Prevalence and characterization of ESBL- and AmpC-producing Enterobacteriaceae on retail vegetables

International Journal of Food Microbiology

Volumn 204, Issue , 2015, Pages 1-8

  van Hoek, Angela H A M ^a   Veenman, Christiaan ^a   van Overbeek, Wendy M ^a   Lynch, Gretta ^a   de Roda Husman, Ana Maria ^a,b   Blaak, Hetty ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Conventional; E. coli; Fresh produce; Organic; Supermarket

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; BETA LACTAMASE AMPC; BORONIC ACID DERIVATIVE; CEFOTAXIME; CEFTAZIDIME; CEPHALOSPORIN; CHLORAMPHENICOL; EXTENDED SPECTRUM BETA LACTAMASE; NALIDIXIC ACID; STREPTOMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE; AMPC BETA-LACTAMASES; BACTERIAL PROTEIN; BETA LACTAMASE; CEPHALOSPORIN DERIVATIVE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIUM DETECTION; BLANCHED CELERY; BUNCHED CARROT; BUTTERHEAD LETTUCE; CEDECCA; CHICORY; CITROBACTER FREUNDII; ENDIVE; ENTEROBACTER; ENTEROBACTERIACEAE; ESCHERICHIA COLI; FOOD CONTAMINATION; FOOD INTAKE; GENE IDENTIFICATION; HAFNIA ALVEI; ICEBERG LETTUCE; LEAFY VEGETABLE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PANTOEA; PLANT BULB; PLANT ROOT; PUBLIC HEALTH; RADISH; RAHNELLA AQUATILIS; RAW FOOD; RISK; SERRATIA; SERRATIA FONTICOLA; SERRATIA PLYMUTHICA; SOIL; SPRING ONION; VEGETABLE; ANALYSIS; DRUG EFFECTS; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MULTIDRUG RESISTANCE; NETHERLANDS; PREVALENCE;

APIUM GRAVEOLENS VAR. DULCE; CICHORIUM INTYBUS; CITROBACTER FREUNDII; DAUCUS CAROTA; ENTEROBACTER; ENTEROBACTERIACEAE; ESCHERICHIA COLI; HAFNIA ALVEI; LACTUCA; PANTOEA; RAHNELLA AQUATILIS; RAPHANUS SATIVUS; SERRATIA FONTICOLA; SERRATIA PLYMUTHICA;

BACTERIAL PROTEINS; BETA-LACTAMASES; CEPHALOSPORINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROBACTERIACEAE; FOOD CONTAMINATION; HUMANS; NETHERLANDS; PREVALENCE; VEGETABLES;

EID: 84925598096     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.03.014     Document Type: Article

References (44)

