JWARP  Vol.5 No.11 , November 2013
Presence of Multidrug-Resistant E. coli, Enterococcus spp. and Salmonella spp. in Lakes and Fountains of Porto, Portugal
ABSTRACT

Urban lakes and fountains provide recreational activities that could facilitate the contact between humans, animals and biological agents. The objective of this work was to assess the water quality and safety of 17 lakes and 13 fountains in the city of Porto (Portugal), by detecting the presence of Escherichia coli, enterococci and Salmonella spp., and analyzing their antimicrobial resistance. (For more information,please refer to the pdf.)


Cite this paper
C. Flores, L. Loureiro, L. Bessa and P. Costa, "Presence of Multidrug-Resistant E. coli, Enterococcus spp. and Salmonella spp. in Lakes and Fountains of Porto, Portugal," Journal of Water Resource and Protection, Vol. 5 No. 11, 2013, pp. 1117-1126. doi: 10.4236/jwarp.2013.511117.
References
[1]   G. Howard, “Water Safety Plans for Small Systems: A Model for Applying HACCP Concepts for Cost-Effective Monitoring in Developing Countries,” Water Science Technology, Vol. 47, No. 3, 2003, pp. 215-220.

[2]   J. M. Vieira, “A Strategic Approach for Water Safety Plans Implementation in Portugal,” Journal of Water and Health, Vol. 9, No. 1, 2011, pp. 107-116.
http://dx.doi.org/10.2166/wh.2010.150

[3]   C. F. Marrs, L. Zhang, P. Tallman, S. Manning, P. Somsel, R. Raz, R. Colodner, M. E. Jantunen, A. Siitonen, H. Saxen and B. Foxman, “Escherichia coli Virulence Gene Distributions Show Interesting Difference Between Urinary Tract Infection, Fecal and Periurethral Isolate Collections,” Journal of Medical Microbiology, Vol. 51, No. 2, 2002, pp. 138-142.

[4]   O. Clermont, S. Bonacorsi and E. Bingen, “Rapid and Simple Determination of the Escherichia coli Phylogenetic Group,” Applied and Environmental Microbiology, Vol. 66, No. 10, 2000, pp. 4555-4558.
http://dx.doi.org/10.1128/AEM.66.10.4555-4558.2000

[5]   E. F. Boyd and D. L. Hartl, “Chromosomal Regions Specific to Pathogenic Isolates of Escherichia coli Have a Phylogenetically Clustered Distribution,” Journal of Bacteriology, Vol. 180, No. 5, 1998, pp. 1159-1165.

[6]   J. P. Euzéby, “List of Prokaryotic Names with Standing in Nomenclature,” 1997.
http://www.bacterio.cict.fr/e/enterococcus.html

[7]   T. M. Scott, T. M. Jenkins, J. Lukasik and J. B. Rose, “Potential Use of a Host Associated Molecular Marker in Enterococcus faecium as an Index of Human Fecal Pollution,” Environmental Science and Technology, Vol. 39, No. 1, 2005, pp. 283-287.
http://dx.doi.org/10.1021/es035267n

[8]   R. L. Whitman, K. Przybyla-Kelly, D. A. Shively and M. N. Byappanahalli, “Incidence of the Enterococcal Surface Protein (esp) Gene in Human and Animal Fecal Sources,” Environmental Science and Technology, Vol. 141, No. 17, 2007, pp. 6090-6095. http://dx.doi.org/10.1021/es070817t

[9]   NRC (National Research Council), “Evaluation of Risk: A Phased Approach to Monitoring Microbial Water Quality,” In: Indicators for Waterborne Pathogens, The National Academic Press, Washington DC, 2004, pp. 13-16.

