Hospital-Adapted Clonal Complex 17 Enterococcus Faecium Found among Sand Enterococcal Isolates

DOI: 10.4236/jep.2012.31010   PDF   HTML     4,575 Downloads   7,423 Views   Citations


Though poorly studied, sand is an environment with an extended degree of interaction with man. Enterococcal strains can be found in sand but we do not know to what extent these ubiquitous opportunistic nosocomial pathogens isolated from sand carry antimicrobial resistances and virulence traits. In an attempt to fill in this knowledge gap, two distinct types of sand (beach and children playground) were examined concerning composition in enterococcal species, genetic diversity of isolates and abundance of resistance to antimicrobials and virulence traits. Five different species were found, namely Enterococcus faecium, Enterococcus faecalis, Enterococcus hirae, Enterococcus flavescens and Enterococcus casseliflavus. Although genetic diversity was evident, two different E. faecium clones, common to the two types of sand, were detected, suggesting the existence of clones well adapted to this specific environment or from a common source. E. faecium was associated with multiple antibiotic resistances, including to fluoroquinolones and tetracycline that are commonly used by veterinarians and clinicians. Among the multiresistant E. faecium strains from beach sand, two were from sequence type (ST) 442, which belongs to the wide-spread Hospital-adapted clade CC17. They both carried the esp gene and the genomic island associated with CC17. The other virulence factors screened were disseminated among E. faecalis strains, but seldom detected in the other species, evidencing the existence, in these environments, of E. faecalis strains carrying the same virulence factors as the clinical ones. The present work thus stresses the need to follow-up the presence and characterization of enterococcal strains from both beach and children playground sands and of including these environments in the epidemiological global analysis of enterococcal isolates.

Share and Cite:

D. Pinto, M. Ruivo, P. Vandamme and M. Lopes, "Hospital-Adapted Clonal Complex 17 Enterococcus Faecium Found among Sand Enterococcal Isolates," Journal of Environmental Protection, Vol. 3 No. 1, 2012, pp. 74-82. doi: 10.4236/jep.2012.31010.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] M. F. S. Lopes, T. Ribeiro, M. Abrantes, J. J. F. Marques, R. Tenreiro and M. T. B. Crespo, “Antimicrobial Resis- tance Profiles of Dairy and Clinical Isolates and Type Strains of Enterococci,” International Journal of Food Microbiology, Vol. 103, No. 2, 2005, pp. 191-198. doi:10.1016/j.ijfoodmicro.2004.12.025
[2] A. J. de Oliveira and J. M. Watanabe-Pinhata, “Antim- icrobial Resistance and Species Composition of Entero- coccus spp. Isolated from Waters and Sands of Marine Recreational Beaches in Southeastern Brazil,” Water Research, Vol. 42, No. 8-9, 2008, pp. 2242-2250. doi:10.1016/j.watres.2007.12.002
[3] E. W. Alm, J. Burke and A. Spain, “Fecal Indicator Bacteria Are Abundant in Wet Sand at Freshwater Beaches,” Water Research, Vol. 37, No. 16, 2003, pp 3978-3982. doi:10.1016/S0043-1354(03)00301-4
[4] R. L. Whitman, D. A. Shively, H. Pawlik, M. B. Nevers and M.N. Byappanahalli, “Occurrence of Escherichia coli and Enterococci in Cladophora (Chlorophyta) in Nearshore Water and Beach Sand of Lake Michigan,” Applied and Environmental Microbiology, Vol. 69, No. 8, 2003, pp. 4714-4719. doi:10.1128/AEM.69.8.4714-4719.2003
[5] P. G. Hartel, K. Rodgers, J. A. Fisher, J. L. McDonald, L. C. Gentit, E. Otero, Y. Rivera-Torres, T. L. Bryant and S. H. Jones, “Survival and Regrowth of Fecal Enterococci in Desiccated and Rewetted Sediments,” Proceedings of the 2005 Georgia Water Resources Conference, Athens, 25-27 April 2005.
[6] D. M. Ferguson, D. F. Moore, M. A. Getrich and M. H. Zhowandai, “Enumeration and Speciation of Enterococci Found in Marine and Intertidal Sediments and Costal Water in Southern California,” Journal of Applied Micro- biology, Vol. 99, No. 3, 2005, pp. 598-608. doi:10.1111/j.1365-2672.2005.02660.x
[7] P. M. M. da Costa, P. M. Vaz-Pires and F. M. Bernardo, “Antibiotic Resistance of Enterococcus spp. Isolated from Wastewater and Sludge of Poultry Slaughterhouses,” Jour- nal of Environmental Science and Health B, Vol. 41, No. 8, 2006, pp. 1393-1403. doi:10.1080/03601230600964258
[8] L. Mannu, A. Paba, E. Daga, R. Comunian, S. Zanetti, I. Duprè and L. A. Sechi, “Comparision of the Incidence of Virulence Determinants and Antibiotic Resistance between Enterococcus faecium Strains of Dairy, Animal and Clinical Origin,” International Journal of Food Microbiology, Vol. 88, No. 2-3, 2003, pp. 291-304. doi:10.1016/S0168-1605(03)00191-0
[9] J. Peters, K. Mac, H. Wichmann-Schauer, G. Klein and L. Ellerbroek, “Species Distribution and Antibiotic Resistance Patterns of Enterococci Isolated from Food of Animal Origin in Germany,” International Journal of Food Microbiology, Vol. 88, No. 2-3, 2003, pp. 311-314. doi:10.1016/S0168-1605(03)00193-4
[10] P. Poeta, D. Costa, Y. Sáenz, N. Klibi, F. Ruiz-Larrea and C. Torres, “Characterization of Antibiotic Resistance Genes and Virulence Factors in Faecal Enterococci of Wild Animals in Portugal,” Journal of Veterinary Medicine. B Infectious Disease and Veterinary Public Health, Vol. 52, No. 9, 2005, pp. 396-402.
[11] G. Kayaoglu and D. Orstavik, “Virulence Factors of Enterococcus faecalis: Relationship to Endodontic Disease,” Critical Reviews in Oral Biology and Medicine, Vol. 15, No. 5, 2004, pp. 308-320. doi:10.1177/154411130401500506
[12] S. M. McBride, V. A. Fischetti, D. J. Leblanc, R. C. Moellering Jr. and M. S. Gilmore, “Genetic Diversity among Enterococcus faecalis,” PLoS ONE, Vol. 2, No. 7, 2007, p. e582. doi:10.1371/journal.pone.0000582
[13] A. M. Lowe, P. A. Lambert and A. W. Smith, “Cloning of an Enterococcus faecalis Endocarditis Antigen: Homology with Adhesins from Some Oral Streptococci,” Infection and Immunity, Vol. 63, No. 12, 1995, pp. 703-706.
[14] M. F. S. Lopes, A. P. Sim?es, R. Tenreiro, J. J. Marques and M. T. Crespo, “Activity and expression of a Virulence Factor, Gelatinase, in Dairy Enterococci,” International Journal of Food Microbiology, Vol. 112, No. 3, 2006, pp. 208-214. doi:10.1016/j.ijfoodmicro.2006.09.004
[15] T. Semedo, M. A. Santos, M. F. Lopes, J. J. Figueiredo Marques, M. T. Barreto Crespo and R. Tenreiro, “Virulence Factors in Food, Clinical and Reference Enterococci: A Common Trait in the Genus?” Systematic and Applied Microbiology, Vol. 26, No. 1, 2003, pp. 13-22. doi:10.1078/072320203322337263
[16] P. Serror, T. Sasaki, S. D. Ehrlich and E. Maguin, “Electrotransformation of Lactobacillus delbrueckii subsp. bulgaricus and L. delbrueckii subsp. lactis with Various Plasmids,” Applied and Environmental Microbiology, Vol. 68, No. 1, 2002, pp. 46-52. doi:10.1128/AEM.68.1.46-52.2002
[17] P. Svec, M. Vancanneyt, M. Seman, C. Snauwaert, K. Lefebvre, I. Sedlácek and J. Swings, “Evaluation of (GTG)5- PCR for Identification of Enterococcus spp.,” FEMS Microbiology Letters, Vol. 247, No. 1, 2005, pp. 59-63. doi:10.1016/j.femsle.2005.04.030