1. Abbott S.L., Cheung W.K., Janda J.M. The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J. Clin. Microbiol. 2003, 41:2348-2357.
2. Ambler R.P. The structure of β-lactamases. Philos. Trans. R. Soc. B Biol. Sci. 1980, 289:321-331.
3. Blaak H., van Hoek A.H.A.M., Veenman C., Docters van Leeuwen A.E., Lynch G., van Overbeek W.M., de Roda Husman A.M. Extended spectrum β-lactamase- and constitutively AmpC-producing Enterobacteriaceae on fresh produce and in the agricultural environment. Int. J. Food Microbiol. 2014, 168-169:8-16.
4. Bush K., Jacoby G.A. Updated functional classification of β-lactamases. Antimicrob. Agents Chemother. 2010, 54:969-976.
5. Cantón R., Novais A., Valverde A., Machado E., Peixe L., Baquero F., Coque T.M. Prevalence and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 2008, 14(Suppl. 1):144-153.
6. Carattoli A. Animal reservoirs for extended spectrum β-lactamase producers. Clin. Microbiol. Infect. 2008, 14(Suppl. 1):117-123.
7. Claycamp H.G., Hooberman B.H. Antimicrobial resistance risk assessment in food safety. J. Food Prot. 2004, 67:2063-2071.
8. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing; Twentieth Informational Supplement M100-S22 2012, CLSI, Wayne, PA, USA.
9. Coque T.M., Baquero F., Cantón R. Increasing prevalence of ESBL-producing Enterobacteriaceae in Europe. Eurosurveillance 2008, 13. (pii=19044).
10. Coudron P.E. Inhibitor-based methods for detection of plasmid-mediated AmpC beta-lactamases in Klebsiella spp., Escherichia coli, and Proteus mirabilis. J. Clin. Microbiol. 2005, 43:4163-4167.
11. Crompton I.E., Cuthbert B.K., Lowe G., Waley S.G. β-Lactamases inhibitors. The inhibition of serine β-lactamases by specific boronic acids. Biochem. J. 1988, 251:453-459.
12. Dallenne C., Da Costa A., Decré D., Favier C., Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important b-lactamases in Enterobacteriaceae. J. Antimicrob. Chemother. 2010, 65:490-495.
13. De Maayer P., Chan W.Y., Rezzonico F., Buhlmann A., Venter S.N., Blom J., Goesmann A., Frey J.E., Smits T.H., Duffy B., Coutinho T.A. Complete genome sequence of clinical isolate Pantoea ananatis LMG 5342. J. Bacteriol. 2012, 194:1615-1616.
14. Djordjevic S.P., Stokes H.W., Roy Chowdhury P. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front. Microbiol. 2013, 4:86.
15. Edelstein M., Pimkin M., Palagin I., Edelstein I., Stratchounski L. Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob. Agents Chemother. 2003, 47:3724-3732.
16. Eder W., Ludwig W., Huber R. Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of Kebrit Deep, Red Sea. Arch. Microbiol. 1999, 172:213-218.
17. EFSA Scientific opinion on the risk posed by pathogens in food of non-animal origin. Part 1 (outbreak data analysis and risk ranking of food/pathogen combinations). EFSA J. 2013, 11:3025.
18. Egea P., López-Cerero L., Navarro M.D., Rodríguez-Baňo J., Pascual A. Assessment of the presence of extended-spectrum beta-lactamase-producing Escherichia coli in eggshells and ready-to-eat products. Eur. J. Clin. Microbiol. Infect. Dis. 2011, 30:1045-1047.
19. EUCAST http://www.eucast.org/.
20. Ewers C., Bethe A., Semmler T., Guenther S., Wieler L.H. Extended-spectrum β-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, 18:646-655.
21. Frank C., Werber D., Jakob D.V.M., Cramer P., Askar M., Faber M., an der Heiden M., Bernard H., Fruth A., Prager R., Spode A., Wadl M., Zoufaly A., Jordan S., Kemper M.J., Follin P., Müller L., King L.A., Rosner B., Buchholz U., Stark K., Krause G. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N. Engl. J. Med. 2011, 365:1771-1780.
22. Franz E., van Bruggen A.H. Ecology of E. coli O157:H7 and Salmonella enterica in the primary vegetable production chain. Crit. Rev. Microbiol. 2008, 34:143-161.
23. Franz E., Semenov A.V., van Bruggen A.H. Modelling the contamination of lettuce with Escherichia coli O157:H7 from manure-amended soil and the effect of intervention strategies. J. Appl. Microbiol. 2008, 105:1569-1584.
24. Hassan S.A., Altalhi A.D., Gherbawy Y.A., El-Deeb B.A. Bacterial load of fresh vegetables and their resistance to the currently used antibiotics in Saudi Arabia. Foodborne Pathog. Dis. 2011, 8:1011-1018.
