Skip to main content
Log in

The prevalence of antibiotic-resistant bacteria (ARB) in waters of the Lower Ballona Creek Watershed, Los Angeles County, California

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Screening for the prevalence of antibiotic-resistant bacteria (ARB) was done at the Ballona Creek and Wetlands, an urban-impacted wetland system in Los Angeles, California. The goals were (1) to assess the overall prevalence of ARB, and (2) compare differences in ARB abundance and the types of antibiotic resistance (AR) among the following sample types: lagoon water from Del Rey Lagoon, urban runoff from Ballona Creek, and water from the Ballona Wetlands (tidal water flooding in from the adjacent estuary, and ebbing out from the salt marsh). Antibiotic resistance distributions were analyzed using the Kolmogorov-Smirnov test to develop the cumulative frequency of bacteria having resistance of up to eight antibiotics. Distributions from the environmental water samples were compared to unchlorinated secondary effluent from the Hyperion Water Reclamation Plant that was used as comparator samples likely to have an abundance of ARB. As expected, densities of total and ARB were highest in secondary effluent, followed by urban runoff. Samples of water flooding into the wetlands showed similar results to urban runoff; however, a reduction in densities of total and ARB occurred in water ebbing out of the wetlands. During preliminary work to identify ARB species, several bacterial species of relevance to human illness (e.g., Staphylococcus aureus, Enterococcus hirae, Pseudomonas aeruginosa, Aeromonas veronii, Enterobacter cancerogenus, Serratia marcescens, Pseudomonas stutzeri, and Staphylococcus intermedius) were isolated from sampled waters. If wetlands are a sink for ARB, construction and restoration of wetlands can help in the mediation of this human and environmental health concern.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4.

Similar content being viewed by others

References

  • Amos, G. C. A., Hawkey, P. M., Gaze, W. H., & Wellington, E. M. (2014). Waste water effluent contributes to the dissemination of CTX-M-15 in the natural environment. Journal of Antimicrobial Chemotherapy, 69, 1785–1791. doi:10.1093/jac/dku079.

    Article  CAS  Google Scholar 

  • Andersson, D. I., & Levin, B. R. (1999). The biological cost of antibiotic resistance. Current Opinion in Microbiology, 2(5), 489–493.

    Article  CAS  Google Scholar 

  • Andrews, J. M. (2001). Determination of minimum inhibitory concentrations. Journal of Antimicrobial Chemotherapy, 48(suppl 1), 5–16.

    Article  CAS  Google Scholar 

  • APHA. (1980). Standard methods for the examination of water and wastewater (15th ed.). Washington, D.C.: APHA-AWWAWPCF.

    Google Scholar 

  • Ash, R. J., Mauck, B., & Morgan, M. (2002). Antibiotic resistance of gram-negative bacteria in rivers, United States. Emerging Infectious Diseases, 8(7), 713–716.

    Article  Google Scholar 

  • Ataie-Ashtiani, B., Volker, R. E., & Lockington, D. A. (1999). Tidal effects on sea water intrusion in unconfined aquifers. Journal of Hydrology, 216(1), 17–31.

    Article  Google Scholar 

  • Badiaga, S., Raoult, D., & Brouqui, P. (2008). Preventing and controlling emerging and reemerging transmissible diseases in the homeless. Emerging Infectious Diseases., 14(9), 1353–1359.

    Article  Google Scholar 

  • Barkovskii, A. L., Babb, C. M., Hurley, D., & Shin, E. (2015). Origins and environmental mobility of antibiotic resistance genes, virulence factors and bacteria in a tidal creek’s watershed. Journal of Applied Microbiology, 118(3), 764–776.

    Article  CAS  Google Scholar 

  • Bauer, A. W., Kirby, W. M., Sherris, J. C. T., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45(4), 493.

    CAS  Google Scholar 

  • Center for Disease Control and Prevention (2013) Reported Tuberculosis in the United States. Available at: http://www.cdc.gov/tb/statistics/reports/2012/pdf/report2012.pdf. Accessed 15 January 2016.

  • Choi, S., Chu, W., Brown, J., Becker, S. J., Harwood, V. J., & Jiang, S. C. (2003). Application of enterococci antibiotic resistance patterns for contamination source identification at Huntington Beach, California. Marine Pollution Bulletin, 46(6), 748–755.

    Article  CAS  Google Scholar 

  • City of Los Angeles, Bureau of Sanitation (2013). Available at: http://www.lacitysan.org/ Accessed 10 October 2015.

  • Cox, P., Griffith, M., Angles, M., Deere, D., & Ferguson, C. (2005). Concentrations of pathogens and indicators in animal feces in the Sydney watershed. Applied and Environmental Microbiology, 71(10), 5929–5934.