[10]   O. Savichtcheva and S. Okabe, “Alternative Indicators of Fecal Pollution: Relations with Pathogens and Conventional Indicators, Current Methodologies for Direct Pathogen Monitoring and Future Application Perspectives,” Water Research, Vol. 40, No. 13, 2006, pp. 2463-2476.
http://dx.doi.org/10.1016/j.watres.2006.04.040

[11]   S. Eriksson, S. Lucchini, A. Thompson, M. Rhen and J. C. D. Hinton, “Unravelling the Biology of Macrophage Infection by Gene Expression Profiling of Intracellular Salmonella enteric,” Molecular Microbiology, Vol. 47, No. 1, 2003, pp. 103-118.
http://dx.doi.org/10.1046/j.1365-2958.2003.03313.x

[12]   F. G. Portillo, “Salmonella Intracellular Proliferation: Where, When and How?” Microbes and Infection, Vol. 3, No. 14-15, 2001, pp. 1305-1311.
http://dx.doi.org/10.1016/S1286-4579(01)01491-5

[13]   R. I. Aminov, “The Role of Antibiotics and Antibiotic Resistance in Nature,” Environmental Microbiology, Vol. 11, No. 12, 2009, pp. 2970-2988.
http://dx.doi.org/10.1111/j.1462-2920.2009.01972.x

[14]   M. H. Wilcox, “The Tide of Antimicrobial Resistance and Selection,” International Journal of Antimicrobial Agents, Vol. 34, No. 3, 2009, pp. S6-S10.
http://dx.doi.org/10.1016/S0924-8579(09)70550-3

[15]   M. G. Cormican, S. A. Marshall and R. N. Jones, “Detection of Extended-Spectrum Beta-Lactamase (ESBL)-Producing Strains by the Etest ESBL Screen,” Journal of Clinical Microbiology, Vol. 34, No. 8, 1996, pp. 1880-1884.

[16]   M. Mohammadi-Mehr and M. Feizabadi, “Antimicrobial Resistance Pattern of Gram-Negative Bacilli Isolated from Patients at ICUs of Army Hospitals in Iran,” Iranian Journal of Microbiology, Vol. 3, No. 1, 2011, pp. 26-30.

[17]   A. Tello, B. Austin and T. C. Telfer, “Selective Pressure of Antibiotic Pollution on Bacteria of Importance to Public Health,” Environmental Health Perspectives, Vol. 120, No. 8, 2012, pp. 1100-1106.
http://dx.doi.org/10.1289/ehp.1104650

[18]   T. Kenzaka, K. Tani and M. Nasu, “High-Frequency Phage-Mediated Gene Transfer in Freshwater Environments Determined at Single-Cell Level,” ISME Journal, Vol. 4, No. 5, 2010, pp. 648-659.
http://dx.doi.org/10.1038/ismej.2009.145

[19]   A. Moura, C. Oliveira, I. Henriques, K. Smalla and A. Correia, “Broad Diversity of Conjugative Plasmids in Integron-Carrying Bacteria from Wastewater Environments,” FEMS Microbiology Letters, Vol. 330, No. 2, 2012, pp. 157-164.
http://dx.doi.org/10.1111/j.1574-6968.2012.02544.x

[20]   E. Shoeb, U. Badar, J. Akhter, H. Shams, M. Sultana and M. A. Ansari, “Horizontal Gene Transfer of Stress Resistance Genes Through Plasmid Transport,” World Journal of Microbiology and Biotechnology, Vol. 28, No. 3, 2012, pp. 1021-1025.
http://dx.doi.org/10.1007/s11274-011-0900-6

[21]   Y. Suzuki, N. Kanda and T. J. Furukawa, “Abundance of Enterococcus species, Enterococcus fecalis and Enterococcus faecium, Essential Indicators of Fecal Pollution, in River Water,” Journal of Environmental Science and Health Part A, Vol. 47, No. 11, 2012, pp. 1500-1505.
http://dx.doi.org/10.1080/10934529.2012.680315

[22]   K. C. Pinto, E. M. Hachich, M. I. Sato, M. Di Bari, M. C. Coelho, M. H. Matté, C. C. Lamparelli and M. T. Razzolini, “Microbiological Quality Assessment of Sand and Water from Three Selected Beaches of South Coast, Sao Paulo State, Brazil,” Water Science and Technology, Vol. 66, No. 11, 2012, pp. 2475-2482.
http://dx.doi.org/10.2166/wst.2012.494

[23]   CLSI (Clinical and Laboratory Standards Institute), “Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals,” Approved Standard—Third Edition, CLSI document M31A3, Wayne, Pa, 2008.