25. Heaton J.C., Jones K. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J. Appl. Microbiol. 2008, 104:613-626.
26. Huijbers P.M.C., Graat E.A.M., Haenen A.P.J., van Santen M.G., van Essen-Zandbergen A., Mevius D.J., van Duijkeren E., van Hoek A.H.A.M. Extended-spectrum and AmpC β-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, 69:2669-2675.
27. Humeniuk C., Arlet G., Gautier V., Grimont P., Labia R., Philippon A. β-Lactamases of Kluyvera ascorbata, probable progenitors of some plasmid-encoded CTX-M types. Antimicrob. Agents Chemother. 2002, 46:3045-3049.
28. Jacobs J.A., Schot C.S., Schouls L.M. Haemolytic activity of the 'Streptococcus milleri group' and relationship between haemolysis restricted to human red blood cells and pathogenicity in S. intermedius. J. Med. Microbiol. 2000, 49:55-62.
29. Jacoby G.A. AmpC β-lactamases. Clin. Microbiol. Rev. 2009, 22:161-182.
30. Lynch M.F., Tauxe R.V., Hedberg C.W. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol. Infect. 2009, 307-315.
31. Mesa R.J., Blanc V., Blanch A.R., Cortés P., González J.J., Lavilla S., Miró E., Muniesa M., Saco M., Tórtola M.T., Mirelis B., Coll P., Llagostera M., Prats G., Navarro F. Extended-spectrum β-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms and sewage). J. Antimicrob. Chemother. 2006, 58:211-215.
32. Nethmap_MARAN 2014 Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2013 http://www.swab.nl.
33. Olaimat A.N., Holley R.A. Factors influencing the microbial safety of fresh produce: a review. Food Microbiol. 2012, 32:1-19.
34. Olson A.B., Silverman M., Boyd D.A., McGeer A., Willey B.M., Pong-Porter V., Daneman N., Mulvey M.R. Identification of a progenitor of the CTX-M-9 group of extended-spectrum β-lactamases from Kluyvera georgiana isolated in Guyana. Antimicrob. Agents Chemother. 2001, 49:2112-2115.
35. Raphael E., Wong L.K., Riley L.W. Extended-spectrum beta-lactamase gene sequences in Gram-negative saprophytes on retail organic and nonorganic spinach. Appl. Environ. Microbiol. 2011, 77:1601-1607.
36. Reuland E.A., Al Naiemi N., Raadsen S.A., Savelkoul P.H.M., Kluytmans J.A.J.W., Vandenbroucke-Grauls C.M.J.E. Prevalence of ESBL-producing Enterobacteriaceae in raw vegetables. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 10.1007/s10096-014-2142-7.
37. Ruimy R., Brisabois A., Bernede C., Skurnik D., Barnat S., Arlet G., Momcilovic S., Elbaz S., Moury F., Vibet M.A., Courvalin P., Guillemot D., Andremont A. Organic and conventional fruits and vegetables contain equivalent counts of Gram-negative bacteria expressing resistance to antibacterial agents. Environ. Microbiol. 2010, 12:608-615.
38. Schwaiger K., Helmke K., Holzel C.S., Bauer J. Antibiotic resistance in bacteria isolated from vegetables with regards to the marketing stage (farm vs. supermarket). Int. J. Food Microbiol. 2011, 148:191-196.
39. Smet A., Rasschaert G., Martel A., Persoon D., Dewulf J., Butaye P., Catry B., Haesebrouck F., Herman L., Heyndrickx M. In situ ESBL conjugation from avian to human Escherichia coli during cefotaxime administration. J. Appl. Microbiol. 2011, 110:541-549.
40. Snary E.L., Kelly L.A., Davison H.C., Teale C.J., Wooldridge M. Antimicrobial resistance: a microbial risk assessment perspective. J. Antimicrob. Chemother. 2004, 53:906-917.
41. Teunis P.F.M., Rutjes S.A., Westrell T., de Roda Husman A.M. Characterization of drinking water treatment for virus risk assessment. Water Res. 2009, 43:395-404.
42. Tyler H.L., Triplett E.W. Plants as a habitat for beneficial and/or human pathogenic bacteria. Annu. Rev. Phytopathol. 2008, 46:53-73.
43. Walsh C., Fanning S. Antimicrobial resistance in foodborne pathogens-a cause for concern?. Curr. Drug Targets 2008, 9:808-815.
44. Yagi T., Wachino J., Kurokawa H., Suzuki S., Yamane K., Doi Y., Shibata N., Kato H., Shibayama K., Arakawa Y. Practical methods using boronic acid compounds for identification of class C β-lactamase-producing Klebsiella pneumoniae and Escherichia coli. J. Clin. Microbiol. 2005, 43:2551-2558.