    Article  CAS  Google Scholar 

  • Cummings, D. E., Archer, K. F., Arriola, D. J., Baker, P. A., Faucett, K. G., Laroya, J. B., et al. (2010). Broad dissemination of plasmid-mediated quinolone resistance genes in sediments of two urban coastal wetlands. Environmental Science & Technology, 45(2), 447–454.

    Article  Google Scholar 

  • Dorsey, J. H. (2006). Densities of fecal indicator bacteria in tidal waters of the Ballona Wetlands, Los Angeles County, California. Bulletin, Southern California Academy of Sciences, 105(2), 59–75.

    Article  Google Scholar 

  • Dorsey, J. H., Carter, P. M., Bergquist, S., & Sagarin, R. (2010). Reduction of fecal indicator bacteria (FIB) in the Ballona Wetlands saltwater marsh (Los Angeles County, California, USA) with implications for restoration actions. Water Research, 44(15), 4630–4642.

    Article  CAS  Google Scholar 

  • Dorsey, J. H., Carmona-Galindo, V. D., Leary, C., Huh, J., & Valdez, J. (2013). An assessment of fecal indicator and other bacteria from an urbanized lagoon in the City of Los Angeles, California, USA. Enviromental Monioring and Assessment, 185(3), 2647–2669.

    Article  CAS  Google Scholar 

  • Dzidic, S., & Bedeković, V. (2003). Horizontal gene transfer-emerging multidrug resistance in hospital bacteria. Acta Pharmacologica Sinica, 24(6), 519–526.

    CAS  Google Scholar 

  • Eadie, W. T., Drijard, D., James, F. E., Roos, M., & Sadoulet, B. (1971). Statistical methods in experimental physics (pp. 269–271). Amsterdam: North-Holland.

    Google Scholar 

  • Ghosh, S., Ramsden, S. J., & LaPara, T. M. (2009). The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants. Applied Microbiology and Biotechnology, 84(4), 791–796.

    Article  CAS  Google Scholar 

  • Harwood, V. J., Whitlock, J., & Withington, V. (2000). Classification of antibiotic resistance patterns of indicator bacteria by discriminant analysis: use in predicting the source of fecal contamination in subtropical waters. Applied and Environmental Microbiology, 66(9), 3698–3704.

    Article  CAS  Google Scholar 

  • Hazen, T. C., Jiménez, L., López de Victoria, G., & Fliermans, C. B. (1991). Comparison of bacteria from deep subsurface sediment and adjacent groundwater. Microbial Ecology, 22(1), 293–304.

  • Hench, K. R., Bissonnette, G. K., Sexstone, A. J., Coleman, J. G., Garbutt, K., & Skousen, J. G. (2003). Fate of physical, chemical, and microbial contaminants in domestic wastewater following treatment by small constructed wetlands. Water Research, 37(4), 921–927.

    Article  CAS  Google Scholar 

  • Hidron, A. I., Kourbatova, E. V., Halvosa, J. S., Terrell, B. J., McDougal, L. K., Tenover, F. C., et al. (2005). Risk factors for colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clinical Infectious Diseases, 41(2), 159–166.

    Article  Google Scholar 

  • Hooton, T. M., & Stamm, W. E. (1997). Diagnosis and treatment of uncomplicated urinary tract infection. Infectious Disease Clinics of North America, 11(3), 551–581.

    Article  CAS  Google Scholar 

  • Huang, J. J., Hu, H. Y., Lu, S. Q., Li, Y., Tang, F., Lu, Y., & Wei, B. (2012). Monitoring and evaluation of antibiotic-resistant bacteria at a municipal wastewater treatment plant in China. Environment International, 42, 31–36.

    Article  CAS  Google Scholar 

  • Johnston, K. K., Del Giudice-Tuttle, E., Medel, I. D., Bergquist, S., Cooper, D. S., Dorsey, J., & Anderson, S. (2011). The Ballona Wetlands Ecological Reserve Baseline Assessment Program: year one report Santa Monica Bay restoration commission. Los Angeles: Prepared for the California State Coastal Conservancy.

    Google Scholar 

  • Johnston, K. K., Del Giudice-Tuttle, E., Medel, I. D., Piechowski, C. J., Cooper, D. S., Dorsey, J., & Anderson, S. (2012). The Ballona Wetlands Ecological Reserve Baseline Assessment Program: second year report. Santa Monica Bay restoration commission. Los Angeles: Prepared for the California State Coastal Conservancy.

    Google Scholar 

  • Johnston, K., Dorsey, J. H., & Saez, J. (2015). Stratification and loading of fecal indicator bacteria (FIB) in a tidally muted urban salt marsh. Environmental Monitoring and Assessment., 187, 58–77. doi:10.1007/s10661-015-4314-z.

