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Characterization of Staphylococcus aureus in Goose Feces from State Parks in Northeast Ohio

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Abstract

Staphylococcus aureus can colonize a range of species. Although numerous studies have isolated pathogenic bacteria from wild birds, very little is known regarding S. aureus and their potential to spread methicillin-resistant (MRSA) strains. The objective of this study was to determine the presence and molecular characteristics of S. aureus in geese fecal samples collected from ten state parks across Northeast Ohio (NEO). A total of 182 fecal samples from Canada geese (Branta canadensis) were collected in April 2015. Isolates were characterized using multi-locus sequence (MLST) and spa typing, as well as PCR to detect the presence of Panton–Valentine leukocidin (PVL), mecA, and scn genes. Antibiotic susceptibility testing was done via Vitek-2 system. The overall contamination by S. aureus in fecal samples was 7.1% (13/182); 7/182 (3.8%) were MRSA and 6/182 (3.3%) were methicillin-susceptible S. aureus (MSSA). One isolate was positive for PVL. A total of eight different spa types were observed. MLST included ST5, ST8, ST291, ST298, and ST2111. One (7.7%) MSSA isolate was multi-drug resistant. The S. aureus contamination in NEO state parks ranged from 0% (park 1, 4, 8, 9) to 35% (7/20) (park 5). Parks 2, 3, 6, and 7 had 5% (1/20) positive. The results of this study indicate that the feces of geese collected at various state parks in NEO may harbor S. aureus.

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References

  • Allen, H. K., J. Donato, H. H. Wang, K. A. Cloud-Hansen, J. Davies and J. Handelsman (2010). “Call of the wild: antibiotic resistance genes in natural environments.” Nature Reviews Microbiology 8(4): 251-259.

    Article  CAS  PubMed  Google Scholar 

  • Borjesson, S., A. Matussek, S. Melin, S. Lofgren and P. E. Lindgren (2009). “Methicillin-resistant Staphylococcus aureus (MRSA) in municipal wastewater: an uncharted threat?” J Appl Microbiol.

  • Bosgelmez-Tinaz, G., S. Ulusoy, B. Aridogan and F. Coskun-Ari (2006). “Evaluation of different methods to detect oxacillin resistance in Staphylococcus aureus and their clinical laboratory utility.” Eur J Clin Microbiol Infect Dis 25(6): 410-412.

    Article  CAS  PubMed  Google Scholar 

  • Brooks, J. P., A. Adeli and M. R. McLaughlin (2014). “Microbial ecology, bacterial pathogens, and antibiotic resistant genes in swine manure wastewater as influenced by three swine management systems.” Water Res 57: 96-103.

    Article  CAS  PubMed  Google Scholar 

  • Cordell, H. K., C. J. Betz and G. T. Green (2008). “Nature-based outdoor recreation trends and wilderness.”

  • Dantes, R., Y. Mu, R. Belflower, D. Aragon, G. Dumyati, L. H. Harrison, F. C. Lessa, R. Lynfield, J. Nadle and S. Petit (2013). “National burden of invasive methicillin-resistant Staphylococcus aureus infections, United States, 2011.” JAMA internal medicine 173(21): 1970–1978.

    PubMed  Google Scholar 

  • Dimitracopoulos, G., C. Sakellariou and J. Papavassiliou (1976). “Staphylococci from the feces of different animal species: biotypes of Staphylococcus aureus strains of sheep and goat origin.” Applied and environmental microbiology 32(1): 53-55.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dolbeer, R. A., J. L. Seubert and M. J. Begier (2014). “Population trends of resident and migratory Canada geese in relation to strikes with civil aircraft.” Human-Wildlife Interactions 8(1): 88.

    Google Scholar 

  • Enright, M. C., N. P. Day, C. E. Davies, S. J. Peacock and B. G. Spratt (2000). “Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus.” J Clin Microbiol 38(3): 1008-1015.

    CAS  PubMed  PubMed Central  Google Scholar 

  • French, L. and J. A. Parkhurst (2009). “Managing wildlife damage: Canada goose (Branta canadensis).”

  • Gerba, C. P. and J. E. Smith (2005). “Sources of pathogenic microorganisms and their fate during land application of wastes.” Journal of Environmental Quality 34(1): 42-48.

    CAS  PubMed  Google Scholar 

  • Gómez, P., C. Lozano, M. C. Camacho, J.-F. Lima-Barbero, J.-M. Hernández, M. Zarazaga, Ú. Höfle and C. Torres (2015). “Detection of MRSA ST3061-t843-mecC and ST398-t011-mecA in white stork nestlings exposed to human residues.” Journal of Antimicrobial Chemotherapy: dkv314.

  • Gorwitz, R. J., D. Kruszon-Moran, S. K. McAllister, G. McQuillan, L. K. McDougal, G. E. Fosheim, B. J. Jensen, G. Killgore, F. C. Tenover and M. J. Kuehnert (2008). “Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001–2004.” Journal of Infectious Diseases 197(9): 1226–1234.

