Pathogenic and commensal Escherichiacoli from irrigation water show potential in transmission of extended spectrum and AmpC β-lactamases determinants to isolates from lettuce

Microbial Biotechnology

Volumn 8, Issue 3, 2015, Pages 462-473

  Njage, Patrick M K ^a,b   Buys, Elna M ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE AMPC; EXTENDED SPECTRUM BETA LACTAMASE; WATER; ANTIINFECTIVE AGENT; BETA LACTAM; BETA LACTAMASE;

ARTICLE; BACTERIAL TRANSMISSION; BACTERIUM ISOLATE; BACTERIUM ISOLATION; COMMENSAL ESCHERICHIA COLI; CONJUGATION; CONTROLLED STUDY; GENE FREQUENCY; GENE TRANSFER; GENETIC SIMILARITY; GENOTYPE; IN VITRO STUDY; LETTUCE; NONHUMAN; PHENOTYPE; PHYLOGENY; ANTIBIOTIC RESISTANCE; BACTERIUM CONJUGATION; CLUSTER ANALYSIS; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; HORIZONTAL GENE TRANSFER; IRRIGATION (AGRICULTURE); ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR TYPING;

ESCHERICHIA COLI; LACTUCA;

AGRICULTURAL IRRIGATION; ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; BETA-LACTAMS; CLUSTER ANALYSIS; CONJUGATION, GENETIC; ESCHERICHIA COLI; GENE TRANSFER, HORIZONTAL; GENOTYPE; LETTUCE; MOLECULAR TYPING; WATER MICROBIOLOGY;

EID: 84928091702     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12234     Document Type: Article

References (62)

