Epidemic Escherichia coli ST131 and Enterococcus faecium ST17 in coastal marine sediments from an Italian beach

Environmental Science and Technology

Volumn 47, Issue 23, 2013, Pages 13772-13780

  Vignaroli, C ^a   Luna, G M ^b   Pasquaroli, S ^a   Di Cesare, A ^a   Petruzzella, R ^a   Paroncini, P ^a   Biavasco, F ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b CNR ISMAR National Research Council Institute of Marine Sciences   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL RESISTANCES; COASTAL ENVIRONMENTS; COASTAL MARINE SEDIMENTS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; FECAL INDICATOR BACTERIA; MULTILOCUS SEQUENCE TYPING; PULSED FIELD GEL ELECTROPHORESIS;

BACILLI; BIODIVERSITY; CLONING; COASTAL ZONES; ELECTROPHORESIS; RECOVERY; SEDIMENTS; SUBMARINE GEOLOGY; WATER QUALITY;

ESCHERICHIA COLI;

AMPICILLIN; ANTIBIOTIC AGENT; CEFOTAXIME; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; DALFOPRISTIN PLUS QUINUPRISTIN; ERYTHROMYCIN; GENTAMICIN; LINEZOLID; NALIDIXIC ACID; STREPTOMYCIN; SULFONAMIDE; TETRACYCLINE; VANCOMYCIN; VIRULENCE FACTOR; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BATHING WATER; BEACH; CLONE; COAST; COASTAL ZONE; COLIFORM BACTERIUM; ELECTROKINESIS; HEALTH RISK; MARINE SEDIMENT; PATHOGENICITY; PUBLIC HEALTH; VIRULENCE; WATER QUALITY;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BATH; BROTH DILUTION; COASTAL WATERS; CONTROLLED STUDY; DISK DIFFUSION; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; FECAL COLIFORM; FECAL INDICATOR BACTERIUM; FECES; GENETIC VARIABILITY; HUMAN; ITALY; MARINE ENVIRONMENT; MULTIDRUG RESISTANCE; MULTILOCUS SEQUENCE TYPING; PUBLIC HEALTH; PULSED FIELD GEL ELECTROPHORESIS; SEASHORE; SEDIMENT; WATER POLLUTANT; WATER POLLUTION INDICATOR; WATER QUALITY; DRUG EFFECTS; ECOSYSTEM; ESCHERICHIA COLI INFECTIONS; GENETICS; GRAM-POSITIVE BACTERIAL INFECTIONS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

ADRIATIC SEA; ITALY; MEDITERRANEAN SEA;

ANTI-INFECTIVE AGENTS; DRUG RESISTANCE, BACTERIAL; ECOSYSTEM; ENTEROCOCCUS FAECIUM; ENVIRONMENTAL MICROBIOLOGY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FECES; GENETIC VARIATION; GEOLOGIC SEDIMENTS; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; ITALY; VIRULENCE; VIRULENCE FACTORS;

EID: 84889837589     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es4019139     Document Type: Article

References (56)

