Abstract
Antimicrobial resistance of marine heterotrophic bacteria to different antimicrobials agents were evaluated in seawater, dry and wet sands from three marine recreational beaches with different pollution levels. In all studied beaches, the greatest frequencies of resistance were found in relation to penicillin. On Gonzaguinha, the most polluted beach, 72.3% of all isolated strains showed simple resistance, whilst 8.33% had multiple resistance. The values found on Ilha Porchat beach, were 70.8% and 6.9% for simple and multiple resistances, respectively. On Guaraú, the less polluted beach, only 35.3% of isolated strains had simple resistance. Multiple resistance was not observed. While samples from Gonzaguinha and Ilha Porchat beach showed isolated strains resistant to seven and six different antimicrobial agents, respectively, samples from Guaraú beach were resistant only to penicillin and erytromicin. The positive correlations obtained between the degree of seawater contamination and frequency and variability of bacterial resistance indicate that polluted marine recreational waters and sands are sources of resistant bacteria contributing thus, to the dissemination of bacterial resistance.
Similar content being viewed by others
References
Alm, E. W., Burke, J., & Spain, A. (2003). Fecal indicator bacteria are abundant in wet sand at freshwater beaches. Water Research, 37(16), 3978–3982.
Arvanitidou, M., Katsouyannopoulos, V. & Tsakris, A. (2001). Antibiotic resistance patterns of enterococci isolated from coastal bathing waters. Journal of Medical Microbiology, 50, 1001–1005.
Austin, N. B. (1988). Marine microbiology (1st Ed., 238p.). Cambridge: Cambridge University Press.
Blom, M., Sorensen, T. L., Poulsen, R. L., Frimodt-Moller, N., Monnet, D. L., Aarestrup, F. M., et al. (2000). Ingestion of vancomycin-resistant Enterococcus faecium strains of food animal origin by human healthy volunteers: A randomized double-bind study. In: 40th ICAAC Abstracts (p. 432). Ontario, Canada.
Bonilla, T. D., Nowosielski, K., Cuvelier, M., Hartz, A., Green, M., Esiobu, N., et al. (2007). Prevalence and distribution of fecal indicator organisms in South Florida beach sand and preliminary assessment of health effects associated with beach sand exposure. Marine Pollution Bulletin, 54(9), 1472–1482.
Brown, A. C., & McLanchlan, A. (1990). Ecology of sandy shores (328 p). Amsterdam: Elsevier.
Bya, A. M., Bryton, P. R., Brown, V. R., Grimes, D. J., Russek-Cohen, E., & Cowell, R. R. (1986). Coincident plasmids and antimicrobial resistance in marine bacteria isolated from polluted and unpolluted Atlantic Ocean samples. Applied and Environmental Microbiology, 51, 1285–1292.
Carroll, S., Hargreaves, M., & Goonetilleke, A. (2005). Sourcing faecal pollution from onsite wastewater treatment systems in surface waters using antibiotic resistance analysis. Journal of Applied Microbiology, 99, 471–482.
CETESB, Companhia de Tecnologia e Saneamento Ambiental (2006). Reltório de qualidade das águas litorâneas do Estado de São Paulo: Balneabilidade das praias 2005. São Paulo, Brasil: Companhia de Tecnologia de Saneamento Ambiental.
CETESB, Companhia de Tecnologia e Saneamento Ambiental (2008). Reltório de qualidade das águas litorâneas do Estado de São Paulo: Balneabilidade das praias 2007. São Paulo, Brasil: Companhia de Tecnologia de Saneamento Ambiental.
Chandrasekarn, S., Venkatesh, B., & Laithakumari, D. (1998). Transfer and expression of a multiple antibiotic resistance plasmid in marine bacteria. Current Microbiology, 37, 347–351.
Davies, J. (1994). Inactivation of antibiotics and the dissemination of resistance genes. Science, 15, 375–382.
Davies, C. M., & Bavor, H. J. (2000). The fate of storm water associated bacteria in constructed wetland and water pollution control pond systems. Journal of Applied Microbiology, 89(2), 349–460.
Davies, C. M., Long, J. A. H., Donald, M., & Ashbolt, N. J. (1995). Survival of fecal microorganism in marine and freshwater sediments. Applied Environmental Microbiology, 61(5), 1888–1896.
Davies-Colley, R. J., Donnison, A. M., Speed, D. J., Ross, C. M., & Nagels, J. W. (1999). Inactivation of fecal indicator microorganisms in waste stabilization ponds: Interactions of environmental factors with sunlight. Water Research, 33(5), 1220–1230.