    Article  Google Scholar 

  • Kaushal, S. S., Groffman, P. M., Band, L. E., Elliott, E. M., Shields, C. A., & Kendall, C. (2011). Tracking nonpoint source nitrogen pollution in human-impacted watersheds. Environmental Science & Technology, 45(19), 8225–8232.

    Article  CAS  Google Scholar 

  • Khachatourians, G. G. (1998). Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. Canadian Medical Association Journal, 159(9), 1129–1136.

    CAS  Google Scholar 

  • Kim, S., & Aga, D. S. (2007). Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. Journal of Toxicology and Environmental Health, Part B, 10(8), 559–573.

    Article  CAS  Google Scholar 

  • Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., & Active Bacterial Core surveillance (ABCs) MRSA Investigators. (2007). Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA, 298(15), 1763–1771.

    Article  CAS  Google Scholar 

  • Koivunen, J., Siitonen, A., & Heinonen-Tanski, H. (2003). Elimination of enteric bacteria in biological–chemical wastewater treatment and tertiary filtration units. Water Research, 37(3), 690–698.

    Article  CAS  Google Scholar 

  • Kümmerer, K. (2004). Resistance in the environment. Journal of Antimicrobial Chemotherapy, 54(2), 311–320.

    Article  Google Scholar 

  • LA Stormwater (2016) LA Sanitation District. Available at: http://www.lastormwater.org/about-us/about-watersheds/ballona-creek/ Accessed 21 March 2016.

  • Lederberg, J., & Lederberg, E. M. (1952). Replica plating and indirect selection of bacterial mutants. Journal of Bacteriology, 63, 399–406.

    CAS  Google Scholar 

  • Liu, L., Liu, C., Zheng, J., Huang, X., Wang, Z., Liu, Y., & Zhu, G. (2013). Elimination of veterinary antibiotics and antibiotic resistance genes from swine wastewater in the vertical flow constructed wetlands. Chemosphere, 91(8), 1088–1093.

    Article  CAS  Google Scholar 

  • Los Angeles Almanac (2014) Homelessness in Los Angeles County. Available at: http://www.laalmanac.com/social/so14.htm Accessed 21 March 2016.

  • Los Angeles Department of Public Works (2017) Department of Public Works. Available at:http://dpw.lacounty.gov/ Accessed 5 August 2013.

  • May, J. R., & Delves, D. M. (1964). Ampicillin in the treatment of Haemophilus influenzae infections of the respiratory tract. Thorax, 19(4), 298–305.

    Article  CAS  Google Scholar 

  • Mudryk, Z. J. (2005a). Occurrence and distribution antibiotic resistance of heterotrophic bacteria isolated from a marine beach. Marine Pollution Bulletin, 50(1), 80–86.

    Article  CAS  Google Scholar 

  • Murray, P., Baron, E., Jorgensen, J., Landry, M., & Pfaller, M. (2007). Manual of clinical microbiology (9th ed.). Washington, DC: ASM Press.

    Google Scholar 

  • National Ocean and Atmospheric Administration (NOAA), (2017). Tides and Currents, Observed water levels at Station 9410840, Santa Monica Pier. Available at: https://tidesandcurrents.noaa.gov Accessed 01 May 2013.

  • Nesme, J., Cécillon, S., Delmont, T. O., Monier, J. M., Vogel, T. M., & Simonet, P. (2014). Large-scale metagenomic-based study of antibiotic resistance in the environment. Current Biology, 24(10), 1096–1100.

    Article  CAS  Google Scholar 

  • Noble, R. T., Lee, I. M., & Schiff, K. C. (2004). Inactivation of indicator micro-organisms from various sources of faecal contamination in seawater and freshwater. Journal of Applied Microbiology, 96, 464–472.

    Article  CAS  Google Scholar 

  • Österblad, M., Leistevuo, T., & Huovinen, P. (1995). Screening for antimicrobial resistance in fecal samples by the replica plating method. Journal of Clinical Microbiology, 33, 3146–3149.

    Google Scholar 

  • Pruden, A., Arabi, M., & Storteboom, H. N. (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46(21), 11541–11549.

    Article  CAS  Google Scholar 

  • Reimer, L. G., Stratton, C. W., & Reller, L. B. (1981). Minimum inhibitory and bactericidal concentrations of 44 antimicrobial agents against three standard control strains in broth with and without human serum. Antimicrobial Agents and Chemotherapy, 19(6), 1050–1055.

    Article  CAS  Google Scholar 

  • Rizzo, L., Manaia, C., Merlin, C., Schwartz, T., Dagot, C., Ploy, M. C., et al. (2013). Urban wastewater treatment plants as hotspots for antibiotic-resistant bacteria and genes spread into the environment: a review. Science of the Total Environment, 447, 345–360.