    Article  PubMed  Google Scholar 

  • Graczyk, T. K., R. Fayer, J. M. Trout, E. J. Lewis, C. A. Farley, I. Sulaiman and A. A. Lal (1998). “Giardia sp. Cysts and infectious Cryptosporidium parvum oocysta in the feces of migratory Canada Geese (Branta Canadensis).” Appl Environ Microbiol 64(7): 2736–2738.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Graham, J. P., J. H. Leibler, L. B. Price, J. M. Otte, D. U. Pfeiffer, T. Tiensin and E. K. Silbergeld (2008). “The animal-human interface and infectious disease in industrial food animal production: rethinking biosecurity and biocontainment.” Public health reports: 282–299.

  • Graham, P. L., 3rd, S. X. Lin and E. L. Larson (2006). “A U.S. population-based survey of Staphylococcus aureus colonization.” Ann Intern Med 144(5): 318–325.

    Article  PubMed  Google Scholar 

  • Huijsdens, X. W., B. J. Van Dijke, E. Spalburg, M. G. van Santen-Verheuvel, M. E. Heck, G. N. Pluister, A. Voss, W. J. Wannet and A. J. De Neeling (2006). “Community-acquired MRSA and pig-farming.” Annals of Clinical Microbiology and Antimicrobials 5(1): 1.

    Article  Google Scholar 

  • Institute, C. a. L. S. (2012). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Second Informational Supplement. Wayne, PA, Clinical and Laboratory Standards Institute.

    Google Scholar 

  • Kadariya, J., T. C. Smith and D. Thapaliya (2014). “Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health.” BioMed research international 2014.

  • Koreen, L., S. V. Ramaswamy, E. A. Graviss, S. Naidich, J. M. Musser and B. N. Kreiswirth (2004). “spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation.” J Clin Microbiol 42(2): 792–799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonard, F. and B. Markey (2008). “Meticillin-resistant Staphylococcus aureus in animals: a review.” The Veterinary Journal 175(1): 27–36.

    Article  CAS  PubMed  Google Scholar 

  • Lina, G., Y. Piemont, F. Godail-Gamot, M. Bes, M. O. Peter, V. Gauduchon, F. Vandenesch and J. Etienne (1999). “Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia.” Clin Infect Dis 29(5): 1128–1132.

    Article  CAS  PubMed  Google Scholar 

  • Llarena, A. K., C. Skarp‐de Haan, M. Rossi and M. L. Hänninen (2015). “Characterization of the Campylobacter jejuni population in the barnacle geese reservoir.” Zoonoses and public health 62(3): 209-221.

    Article  PubMed  Google Scholar 

  • Loncaric, I., A. Kübber-Heiss, A. Posautz, G. L. Stalder, D. Hoffmann, R. Rosengarten and C. Walzer (2013). “Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife.” Journal of Antimicrobial Chemotherapy 68(10): 2222–2225.

    CAS  PubMed  Google Scholar 

  • Magiorakos, A. P., A. Srinivasan, R. Carey, Y. Carmeli, M. Falagas, C. Giske, S. Harbarth, J. Hindler, G. Kahlmeter and B. Olsson‐Liljequist (2012). “Multidrug‐resistant, extensively drug‐resistant and pandrug‐resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.” Clinical Microbiology and Infection 18(3): 268–281.

    Article  CAS  PubMed  Google Scholar 

  • Mediavilla, J. R., L. Chen, A. C. Uhlemann, B. M. Hanson, M. Rosenthal, K. Stanak, B. Koll, B. C. Fries, D. Armellino, M. E. Schilling, D. Weiss, T. C. Smith, F. D. Lowy and B. N. Kreiswirth (2012). “Methicillin-Susceptible Staphylococcus aureus ST398, New York and New Jersey, USA.” Emerging Infectious Diseases 18(4): 700–702.

    Article  PubMed  PubMed Central  Google Scholar 

  • Middleton, J. and A. Ambrose (2005). “Enumeration and antibiotic resistance patterns of fecal indicator organisms isolated from migratory Canada geese (Branta canadensis).” Journal of wildlife diseases 41(2): 334–341.

    Article  CAS  PubMed  Google Scholar 

  • Morgan, M. (2008). “Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis?” Journal of Antimicrobial Chemotherapy 62(6): 1181–1187.

    Article  CAS  PubMed  Google Scholar 

  • Moriarty, E. M., L. Weaver, L. W. Sinton and B. Gilpin (2012). “Survival of Escherichia coli, enterococci and Campylobacter jejuni in Canada goose faeces on pasture.” Zoonoses Public Health 59(7): 490–497.

    Article  CAS  PubMed  Google Scholar 

  • Nemati, M., K. Hermans, U. Lipinska, O. Denis, A. Deplano, M. Struelens, L. A. Devriese, F. Pasmans and F. Haesebrouck (2008). “Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398.” Antimicrobial agents and chemotherapy 52(10): 3817–3819.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pergams, O. R. and P. A. Zaradic (2008). “Evidence for a fundamental and pervasive shift away from nature-based recreation.” Proceedings of the National Academy of Sciences 105(7): 2295-2300.

