Escherichia coli and Salmonella spp. isolated from Australian meat chickens remain susceptible to critically important antimicrobial agents
Autoři:
Sam Abraham aff001; Mark O’Dea aff001; Shafi Sahibzada aff001; Kylie Hewson aff002; Anthony Pavic aff003; Tania Veltman aff004; Rebecca Abraham aff001; Taha Harris aff003; Darren J. Trott aff004; David Jordan aff005
Působiště autorů:
Antimicrobial Resistance and Infectious Disease Laboratory, Murdoch University, Murdoch, Western Australia, Australia
aff001; Australian Chicken Meat Federation, Sydney, New South Wales, Australia
aff002; Birling Avian Laboratories, Bringelly, New South Wales, Australia
aff003; Australian Centre for Antimicrobial Resistance Ecology, School of Animal and Veterinary Sciences, The University of Adelaide, Roseworthy, South Australia, Australia
aff004; New South Wales Department of Primary Industries, Wollongbar, New South Wales, Australia
aff005
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224281
Souhrn
The World Health Organisation has defined “highest priority critically important antimicrobials” (CIAs) as those requiring the greatest control during food production. Evidence demonstrating that restricted antimicrobial usage prevents the emergence of resistance to CIA’s amongst pathogenic and commensal organisms on a production system-wide scale would strengthen international efforts to control antimicrobial resistance (AMR). Therefore, in a designed survey of all major chicken-meat producers in Australia, we investigated the phenotypic AMR of E. coli (n = 206) and Salmonella (n = 53) from caecal samples of chickens at slaughter (n = 200). A large proportion of E. coli isolates (63.1%) were susceptible to all tested antimicrobials. With regards to CIA resistance, only two E.coli isolates demonstrated resistance to fluoroquinolones, attributed to mutations in the quinolone resistance-determining regions of gyrA. Antimicrobial resistance was observed for trimethoprim/sulfamethoxazole (8.7%), streptomycin (9.7%), ampicillin (14.1%), tetracycline (19.4%) and cefoxitin (0.5%). All Salmonella isolates were susceptible to ceftiofur, chloramphenicol, ciprofloxacin, colistin, florfenicol, gentamicin and tetracycline. A low frequency of Salmonella isolates exhibited resistance to streptomycin (1.9%), ampicillin (3.8%), and cefoxitin (11.3%). AMR was only observed among Salmonella Sofia serovars. None of the Salmonella isolates exhibited a multi-class-resistant phenotype. Whole genome sequencing did not identify any known resistance mechanisms for the Salmonella isolates demonstrating resistance to cefoxitin. The results provide strong evidence that resistance to highest priority CIA’s is absent in commensal E. coli and Salmonella isolated from Australian meat chickens, and demonstrates low levels of resistance to compounds with less critical ratings such as cefoxitin, trimethoprim/sulfamethoxazole, and tetracycline. Apart from regulated exclusion of CIAs from most aspects of livestock production, vaccination against key bacterial pathogens and stringent biosecurity are likely to have contributed to the favorable AMR status of the Australian chicken meat industry. Nevertheless, industry and government need to proactively monitor AMR and antimicrobial stewardship practices to ensure the long-term protection of both animal and human health.
Klíčová slova:
Meat – Livestock – Antimicrobial resistance – Poultry – Salmonella – Chickens – Tetracyclines – Salmonella typhimurium
Zdroje
1. WHO. Critically important antimicrobials for human medicine-5th revision. Geneva, Switzerland: World Health Organization; 2017. 41 p.
2. Hudson JA, Frewer LJ, Jones G, Brereton PA, Whittingham MJ, Stewart G. The agri-food chain and antimicrobial resistance: A review. Trends Food Sci Technol. 2017;69:131–47.
3. Marshall BM, Levy SB. Food Animals and Antimicrobials: Impacts on Human Health. Clin Microbiol Rev. 2011;24(4):718–33. doi: 10.1128/CMR.00002-11 21976606
4. Lambrecht E, Van Meervenne E, Boon N, Van de Wiele T, Wattiau P, Herman L, et al. Characterization of cefotaxime- and ciprofloxacin-resistant commensal Escherichia coli originating from belgian farm animals indicates high antibiotic resistance transfer rates. Microb Drug Resist. 2018;24(6):707–17. doi: 10.1089/mdr.2017.0226 29148895
5. Roth N, Käsbohrer A, Mayrhofer S, Zitz U, Hofacre C, Domig KJ. The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: A global overview. Poult Sci. 2019;98(4):1791–804. doi: 10.3382/ps/pey539 30544256