    Article  CAS  Google Scholar 

  • Santa Monica Bay Restoration Commission (2011). Bay Restoration Commission. Available at: http://www.santamonicabay.org/ Accessed 30 April 2013.

  • Sayah, R. S., Kaneene, J. B., Johnson, Y., & Miller, R. (2005). Patterns of antimicrobial resistance observed in Escherichia coli isolates obtained from domestic-and wild-animal fecal samples, human septage, and surface water. Applied and Environmental Microbiology, 71(3), 1394–1404.

    Article  CAS  Google Scholar 

  • Schwartz, T., Kohnen, W., Jansen, B., & Obst, U. (2003). Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiology Ecology, 43(3), 325–335.

    Article  CAS  Google Scholar 

  • Seybold, U., Kourbatova, E. V., Johnson, J. G., Halvosa, S. J., Wang, Y. F., King, M. D., & Blumberg, H. M. (2006). Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care—associated blood stream infections. Clinical Infectious Diseases, 42(5), 647–656.

    Article  CAS  Google Scholar 

  • Sidrach-Cardona, R., Hijosa-Valsero, M., Marti, E., Balcázar, J. L., & Becares, E. (2014). Prevalence of antibiotic-resistant fecal bacteria in a river impacted by both an antibiotic production plant and urban treated discharges. Science of the Total Environment, 488, 220–227.

    Article  Google Scholar 

  • Stein, E.D., Tiefenthaler, L.L., 2004. Characterization and source identification of dry weather metals and bacteria in Ballona Creek. In: Weisberg, S., Elmore, D. (Eds.), Southern California Coastal Water Research Project, Biennial Report 2003e2004.

  • Tadesse, D. A., Zhao, S., Tong, E., Ayers, S., Singh, A., Bartholomew, M. J., & McDermott, P. F. (2012). Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950–2002. Emerging Infectious Diseases, 18(5), 741–749.

    Article  CAS  Google Scholar 

  • U.S. Department of Health and Human Services (2012) Urinary Tract Infection in Adults Available at: http://www.niddk.nih.gov/health-information/health-topics/urologic-disease/urinary-tract-infections-in-adults/Pages/facts.aspx#common Accessed 19 February 2016.

  • Waksman, S. A., & Woodruff, H. B. (1940). The soil as a source of microorganisms antagonistic to disease-producing bacteria. Journal of Bacteriology, 40(4), 581.

    CAS  Google Scholar 

  • Walsh, F., & Duffy, B. (2013). The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria.

  • Washington II, J. A., & Barry, A. L. (1974). Dilution test procedures. In E. H. Lennette, E. H. Spaulding, & J. P. Truant (Eds.), Manual of clinical microbiology (2nd ed., pp. 410–417). Washington, D.C.: American Society for Microbiology.

    Google Scholar 

  • West, J. (2001). Ballona Wetland. Handbook for Restoring Tidal Wetlands, JB Zedler, CRC Press, Boca Raton 10–20.

  • Whitlock, J. E., Jones, D. T., & Harwood, V. J. (2002). Identification of the sources of fecal coliforms in an urban watershed using antibiotic resistance analysis. Water Research, 36(17), 4273–4282.

    Article  CAS  Google Scholar 

  • Wilson, K. (1987). Preparation of genomic DNA from bacteria. Current protocols in molecular biology, 2–4.

  • Wu, S., Carvalho, P. N., Müller, J. A., Manoj, V. R., & Dong, R. (2016). Sanitation in constructed wetlands: A review on the removal of human pathogens and fecal indicators. Science of the Total Environment, 541, 8–22.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge many students in LMU’s College of Science and Engineering who worked on this project. Many were supported through Rains Scholarship and the Summer Undergraduate Research Program funding, both through Loyola Marymount University. Additional funding was provided by LMU’s Department of Biology for laboratory supplies and materials. Karina Johnston (Santa Monica Bay Foundation) arranged access into the Ballona Wetlands Ecological Reserve. Leslie Sidio (Hyperion Water Reclamation Plant) provided samples of secondary effluent for testing. David Cummings (Point Loma Nazarene University) kindly reviewed a draft manuscript, and provided excellent recommendations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephanie Kawecki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawecki, S., Kuleck, G., Dorsey, J.H. et al. The prevalence of antibiotic-resistant bacteria (ARB) in waters of the Lower Ballona Creek Watershed, Los Angeles County, California. Environ Monit Assess 189, 261 (2017). https://doi.org/10.1007/s10661-017-5964-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-017-5964-9

Keywords

Navigation