1. Aijuka, M., Charimba, G., Hugo, C.J., and Buys, E.M. (2014) Characterization of bacterial pathogens in rural and urban irrigation water. J Water Health. doi:10.2166/wh.2014.228.
2. Bezanson, G.S., MacInnis, R., Potter, G., and Hughes, T. (2008) Presence and potential for horizontal transfer of antibiotic resistance in oxidase-positive bacteria populating raw salad vegetables. Int J Food Microbiol 127: 37-42.
3. Bhutani, N., Talreja, D., Walia, S., Muraleedharan, C., Kumar, A., Rana, S.W., etal. (2012) Molecular analysis of Extended-Spectrum Beta-Lactamases (ESBLs) gene sequences of bacteria on retail lettuce and relatedness to clinical isolates. 52nd Interscience Conference on Antimicrobial Agents and Chemotherapy, San Francisco [WWW document]. URL http://www.abstractsonline.com/Plan/ViewAbstract.aspx?sKey=4ca432d4-62da-4f34-a6b9-fbfe2e656547&cKey=8fdcb57a-a59e-48d4-b806-5bb05c4cecc9&mKey={6B114A1D-85A4-4054-A83B-04D8B9B8749F}]Ent]
4. Boehme, S., Werner, G., Klare, I., Reissbrodt, R., and Witte, W. (2004) Occurrence of antibiotic resistant enterobacteria in agricultural foodstuffs. Mol Nutr Food Res 48: 522[Ent[#x2013;531.
5. Börjesson, S., Egervärn, M., Finn, M., Tillander, I., Wiberg, C., and Englund, S. (2011) High prevalence of ESBL-producing Escherichia coli in chicken meat imported into Sweden. Clin Microbiol Infect 17 (Suppl. 4): O353.
6. Bush, K., and Jacoby, G.A. (2010) Updated functional classification of beta-lactamases. Antimicrob Agents Chemother 54: 969-976.
7. Carattoli, A. (2009) Animal reservoirs for extended spectrum β-lactamase producers. Clin Microbiol Infect 14: 117-123.
8. Cocconcelli, P.S., Cattivelli, D., and Gazzola, S. (2003) Gene transfer of vancomycin and tetracycline resistances among Enterococcus faecalis during cheese and sausage fermentations. Int J Food Microbiol 88: 315-323.
9. Da Silva, G.J., and Mendonça, N. (2012) Association between antimicrobial resistance and virulence in Escherichia coli. Virulence 3: 18-28.
10. Dahmen, S., Metayer, V., Gay, E., Madec, J.-Y., and Haenni, M. (2013) Characterization of extended-spectrum beta-lactamase (ESBL)-carrying plasmids and clones of Enterobacteriaceae causing cattle mastitis in France. Vet Microbiol 162: 793-799.
11. Dallenne, C., Da Costa, A., Decré, D., Favier, C., and Arlet, G. (2010) Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother 65: 490-495.
12. Depoorter, P., Persoons, D., Uyttendaele, M., Butaye, P., De Zutter, L., Dierick, K., etal. (2012) Assessment of human exposure to 3rd generation cephalosporin resistant E. coli (CREC) through consumption of broiler meat in Belgium. Int J Food Microbiol 159: 30-38.
13. Dierikx, C., van der Goot, J., Fabri, T., van Essen-Zandbergen, A., Smith, H., and Mevius, D. (2013) Extended spectrum beta-lactamase- and AmpC-beta-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother 68: 60-67.
14. Duriez, P., Clermont, O., Bonacorsi, S., Bingen, E., Chaventre, A., Elion, J., etal. (2001) Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147: 1671-1676.
15. EFSA (2010) The community summary report on antimicrobial resistance in zoonotic agents from animals and food in the European Union in 2004-2007. EFSA J 8: 1309-1615. [WWW document]. URL http://www.efsa.europa.eu/en/efsajournal/doc/1309.pdf
16. EFSA (2011) Scientific opinion on the public health risks of bacterial strains producing extended-spectrum beta-lactamases in food and food-producing animals. EFSA J 9: 2322. doi:10.2903/j.efsa.2011.2322. [WWW document]. URL www.efsa.europa.eu/efsajournal
17. Falagas, M.E., and Karageorgopoulos, D.E. (2009) Extended-spectrum beta-lactamase-producing organisms. J Hosp Infect 73: 345-354.
18. FAO/WHO/OIE (2007) Report of the FAO/WHO/OIE expert meeting: joint FAO/WHO/OIE expert meeting on critically important antimicrobials. FAO, Rome, Italy [WWW document]. URL http://www.who.int/foodborne_disease/resources/Report_CIA_Meeting.pdf
19. FDA (2013) National antimicrobial resistance monitoring systems [WWW Document]. URL http://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/UCM334896.pdf
20. Goullet, P., and Picard, B. (1986) Comparative esterase electrophoretic polymorphism of Escherichia coli isolates obtained from animal and human sources. J Gen Microbiol 132: 1843-1851.