Erdem-Kimiran, A., Arslan, E. O., Yurudu, N. O. S., Zeybek, Z., Dogruoz, N., & Cotuk, A. (2007). Isolation and identification of enterococci from seawater samples: Assessment of their resistance to antibiotics and heavy metals. Environmental Monitoring Assessment, 125, 219–228.
Gangle, B. J. (2005). Sources and occurrence of antibiotic resistance in the environment (125 p.). Thesis (Master of Science), Faculty of the Graduate School of the University of Maryland, College Park.
Ghinsberg, R. C., Leibowitz, P., Witkin, H., Mates, A., Seinberg, Y., Bar, D. L., et al. (1994). Monitoring of selected bacteria and fungi in sand and seawater along the Tel Aviv coast. MAP Technical Report Series, 87, 65–81.
Gomes-Lus, R. (1998). Evolution of bacterial resistance to antibiotics during the last three decades. International Microbiology, 1, 279–284.
Goni-Urriza, M., Capdepuy, M., Arpin, C., Raymond, N., Caumette, C., & Quentin, C. (2000). Impact of an urban effluent on antibiotic resistance of riverine Enterobacteriaceae an Aeromonas spp. Applied Environmental Microbiology, 1, 125–132.
Hagedorn, C., Robinson, S. L., Filtz, J. R., Gurbbs, S. M., Angier, T. A., & Reneau, R. B. Jr., (1999). Determing sources of fecal pollution in a rural Virginia watershed with antibiotic resistance patterns in fecal streptococci. Applied and Environmental Microbiology, 65(12), 5522–5531.
Halling-Sorensen, B. J., Nielsen, S. N., Lanzky, P. F., & Ingerslev, F. (1998). Occurrence, fate and effects of pharmaceutical substances in the environment—A review. Chemosphere, 36, 357–393.
Harwood, V. J., Whitlock, J., & Withington, V. (2000). Classification of antibiotic resistance patterns of indicator bacteria by discriminant analysis: Using in predicting the source of fecal contamination in subtropical waters. Applied and Environmental Microbiology, 66, 3698–3704.
Hermansson, M. A., Jones, G. W., & Kkjelleberg, S. (1987). Frequency of antibiotic and heavy metal resistance, pigmentation and plasmids in bacteria of the marine air-water interface. Applied Environmental Microbiology, 53, 2338–2342.
Hirsch, R., Ternes, T., Haberer, K., & Kratz, K. (1999). Occurrence of antibiotics in the aquatic environment. The Science of the Total Environment, 225, 109–118.
Huycke, M. M., Sahm, D. F., & Gilmore, M. S. (1998). Multiple-drug resistant enterococci: The nature of the problem and an agenda for the future. Emerging Infectious Diseases, 4(2), 239–249.
Irvensen, A., Kühn, I., Rahman, M., Franklin, A., Burman, L. G., & Olsson-Lijequist, T. (2004) Evidence for a transmission between humans and the environment of nosocomial strain of Enterococcus faecium. Environmental Microbiology, 6, 55–59.
Kühn, I., Iversen, A., Burman, L. G., Olsson-Liljequist, B., Franklin, A., Finn, M., et al. (2000). Epidemiolgy and ecology of enterococci, with special reference to antibiotic resistant strains, in animals, humans and the environment. Example of an ongoing project within the European research programme. International Journal of Antimicrobial Agents, 14(4), 337–342.
Kühn, I., Iversen, A., Finn, M., Greko, C., Burman, L. G., Blanch, A. R., et al. (2005). Occurrence and relatedness of vancomycin-resistant enterococci in animals, humans, and the environment in different European regions. Applied and Environmental Microbiology, 71(9), 5383–5390.
Lobova, T. I., Makisimova, E. Y., Popova, L. Y., & Pechurkin, N. S. (2002). Geographical and sazonal distribution of multipe antibiotic resistance of heterotrophic bacteria of Lake Shira. Aquatic Ecology, 36, 299–307.
Marcinek, H., Wirth, R., Muscholl-Silberhorn, A., & Gauer, M. (1998). Enterococcus faecalis gene transfer under natural conditions in municipal sewage water treatment plants. Applied and Environmental Microbiology, 64(2), 626–632.
