JEP  Vol.5 No.6 , May 2014
Survival of Epidemic, Clinical, Faecal and Recreational Beach Enterococci Strains with Putative Virulence Genes in Marine and Fresh Waters
Abstract: Culturable faecal coliform, epidemic, clinical, faecal and recreational beach enterococci strains possessing putative virulence genes were enumerated over the course of 5 weeks to comparatively assess their persistence in tropical marine and fresh waters. For the clinical and epidemic strains tested, it took 2.38 ± 0.45 days for a 1-log reduction (T90) in marine water. A higher T90 average of 2.51 ± 0.08 was observed for the commensal and environmental strains. Generally, lower T90 values of 2.14 ± 0.26 and 2.15 ± 0.16 days respectively were observed for hospital and community acquired enterococci strains in fresh water mesocosms subjected to tropical ambient temperature. Beach water enterococci and enterococci recovered from faeces of humans survived for up to 20 days and 23 days respectively in fresh and marine waters. The epidemic strain, MMH594, an esp-positive clinical bacteremia isolate that previously caused multiple infections in a hospital ward outbreak fares favourably well in tropical marine and fresh aquatic environments. For enterococci, the decay rate was approximately 13% higher in fresh water than was observed for marine water. On the contrary, for E. coli, the decay rate was approximately 17% lower in fresh water than was observed in marine water. Generally, the whole, the population trends of E. coli and enterococci in fresh and marine water mesocosms did not reveal any evidence of growth. Our findings suggest that potentially pathogenic bacteria can resume active growth after three weeks of being harboured by the reservoir-beach sand and still pose threat to public health.
Cite this paper: Ahmad, A. , Dada, A. and Usup, G. (2014) Survival of Epidemic, Clinical, Faecal and Recreational Beach Enterococci Strains with Putative Virulence Genes in Marine and Fresh Waters. Journal of Environmental Protection, 5, 482-492. doi: 10.4236/jep.2014.56051.

[1]   Haller, L., Pote, J., Loizeau, J.-L. and Wildi, W. (2009) Distribution and Survival of Faecal Indicator Bacteria in the Sediments of the Bay of Vidy, Lake Geneva, Switzerland. Ecological Indicators, 9, 540-547.

[2]   An, Y.-J., Kampbell, D.H. and Breidenbach, G.P. (2002) Escherichia coli and Total Coliforms in Water and Sediments at Lake Marinas. Environmental Pollution, 120, 771-778.

[3]   Noble, R.T., Moore, D.F., Leecaster, M.K., McGee, C.D. and Weisberg, S.B. (2003) Comparison of Total Coliform, Fecal Coliform, and Enterococcus Bacterial Indicator Response for Ocean Recreational Water Quality Testing. Water Research, 37, 1637-1643.

[4]   USEPA (2000) Improved Enumeration Methods for the Recreational Water Quality Indicators: Enterococci and Escherichia coli EPA-821/ R-97/004. U.S. Environmental Protection Agency, Washington DC.

[5]   EU (2006) European Directive 2006/7/CE 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.

[6]   Shibata, T., Solo-Gabriele, H.M., Fleming, L.E. and Elmir, S. (2004) Monitoring Marine Recreational Water Quality Using Multiple Microbial Indicators in an Urban Tropical Environment. Water Research, 38, 3119-3131.

[7]   Jett, B.D., Huycke, M.M. and Gilmore, M.S. (1994) Virulence of Enterococci. Clinical Microbiology Reviews, 7, 462-478.

[8]   Vergis, E.N., Shankar, N., Chow, J.W., Hayden, M.K., Snydman, D.R., Zervos, M.J., Linden, P.K., Wagener, M.M. and Muder, R.R. (2002) Association between the Presence of Enterococcal Virulence Factors Gelatinase, Hemolysin, and Enterococcal Surface Protein and Mortality among Patients with Bacteremia Due to Enterococcus faecalis. Clinical Infectious Diseases, 35, 570-575.

[9]   Semedo, T., Santos, M.A., Lopes, M.F., Marques, J.J.F., Crespo, M.T. and Tenreiro, R. (2003) Virulence Factors in Food, Clinical and Reference Enterococci: A Common Trait in the Genus? Systematic and Applied Microbiology, 26, 13-22.

[10]   Dada, A.C., Ahmad, A., Usup, G. and Heng, L.Y. (2012) Antibiotic Resistance and Virulence Among Enterococci Isolated from Teluk Kemang Beach, Malaysia. Water Quality, Exposure and Health, 1-10.

[11]   Facklam, R. and Elliott, J. (1995) Identification, Classification, and Clinical Relevance of Catalase-Negative, Gram-Positive Cocci, Excluding the Streptococci and Enterococci. Clinical Microbiology Reviews, 8, 479-495.

[12]   Facklam, R. (2002) What Happened to the Streptococci: Overview of Taxonomic and Nomenclature Changes. Clinical Microbiology Reviews, 15, 613-630.

[13]   Dutka-Malen, S., Evers, S. and Courvalin, P. (1995) Detection of Glycopeptide Resistance Genotypes and Identification to the Species Level of Clinically Relevant Enterococci by PCR. Journal of Clinical Microbiology, 33, 24-27.

[14]   Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D. and Goossens, H. (2004) Development of a Multiplex PCR for the Detection of asa1, gelE, cylA, esp, and hyl Genes in Enterococci and Survey for Virulence Determinants among European Hospital Isolates of Enterococcus faecium. Journal of clinical microbiology, 42, 4473-4479.