21. Grasselli, E., François, P., Gutacker, M., Gettler, B., Benagli, C., Convert, M., etal. (2008) Evidence of horizontal gene transfer between human and animal commensal Escherichia coli strains identified by microarray. FEMS Immunol Med Microbiol 53: 351-358.
22. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
23. Hassan, S., Altalhi, A., Gherbawy, Y., and El-Deeb, B. (2011) Bacterial load of fresh vegetables and their resistance to the currently used antibiotics in Saudi Arabia. Foodborne Pathog Dis 8: 1011-1018.
24. Holvoet, K., Sampers, I., Callens, B., Dewulf, J., and Uyttendaele, M. (2013) Moderate prevalence of antimicrobial resistance in Escherichia coli isolates from lettuce, irrigation water, and soil. Appl Environ Microbiol 79: 6677-6683.
25. Jacoby, G.A. (2009) AmpC b-Lactamases. Clin Microbiol Rev 22: 161-182.
26. Kluytmans, J.A., Overdevest, I.T., Willemsen, I., Kluytmans-van den Bergh, M.F., van der Zwaluw, K., Heck, M., etal. (2013) Extended-spectrum β-Lactamase-producing Escherichia coli from retail chicken meat and humans: comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis 56: 478-487.
27. Li, X.Z., Mehrotra, M., Ghimire, S., and Adewoye, L. (2007) Beta-lactam resistance and beta-lactamases in bacteria of animal origin. Vet Microbiol 121: 197-214.
28. Lynch, M.F., Tauxe, R.V., and Hedberg, C.W. (2009) The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect 137: 307-315.
29. Ma, J., Liu, J.H., Lv, L., Zong, Z., Sun, Y., Zheng, H., etal. (2012) Characterization of extended-spectrum β-lactamase genes found among Escherichia coli isolates from duck and environmental samples obtained on a duck farm. Appl Environ Microbiol 78: 3668-3673.
30. Malik, R., Ivan, J., Javorsky, P., and Pristas, P. (2005) Seasonal dynamics of antibiotic-resistant Enterobacteriaceae in the gastrointestinal tract of domestic sheep. Folia Microbiol 50: 349-352.
31. Manges, A.R., and Johnson, J.R. (2012) Food-borne origins of Escherichia coli causing extraintestinal infections. Clin Infect Dis 55: 712-719.
32. Mohapatra, B.R., Broersma, K., and Mazumder, A. (2007) Comparison of five rep-PCR genomic fingerprinting methods for differentiation of fecal Escherichia coli from humans, poultry and wild birds. FEMS Microbiol Lett 277: 98-106.
33. Moland, E.S., Hong, S.G., Thomson, K.S., Larone, D.H., and Hanson, N.D. (2007) A Klebsiella pneumoniae isolate producing at least eight different beta-lactamases including an AmpC and KPC beta-lactamase. Antimicrob Agents Chemother 51: 800-801.
34. Mølbak, L., Licht, T.R., Kvist, T., Kroer, N., and Andersen, S.R. (2003) Plasmid transfer from Pseudomonas putida to the indigenous bacteria on alfalfa sprouts: characterization, direct quantification, and in situ location of transconjugant cells. Appl Environ Microbiol 69: 5536-5542.
35. Moubareck, C., Lecso, M., Pinloche, E., Butel, M.J., and Doucet-Populaire, F. (2007) Inhibitory impact of bifidobacteria on the transfer of beta-lactam resistance among Enterobacteriaceae in the gnotobiotic mouse digestive tract. Appl Environ Microbiol 73: 855-860.
36. Olsen, J.E., Brown, D.J., Skov, M.M., and Christensen, J.P. (1993) Bacterial typing methods suitable for epidemiological analysis, applications in investigations of salmonellosis among livestock. Vet Q 15: 125-135.
37. Paterson, D.L. (2006) Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med 119: S20-S28.
38. Paterson, D.L., and Bonomo, R.A. (2005) Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev 18: 657-686.
39. Pitout, J.D., and Laupland, K.B. (2008) Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8: 159-166.
40. Pitout, J.D.D., Sanders, C.C., and Sanders, W.E., Jr (1997) Antimicrobial resistance with focus on beta-lactam resistance in gram-negative bacilli. Am J Med 103: 51-59.
41. Raphael, E., Wong, L.K., and Riley, L.W. (2011) Extended-spectrum Beta-lactamase gene sequences in Gram-negative saprophytes on retail organic and nonorganic spinach. Appl Environ Microbiol 77: 1601-1607.
42. Reuland, E.A., Al Naiemi, N., Rijnsburger, M.C., Savelkoul, P.H., and Vandenbroucke-Grauls, C.M. (2011a) Prevalence of ESBL-producing Enterobacteriaceae (ESBL-E) in raw vegetables. Clin Microbiol Infect 17 (S4): O102.
