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Diversity and Antimicrobial Resistance of Enterococcus from the Upper Oconee Watershed, Georgia S

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Diversity and Antimicrobial Resistance of Enterococcus from the Upper Oconee Watershed, Georgia S Journal of Applied Microbiology ISSN 1364-5072 ORIGINAL ARTICLE Diversity and antimicrobial resistance of Enterococcus from the Upper Oconee Watershed, Georgia S. Cho1, L.M. Hiott2, J.M. McDonald3, J.B. Barrett2, E.A. McMillan1, S.L. House2, E.S. Adams2, J.G. Frye2 and C.R. Jackson2 1 Department of Microbiology, University of Georgia, Athens, GA, USA 2 Bacterial Epidemiology and Antimicrobial Resistance Research Unit, USDA-ARS Russell Research Center, Athens, GA, USA 3 Lewis F. Rogers Institute for Environmental and Spatial Analysis, University of North Georgia, Oakwood, GA, USA Keywords Abstract antimicrobial resistance, diversity, Enterococcus, prevalence, water. Aim: It is well-known that enterococci are abundant in the environment; however, the role of surface water as a reservoir of antimicrobial-resistant Correspondence enterococci remains largely undefined. In this study, surface water samples Charlene R. Jackson, Richard B. Russell were collected over a 2-year period from the Upper Oconee watershed, Athens, Research Center, 950 College Station Road, GA to examine enterococci and their antimicrobial resistance. Athens, GA 30605, USA. Methods and Results: Approximately 97% (445/458) of the samples were E-mail: [email protected] positive for enterococci and a total of 637 enterococci were isolated. The J.G.F. and C.R.J. are joint senior authors on predominant species were Enterococcus casseliflavus (33Á6%) followed by this work. Enterococcus faecalis (26Á5%) and Enterococcus hirae (13Á2%). Regardless of species, the highest levels of resistance were to lincomycin (88Á5%) and 2019/2072: received 26 March 2019, revised tetracycline (13%); isolates also exhibited resistance to newer antimicrobials, 15 November 2019 and accepted 3 Decem- daptomycin (8Á9%) and tigecycline (6Á4%). Multidrug resistance (resistance ≥3 ber 2019 antimicrobial classes) was observed to as many as five classes of antimicrobials. Resistant enterococci appeared to be randomly dispersed over the seasons doi:10.1111/jam.14550 rather than clustered by species or antimicrobial resistance. Conclusions: This study demonstrated that surface waters contain a large population of diverse species of antimicrobial-resistant enterococci, including resistance to new antimicrobials. Significance and Impact of the Study: These results may indicate the potential of human intestinal illness and/or colonization of the human gut with resistant enterococci as enterococci correlate with increased disease risk to humans during recreational exposure to water. illness is less severe causing symptoms such as vomiting Introduction and headaches as a result of production of biogenic ami- Enterococci are a diverse group of bacteria with impor- nes from ingestion of enterococci in fermented foods tance in several areas including clinical medicine, food- (Tham et al. 1990; Gardin et al. 2001; Giraffa 2002). On borne illness, food processing and microbial risk the other hand, enterococci have beneficial qualities that assessment. In clinical medicine, they are a leading cause have made them useful as probiotics and as indicators of of nosocomial infections and have been implicated in faecal contamination in water bodies (Foulquie Moreno bacteraemia, endocarditis and urinary tract infections et al. 2006; Byappanahalli et al. 2012). As natural inhabi- (Murray 1990; Huycke et al. 1991; Jett et al. 1994). Treat- tants of the gastrointestinal tract of humans and animals, ment of enterococcal infections in clinical medicine is enterococci have been used as indicators of faecal pollu- often complicated due to intrinsic and acquired resistance tion along with Escherichia coli (Roslev and Bukh 2011). in the bacteria (Murray 1990; Facklam et al. 2002; Malani Of the two bacteria, enterococci are thought to be better et al. 2002; Huijbers et al. 2015)). Enterococcal foodborne indicators of the possible presence of bacterial pathogens Journal of Applied Microbiology 128, 1221--1233 © 2019 The Society for Applied Microbiology 1221 Diversity of enterococci in water S. Cho et al. in surface water as their occurrence, particularly at high Materials and methods levels, is associated with the risk of contracting human gastroenteritis during swimming-related activities (Tur- Sampling of river water bow et al. 2003). As enterococci are generally not considered important The rivers and streams sampled in this study were located pathogens outside the hospitals and healthcare settings, in the Upper Oconee watershed, Georgia, USA (USGS studies reporting enterococci from the environment are Cataloging unit 03070101). The sampling sites were scarce. Most studies on water sources