1. Halliday, E.; Gast, R. J. Bacteria in beach sands: An emerging challenge in protecting coastal water quality and bather health Environ. Sci. Technol. 2011, 45, 370-379
2. Byappanahalli, M. N.; Nevers, M. B.; Korajkic, A.; Staley, Z. R.; Harwood, V. J. Enterococci in the environment Microbiol. Mol. Biol. Rev. 2012, 76, 685-706
3. European Community Commission (ECC). Directive 2006/7/EC of the European Parliament and of the Council of 15 February 2006 concerning the management of bathing water quality and repealing Directive 76/160/EEC; 2006; 64, pp 37-51.
4. U.S. Environmental Protection Agency. Recreational Water Quality Criteria, EPA 820-F-12-058; Office of Water: Washington, DC, 2012.
5. Anderson, K. L.; Whitlock, J. E.; Harwood, V. J. Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments Appl. Environ. Microbiol. 2005, 71, 3041-3048
6. Haller, L.; Poté, J.; Loizeau, J. L.; Wildi, W. Distribution and survival of faecal indicator bacteria in the sediments of the Bay of Vidy, Lake Geneva, Switzerland Ecol. Indic. 2009, 9, 540-547
7. González-Fernández, D.; Garrido-Pérez, M. C.; Nebot-Sanz, E.; Sales-Márquez, D. Fecal pollution in coastal marine sediments from a semi-enclosed deep embayment subjected to anthropogenic activities: An issue to be considered in environmental quality management frameworks development EcoHealth 2010, 7, 473-484
8. Di Cesare, A.; Vignaroli, C.; Luna, G. M.; Pasquaroli, S.; Biavasco, F. Antibiotic-resistant enterococci in seawater and sediments from a coastal fish farm Microb. Drug Resist. 2012, 18, 502-509
9. Byappanahalli, M. N.; Withman, R. L.; Shively, D. A.; Sadowsky, M. J.; Ishii, S. Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed Environ. Microbiol. 2006, 8, 504-513
10. Ishii, S.; Ksoll, W. B.; Hicks, R. E; Sadowsky, M. J. Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds Appl. Environ. Microbiol. 2006, 72, 612-621
11. Pachepsky, Y. A.; Shelton, D. R. Escherichia coli and fecal coliforms in freshwater and estuarine sediments Crit. Rev. Environ. Sci. Technol. 2011, 41, 1067-1110
12. Craig, D. L.; Fallowfield, H. J.; Cromar, N. J. Use of microcosms to determine persistence of Escherichia coli in recreational coastal water and sediment and validation with in situ measurements J. Appl. Microbiol. 2004, 96, 922-930
13. Luna, G. M.; Vignaroli, C.; Rinaldi, C.; Pusceddu, A.; Nicoletti, L.; Gabellini, M.; Danovaro, R.; Biavasco, F. Extraintestinal Escherichia coli carrying virulence genes in coastal marine sediments Appl. Environ. Microbiol. 2010, 76, 5659-5668
14. Kaper, J. B.; Nataro, J. P.; Mobley, H. L. T. Pathogenic Escherichia coli Nat. Rev. Microbiol. 2004, 2, 123-140
15. Fisher, K.; Phillips, C. The ecology, epidemiology and virulence of Enterococcus Microbiology 2009, 155, 1749-1757
16. Arias, C. A.; Murray, B. E. The rise of the Enterococcus: Beyond vancomycin resistance Nat. Rev. Microbiol. 2012, 10, 266-278
17. Picard, B.; Garcia, J. S.; Gouriou, S.; Duriez, P.; Brahimi, N.; Bingen, E.; Elion, J.; Denamur, E. The link between phylogeny and virulence in Escherichia coli extraintestinal infection Infect. Immun. 1999, 67, 546-553
18. Le Gall, T.; Clermont, O.; Gouriou, S.; Picard, B.; Nassif, X.; Denamur, E.; Tenaillon, O. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains Mol. Biol. Evol. 2007, 24, 2373-2384
19. Kayser, F. H. Safety aspects of enterococci from the medical point of view Int. J. Food Microbiol. 2003, 88, 255-262
20. Levy, S. B.; Marshall, B. Antibacterial resistance worldwide: Causes, challenges and responses Nat. Med. 2004, 10, S122-129
21. French, G. L. The continuing crisis in antibiotic resistance Int. J. Antimicrob. Agents 2010, 36, S3-7
22. Craun, G. F.; Calderon, R. L.; Craun, M. F. Outbreaks associated with recreational water in the United States Int. J. Environ. Health Res. 2005, 15, 243-262
