Detection of extended-spectrum beta-lactamase (ESBL)-producing escherichia coli on flies at poultry farms

Applied and Environmental Microbiology

Volumn 80, Issue 1, 2014, Pages 239-246

  Blaak, Hetty ^a   Hamidjaja, Raditijo A ^a   Van Hoek, Angela H A M ^a   De Heer, Lianne ^a   De Roda Husman, Ana Maria ^a   Schets, Franciska M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE ROUTES; CHICKEN MEAT; ESCHERICHIA COLI BACTERIA; GENETIC BACKGROUNDS; HOUSE-FLIES; HUMAN POPULATION; PHYLOGENETIC GROUPS; POULTRY FARMS;

LAKES; MANURES;

ESCHERICHIA COLI;

COLIFORM BACTERIUM; DATA SET; DETECTION METHOD; ENZYME ACTIVITY; FLY; MANURE; POPULATION STRUCTURE; POULTRY;

BETA LACTAMASE;

ANIMAL; ARTICLE; CHICKEN; CLASSIFICATION; DIPTERA; DNA SEQUENCE; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; MANURE; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; NETHERLANDS; SECRETION (PROCESS);

ANIMALS; BETA-LACTAMASES; CHICKENS; DIPTERA; ESCHERICHIA COLI; GENOTYPE; HUMANS; MANURE; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; NETHERLANDS; SEQUENCE ANALYSIS, DNA; WATER MICROBIOLOGY;

EID: 84891057937     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02616-13     Document Type: Article

References (45)