are focused either located in the Middle Oconee River, North Oconee River on water quality, human-specific species, Enterococcus fae- and the tributaries that drain into these rivers (Fig. 1). calis and E. faecium, or on polluted water environments Sample sites were selected to represent a range of land such as hospital-impacted wastewater and agricultural uses, such as forested, agricultural, residential, recre- run-off (Sadowy and Luczkiewicz 2014; Kapoor et al. ational and industrial. One litre water samples from each 2015; Nishiyama et al. 2015). Less attention has been site were collected seasonally four times a year with the given to enterococci in natural water environments and assistance of the UOWN. Since 2008, UOWN has assem- on different species of Enterococcus. Resistant enterococci bled a team of volunteers to collect water samples from present in water sources can potentially transfer resistance the Upper Oconee watershed on a quarterly basis. The genes to bacterial pathogens in the environment or to number of locations sampled varied from 80 to 100 dur- bacteria in the human gastrointestinal tract after ingestion ing the Spring collection, which is the UOWN’s largest of contaminated water during recreational activities collection event, River Rendezvous. The annual River (Murray 1990; Facklam et al. 2002; Malani et al. 2002; Rendezvous event enlists over 100 volunteers to sample Huijbers et al. 2015). Since resistance in enterococci may approximately 100 locations in the watershed to evaluate vary according to species, species identification is an the health of the watershed through chemical and biolog- important factor to consider when characterizing antimi- ical sample analysis. During the remaining quarterly col- crobial resistance. lections, 30 to 60 water samples were collected depending Bacterial diversity and prevalence in surface water are on available volunteers and access to the sampling sites. subject to change due to both point and nonpoint (e.g. A total of 29 locations were routinely sampled to serve as agricultural run-off, storm water routes) sources as well controls with nine sites sampled all eight times, eight sites as seasonal influences such as water temperature and sampled seven times and 12 sites sampled six times. rainfall (Singer et al. 2006; Lanthier et al. 2011). In order to better understand human health risks associ- Isolation and identification of bacteria ated with the presence of enterococci in surface water impacted by nonpoint source contamination, studies are Filtration and enrichment of water samples were per- needed to identify the differences in enterococcal species formed as previously described (Cho et al. 2018). Briefly, composition, antimicrobial resistance of those species 0Á5 g of cellulose filter powder (Aqua DewTM, Lahore, and changes in the composition over time. In this Pakistan) was added to water samples (1 L), which was study, the occurrence, species distribution and antimi- then filtered onto 47-mm glass fibre filters (Pall Corpora- crobial susceptibility of enterococci from surface water tion, Ann Arbor, MI). The glass fibre filter and cellulose from the Upper Oconee watershed in northeastern filter powder were incubated in 25 ml of buffered pep- Georgia were evaluated. The Oconee River is formed by tone (BP; BD DifcoTM, Franklin Lakes, NJ) water for 24 h the convergence of the North Oconee River and the at 37°C. For Enterococcus isolation, 0Á1 ml of BP enrich- Middle Oconee River just south of Athens, Georgia, and ment was streaked on selective agar plates and incubated is used for municipal, industrial, agricultural and recre- for 24 h at 37°C. In order to test for the efficacy of the ational purposes (Environmental Protection Division media, multiple media were used until Enterococcosel 1998). Samples were collected quarterly, once each sea- (BD Difco) was chosen as the media of use from 2015 son, at different locations in the Upper Oconee water- Fall onward. For 2015 Winter, Enterococcosel and mE shed, for 2 years by the Upper Oconee Watershed agar (BD Difco) were used; for 2015 Spring, mE agar was Network (UOWN) (http://www.uown.org). Enterococci used; for 2015 Summer, Enterococcosel, mE agar and were isolated from the samples, identified to species and CHROMagar Enterococcus (not on market, CHROMagar tested for resistance to antimicrobials used in clinical Microbiology, Paris, France) were used. One colony hav- medicine and agriculture. The results of this study will ing the typical appearance of Enterococcus from each pos- improve the understanding of the dynamics of entero- itive plate was confirmed and its species was determined cocci in a surface water system which may impact using multiplex PCR as previously described (Jackson human health. et al. 2004). An exception was the Summer of 2015 when 1222 Journal of Applied Microbiology 128, 1221--1233 © 2019 The
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