[15]   Lleò, M.D.M., Bonato, B., Benedetti, D. and Canepari, P. (2005) Survival of Enterococcal Species in Aquatic Environments. FEMS Microbiology Ecology, 54, 189-196.

[16]   Halvorson, H. and Ziegler, N. (1933) Application of Statistics to Problems in Bacteriology: I. A Means of Determining Bacterial Population by the Dilution Method. Journal of Bacteriology, 25, 101-121.

[17]   Giard, J.C., Laplace, J.M., Rince, A., Pichereau, V., Benachour, A., Leboeuf, C., Flahaut, S., Auffray, Y. and Hartke, A. (2001) The Stress Proteome of Enterococcus faecalis. Electrophoresis, 22, 2947-2954.

[18]   Liu, Y.F., Gao, X.J., Cong, Y.T., Peng, Y.H. and Liu, Y. (2004) Research on the Storage Methods of Lactic Acid Bacteria Strains Separated from DVS. Nature and Science, 2, 49.

[19]   Iguchi, A., Osawa, R., Kawano, J., Shimizu, A., Terajima, J. and Watanabe, H. (2002) Effects of Repeated Subculturing and Prolonged Storage at Room Temperature of Enterohemorrhagic Escherichia coli O157: H7 on Pulsed-Field Gel Electrophoresis Profiles. Journal of Clinical Microbiology, 40, 3079-3081.

[20]   Tolba, O., Loughrey, A., Goldsmith, C.E., Millar, B.C., Rooney, P.J. and Moore, J.E. (2008) Survival of Epidemic Strains of Healthcare (HA-MRSA) and Community-Associated (CA-MRSA) Meticillin-Resistant Staphylococcus aureus (MRSA) in River-, Sea- and Swimming Pool Water. International Journal of Hygiene and Environmental Health, 211, 398-402.

[21]   Levin-Edens, E., Bonilla, N., Meschke, J.S. and Roberts, M.C. (2011) Survival of Environmental and Clinical Strains of Methicillin-Resistant Staphylococcus aureus [MRSA] in Marine and Fresh Waters. Water Research, 45, 5681-5686.

[22]   Shankar, V., Baghdayan, A.S., Huycke, M.M., Lindahl, G. and Gilmore, M.S. (1999) Infection-Derived Enterococcus faecalis Strains Are Enriched in Esp, a Gene Encoding a Novel Surface Protein. Infection and Immunity, 67, 193-200.

[23]   Anderson, K.L., Whitlock, J.E. and Harwood, V.J. (2005) Persistence and Differential Survival of Fecal Indicator Bacteria in Subtropical Waters and Sediments. Applied and Environmental Microbiology, 71, 3041-3048.

[24]   Ahmad, A., Dada, A.C., Usup, G. and Heng, L.Y. (2013) Validation of the Enterococci Indicator for Bacteriological Quality Monitoring of Beaches in Malaysia Using a Multivariate Approach. SpringerPlus, 2, 425.

[25]   Desmarais, T.R., Solo-Gabriele, H.M. and Palmer, C.J. (2002) Influence of Soil on Fecal Indicator Organisms in a Tidally Influenced Subtropical Environment. Applied and Environmental Microbiology, 68, 1165-1172.

[26]   Solo-Gabriele, H.M., Wolfert, M.A., Desmarais, T.R. and Palmer, C.J. (2000) Sources of Escherichia coli in a Coastal Subtropical Environment. Applied and Environmental Microbiology, 66, 230-237.

[27]   Medema, G., Bahar, M. and Schets, F. (1997) Survival of Cryptosporidium parvum, Escherichia coli, Faecal Enterococci and Clostridium perfringens in River Water: Influence of Temperature and Autochthonous Microorganisms. Water Science and Technology, 35, 249-252.

[28]   Lleo, M., Bonato, B., Tafi, M., Signoretto, C., Boaretti, M. and Canepari, P. (2001) Resuscitation Rate in Different Enterococcal Species in the Viable but Non-Culturable State. Journal of Applied Microbiology, 91, 1095-1102.

[29]   del Mar Lleo, M., Tafi, M.C. and Canepari, P. (1998) Nonculturable Enterococcus faecalis Cells Are Metabolically Active and Capable of Resuming Active Growth. Systematic and Applied Microbiology, 21, 333-339.

[30]   Isobe, K.O., Tarao, M., Chiem, N.H., Minh, L.Y. and Takada, H. (2004) Effect of Environmental Factors on the Relationship between Concentrations of Coprostanol and Fecal Indicator Bacteria in Tropical (Mekong Delta) and Temperate (Tokyo) Freshwaters. Applied and Environmental Microbiology, 70, 814-821.

[31]   Fujioka, R. and Unutoa, T. (2006) Comparative Stability and Growth Requirements of S. aureus and Faecal Indicator Bacteria in Seawater. Water Science and Technology, 54, 169-175.

[32]   Masmoudi, S., Denis, M. and Maalej, S. (2010) Inactivation of the Gene katA or sodA affects the Transient Entry into the Viable but Non-Culturable Response of Staphylococcus aureus in Natural Seawater at low Temperature. Marine Pollution Bulletin, 60, 2209-2214.

[33]   McFeters, G.A. and Terzieva, S.I. (1991) Survival of Escherichia coli and Yersinia enterocolitica in Stream Water: Comparison of Field and Laboratory Exposure. Microbial Ecology, 22, 65-74.