6. EFSA. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2016. EFSA journal. 2018;16(2):e05182.
7. Apostolakos I, Piccirillo A. A review on the current situation and challenges of colistin resistance in poultry production. Avian Pathol. 2018;47(6):546–58. doi: 10.1080/03079457.2018.1524573 30226397
8. Mukerji S, O’Dea M, Barton M, Kirkwood R, Lee T, Abraham S. Development and transmission of antimicrobial resistance among Gram-negative bacteria in animals and their public health impact. Essays Biochem. 2017;61(1):23–35. doi: 10.1042/EBC20160055 28258227
9. Barlow RS, McMillan KE, Duffy LL, Fegan N, Jordan D, Mellor GE. Prevalence and antimicrobial resistance of Salmonella and Escherichia coli from Australian cattle populations at slaughter. J Food Prot. 2015;78(5):912–20. doi: 10.4315/0362-028X.JFP-14-476 25951384
10. Van Breda LK, Dhungyel OP, Ginn AN, Iredell JR, Ward MP. Pre- and post-weaning scours in southeastern Australia: A survey of 22 commercial pig herds and characterisation of Escherichia coli isolates. PLOS ONE. 2017;12(3):e0172528. doi: 10.1371/journal.pone.0172528 28273152
11. Abraham S, Jordan D, Wong HS, Johnson JR, Toleman MA, Wakeham DL, et al. First detection of extended-spectrum cephalosporin-and fluoroquinolone-resistant Escherichia coli in Australian food-producing animals. J Glob Antimicrob Resist. 2015;3(4):273–7. doi: 10.1016/j.jgar.2015.08.002 27842872
12. Kidsley AK, Abraham S, Bell JM, O’Dea M, Laird TJ, Jordan D, et al. Antimicrobial susceptibility of Escherichia coli and Salmonella spp. Isolates from healthy pigs in australia: Results of a pilot national survey. Frontiers in microbiology. 2018;9:1207-. doi: 10.3389/fmicb.2018.01207 30038598
13. Sparham SJ, Kwong JC, Valcanis M, Easton M, Trott DJ, Seemann T, et al. Emergence of multidrug resistance in locally-acquired human infections with Salmonella Typhimurium in Australia owing to a new clade harbouring blaCTX-M-9. Int J Antimicrob Agents. 2017;50(1):101–5. doi: 10.1016/j.ijantimicag.2017.02.014 28476613
14. Wong L, Selvanathan EA, Selvanathan S. Modelling the meat consumption patterns in Australia. Economic Modelling. 2015;49:1–10.
15. ABARES. Agricultural commodities: March quarter 2017. Canberra, Australia: Australian Bureau of Agricultural and Resource Economics and Sciences; 2017. 271 p.
16. DAFF. Pilot surveillance program for Antimicrobial resistance in bacteria of animal origin. Australian Government Department of Agriculture, Fisheries and Forestry Canberra; 2007.
17. Vangchhia B, Blyton MDJ, Collignon P, Kennedy K, Gordon DM. Factors affecting the presence, genetic diversity and antimicrobial sensitivity of Escherichia coli in poultry meat samples collected from Canberra, Australia. Environmental Microbiology. 2018;20(4):1350–61. doi: 10.1111/1462-2920.14030 29266683
18. McLellan JE, Pitcher JI, Ballard SA, Grabsch EA, Bell JM, Barton M, et al. Superbugs in the supermarket? Assessing the rate of contamination with third-generation cephalosporin-resistant gram-negative bacteria in fresh Australian pork and chicken. Antimicrobial Resistance & Infection Control. 2018;7(1):30.
19. Vangchhia B, Abraham S, Bell JM, Collignon P, Gibson JS, Ingram PR, et al. Phylogenetic diversity, antimicrobial susceptibility and virulence characteristics of phylogroup F Escherichia coli in Australia. Microbiology. 2016;162(11):1904–12. doi: 10.1099/mic.0.000367 27666313
20. NARMS. Sampling for the national antimicrobial resistance monitoring system. 2014.
21. O’Dea M, Sahibzada S, Jordan D, Laird T, Lee T, Hewson K, et al. Genomic, antimicrobial resistance and public health insights into Enterococcus spp. from Australian chickens. J Clin Microbiol. 2019:JCM.00319-19.