Meirelles-Pereira, F., Pereira, A. M. S., Silva, M. C. G., Gonçalves, V. D., Brum, P. R., Castro, E. A. R., et al. (2002). Ecological aspects of the antimicrobial resistance in bacteria of importance to human infections. Brazilian Journal of Microbiology, 33(4), 287–293.
Mendes, B., Nascimento, M. J., & Oliveira, J. S. (1993). Preliminary characterization and proposal of microbiological quality standard of sand beaches. Water Science and Technology, 27, 453–456.
Miranda, C. D., & Zemelman, R. (2001). Antibiotic resistent bactéria in fish from the Concepción Bay, Chile. Marine Pollution Bulletin, 42, 1096–1102.
Mudryk, Z. J. (2005). Occurrence and distribution antibiotic resistance of heterotrophic bacteria isolated from a marine beach. Marine Pollution Bulletin, 50, 80–86.
NCCLS (2003). Performance Standards for Antimicrobial Disk Susceptibility Tests (8a Ed., Vol. 23).
Oliveira, A. J. F. C., Hollnagel, H. C., Mesquita, H. de. S. L., & Fontes, R. F. C. (2007). Physical, chemical and microbiological characterization of the intertidal sediments of Pereque Beach, Guarujá (SP), Brazil. Marine Pollution Bulletin, 54, 921–927.
Oliveira, A. J. F. C., & Pinhata, J. M. W. (2008). Antimicrobial resistance and species composition of Enterococcus spp. Isolated from waters and sands of marine recreational beaches in Southeastern Brazil. Water Research, 42, 2242–2250.
Oshiro, R., & Fujioka, R. (1995). Sand, soil and pigeon droppings: Sources of indicator bacteria in the waters of Hanauma Bay, Oahu, Hawaii. Water Science Technology, 31, 251–254.
Papadakis, J. A., Mavridou, A., Richardson, S. C., Lampiri, M., & Marcelou, U. (1997). Bather-related microbial and yeast populations in sand and seawater. Water Research, 31(4), 799–804.
Pianetti, A., Bruscolini, F., Sabatini, L., & Colantoni, P. (2004). Microbial characteristics of marine sediments in bathing área along Pesaro-Gabicce coast (Italy): A preliminary study. Journal of Applied Microbiology, 97, 682–689.
Sandaa, R. A. (1993). Transfer and maintenance of the plasmid RP4 in marine sediments. Microbiology Release, 2, 115–119.
Sato, M. I. Z., Bari, M. D., Lamparelli, C. C., Truzzi, A. C., Coelho, M. C. L. S., & Hachich, E. M. (2005). Sanitary quality of sands from marine recreational beaches of São Paulo, Brazil. Brazilian Journal of Microbiology, 36(4), 321–326.
Schwartz, T., Kohnen, W., Jansen, B., & Obst, U. (2003). Detection of antibiotic-resistance bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. Microbiology Ecology, 43, 325–335.
Sinton, L. W., Davies-Colley, R. J., & Bell, R. G. (1994). Inactivation of enterococci and fecal coliforms from sewage and meat-works effluents in seawater chambers. Applied Environmental Microbiology, 60(6), 2040–2048.
Smith, H. W. (1971). Incidence of R + Escherichia coli in coastal bathing waters of Britain. Nature, 234, 155–156.
Tejedor, J. M. T., Gonzalez, M. M., Pita, T. M., Lupiola, G. P., & Martín, B. J. L. (2001). Identification and antibiotic resistance of faecal enterococci isolated from water samples. International Journal of Hygiene and Environmental Health, 203, 363–368.
Tendencia, E. A., & De La Pena, L. D. (2001). Antibiotic resistance of bacteria from shrimp ponds. Aquaculture, 195, 193–204.
Villar, C., De Cabro, L., Vaithiyanathan, P., & Bonetto, C. (1999). Pore water N and P concentration in a floodplain marsh of the Lower Parana River. Hydrobiologia, 392(1), 65–71.
Whitman, R. L., & Nevers, M. B. (2003). Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Applied and Environmental Microbiology, 69(9), 5555–5562.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fernandes Cardoso de Oliveira, A.J., Ranzani de França, P.T. & Pinto, A.B. Antimicrobial resistance of heterotrophic marine bacteria isolated from seawater and sands of recreational beaches with different organic pollution levels in southeastern Brazil: evidences of resistance dissemination. Environ Monit Assess 169, 375–384 (2010). https://doi.org/10.1007/s10661-009-1180-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10661-009-1180-6