[18] S. M. Naser, F. L. Thompson, B. Hoste, D. Gevers, P. Dawyndt, M. Vancanneyt and J. Swings, “Application of Multilocus Sequence Analysis (MLSA) for Rapid Identification of Enterococcus species Based on rpoA and pheS Genes,” Microbiology, Vol. 151, No. 7, 2005, pp. 2141- 2150. doi:10.1099/mic.0.27840-0
[19] T. Ribeiro, M. Abrantes, M. F. Lopes and M. T. Crespo, “Vancomycin-Susceptible Dairy and Clinical Enterococcal Isolates Carry vanA and vanB Genes,” International Journal of Food Microbiology, Vol. 113, No. 3, 2007, pp. 289-295. doi:10.1016/j.ijfoodmicro.2006.08.010
[20] National Committee for Clinical Laboratory Standards, Performance Standards for Antimicrobial Susceptibility Testing, Eleventh-Informational Supplement. Disk dif- fusion, M100-S11, NCCLS, Villanova, 2001,.
[21] T. C. Ribeiro, V. Pinto, F. Gaspar, M. F. S. Lopes, “Enterococcus hirae Causing Wound Infections in a Hospital,” Journal of Clinical Chinese Medicine, Vol. 3, No. 3, 2008, pp. 150-152. doi:10.1086/367711
[22] L. B. Rice, L. Carias, S. Rudin, C. Vael, H. Goossens, C. Konstabel, I. Klare, S. R. Nallapareddy, W. Huang and B. E. Murray, “A Potential Virulence Gene, hylEfm, Predominates in Enterococcus faecium of Clinical Origin,” Journal of Infectious Disease, Vol. 187, No. 3, 2003, pp. 508-512.
[23] E. Heikens, W. van Schaik, H. L. Leavis, M. J. M. Bonten and R. J. L. Willems, “Identification of a Novel Genomic Island Specific to Hospital-Acquired Clonal Complex 17 Enterococcus faecium Isolates,” Applied and Environmental Microbiology, Vol. 74, No. 22, 2008, pp. 7094- 7097. doi:10.1128/AEM.01378-08
[24] W. L. Homan, D. Tribe, S. Poznanski, M. Li, G. Hogg, E. Spalburg, J. D. A. van Embden and R. J. L. Willems, “Multilocus Sequence Typing Scheme for Enterococcus faecium,” Journal of Clinical Microbiology, Vol. 40, No. 6, 2002, pp. 1963-1971. doi:10.1128/JCM.40.6.1963-1971.2002
[25] H. Li-Ming and H. Zhenli, “Water Quality Prediction of Marine Recreational Beaches Receiving Watershed Baseflow and Stormwater Runoff in Southern California, USA,” Water Research, Vol. 42, No. 10-11, 2008, pp. 2563-2573. doi:10.1016/j.watres.2008.01.002
[26] A. Pianetti, F. Bruscolini, L. Sabatini and P. Colantoni, “Microbial Characteristics of Marine Sediments in Bathing Area along Pesaro-Gabicce Coast (Italy): A Preliminary Study,” Journal of Applied Microbiology, Vol. 97, No. 4, 2004, pp. 682-689. doi:10.1111/j.1365-2672.2004.02352.x
[27] H. L. Leavis, R. J. Willems, W. J. van Wamel, F. H. Schuren, M. P. Caspers and M. J. Bonten, “Insertion Se- quence-Driven Diversification Creates a Globally Dis- persed Emerging Multiresistant Subspecies of E. faecium,” PLoS Pathogens, Vol. 3, No. 1, 2007, p. e7. doi:10.1371/journal.ppat.0030007
[28] H. L. Leavis, M. J. Bonten and R. J. Willems, “Identification of High-Risk Enterococcal Clonal Complexes: Glo- bal Dispersion and Antibiotic Resistance,” Current Opi- nion in Microbiology, Vol. 9, No. 5, 2006, pp. 454-460. doi:10.1016/j.mib.2006.07.001
[29] M. Kawalec, J. Kedzierska, A. Gajda, E. Sadowy, J. Wegrzyn, S. Naser, A. B. Skotnicki, M. Gniadkowski and W. Hryniewicz, “Hospital Outbreak of Vancomycin-Resis- tant Enterococci Caused by a Single Clone of Enterococ- cus raffinosus and Several Clones of Enterococcus faecium,” Clinical Microbiology Infections, Vol. 13, No. 9, 2007, pp. 893-901. doi:10.1111/j.1469-0691.2007.01774.x
[30] J. Top, R. Willems, H. Block, M. de Regt, K. Jalink, A. Troelstra, B. Goorhuis and M. Bonten, “Ecological Replacement of Enterococcus faecalis by Multiresistant Clonal Complex 17 Enterococcus faecium,” Clinical Microbiology of Infections, Vol. 13, No. 3, 2007, pp. 316- 319. doi:10.1111/j.1469-0691.2006.01631.x
[31] M. F. Lopes, T. Ribeiro, M. P. Martins, R. Tenreiro and M. T. Crespo, “Gentamicin Resistance in Dairy and Clinical Enterococcal Isolates and in Reference Strains,” Jour- nal of Antimicrobial Chemotherapy, Vol. 52, No. 2, 2003, pp. 214-219. doi:10.1093/jac/dkg304
[32] F. C. Tenover, R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray, D. H. Persin and B. Swamina- than, “Interpreting Chromosomal DNA Restriction Pat- terns Produced by Pulsed-Field Gel Electrophoresis: Cri- teria for Bacterial Strain Typing,” Journal of Clinical Microbiology, Vol. 33, No. 9, 1995, pp. 2233-2239.
[33] 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 Micro- biology, Vol. 42, No. 8, 2004, pp. 3558-3565. doi:10.1128/JCM.42.8.3558-3565.2004
[34] C. A. Arias, B. Robredo, K. V. Singh, C. Torres, D. Panesso and B. E. Murray, “Rapid Identification of Enterococcus hirae and Enterococcus durans by PCR and detection of a Homologue of the E. hirae mur-2 Gene in E. durans,” Journal of Clinical Microbiology, Vol. 44, No. 8, 2006, pp. 1567-1570. doi:10.1128/JCM.44.4.1567-1570.2006
[35] F. Depardieu, B. Perichon and P. Courvalin, “Detection of the Van Alphabet and Identification of Enterococci and Staphylococci at the Species Level by Multiplex PCR,” Journal of Clinical Microbiology, Vol. 42, No. 12, 2004, pp. 5857-5860. doi:10.1128/JCM.42.12.5857-5860.2004

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.