22. International Organization for Standardization. Microbiology of food and animal feeding stuffs—horizontal method for the detection of Salmonella spp. ISO 6579: 2002, MOD: ISO; 2009.
23. EUCAST. Breakpoint tables for interpretation of MICs and zone diameters: Version 8.1, valid from 2018-05-15: The European Committee on Antimicrobial Susceptibility Testing; 2018 [http://www.eucast.org.
24. Turnidge J, Kahlmeter G, Kronvall G. Statistical characterisation of bacterial wild-type MIC value distributions and the determination of epidemiological cut-off values. Clinical Microbiology and Infection. 2006;12(5):418–25. doi: 10.1111/j.1469-0691.2006.01377.x 16643517
25. Simjee S, McDermott P, Trott DJ, Chuanchuen R. Present and future surveillance of antimicrobial resistance in animals: Principles and practices. In: Schwarz S, Cavaco LM, Shen J, editors. Antimicrobial Resistance in Bacteria from Livestock and Companion Animals. 6. 2018/07/14 ed. United States: American Society of Microbiology; 2018.
26. Abraham S, Kirkwood RN, Laird T, Saputra S, Mitchell T, Singh M, et al. Dissemination and persistence of extended-spectrum cephalosporin-resistance encoding IncI1-bla CTXM-1 plasmid among Escherichia coli in pigs. The ISME journal. 2018;12(10):2352–62. doi: 10.1038/s41396-018-0200-3 29899511
27. CIPARS. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS). Guelph, Ontario: Public Health Agency of Canada; 2018.
28. NARMS. National Antimicrobial Resistance Monitoring System: NARMS integrated report, 2015. Laurel, MD: U.S. Department of Health and Human Services, Services USDoHaH; 2017. Contract No.: October 2018.
29. Pande VV, Gole VC, McWhorter AR, Abraham S, Chousalkar KK. Antimicrobial resistance of non-typhoidal Salmonella isolates from egg layer flocks and egg shells. Int J Food Microbiol. 2015;203:23–6. doi: 10.1016/j.ijfoodmicro.2015.02.025 25770430
30. APVMA. Quantity of antimicrobial products sold for veterinary use in Australia. Authority APaVM, editor. Canberra, Australia 2014. 73 p.
31. DANMAP. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. 2016. p. 1–142.
32. Dutil L, Irwin R, Finley R, Ng LK, Avery B, Boerlin P, et al. Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg Infect Dis. 2010;16(1):48–54. doi: 10.3201/eid1601.090729 20031042
33. Escherichia coli [Internet]. 2017. http://mlst.warwick.ac.uk/mlst/dbs/Ecoli.
34. Blaak H, van Hoek AH, Hamidjaja RA, van der Plaats RQ, Kerkhof-de Heer L, de Roda Husman AM, et al. Distribution, numbers, and diversity of esbl-producing E. coli in the poultry farm environment. PLOS ONE. 2015;10(8):e0135402. doi: 10.1371/journal.pone.0135402 26270644
35. DANMAP. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Statens Serum Institut; 2015.
36. Alikhan N-F, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLOS Genetics. 2018;14(4):e1007261. doi: 10.1371/journal.pgen.1007261 29621240
37. Mukerji S, Stegger M, Truswell AV, Laird T, Jordan D, Abraham RJ, et al. Resistance to critically important antimicrobials in Australian seagulls (Chroicocephalus novaehollandiae) and evidence of anthropogenic origins. J Antimicrob Chemotherin press.
38. DAFF. Importing fertile eggs (poultry): Australian Government Department of Agriculture, Fisheries and Forestry Canberra; 2019 [http://www.agriculture.gov.au/import/goods/live-animals/fertile-egg-imports.
39. Badger S, Abraham S, Saputra S, Trott DJ, Turnidge J, Mitchell T, et al. Relative performance of antimicrobial susceptibility assays on clinical Escherichia coli isolates from animals. Vet Microbiol. 2018;214:56–64. doi: 10.1016/j.vetmic.2017.12.008 29408033
40. JETACAR. The use of antibiotics in food-producing animals: antibiotic-resistant bacteria in animals and humans. Commonwealth department of health and aged care, Commonwealth department of agriculture, fisheries and forestry, Australia., AustraliaCo; 1999.
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Eliquis (apixaban) nově hrazen ze zdravotního pojištění
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs