Occurrence of and risk factors for extended-spectrum cephalosporin-resistant Enterobacteriaceae determined by sampling of all Norwegian broiler flocks during a six month period


Autoři: Solveig Sølverød Mo aff001;  Anne Margrete Urdahl aff001;  Live Lingaas Nesse aff001;  Jannice Schau Slettemeås aff001;  Silje Nøstvedt Ramstad aff001;  Mona Torp aff001;  Madelaine Norström aff002
Působiště autorů: Department of Animal Health, Welfare and Food Safety, Norwegian Veterinary Institute, Oslo, Norway aff001;  Department of Analysis and Diagnostics, Norwegian Veterinary Institute, Oslo, Norway aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223074

Souhrn

All broiler flocks reared and slaughtered in Norway from May-October 2016 (n = 2110) were screened for the presence of extended-spectrum cephalosporin (ESC) -resistant Enterobacteriaceae. Furthermore, we investigated possible risk factors for occurrence of such bacteria in broiler flocks. The odds of a flock being positive for ESC-resistant Enterobacteriaceae increased if the previous flock in the same house was positive, and if the flock was reared during September-October. However, we cannot exclude seasonal fluctuations in occurrence of ESC-resistant Enterobacteriaceae during the months November to April. The overall occurrence of ESC-resistant Enterobacteriaceae was 10.4%, and primarily linked to the presence of blaCMY (82.6%) in positive isolates. We describe the first findings of Escherichia coli with blaCTX-M-1, Klebsiella pneumoniae with both blaCTX-M-15 and blaSHV-12, and K. pneumoniae with blaCMY isolated from Norwegian broiler production. This study gives us a unique overview and estimate of the true occurrence of ESC-resistant Enterobacteriaceae in Norwegian broilers over a six-month period. To the best of our knowledge, this is the most comprehensive study performed on the occurrence of ESC-resistant Enterobacteriaceae in a broiler population.

Klíčová slova:

Antimicrobial resistance – Enterobacteriaceae – Escherichia coli – Klebsiella pneumoniae – Medical risk factors – Polymerase chain reaction – Campylobacter – Norwegian people


Zdroje

1. Briñas L, Moreno MA, Zarazaga M, Porrero C, Sáenz Y, García M, et al. Detection of CMY-2, CTX-M-14, and SHV-12 beta-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrob Agents Chemother. 2003;47(6):2056–8. doi: 10.1128/AAC.47.6.2056-2058.2003 12760899

2. Carattoli A. Animal reservoirs for extended spectrum beta-lactamase producers. Clin Microbiol Infect. 2008;14 Suppl 1:117–23. Epub 2007/12/25. doi: 10.1111/j.1469-0691.2007.01851.x 18154535.

3. Dierikx C, van Essen-Zandbergen A, Veldman K, Smith H, Mevius D. Increased detection of extended spectrum beta-lactamase producing Salmonella enterica and Escherichia coli isolates from poultry. Vet Microbiol. 2010;145(3–4):273–8. doi: 10.1016/j.vetmic.2010.03.019 20395076.

4. Doi Y, Paterson DL, Egea P, Pascual A, López-Cerero L, Navarro MD, et al. Extended-spectrum and CMY-type beta-lactamase-producing Escherichia coli in clinical samples and retail meat from Pittsburgh, USA and Seville, Spain. Clin Microbiol Infect. 2010;16(1):33–8. doi: 10.1111/j.1469-0691.2009.03001.x 19681957.

5. Ewers C, Bethe A, Semmler T, Guenther T, Wieler LH. Extended-spectrum beta-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect. 2012;18:646–55. doi: 10.1111/j.1469-0691.2012.03850.x 22519858

6. Hiroi M, Yamazaki F, Harada T, Takahashi N, Iida N, Noda Y, et al. Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in food-producing animals. J Vet Med Sci. 2012;74(2):189–95. Epub 2011/10/08. doi: 10.1292/jvms.11-0372 21979457.

7. Smet A, Martel A, Persoons D, Dewulf J, Heyndrickx M, Catry B, et al. Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal Escherichia coli Isolates in Belgian broiler farms. Antimicrob Agents Chemother. 2008;52(4):1238–43. doi: 10.1128/AAC.01285-07 18227190

8. NORM/NORM-VET. NORM/NORM-VET 2006. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø/Oslo. ISSN:1502-2307: 2007.

9. Sunde M, Tharaldsen H, Slettemeås JS, Norström M, Carattoli A, Bjorland J. Escherichia coli of animal origin in Norway contains a blaTEM-20-carrying plasmid closely related to blaTEM-20 and blaTEM-52 plasmids from other European countries. J Antimicrob Chemother. 2009;63(1):215–6. Epub 2008/10/31. doi: 10.1093/jac/dkn445 18971216.

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

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

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

13. Mo SS, Norström M, Slettemeås JS, Løvland A, Urdahl AM, Sunde M. Emergence of AmpC-producing Escherichia coli in the broiler production chain in a country with a low antimicrobial usage profile. Vet Microbiol. 2014;171(3–4):315–20. doi: 10.1016/j.vetmic.2014.02.002 24629773.

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

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

16. Animalia. Actions to combat antimicrobial resistance works (Tiltak mot antibiotikaresistens virker; in Norwegian) https://www.animalia.no/no/Dyr/antibiotikaresistens/aktuelt—antibiotikaresistens/tiltak-mot-antibiotikaresistens-virker/ (last accessed 08.03.2019)2015 [08.03.2019].

17. Animalia. Continued decrease in the occurrence of resistant bacteria in poultry (Fortsatt nedgang i forekomst av resistente bakterier hos fjørfe; in Norwegian) https://www.animalia.no/no/animalia/aktuelt/fortsatt-nedgang-i-forekomst-av-resistente-bakterier-hos-fjorfe/ (last accessed 08.03.2019)2016 [08.03.2019].

18. Animalia. Status for the poultry industry action plan against resistant bacteria in 2016 (Status for fjørfenæringas handlingsplan mot resistante bakterier i 2016; in Norwegian) https://www.animalia.no/no/animalia/aktuelt/status-for-fjorfenaringas-handlingsplan-mot-resistente-bakterier-i-2016/ (last accessed 08.03.2019)2017 [08.03.2019].

19. Animalia. Action plan: No detection of ESBL in samples from imported poultry in 2017 (Handlingsplan: Ingen funn av ESBL i prøver fra fjørfeimporter i 2017; in Norwegian) https://www.animalia.no/no/Dyr/antibiotikaresistens/aktuelt—antibiotikaresistens/fjorfenaringas-handlingsplan-ingen-funn-av-esbl-i-prover-fra-fjorfeimporter-i-2017/ (last accessed 08.03.2019)2018 [08.03.2019].

20. Refsum T. Antimicrobial use in the Norwegian poultry production (Antibiotikabehandling i norsk fjørfeproduksjon; in Norwegian). Go’ mørning 2015.

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

22. Agersø Y, Jensen JD, Hasman H, Pedersen K. Spread of extended spectrum cephalosporinase-producing Escherichia coli clones and plasmids from parent animals to broilers and to broiler meat in a production without use of cephalosporins. Foodborne Pathog Dis. 2014;11(9):740–6. doi: 10.1089/fpd.2014.1742 24972048.

23. Dierikx C, van der Goot J, Fabri T, van Essen-Zandbergen A, Smith H, Mevius D. Extended-spectrum-beta-lactamase- and AmpC-beta-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother. 2013;68(1):60–7. Epub 2012/09/06. doi: 10.1093/jac/dks349 22949623.

24. Hiroi M, Matsui S, Kubo R, Iida N, Noda Y, Kanda T, et al. Factors for occurrence of extended-spectrum beta-lactamase-producing Escherichia coli in broilers. J Vet Med Sci. 2012;74(12):1635–7. doi: 10.1292/jvms.11-0479 22786468.

25. Laube H, Friese A, von Salviati C, Guerra B, Käsbohrer A, Kreienbrock L, et al. Longitudinal Monitoring of extended-spectrum-beta-lactamase/AmpC-Producing Escherichia coli in German Broiler Chicken Fattening Farms. Appl Environ Microbiol. 2013;79(16):4815–20. Epub 2013/06/12. doi: 10.1128/AEM.00856-13 23747697.

26. Nilsson O, Börjesson S, Landén A, Bengtsson B. Vertical transmission of Escherichia coli carrying plasmid-mediated AmpC (pAmpC) through the broiler production pyramid. J Antimicrob Chemother. 2014;69(6):1497–500. doi: 10.1093/jac/dku030 24550380.

27. Newell DG, Fearnley C. Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol. 2003;69(8):4343–51. doi: 10.1128/AEM.69.8.4343-4351.2003 12902214

28. Torp M, Opheim M, Vigerust M, Bergsjø B, Hofshagen M. The surveillance programme for Campylobacter spp in broiler flocks in Norway 2016. Oslo, ISSN 1894-5678: 2017.

29. Heier BT, Tarpei A, Kalberg S, Bergsjø B. The surveillance programmes for Salmonella in live animals, eggs and meat in Norway 2016. Oslo, Norway: Norwegian Veterinary Institute, 2017 ISSN 1894-5678.

30. Schmidt GV, Mellerup A, Christiansen LE, Stahl M, Olsen JE, Angen O. Sampling and Pooling Methods for Capturing Herd Level Antibiotic Resistance in Swine Feces using qPCR and CFU Approaches. PLoS One. 2015;10(6):e0131672. doi: 10.1371/journal.pone.0131672 26114765

31. Perez-Perez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol. 2002;40(6):2153–62. doi: 10.1128/JCM.40.6.2153-2162.2002 12037080

32. Agersø Y, Aarestrup FM, Pedersen K, Seyfarth AM, Struve T, Hasman H. Prevalence of extended-spectrum cephalosporinase (ESC)-producing Escherichia coli in Danish slaughter pigs and retail meat identified by selective enrichment and association with cephalosporin usage. J Antimicrob Chemother. 2012;67(3):582–8. doi: 10.1093/jac/dkr507 22207594.

33. Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM. beta-Lactamases among extended-spectrum beta-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother. 2005;56(1):115–21. doi: 10.1093/jac/dki190 15941775.

34. Kapperud G, Skjerve E, Vik L, Hauge K, Lysaker A, Aalmen I, et al. Epidemiological investigation of risk factors for campylobacter colonization in Norwegian broiler flocks. Epidemiol Infect. 1993;111(2):245–55. doi: 10.1017/s0950268800056958 8405152

35. Hofshagen M, Jonsson ME, Opheim M. The surveillance and control programme for Campylobacter in broiler flocks in Norway. Oslo, Norway: Norwegian Veterinary Institute, 2008.

36. Jonsson ME, Chriel M, Norstrom M, Hofshagen M. Effect of climate and farm environment on Campylobacter spp. colonisation in Norwegian broiler flocks. Prev Vet Med. 2012;107(1–2):95–104. Epub 2012/06/08. doi: 10.1016/j.prevetmed.2012.05.002 22673580.

37. Lyngstad TM, Jonsson ME, Hofshagen M, Heier BT. Risk factors associated with the presence of Campylobacter species in Norwegian broiler flocks. Poult Sci. 2008;87(10):1987–94. doi: 10.3382/ps.2008-00132 18809860.

38. Chowdhury S, Sandberg M, Themudo GE, Ersboll AK. Risk factors for Campylobacter infection in Danish broiler chickens. Poult Sci. 2012;91(10):2701–9. Epub 2012/09/20. doi: 10.3382/ps.2012-02412 22991560.

39. Day MJ, Rodriguez I, van Essen-Zandbergen A, Dierikx C, Kadlec K, Schink AK, et al. Diversity of STs, plasmids and ESBL genes among Escherichia coli from humans, animals and food in Germany, the Netherlands and the UK. J Antimicrob Chemother. 2016;71(5):1178–82. doi: 10.1093/jac/dkv485 26803720.

40. Egea P, López-Cerero L, Torres E, Gómez-Sánchez Mdel C, Serrano L, Navarro Sánchez-Ortiz MD, et al. Increased raw poultry meat colonization by extended spectrum beta-lactamase-producing Escherichia coli in the south of Spain. Int J Food Microbiol. 2012;159(2):69–73. doi: 10.1016/j.ijfoodmicro.2012.08.002 23072690.

41. Huijbers PM, Graat EA, Haenen AP, van Santen MG, van Essen-Zandbergen A, Mevius DJ, et al. Extended-spectrum and AmpC beta-lactamase-producing Escherichia coli in broilers and people living and/or working on broiler farms: prevalence, risk factors and molecular characteristics. J Antimicrob Chemother. 2014;69(10):2669–75. doi: 10.1093/jac/dku178 24879667.

42. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, et al. Extended-spectrum beta-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis. 2011;17(7):1216–22. Epub 2011/07/19. doi: 10.3201/eid1707.110209 21762575

43. Vogt D, Overesch G, Endimiani A, Collaud A, Thomann A, Perreten V. Occurrence and genetic characteristics of third-generation cephalosporin-resistant Escherichia coli in Swiss retail meat. Microb Drug Resist. 2014;20(5):485–94. doi: 10.1089/mdr.2013.0210 24773305.

44. DANMAP. DANMAP 2014. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Copenhagen. ISSN 1600-2032: 2015 ISSN 1600-2032.

45. Börjesson S, Bengtsson B, Jernberg C, Englund S. Spread of extended-spectrum beta-lactamase producing Escherichia coli isolates in Swedish broilers mediated by an incl plasmid carrying bla(CTX-M-1). Acta Vet Scand. 2013;55:3. doi: 10.1186/1751-0147-55-3 23336334

46. SWEDRES/SVARM. SWEDRES/SVARM 2015. Consumption of antibiotics and occurrence of antibiotic resistance in Sweden. Uppsala/Solna. ISSN 1650-6332: 2016 ISSN 1650-6332.


Článek vyšel v časopise

PLOS One


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Léčba bolesti v ordinaci praktického lékaře
nový kurz
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Léčba akutní pooperační bolesti
Autoři: doc. MUDr. Jiří Málek, CSc.

Nové antipsychotikum kariprazin v léčbě schizofrenie
Autoři: prof. MUDr. Cyril Höschl, DrSc., FRCPsych.

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se