[24]   L. Drieux, F. Brossier, W. Sougakoff and V. Jarlier, “Phenotypic Detection of Extendended-Spectrum Beta Lactamase Production in Enterobacteriaceae: Review and Bench Guide,” Clinical Microbiology and Infection, Vol. 14, No. S1, 2008, pp. 90-103.
http://dx.doi.org/10.1111/j.1469-0691.2007.01846.x

[25]   T. A. Chapman, X. Y. Wu, I. Barchia, K. A. Bettelheim, S. Driesen, D. Trott, M. Wilson and J. J. Chin, “Comparison of Virulence Gene Profiles of Escherichia coli Strains Isolated from Healthy and Diarrheic Swine,” Applied Environmental Microbiology, Vol. 72, No. 7, 2006, pp. 4782-4795. http://dx.doi.org/10.1128/AEM.02885-05

[26]   C. R. Jackson, P. J. Fedorka-Cray and J. B. Barrett, “Use of a Genus- and Species-Specific Multiplex PCR for Identification of Enterococci,” Journal of Clinical Microbiology, Vol. 42, No. 8, 2004, pp. 3558-3565.
http://dx.doi.org/10.1128/JCM.42.8.3558-3565.2004

[27]   H. K. Allen, J. Donato, H. H. Wang, K. A. Cloud-Hansen, J. Davies and J. A. Handelsman, “Call of the Wild: Antibiotic Resistance Genes in Natural Environments,” Nature Reviews Microbiology, Vol. 8, No. 4, 2010, pp. 251-259. http://dx.doi.org/10.1038/nrmicro2312

[28]   G. D. Wright, “Antibiotic Resistance in the Environment: A Link to the Clinic?” Current Opinion in Microbiology, Vol. 13, No. 5, 2010, pp. 589-589.
http://dx.doi.org/10.1016/j.mib.2010.08.005

[29]   L. R. Fogarty, S. K. Haack, M. J. Wolcott and R. L. Whitman, “Abundance and Characteristics of the Recreational Water Quality Indicator Bacteria Escherichia coli and Enterococci in Gull Faeces,” Journal of Applied Microbiology, Vol. 94, No. 5, 2003, pp. 865-878.
http://dx.doi.org/10.1046/j.1365-2672.2003.01910.x

[30]   T. Radimersky, P. Frolkova, D. Janoszowska, M. Dolejska, P. Svec, E. Roubalova, P. Cikova, A. Cizek and I. Literak, “Antibiotic Resistance in Fecal Bacteria (Escherichia coli, Enterococcus spp.) in Feral Pigeons,” Journal of Applied Microbiology, Vol. 109, No. 5, 2010, pp. 1687-1695.

[31]   C. R. Jackson, P. J. Fedorka-Cray, J. A. Davis, J. B. Barrett, J. H. Brousse, J. Gustafson and M. Kucher, “Mechanisms of Antimicrobial Resistance and Genetic Relatedness Among Enterococci Isolated from Dogs and Cats in the United States,” Journal of Applied Microbiology, Vol. 108, No. 6, 2010, pp. 2171-2179.

[32]   E. K. Leonard, D. L. Pearl, R. L. Finley, N. Janecko, R. J. Reid-Smith, A. S. Peregrine and J. S. Weese, “Comparison of Antimicrobial Resistance Patterns of Salmonella spp. and Escherichia coli Recovered from Pet Dogs from Volunteer Households in Ontario (2005-06),” Journal of Antimicrobial Chemotherapy, Vol. 67, No. 1, 2012, pp. 174-181. http://dx.doi.org/10.1093/jac/dkr430

[33]   C. Murphy, R. J. Reid-Smith, J. F. Prescott, B. N. Bonnett, C. Poppe, P. Boerlin, J. S. Weese, N. Janecko and S. A. McEwen, “Occurrence of Antimicrobial-Resistant Bacteria in Healthy Dogs and Cats Presented to Private Veterinary Hospitals in Southern Ontario: A Preliminary Study,” The Canadian Veterinary Journal, Vol. 50, No. 10, 2009, pp. 1047-1053.