43. Reuland, E.A., Al Naiemi, N., Rijnsburger, M.C., Savelkoul, P.H., and Vandenbroucke-Grauls, C.M. (2011b) Prevalence of ESBL-producing Enterobacteriaceae (ESBL-E) in raw vegetables. Ned Tijdschr Med Microbiol 19: S46.
44. Ruimy, R., Brisabois, A., Bernede, C., Skurnik, D., Barnat, S., Arlet, G., etal. (2010) Organic and conventional fruits and vegetables contain equivalent counts of Gram-negative bacteria expressing resistance to antibacterial agents. Environ Microbiol 12: 608-615.
45. Salamon, H., Behr, M.A., Rhee, J.T., and Small, P.M. (2000) Genetic distances for the study of infectious disease epidemiology. Am J Epidemiol 151: 324-334.
46. Sayah, R.S., Kaneene, J.B., Johnson, Y., and Miller, R. (2005) Patterns of antimicrobial resistance observed in Escherichia coli isolates obtained from domestic- and wild-animal fecal samples, human septage, and surface water. Appl Environ Microbiol 71: 1394-1404.
47. Shah, A.A., Hasan, H., Ahmed, S., and Hameed, A. (2004) Extended spectrum β-lactamases (ESβLs): characterization, epidemiology and detection. Crit Rev Microbiol 30: 25-32.
48. Smet, A., Rasschaert, G., Martel, A., Persoons, D., Dewulf, J., Butaye, P., etal. (2003) Extended-spectrum beta-lactamases: implications for the clinical microbiology laboratory, therapy, and infection control. J Infect 47: 273-295.
49. Smet, A., Martel, A., Persoons, D., Dewulf, J., Heyndrickx, M., Catry, B., etal. (2008) Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal Escherichia coli isolates in Belgian broiler farms. Antimicrob Agents Chemother 52: 1238-1243.
50. Smet, A., Martel, A., Persoons, D., Dewulf, J., Heyndrickx, M., Herman, L., etal. (2010) Broad-spectrum β-lactamases among Enterobacteriaceae of animal origin: molecular aspects, mobility and impact on public health. FEMS Microbiol Rev 34: 295-316.
51. Smith, J.L., Fratamico, P.M., and Gunther, N.W. (2007) Extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis 4: 134-163.
52. Stürenburg, E., and Mack, D. (2003) Extended-spectrum β-lactamases: implications for the clinical microbiology laboratory, therapy, and infection control. J Infect 47: 273-295.
53. Sundsfjord, A., Simonsen, G.S., Haldorsen, B.C., Haaheim, S.O., Hjelmevoll, S.O., Littauer, P., and Dahl, K.H. (2004) Genetic methods for detection of antimicrobial resistance. APMIS 112: 815-837.
54. Tadesse, D.A., Zhao, S., Tong, E., Ayers, S., Singh, A., Bartholomew, M.J., and McDermott, P.F. (2012) Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002. Emerg Infect Dis 18: 741-749.
55. Toomey, N., Monaghan, A., Fanning, S., and Bolton, D. (2009) Transfer of antibiotic resistance marker genes between lactic acid bacteria in model rumen and plant environments. Appl Environ Microbiol 75: 3146-3152.
56. Torres, C., and Zarazaga, M. (2007) BLEE en animales y su importancia en la transmision a humanos. Enferm Infecc Microbiol Clin 25: 1-9.
57. Weigel, R.M., Nucera, D., Qiao, B., Teferedegne, B., Suh, D.K., Barber, D.A., etal. (2007) Testing an ecological model for transmission of Salmonella enterica in swine production ecosystems using genotyping data. Prev Vet Med 81: 274-289.
58. WHO (2011) Tackling antibiotic resistance from a food safety perspective in Europe. World Health Organisation [WWW Document]. URL http://www.euro.who.int/__data/assets/pdf_file/0005/136454/e94889.pdf
59. Wiegand, I., Geiss, H.K., Mack, D., Sturenburg, E., and Seifert, H. (2007) Detection of extended spectrum β-lactamases among Enterobacteriaceae by use of semi-automated microbiology systems and manual detection procedures. J Clin Microbiol 45: 1167-1174.
60. Witte, W. (2000) Ecological impact of antibiotic use in animals on different complex microflora: environment. Int J Antimicrob Agents 14: 321-325.
61. Woerther, P.L., Angebault, C., Jacquier, H., Hugede, H.C., Janssens, A.C., Sayadi, S., etal. (2011) Massive increase, spread, and exchange of extended spectrum β-lactamase-encoding genes among intestinal Enterobacteriaceae in hospitalized children with severe acute malnutrition in Niger. Clin Infect Dis 53: 677-685.
62. Woodall, C.A. (2003) DNA transfer by conjugation. In E. coli Plasmid Vectors: Methods and Applications. Casali, N., and Preston, A. (eds). Totowa, NJ, USA: Springer Science and Business Media, pp. 61-64.