Elsevier

Science of The Total Environment

Volume 630, 15 July 2018, Pages 967-976
Science of The Total Environment

Human Bacteroides and total coliforms as indicators of recent combined sewer overflows and rain events in urban creeks

https://doi.org/10.1016/j.scitotenv.2018.02.108Get rights and content

Highlights

  • Measured relationships between fecal indicators, pathogens, CSOs, and rainfall

  • Human Bacteroides and total coliforms correlated with CSOs and rainfall

  • No indicators measured correlated with human pathogens

  • Temporal relationships highlight the importance of survivability of organisms

Abstract

Combined sewer overflows (CSOs) are a known source of human fecal pollution and human pathogens in urban water bodies, which may present a significant public health threat. To monitor human fecal contamination in water, bacterial fecal indicator organisms (FIOs) are traditionally used. However, because FIOs are not specific to human sources and do not correlate with human pathogens, alternative fecal indicators detected using qPCR are becoming of interest to policymakers. For this reason, this study measured correlations between the number and duration of CSOs and mm of rainfall, concentrations of traditional FIOs and alternative indicators, and the presence of human pathogens in two urban creeks. Samples were collected May–July 2016 and analyzed for concentrations of FIOs (total coliforms and E. coli) using membrane filtration as well as for three alternative fecal indicators (human Bacteroides HF183 marker, human polyomavirus (HPoV), pepper mild mottle virus (PMMoV)) and nine human pathogens using qPCR. Four of the nine pathogens analyzed were detected at these sites including adenovirus, Enterohemorrhagic E. coli, norovirus, and Salmonella. Among all indicators studied, human Bacteroides and total coliforms were significantly correlated with recent CSO and rainfall events, while E. coli, PMMoV, and HPoV did not show consistent significant correlations. Further, human Bacteroides were a more specific indicator, while total coliforms were a more sensitive indicator of CSO and rainfall events. Results may have implications for the use and interpretation of these indicators in future policy or monitoring programs.

Introduction

Combined sewer systems are a primary source of contamination of urban water bodies in the United States (Bryan Ellis and Yu, 1995). During rain events, these systems can overflow and release a mix of stormwater and wastewater into receiving waterways. As a result, these combined sewer overflows (CSOs) may introduce infectious pathogens that are found in human sewage into waterways used for drinking or recreation (Bryan Ellis and Yu, 1995; Ferguson et al., 1996; Rodríguez et al., 2012). Pathogens that have been identified in combined sewer outfalls or CSO-impacted waters include pathogenic bacteria such as Campylobacter, E. coli, and Salmonella, enteric viruses including adenovirus and norovirus (the most common cause of waterborne outbreaks), as well as protozoan parasites such as Giardia and Cryptosporidium (Eregno et al., 2016; ten Veldhuis et al., 2010; U.S. EPA, 2004). Recreation in CSO-impacted waters has been associated with an increased risk of gastrointestinal illness, which can adversely impact the health of certain groups including children (Cabelli et al., 1979; Wade et al., 2008) or low-income populations (Cabelli et al., 1979). In addition, pathogens found in CSO-impacted waters have been associated with waterborne disease outbreaks in the United States (Sinclair et al., 2009). For these reasons, CSOs are a potential threat to public and environmental health and may facilitate the spread of waterborne pathogens (Aslan et al., 2011).

Due to the expense and difficulty in isolating human pathogens from environmental samples, fecal indicator organisms (FIOs) are typically used to measure water quality and to create federal and state regulations for recreational water in the United States (United States Environmental Protection Agency (US EPA), 2004). Although epidemiologic studies have linked swimming-associated illness with high levels of FIOs (Wade et al., 2006, Wade et al., 2010), FIOs are not specific to human sources and therefore may not be indicative of contamination from human sewage (Boehm et al., 2009). FIOs may also originate from animal sources, including cats, dogs, and raccoons (Ram et al., 2007) or persist and grow in the environment (Solo-Gabriele et al., 2000), including in sediments and aquatic vegetation (Byappanahalli et al., 2003; Irvine and Pettibone, 1993). Further, it is well known that these indicators do not typically correlate with or are specific enough to predict the presence of pathogens (Bradshaw et al., 2016; Ferguson et al., 1996; Savichtcheva and Okabe, 2006; Wilkes et al., 2009).

Identifying contamination from human sources is important for protecting public health and setting environmental regulations (Field and Samadpour, 2007; Soller et al., 2010). For this reason, markers of human sewage detected using molecular methods have been of interest to both researchers and policy makers as potential alternative indicators of fecal pollution. Examples of these human sewage markers include the HF183 marker for human Bacteroides (Converse et al., 2009; Savichtcheva et al., 2007), human polyomavirus (HPoV) (Rachmadi et al., 2016), and pepper mild mottle virus (PMMoV) (Kuroda et al., 2015), all of which are found in high concentrations in human sewage and may be detected using qPCR. Despite the growing interest in the use of human sewage markers for measuring fecal contamination, there is a lack of research that examines the relationships between concentrations of these alternative indicators and the occurrence of CSOs and rainfall (Sauer et al., 2011; ten Veldhuis et al., 2010).

The purpose of this study was to better understand how concentrations of FIOs, human sewage markers, and human pathogens in urban creeks are related to recent CSOs and rainfall events. This study adds to existing literature by addressing a need to investigate relationships between alternative indicators including human Bacteroides, HPoV, PMMoV, and human pathogens including pathogenic bacteria and viruses in surface water (Field and Samadpour, 2007; Harwood et al., 2014; Wu et al., 2011). To our knowledge this is the only data set in the literature that has measured non-traditional fecal indicators (human Bacteroides, HPoV, PMMoV), total coliforms, E. coli and human pathogens simultaneously in an urban watershed while examining relationships with CSOs and rainfall. Further, this study addresses a need for improved understanding of how different types of traditional and alternative indicators of fecal pollution relate to CSOs and rainfall.

Section snippets

Study sites

Samples were collected from two sites along Cobbs and Tacony Creek in Philadelphia (Fig. 1). The creeks flow year-round and are located in city parks within residential sections of Philadelphia. Although the city parks provide some surrounding green space and tree coverage, Philadelphia as a whole has a large percentage of impervious surface coverage (about 54%). In addition, both sites are downstream of between 9 and 16 combined sewer outfalls which are monitored by the Philadelphia Water

Water quality parameters and traditional fecal indicators

Table 1 includes summary statistics for all relevant water quality parameters outlined by the EPA in the Clean Water Act for regulation of Class II water, which includes water used for primary contact recreation (Clean Water Act, 1983, sec. Part 131—Water Quality Standards sec. Part 131—Water Quality Standards). Although these are not health-based targets and have not been adapted for regulation of these sites by the Pennsylvania Department of Environmental Protection (PA DEP, 2016), these

Conclusions

This study sought to measure the relationships between FIOs, human sewage markers, human pathogens, CSOs, and rainfall in two urban creeks. In general, indicators and sewage markers were correlated with CSO events but not with pathogens. Specifically, total coliforms and human Bacteroides (HF183 marker) were positively correlated with CSO events while E. coli and PMMoV showed occasional correlations and HPoV showed none. Correlations for human Bacteroides existed for CSO events that occurred up

Competing interests statement

The authors declare that there is no conflict of interest regarding the publication of this article.

Acknowledgements

The authors would like to acknowledge the Philadelphia Water Department (PWD) for providing the CSO overflow data presented in the manuscript. Data in this paper were generated with research start-up funds provided by Temple University to the corresponding author. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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