[34]   I. Kühn, A. Iversen, L. G. Burman, B. Olsson-Liljequist, A. Franklin, M. Finn, F. Aarestrup, A. M. Seyfarth, A. R. Blanch, X. Vilanova, H. Taylor, J. Caplin, M. A. Moreno, L. Dominguez, I. A. Herrero and R. Mollby, “Comparison of Enterococci Populations in Animals, Humans, and the Environment—A European Study,” International Journal of Food Microbiology, Vol. 88, No. 2-3, 2003, pp. 133-145.
http://dx.doi.org/10.1016/S0168-1605(03)00176-4

[35]   A. Luczkiewicz, K. Jankowska, S. Fudala-Ksiazek and K. Olańczuk-Neyman, “Antimicrobial Resistance of Fecal Indicators in Municipal Wastewater Treatment Plant,” Water Research, Vol. 44, No. 17, 2010, pp. 5089-5097.
http://dx.doi.org/10.1016/j.watres.2010.08.007

[36]   X. Vilanova, A. Manero, M. Cerdà-Cuéllar and A. R. Blanch, “The Composition and Persistence of Fecal Coliforms and Enterococci Populations in Sewage Treatment Plants,” Journal of Applied Microbiology, Vol. 96, No. 2, 2004, pp. 279-288.
http://dx.doi.org/10.1046/j.1365-2672.2003.02149.x

[37]   J. R. Hayes, L. L. English, P. J. Carter, T. Proescholdt, K. Y. Lee, D. D. Wagner and D. G. White, “Prevalence and Antimicrobial Resistance of Enterococcus Species Isolated from Retail Meats,” Applied and Environmental Microbiology, Vol. 69, No. 12, 2003, pp. 7153-7160.
http://dx.doi.org/10.1128/AEM.69.12.7153-7160.2003

[38]   I. U. Rathnayake, M. Hargreaves and F. Huygens, (2012) “Antibiotic Resistance and Virulence Traits in Clinical and Environmental Enterococcus fecalis and Enterococcus faecium Isolates,” Systematic and Applied Microbiology, Vol. 35, No. 5, 2012, pp. 326-333.
http://dx.doi.org/10.1016/j.syapm.2012.05.004

[39]   P. M. Costa, P. Vaz-Pires and F. Bernardo, “Antimicrobial Resistance in Escherichia coli Isolated in Inflow, Effluent and Sludge from Municipal Wastewater Treatment Plants,” Urban Water Journal, Vol. 4, No. 4, 2007, pp. 275-281. http://dx.doi.org/10.1080/15730620701552523

[40]   J. A. Skyberg, T. J. Johnson, J. R. Johnson, C. Clabots, C. M. Logue and L. K. Nolan, “Acquisition of Avian Pathogenic Escherichia coli Plasmids by a Commensal E. coli Isolate Enhances Its Abilities to Kill Chicken Embryos, Grow in Human Urine, and Colonize the Murine Kidney,” Infection and Immunity, Vol. 74, No. 11, 2006, pp. 6287-6292. http://dx.doi.org/10.1128/IAI.00363-06

[41]   S. Schippa, V. Iebba, V. Totino, F. Santangelo, M. Lepanto, C. Alessandri, F. Nuti, F. Viola, G. Di Nardo, S. Cucchiara, C. Longhi and M. P. Conte, “A Potential Role of Escherichia coli Pathobionts in the Pathogenesis of Pediatric Inflammatory Bowel Disease,” Canadian Journal of Microbiology, Vol. 58, No. 4, 2012, pp. 426-432.
http://dx.doi.org/10.1139/w2012-007

[42]   F. Vandemaele, D. Vandekerchove, M. Vereecken, J. Derijcke, M. Dho-Moulin and B. M. Goddeeris, “Sequence Analysis Demonstrates Conservation of fimH and Variability of fimA Throughout Avian Pathogenic Escherichia coli (APEC),” Veterinary Research, Vol. 34, No. 2, 2003, pp. 153-163.
http://dx.doi.org/10.1051/vetres:2002062

[43]   M. Mellata, J. W. Touchman and R. Curtiss, “Full Sequence and Comparative Analysis of the Plasmid pAPEC-1 of Avian Pathogenic E. coli chiχ7122 (O78:K80:H9),” PLoS ONE, Vol. 4, No. 1, 2009, Article ID: e4232.
http://dx.doi.org/10.1371/journal.pone.0004232

[44]   J. R. Johnson and A. L. Stell, “Extended Virulence Genotypes of Escherichia coli Strains From Patients with Urosepsis in Relation to Phylogeny and Host Compromise,” Journal of Infectious Diseases, Vol. 181, No. 1, 2000, pp. 261-272. http://dx.doi.org/10.1086/315217

[45]   V. Falbo, T. Pace, L. Picci, E. Pizzi and A. Caprioli, “Isolation and Nucleotide Sequence of the Gene Encoding Cytotoxic Necrotizing Factor 1 of Escherichia coli,” Infection and Immunity, Vol. 61, No. 11, 1993, pp. 4909-4914.

