prevetmed.2016.06.011 27435654.

59. Nilsson O, Greko C, Bengtsson B. Environmental contamination by vancomycin resistant enterococci (VRE) in Swedish broiler production. Acta Vet Scand. 2009;51:49. Epub 2009/12/04. doi: 10.1186/1751-0147-51-49 19954525.

60. Heuer OE, Pedersen K, Andersen JS, Madsen M. Vancomycin-resistant enterococci (VRE) in broiler flocks 5 years after the avoparcin ban. Microb Drug Resist. 2002;8(2):133–8. Epub 2002/07/18. doi: 10.1089/107662902760190680 12118518.

61. Nilsson O, Vagsholm I, Bengtsson B. Proof of concept for eradication of vancomycin resistant Enterococcus faecium from broiler farms. Acta Vet Scand. 2013;55:46. Epub 2013/06/14. doi: 10.1186/1751-0147-55-46 23758849.


Článek vyšel v časopise

PLOS One


2019 Číslo 12