23. Dziuban, E. J.; Liang, J. L.; Craun, G. F.; Hill, V.; Yu, P. A.; Painter, J.; Moore, M. R.; Calderon, R. L.; Roy, S. L.; Beach, M. J. Surveillance for waterborne disease and outbreaks associated with recreational water-United States, 2003-2004 MMWR Surveill. Summ. 2006, 55, 1-30
24. Lang, A. L.; Tsai, Y. L.; Mayer, C. L.; Patton, K. C.; Palmer, C. J. Multiplex PCR for detection of the heat-labile toxin gene and shiga-like toxin I and II genes in Escherichia coli isolated from natural waters Appl. Environ. Microbiol. 1994, 60, 3145-3149
25. Hamilton, M. J.; Hadi, A. Z.; Griffith, J. F.; Ishii, S.; Sadowsky, M. J. Large scale analysis of virulence genes in Escherichia coli strains isolated from Avalon Bay, CA Water Res. 2010, 44, 5463-5473
26. de Oliveira, A. J.; Pinhata, J. M. Antimicrobial resistance and species composition of Enterococcus spp. isolated from waters and sands of marine recreational beaches in Southeastern Brazil Water Res. 2008, 42, 2242-2250
27. Bauer, L.; Alm, E. Escherichia coli toxin and attachment genes in sand at Great Lakes recreational beaches J. Great Lakes Res. 2012, 38, 129-133
28. Vignaroli, C.; Luna, G. M.; Rinaldi, C.; Di Cesare, A.; Danovaro, R.; Biavasco, F. New sequence types and multidrug resistance among pathogenic Escherichia coli isolates from coastal marine sediments Appl. Environ. Microbiol. 2012, 78, 3916-3922
29. Pusceddu, A.; Dell'Anno, A.; Fabiano, M.; Danovaro, R. Quantity and bioavailability of sediment organic matter as signatures of benthic trophic status Mar. Ecol.: Prog. Ser. 2009, 375, 41-52
30. Clermont, O.; Bonacorsi, S.; Bingen, E. Rapid and simple determination of Escherichia coli phylogenetic group Appl. Environ. Microbiol. 2000, 66, 4555-4558
31. Vignaroli, C.; Zandri, G.; Aquilanti, L.; Pasquaroli, S.; Biavasco, F. Multidrug-resistant enterococci in animal meat and faeces and co-transfer of resistance from an Enterococcus durans to a human Enterococcus faecium Curr. Microbiol. 2011, 62, 1438-1447
32. Garofalo, C.; Vignaroli, C.; Zandri, G.; Aquilanti, L.; Bordoni, D.; Osimani, A.; Clementi, F.; Biavasco, F. Direct detection of antibiotic resistance genes in specimens of chicken and pork meat Int. J. Food Microbiol. 2007, 113, 75-83
33. CLSI, Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing: Twentieth informational supplement; Technical Report from the Clinical and Laboratory Standards Institute: Wayne, PA, 2010; Document M100-S20, Vol. 30, No. 1.
34. Elhadidy, M.; Elsayyad, A. Uncommitted role of enterococcal surface protein, Esp, and origin of isolates on biofilm production by Enterococcus faecalis isolated from bovine mastitis J. Microbiol., Immunol. Infect. 2012, 46, 80-84
35. Stepanovic, S.; Vukovic, D.; Dakic, I.; Savic, B.; Svabic-Vlahovic, M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation J. Microbiol. Methods 2000, 40, 175-179
36. Biavasco, F.; Foglia, G.; Paoletti, C.; Zandri, G.; Magi, G.; Guaglianone, E.; Sundsfjord, A.; Pruzzo, C.; Donelli, G.; Facinelli, B. VanA-Type Enterococci from humans, animals, and food: Species distribution, population structure, Tn 1546 typing and location, and virulence determinants Appl. Environ. Microbiol. 2007, 73, 3307-3319
37. Moraes, P. M.; Perin, L. M.; Todorov, S. D.; Silva, A., Jr.; Franco, B. D.; Nero, L. A. Bacteriocinogenic and virulence potential of Enterococcus isolates obtained from raw milk and cheese J. Appl. Microbiol. 2012, 113, 318-328
38. Birren, B.; Lai, E. Preparation of DNA for pulsed field analysis. Pulsed Field Gel Electrophoresis: A Practical Guide; Academic Press: San Diego, CA, 1993; pp 25-74.
39. Davies, C. M.; Long, J. A.; Donald, M.; Ashbolt, N. J. Survival of fecal microorganisms in marine and freshwater sediments Appl. Environ. Microbiol. 1995, 61, 1888-1896