[46]   B. K. Dhakal and M. A. Mulvey, “The UPEC Pore-Forming Toxin α Hemolysin Triggers Proteolysis of Host Proteins to Disrupt Cell Adhesion, Inflammatory, and Survival Pathways,” Cell Host & Microbe, Vol. 11, No. 1, 2012, pp. 58-69.
http://dx.doi.org/10.1016/j.chom.2011.12.003

[47]   K. Hamelin, G. Bruant, A. El-Shaarawi, S. Hill, T. A. Edge, J. Fairbrother, J. Harel, C. Maynard, L. Masson and R. Brouseau, “Occurrence of Virulence and Antimicrobial Resistance Genes in Escherichia coli Isolates from Different Aquatic Ecosystems within the St. Clair River and Detroit River Areas,” Applied and Environmental Microbiology, Vol. 73, No. 2, 2007, pp. 477-484.
http://dx.doi.org/10.1128/AEM.01445-06

[48]   R. Simoes, C. Ferreira, J. Goncalves, F. álvares, H. RioMaior, S. Roque, R. Brandao and P. M. da Costa, “Occurrence of Virulence Genes in Multidrug-Resistant Escherichia coli Isolates from Iberian Wolves (Canis lupus signatus) in Portugal,” European Journal of Wildlife Research, Vol. 58, No. 4, 2012, pp. 677-684.
http://dx.doi.org/10.1007/s10344-012-0616-4

[49]   CDC (Centers for Disease Control and Prevention), “National Salmonella Surveillance Overview,” US Department of Health and Human Services, Atlanta, 2011.

[50]   P. A. D. Grimont and F-X. Weill, “Antigenic Formulae of the Salmonella Serovars: WHO Collaborating Centre for Reference and Research on Salmonella,” 9th Edition, Institute Pasteur, 2007, pp. 1-166.

[51]   V. Briones, S. Téllez, J. Goyache, C. Ballesteros, M. del Pilar Lanzarot, L. Domínguez and J. F. Fernández-Garayzábal, “Salmonella Diversity Associated with Wild Reptiles and Amphibians in Spain,” Environmental Microbiology, Vol. 6, No. 8, 2004, pp. 868-871.
http://dx.doi.org/10.1111/j.1462-2920.2004.00631.x

[52]   D. R. Fenlon, “Seagulls (Larus spp.) as Vectors of Salmonellae: An Investigation into the Range of Serotypes and Numbers of Salmonellae in Gull Feces,” Journal of Hygiene, Vol. 86, No. 2, 1981, pp. 195-202.
http://dx.doi.org/10.1017/S0022172400068911

[53]   E. de Sousa, A. B. Júnior, A. A. Pinto, R. Z. Machado, A. O. de Carrasco, J. A. Marciano and K. Werther, “Prevalence of Salmonella spp. Antibodies to Toxoplasma gondii, and Newcastle Disease Virus in Feral Pigeons (Columba livia) in the City of Jaboticabal, Brazil,” Journal of Zoo and Wildlife Medicine, Vol. 41, No. 4, 2010, pp. 603-607.
http://dx.doi.org/10.1638/2008-0166.1

[54]   F. Van Immerseel, F. Pasmans, J. De Buck, I. Rychlik, H. Hradecka, J. M. Collard, C. Wildemauwe, M. Heyndrickx, R. Ducatelle and F. Haesebrouck, “Cats as a Risk for Transmission of Antimicrobial Drug-Resistant Salmonella,” Emerging Infectious Diseases, Vol. 10, No. 12, 2004, pp. 2169-2174. http://dx.doi.org/10.3201/eid1012.040904

 
 
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