1. Cantón R, Novais A, Valverde A, Machado E, Peixe L, Baquero F, Coque TM. 2008. Prevalence and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 14(Suppl. 1):144-153. http://dx.doi.org/10.1111/j.1469-0691.2007.01850.x.
2. Castanheira M, Mendes RE, Rhomberg PR, Jones RN. 2008. Rapid emergence of blaCTX-M among Enterobacteriaceae in U.S. Medical Centers: molecular evaluation from the MYSTIC Program (2007). Microb. Drug Resist. 14:211-216. http://dx.doi.org/10.1089/mdr.2008.0827.
3. Cantón R, Akova M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, Livermore DM, Miriagou V, Naas T, Rossolini GM, Samuelsen O, Seifert H, Woodford N, Nordmann P. 2012. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 18:413-431. http://dx.doi.org/10.1111/j.1469-0691.2012.03821.x.
4. Livermore DM, Canton R, Gniadkowski M, Nordmann P, Rossolini GM, Arlet G, Ayala J, Coque TM, Kern-Zdanowicz I, Luzzaro F, Poirel L, Woodford N. 2007. CTX-M: changing the face of ESBLs in Europe. J. Antimicrob. Chemother. 59:165-174. http://dx.doi.org/10.1093/jac/dkl483.
5. Paterson DL, Bonomo RA. 2005. Extended-spectrum beta-lactamases: a clinical update. Clin. Microbiol. Rev. 18:657-686. http://dx.doi.org/10.1128/CMR.18.4.657-686.2005.
6. Huijbers PM, de Kraker M, Graat EA, van Hoek AH, van Santen MG, de Jong MC, van Duijkeren E, de Greeff SC. 2013. Prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in humans living in municipalities with high and low broiler density. Clin. Microbiol. Infect. 19:E256-E259. http://dx.doi.org/10.1111/1469-0691.12150.
7. Trott D. 2013. Beta-lactam resistance in gram-negative pathogens isolated from animals. Curr. Pharm. Des. 19:239-249. http://dx.doi.org/10.2174/138161213804070339.
8. Mevius DJ, Koene MGJ, Wit B, van Pelt W, Bondt N. 2012. Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2010/2011. Nethmap_MARAN report. http://www.uu.nl/SiteCollectionImages/Fac_DGK/Nieuwsplaatjes/Nieuws/2012/NethmapMaran_Web.pdf.
9. Blaak H, van Rooyen SR, Schuijt MS, Docters van Leeuwen AE, van den Berg HHJL, Lodder-Verschoor F, Italiaander R, Schets FM, de Roda Husman AM. 2011. Prevalence of antibiotic resistant bacteria inthe rivers Meuse, Rhine and New Meuse. RIVM report 703719071. National Institute for Public Health and the Environment, Bilthoven, The Netherlands.
10. Chen H, Shu W, Chang X, Chen JA, Guo Y, Tan Y. 2010. The profile of antibiotics resistance and integrons of extended-spectrum beta-lactamase producing thermotolerant coliforms isolated from the Yangtze River basin in Chongqing. Environ. Pollut. 158:2459-2464. http://dx.doi.org/10.1016/j.envpol.2010.03.023.
11. Dhanji H, Murphy NM, Akhigbe C, Doumith M, Hope R, Livermore DM, Woodford N. 2011. Isolation of fluoroquinolone-resistant O25b: H4-ST131 Escherichia coli with CTX-M-14 extended-spectrum β-lactamase from UK river water. J. Antimicrob. Chemother. 66:512-516. http://dx.doi.org/10.1093/jac/dkq472.
12. Hong H, Chun J, Lee Y. 2004. Detection of extended-spectrum-lactamase-producing, multidrug-resistant environmental isolates of Escherichia coli that bind to human bladder cells. Microb. Drug Resist. 10:184-189. http://dx.doi.org/10.1089/1076629041310145.
13. Guenther S, Ewers C, Wieler LH. 2011. Extended-spectrum betalactamases producing E. coli in wildlife, yet another form of environmental pollution? Front. Microbiol. 2:246. http://dx.doi.org/10.3389/fmicb.2011.00246.
14. Dierikx C, van der Goot J, Fabri T, van Essen-Zandbergen A, Smith H, Mevius D. 2013. Extended-spectrum-beta-lactamase-and AmpC-betalactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J. Antimicrob. Chemother. 68:60-67. http://dx.doi.org/10.1093/jac/dks349.
15. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K, Huijsdens X, Kluytmans J. 2011. Extended-spectrum beta-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg. Infect. Dis. 17:1216-1222. http://dx.doi.org/10.3201/eid1707.110209.
16. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, Platteel T, Fluit AC, van de Sande-Bruinsma N, Scharinga J, Bonten MJ, Mevius DJ. 2011. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin. Microbiol. Infect. 17:873-880. http://dx.doi.org/10.1111/j.1469-0691.2011.03497.x.
17. Greenberg B. 1973. Flies and disease, vol II: biology and disease transmission. Princeton University Press, Princeton, NJ.
18. De Jesus AJ, Olsen AR, Bryce JR, Whiting RC. 2004. Quantitative contamination and transfer of Escherichia coli from foods by houseflies, Musca domestica L. (Diptera: Muscidae). Int. J. Food Microbiol. 93:259-262. http://dx.doi.org/10.1016/j.ijfoodmicro.2003.12.003.
19. Forster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K. 2007. Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol. Res. 101:243-246. http://dx.doi.org/10.1007/s00436-007-0522-y.
20. Forster M, Sievert K, Messler S, Klimpel S, Pfeffer K. 2009. Comprehensive study on the occurrence and distribution of pathogenic microorganisms carried by synanthropic flies caught at different rural locations in Germany. J. Med. Entomol. 46:1164-1166. http://dx.doi.org/10.1603/033.046.0526.
21. Kobayashi M, Sasaki T, Saito N, Tamura K, Suzuki K, Watanabe H, Agui N. 1999. Houseflies: not simple mechanical vectors of enterohemorrhagic Escherichia coli O157:H7. Am. J. Trop. Med. Hyg. 61:625-629.
22. Sasaki T, Kobayashi M, Agui N. 2000. Epidemiological potential of excretion and regurgitation by Musca domestica (Diptera: Muscidae) in the dissemination of Escherichia coli O157: H7 to food. J. Med. Entomol. 37:945-949. http://dx.doi.org/10.1603/0022-2585-37.6.945.