40. Graezyk, T. K.; Sunderland, D.; Awantang, G. N.; Mashinski, Y.; Lucy, F. E.; Graezyk, Z.; Chomiez, L.; Breysse, P. N. Relationships among bather density, levels of human waterborne pathogens, and fecal coliform counts in marine recreational beach water Parasitol. Res. 2010, 106, 1103-1108
41. Ferguson, D. M.; Moore, D. F.; Getrich, M. A.; Zhowandai, M. H. Enumeration and speciation of enterococci found in marine and intertidal sediments and coastal water in southern California J. Appl. Microbiol. 2005, 99, 598-608
42. Petersen, A.; Dalsgaard, A. Species composition and antimicrobial resistance genes of Enterococcus spp., isolated from integrated and traditional fish farms in Thailand Environ. Microbiol. 2003, 5, 395-402
43. Klein, G. Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract Int. J. Food Microbiol. 2003, 88, 123-131
44. Layton, B. A.; Walters, S. P.; Lam, L. H.; Boehm, A. B. Enterococcus species distribution among human and animal hosts using multiplex PCR J. Appl. Microbiol. 2010, 109, 539-547
45. Korajkic, A.; Badgley, B. D.; Brownell, M. J.; Harwood, V. J. Application of microbial source tracking methods in a Gulf of Mexico field setting J. Appl. Microbiol. 2009, 107, 1518-1527
46. Rathnayake, I. U.; Hargreaves, M.; Huygen, F. Antibiotic resistance and virulence traits in clinical and environmental Enterococcus faecalis and Enterococcus faecium isolates Syst. Appl. Microbiol. 2012, 35, 326-33
47. Rogers, B. A.; Sidjabat, H. E.; Paterson, D. L. Escherichia coli O25b-ST131: A pandemic, multiresistant, community-associated strain J. Antimicrob. Chemother. 2011, 66, 1-14
48. Ewers, C.; Grobbel, M.; Stamm, I.; Kopp, P. A.; Diehl, I.; Semmler, T.; Fruth, A.; Beutlich, J.; Guerra, B.; Wieler, L. H.; Guenther, S. Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-b-lactamase-producing Escherichia coli among companion animals J. Antimicrob. Chemother. 2010, 65, 651-660
49. Mora, A.; Herrera, A.; Mamani, R.; López, C.; Alonso, M. P.; Blanco, J. E.; Blanco, M.; Dahabi, G.; García-Garrote, F.; Pita, J. M.; Coira, A.; Bernárdez, M. I.; Blanco, J. Recent emergence of clonal group O25b:K1:H4-B2-ST131 ibeA strains among Escherichia coli poultry isolates, including CTX-M-9-producing strains, and comparison with clinical human isolates Appl. Environ. Microbiol. 2010, 76, 6991-6997
50. Simões, R. R.; Poirel, L.; Martins Da Costa, P.; Nordmann, P. Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli Emerging Infect. Dis. 2010, 16, 110-112
51. Top, J.; Willems, R.; Bonten, M. Emergence of CC17 E. faecium: From commensal to hospital adapted pathogen FEMS Immunol. Med. Microbiol. 2008, 52, 297-308
52. Caplin, J. L.; Hanlon, G. W.; Taylor, H. D. Presence of vancomycin and ampicillin-resistant Enterococcus faecium of epidemic clonal complex-17 in wastewaters from the south coast of England Environ. Microbiol. 2008, 10, 885-892
53. Gonçalves, A.; Igrejas, G.; Radhouani, H.; López, M.; Guerra, A.; Petrucci-Fonseca, F.; Alcaide, E.; Zorrilla, I.; Serra, R.; Torres, C.; Poeta, P. Detection of vancomycin-resistant enterococci from faecal samples of Iberian wolf and Iberian lynx, including Enterococcus faecium strains of CC17 and the new singleton ST573 Sci. Total Environ. 2011, 410-411, 266-268
54. Poulsen, L. L.; Bisgaard, M.; Son, N. T.; Trung, N. V.; An, H. M.; Dalsgaard, A. Enterococcus faecalis clones in poultry and in humans with urinary tract infections, Vietnam Emerging Infect. Dis. 2012, 18, 1096-1100
55. Larsen, J.; Schonheyder, H. C.; Lester, C. H.; Olsen, S. S.; Porsbo, L. J.; Garcia-Migura, L. Porcine-origin gentamicin-resistant Enterococcus faecalis in humans, Denmark Emerging Infect. Dis. 2010, 16, 682-684
56. Morello, E. B.; Froglia, C.; Atkinson, R. J. A.; Moore, P. G. Medium-term impacts of hydraulic clam dredgers on a macrobenthic community of the Adriatic Sea (Italy) Mar. Biol. 2006, 149, 401-413