    Article  Google Scholar 

  • Porrero, M. C., A. Valverde, P. Fernandez-Llario, A. Diez-Guerrier, A. Mateos, S. Lavin, R. Canton, J. F. Fernandez-Garayzabal and L. Dominguez (2014). “Staphylococcus aureus carrying mecC gene in animals and urban wastewater, Spain.” Emerg Infect Dis 20(5): 899-901.

    Article  PubMed  PubMed Central  Google Scholar 

  • Price, L. B., M. Stegger, H. Hasman, M. Aziz, J. Larsen, P. S. Andersen, T. Pearson, A. E. Waters, J. T. Foster and J. Schupp (2012). “Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock.” MBio 3(1): e00305-00311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rankin, S., S. Roberts, K. O’Shea, D. Maloney, M. Lorenzo and C. E. Benson (2005). “Panton valentine leukocidin (PVL) toxin positive MRSA strains isolated from companion animals.” Veterinary microbiology 108(1): 145–148.

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg Goldstein, R. E., S. A. Micallef, S. G. Gibbs, J. A. Davis, X. He, A. George, L. M. Kleinfelter, N. A. Schreiber, S. Mukherjee, A. Sapkota, S. W. Joseph and A. R. Sapkota (2012). “Methicillin-resistant Staphylococcus aureus (MRSA) detected at four U.S. wastewater treatment plants.” Environ Health Perspect 120(11): 1551–1558.

    Article  PubMed  Google Scholar 

  • Shopsin, B., M. Gomez, S. O. Montgomery, D. H. Smith, M. Waddington, D. E. Dodge, D. A. Bost, M. Riehman, S. Naidich and B. N. Kreiswirth (1999). “Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains.” J Clin Microbiol 37(11): 3556–3563.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soge, O. O., J. S. Meschke, D. B. No and M. C. Roberts (2009). “Characterization of methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative Staphylococcus spp. isolated from US West Coast public marine beaches.” J Antimicrob Chemother 64(6): 1148–1155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stegger, M., C. M. Liu, J. Larsen, K. Soldanova, M. Aziz, T. Contente-Cuomo, A. Petersen, S. Vandendriessche, J. N. Jimenez and C. Mammina (2013). “Rapid differentiation between livestock-associated and livestock-independent Staphylococcus aureus CC398 clades.” PloS one 8(11): e79645.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson, J. M., A. Gundogdu, H. M. Stratton and M. Katouli (2013). “Antibiotic resistant Staphylococcus aureus in hospital wastewaters and sewage treatment plants with special reference to methicillin-resistant Staphylococcus aureus (MRSA).” J Appl Microbiol 114(1): 44–54.

    Article  CAS  PubMed  Google Scholar 

  • Tizard, I (2004). “Salmonellosis in wild birds.” Semin Avian Exot Pet 13(2): 50–66.

    Article  Google Scholar 

  • Wan, M. T. and C. C. Chou (2014). “Spreading of beta-lactam resistance gene (mecA) and methicillin-resistant Staphylococcus aureus through municipal and swine slaughterhouse wastewaters.” Water Res 64: 288-295.

    Article  CAS  PubMed  Google Scholar 

  • Wardyn, S. E., L. K. Kauffman and T. C. Smith (2012). “Methicillin-resistant Staphylococcus aureus in central Iowa wildlife.” Journal of wildlife diseases 48(4): 1069–1073.

    Article  PubMed  Google Scholar 

  • Yamahara, K. M., L. M. Sassoubre, K. D. Goodwin and A. B. Boehm (2012). “Occurrence and persistence of bacterial pathogens and indicator organisms in beach sand along the California coast.” Appl Environ Microbiol 78(6): 1733–1745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, L., H. Kassa, M. L. Tischler and L. Xiao (2004). “Host-adapted Cryptosporidium spp. in Canada Geese (Branta Canadensis).” Appl Environ Microbiol 70(7): 4211–4215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by Kent State University start-up funds to Tara C Smith, Ph.D.

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Authors and Affiliations

  1. Department of Biostatistics, Environmental Health Sciences and Epidemiology, College of Public Health, Kent State University, 750 Hilltop Drive, Kent, OH, 44242, USA

    Dipendra Thapaliya, Mark Dalman, Jhalka Kadariya, Katie Little, Victoria Mansell, Mohammed Y. Taha, Dylan Grenier & Tara C. Smith

  2. Ministry of Science and Technology, Baghdad, Iraq

    Mohammed Y. Taha

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  1. Dipendra Thapaliya
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  2. Mark Dalman
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Correspondence to Tara C. Smith.

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Thapaliya, D., Dalman, M., Kadariya, J. et al. Characterization of Staphylococcus aureus in Goose Feces from State Parks in Northeast Ohio. EcoHealth 14, 303–309 (2017). https://doi.org/10.1007/s10393-017-1227-z

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  • DOI: https://doi.org/10.1007/s10393-017-1227-z

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