23. Pava-Ripoll M, Pearson RE, Miller AK, Ziobro GC. 2012. Prevalence and relative risk of Cronobacter spp., Salmonella spp., and Listeria monocytogenes associated with the body surfaces and guts of individual filth flies. Appl. Environ. Microbiol. 78:7891-7902. http://dx.doi.org/10.1128/AEM.02195-12.
24. Shane SM, Montrose MS, Harrington KS. 1985. Transmission of Campylobacter jejuni by the housefly (Musca domestica). Avian Dis. 29:384-391. http://dx.doi.org/10.2307/1590499.
25. Echeverria P, Harrison BA, Tirapat C, McFarland A. 1983. Flies as a source of enteric pathogens in a rural village in Thailand. Appl. Environ. Microbiol. 46:32-36.
26. Fotedar R, Banerjee U, Samantray JC, Shriniwas. 1992. Vector potential of hospital houseflies with special reference to Klebsiella species. Epidemiol. Infect. 109:143-147.
27. Moriya K, Fujibayashi T, Yoshihara T, Matsuda A, Sumi N, Umezaki N, Kurahashi H, Agui N, Wada A, Watanabe H. 1999. Verotoxinproducing Escherichia coli O157:H7 carried by the housefly in Japan. Med. Vet. Entomol. 13:214-216. http://dx.doi.org/10.1046/j.1365-2915.1999.00161.x.
28. Murvosh CM, Taggard CW. 1966. Ecological studies of the housefly. Ann. Entomol Soc. Am. 59:534-547.
29. Nazni WA, Luke H, Wan Rozita WM, Abdullah AG, Sa'diyah I, Azahari AH, Zamree I, Tan SB, Lee HL, Sofian MA. 2005. Determination of the flight range and dispersal of the house fly, Musca domestica (L.) using mark release recapture technique. Trop. Biomed. 22:53-61.
30. Anonymous. 2001. International standard. ISO 16649-2. Microbiology of food and animal feeding stuffs: horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli. Part 2. Colony count technique at 44°C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. International Organization for Standardization, Geneva, Switzerland.
31. Clinical and Laboratory Standards Institute. 2010. Performance standards for antimicrobial susceptibility testing; 20th informational supplement M100-S20. CLSI, Wayne, PA.
32. Dallenne C, Da Costa A, Decre D, Favier C, Arlet G. 2010. Development of a set of multiplex PCR assays for the detection of genes encoding important-lactamases in Enterobacteriaceae. J. Antimicrob. Chemother. 65:490-495. http://dx.doi.org/10.1093/jac/dkp498.
33. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:4555-4558. http://dx.doi.org/10.1128/AEM.66.10.4555-4558.2000.
34. Escobar-Paramo P, Le Menac'h A, Le Gall T, Amorin C, Gouriou S, Picard B, Skurnik D, Denamur E. 2006. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ. Microbiol. 8:1975-1984. http://dx.doi.org/10.1111/j.1462-2920.2006.01077.x.
35. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60: 1136-1151. http://dx.doi.org/10.1111/j.1365-2958.2006.05172.x.
36. Deplano A, Denis O, Rodriguez-Villalobos H, De Ryck R, Struelens MJ, Hallin M. 2011. Controlled performance evaluation of the DiversiLab repetitive-sequence-based genotyping system for typing multidrugresistant health care-associated bacterial pathogens. J. Clin. Microbiol. 49:3616-3620. http://dx.doi.org/10.1128/JCM.00528-11.
37. Dierikx CM, van Duijkeren E, Schoormans AH, van Essen-Zandbergen A, Veldman K, Kant A, Huijsdens XW, van der Zwaluw K, Wagenaar JA, Mevius DJ. 2012. Occurrence and characteristics of extendedspectrum-beta-lactamase-and AmpC-producing clinical isolates derived from companion animals and horses. J. Antimicrob. Chemother. 67: 1368-1374. http://dx.doi.org/10.1093/jac/dks049.
38. Reuland EA, Overdevest IT, Al Naiemi N, Kalpoe JS, Rijnsburger MC, Raadsen SA, Ligtenberg-Burgman I, van der Zwaluw KW, Heck M, Savelkoul PH, Kluytmans JA, Vandenbroucke-Grauls CM. 2013. High prevalence of ESBL-producing Enterobacteriaceae carriage in Dutch community patients with gastrointestinal complaints. Clin. Microbiol. Infect. 19:542-549. http://dx.doi.org/10.1111/j.1469-0691.2012.03947.x.
39. Smet A, Martel A, Persoons D, Dewulf J, Heyndrickx M, Claeys G, Lontie M, Van Meensel B, Herman L, Haesebrouck F, Butaye P. 2010. Characterization of extended-spectrum beta-lactamases produced by Escherichia coli isolated from hospitalized and nonhospitalized patients: emergence of CTX-M-15-producing strains causing urinary tract infections. Microb. Drug Resist. 16:129-134. http://dx.doi.org/10.1089/mdr.2009.0132.
40. Schink AK, Kadlec K, Kaspar H, Mankertz J, Schwarz S. 2013. Analysis of extended-spectrum-beta-lactamase-producing Escherichia coli isolates collected in the GERM-Vet monitoring programme. J. Antimicrob. Chemother. 68:1741-1749. http://dx.doi.org/10.1093/jac/dkt123.
41. Lysyk TJ, Axtell RC. 1986. Movement and distribution of house flies (Diptera: Muscidae) between habitats in two livestock farms. J. Econ. Entomol. 79:993-998.
42. Dolejska M, Duskova E, Rybarikova J, Janoszowska D, Roubalova E, Dibdakova K, Maceckova G, Kohoutova L, Literak I, Smola J, Cizek A. 2011. Plasmids carrying blaCTX-M-1 and qnr genes in Escherichia coliisolates from an equine clinic and a horseback riding centre. J. Antimicrob. Chemother. 66:757-764. http://dx.doi.org/10.1093/jac/dkq500.
43. Usui M, Iwasa T, Fukuda A, Sato T, Okubo T, Tamura Y. 2013. The role of flies in spreading the extended-spectrum beta-lactamase gene from cattle. Microb. Drug Resist. 19:415-420. http://dx.doi.org/10.1089/mdr.2012.0251.
44. Snary EL, Kelly LA, Davison HC, Teale CJ, Wooldridge M. 2004. Antimicrobial resistance: a microbial risk assessment perspective. J. Antimicrob. Chemother. 53:906-917. http://dx.doi.org/10.1093/jac/dkh182.
45. Heller J, Kelly L, Reid SW, Mellor DJ. 2010. Qualitative risk assessment of the acquisition of Meticillin-resistant staphylococcus aureus in pet dogs. Risk Anal. 30:458-472. http://dx.doi.org/10.1111/j.1539-6924.2009.01342.x.