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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

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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.

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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.

    Article  Google Scholar 

  • Arvanitidou, M., Katsouyannopoulos, V. & Tsakris, A. (2001). Antibiotic resistance patterns of enterococci isolated from coastal bathing waters. Journal of Medical Microbiology, 50, 1001–1005.

    CAS  Google Scholar 

  • Austin, N. B. (1988). Marine microbiology (1st Ed., 238p.). Cambridge: Cambridge University Press.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Brown, A. C., & McLanchlan, A. (1990). Ecology of sandy shores (328 p). Amsterdam: Elsevier.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Chandrasekarn, S., Venkatesh, B., & Laithakumari, D. (1998). Transfer and expression of a multiple antibiotic resistance plasmid in marine bacteria. Current Microbiology, 37, 347–351.

    Article  Google Scholar 

  • Davies, J. (1994). Inactivation of antibiotics and the dissemination of resistance genes. Science, 15, 375–382.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Gomes-Lus, R. (1998). Evolution of bacterial resistance to antibiotics during the last three decades. International Microbiology, 1, 279–284.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Miranda, C. D., & Zemelman, R. (2001). Antibiotic resistent bactéria in fish from the Concepción Bay, Chile. Marine Pollution Bulletin, 42, 1096–1102.

    Article  CAS  Google Scholar 

  • Mudryk, Z. J. (2005). Occurrence and distribution antibiotic resistance of heterotrophic bacteria isolated from a marine beach. Marine Pollution Bulletin, 50, 80–86.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Sandaa, R. A. (1993). Transfer and maintenance of the plasmid RP4 in marine sediments. Microbiology Release, 2, 115–119.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Smith, H. W. (1971). Incidence of R + Escherichia coli in coastal bathing waters of Britain. Nature, 234, 155–156.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Tendencia, E. A., & De La Pena, L. D. (2001). Antibiotic resistance of bacteria from shrimp ponds. Aquaculture, 195, 193–204.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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Correspondence to Ana Julia Fernandes Cardoso de Oliveira.

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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

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