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Human-Associated Methicillin-Resistant Staphylococcus aureus from a Subtropical Recreational Marine Beach

  • Environmental Microbiology
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Abstract

Reports of Staphylococcus aureus including methicillin-resistant S. aureus (MRSA) detected in marine environments have occurred since the early 1990s. This investigation sought to isolate and characterize S. aureus from marine waters and sand at a subtropical recreational beach, with and without bathers present, in order to investigate possible sources and to identify the risks to bathers of exposure to these organisms. During 40 days over 17 months, 1,001 water and 36 intertidal sand samples were collected by either bathers or investigators at a subtropical recreational beach. Methicillin-sensitive S. aureus (MSSA) and MRSA were isolated and identified using selective growth media and an organism-specific molecular marker. Antimicrobial susceptibility, staphylococcal cassette chromosome mec (SCCmec) type, pulsed-field gel electrophoresis (PFGE) pattern, multi-locus sequence type (MLST), and staphylococcal protein A (spa) type were characterized for all MRSA. S. aureus was isolated from 248 (37 %) bather nearby water samples at a concentration range of <2–780 colony forming units per ml, 102 (31 %) ambient water samples at a concentration range of <2–260 colony forming units per ml, and 9 (25 %) sand samples. Within the sand environment, S. aureus was isolated more often from above the intertidal zone than from intermittently wet or inundated sand. A total of 1334 MSSA were isolated from 37 sampling days and 22 MRSA were isolated from ten sampling days. Seventeen of the 22 MRSA were identified by PFGE as the community-associated MRSA USA300. MRSA isolates were all SCCmec type IVa, encompassed five spa types (t008, t064, t622, t688, and t723), two MLST types (ST8 and ST5), and 21 of 22 isolates carried the genes for Panton–Valentine leukocidin. There was a correlation (r = 0.45; p = 0.05) between the daily average number of bathers and S. aureus in the water; however, no association between exposure to S. aureus in these waters and reported illness was found. This report supports the concept that humans are a potential direct source for S. aureus in marine waters.

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Acknowledgments

The Florida Department of Health supported data collection in the BEACHES study; the US Environmental Protection Agency (EPA) and the National Oceanographic and Atmospheric Administration (NOAA) facilitated water sample collection for the Ambient Water Study. We also thank the Palm Beach Infectious Disease Institute for providing S. aureus clinical isolates for comparison. This publication represents the personal opinions of the authors and is not the official position of the contributing federal government agencies. No official endorsement of any product or commercial laboratory is made or implied by its use in this study.

Funding

The University of Miami provided financial support through the Interdisciplinary Research Development Initiative. This study was also supported in part by the National Science Foundation (NSF) and the National Institute of Environmental Health Sciences (NIEHS) Oceans and Human Health Center at the University of Miami Rosenstiel School [NSF 0CE0432368/0911373 and NIEHS P50 ES12736] and NSF REU in Oceans and Human Health, the NSF SGER [NSF SGER 0743987] in Oceans and Human Health, the US EPA, the US Centers for Disease Control and Prevention, the Florida Departments of Health and of Environmental Protection, and the European Union Convergence Programme (to ECEHH at PCMD, University of Exeter).

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Authors and Affiliations

  1. Departments of Pediatrics and Microbiology and Immunology, University of Miami Miller School of Medicine, 1600 NW 10th Ave, Miami, FL, 33136, USA

    Lisa R. W. Plano, Anna C. Garza & Suzanne Hower

  2. NSF-NIEHS Oceans and Human Health Center, Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, Miami, FL, 33149, USA

    Lisa R. W. Plano, Tomoyuki Shibata, Jonathan Kish, Christopher D. Sinigalliano, Maribeth L. Gidley, Kelly Withum, Samir M. Elmir, Lora E. Fleming & Helena M. Solo-Gabriele

  3. Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, Miami, FL, 33149, USA

    Tomoyuki Shibata, Christopher D. Sinigalliano & Maribeth L. Gidley

  4. Public Health and Health Education Programs, Northern Illinois University, DeKalb, IL, 60115, USA

    Tomoyuki Shibata

  5. Department of Epidemiology and Public Health, University of Miami Miller School of Medicine, Miami, FL, 33136, USA

    Jonathan Kish & Lora E. Fleming

  6. Public Health Program College of Osteopathic Medicine, Nova Southeastern University, Fort Lauderdale, FL, 33328, USA

    Jay M. Fleisher

  7. Miami-Dade County Health Department, Miami, FL, 33056, USA

    Samir M. Elmir

  8. Bacterial Epidemiology and Antimicrobial Resistance Research Unit, Richard B. Russell Research Center, Agricultural Research Service, US Department of Agriculture, Athens, GA, 30605, USA

    Charlene R. Jackson & John B. Barrett

  9. Departments of Pathology and Microbiology and Immunology, University of Miami Miller School of Medicine, Miami, FL, 33136, USA

    Timothy Cleary

  10. Center for Veterinary Medicine, US Food and Drug Administration, Laurel, MD, 20708, USA

    Maureen Davidson, Johnnie Davis & Sampa Mukherjee

  11. European Centre for Environment and Human Health (ECEHH), Peninsula College of Medicine and Dentistry (PCMD), Truro, Cornwall, TR1 3HD, UK

    Lora E. Fleming

  12. Department of Civil, Architectural, and Environmental Engineering, University of Miami, Coral Gables, FL, 33124, USA

    Helena M. Solo-Gabriele

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  1. Lisa R. W. Plano
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Correspondence to Lisa R. W. Plano.

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Plano, L.R.W., Shibata, T., Garza, A.C. et al. Human-Associated Methicillin-Resistant Staphylococcus aureus from a Subtropical Recreational Marine Beach. Microb Ecol 65, 1039–1051 (2013). https://doi.org/10.1007/s00248-013-0216-1

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