Guidelines for Canadian Recreational Water Quality: Indicators of Fecal Contamination
Purpose of consultation
This guideline technical document evaluated the available information on fecal indicator organisms in recreational waters with the intent of updating/recommending guideline values. The purpose of this consultation is to solicit comments on the proposed guidelines, on the approach used for their development, and on the potential impacts of implementing them.
The document was reviewed by external experts and subsequently revised. We now seek comments from the public. This document is available for a 60-day public consultation period.
Please send comments (with rationale, where required) to Health Canada via email at water-eau@hc-sc.gc.ca.
All comments must be received before January 25, 2022.
Comments received as part of this consultation will be shared with the recreational water quality working group members, along with the name and affiliation of their author. Authors who do not want their name and affiliation shared with recreational water quality working group members should provide a statement to this effect along with their comments.
It should be noted that this guideline technical document will be revised following the evaluation of comments received, and the recreational water quality guidelines will be updated, if required. This document should be considered as a draft for comment only.
Table of Contents
- Foreword
- Using indicators of fecal contamination for recreational water quality management
- 1.0 Guidelines for primary contact recreation
- 2.0 Application of the guideline
- 3.0 E. coli as an indicator of fecal presence
- 4.0 Enterococci as an indicator of fecal pollution
- 5.0 Alternative indicators of fecal pollution
- 6.0 Epidemiological studies for primary contact activities
- 7.0 Water intended for secondary contact recreational activities
- 8.0 References
- Appendix A Abbreviations
Indicators of Fecal Contamination
Foreword
The Guidelines for Canadian Recreational Water Quality are comprised of multiple guideline technical documents that consider the various factors that could interfere with the safety of recreational waters from a human health perspective. They provide guideline values for specific parameters used to monitor water quality hazards and recommend science-based monitoring and risk management strategies. Recreational waters are considered to be any natural fresh, marine or estuarine bodies of water that are used for recreational purposes; this includes lakes, rivers, and human-made constructions (e.g., quarries, artificial lakes) that are filled with untreated natural waters. Jurisdictions may choose to apply these guidelines to other natural waters to which limited treatment is applied (e.g., short-term use of disinfection for an athletic event). However, in such situations, caution should be exercised in applying the guidelines as indicator organisms are easier to disinfect then other disease-causing microorganisms (e.g., protozoan pathogens). Recreational activities that could present a human health risk through intentional or incidental immersion and ingestion include primary contact activities (e.g., swimming, bathing, wading, windsurfing and waterskiing) and secondary contact activities (e.g., canoeing and fishing).
Each guideline technical document has been established on the basis of current, published scientific research related to health effects, aesthetic effects, and beach management considerations. Recreational water quality generally falls under provincial and territorial jurisdiction and therefore the policies and approaches will vary between jurisdictions.
The guideline technical documents are intended to guide decisions by provincial and local authorities that are responsible for the management of recreational waters. For a complete list of the guideline technical documents, please refer to the Guidelines for Canadian Recreational Water Quality summary document on the Health Canada website.
Using indicators of fecal contamination for recreational water quality management
This document outlines how indicators of fecal pollution can be used as one component of a preventive risk management approach alongside other activities, such as environmental health and safety surveys (EHSS) and, in some cases, microbial source tracking (MST) investigations. Recreational waters may be impacted by fecal material containing enteric pathogens from numerous sources, including discharged sewage, treated wastewater effluent, stormwater runoff from agricultural or urban areas, industrial processes, wild or domesticated animals, and even fecal shedding by swimmers. The degree of risk from enteric pathogens varies between sources of fecal contamination, with sewage sources generally considered the most significant (in terms of the highest concentrations of infectious enteric viruses, bacteria and parasitic protozoa). Routine testing of recreational waters for pathogens is generally impractical, due to the variability in the types and quantities of pathogens present at any one time and the degree of difficulty associated with many of the detection methods. Consequently, as part of a risk management approach for recreational waters, authorities monitor for fecal indicators that are present in high numbers in both human and animal feces. Elevated numbers of these indicators in the aquatic environment are used to indicate fecal contamination and an elevated risk of illness.
Guideline values have been developed for Escherichia coli (E. coli) and enterococci. The values consider both the potential health risks associated with recreational activities and the benefits of recreational water use in terms of physical activity and enjoyment. These guideline values are considered to represent an acceptable level of risk for recreational activities.
E. coli and enterococci are recommended as primary indicators of possible fecal pollution and of potentially elevated gastrointestinal illness (GI) risk in recreational waters impacted by human fecal pollution. Quantitative microbial risk assessment studies have shown that, similar to waters contaminated with human fecal pollution, waters impacted by ruminants (e.g., cattle feces) may also present a significant risk to human health. Recreational areas that are not impacted by human or ruminant pollution sources generally contain lower levels of human pathogens, compared to those impacted by human and ruminant feces, at similar levels of E. coli and enterococci. Detection of E. coli and enterococci in these water sources at the guideline levels may therefore represent a lower level of risk to human health. Alternative water quality criteria may be developed for these potentially lower risk recreational waters on a site-specific basis. However, care is needed to ensure that the risk of illness associated with any new criteria does not exceed the acceptable level of risk. Recreational area managers are encouraged to determine the sources of fecal contamination impacting a recreational water site. A variety of options are available, such as environmental health and safety surveys, microbial source tracking methods, as well as alternative indicators, to determine the sources of pollution and the remediation priorities to improve the water quality for recreators.
More details on risk management of recreational water quality are available in the Guidelines for Canadian Recreational Water Quality - Understanding and Managing Risks in Recreational Waters technical document (Health Canada, in publication).
1.0 Guidelines for primary contact recreation
Guidelines for the fecal indicator bacteria Escherichia coli (E. coli) and enterococci have been developed for recreational areas used for primary contact activities (see Table 1 and Table 2). These values consider both the potential health risks and the benefits of recreational water use in terms of physical activity and enjoyment and are considered to represent an acceptable level of risk for recreational activities (see section 6.5).
Fecal indicator bacteria are used to indicate a potential increased risk to human health and are one component of a preventive risk management approach. Both culture-based methods (E. coli and enterococci) and polymerase chain reaction (PCR) based methods (enterococci) can be used for analysis. The choice of method may depend on source water characteristics, the laboratory capacity and the necessity for same-day results. Further information on methods can be found in the guideline technical document on microbiological methods (Health Canada, in preparation-a).
Indicator |
Beach Action Value (BAV)Footnote 4 |
---|---|
E. coli -fresh waterFootnote 3 |
≤ 235 E. coli cfuFootnote 5/100 mL |
Enterococci -marine and fresh water |
≤ 70 enterococci cfuFootnote 5/100 mL |
|
Table 2. Guideline valuesFootnote 1,Footnote 2 using PCR-based methods
Indicator |
Beach Action Value (BAV)Footnote 3 |
---|---|
Enterococci -marine and fresh water |
< 1000 enterococci cce/100 mL |
|
The epidemiological link between E. coli or enterococci concentrations and increased risk of adverse human health outcomes is based on an assessment of sites impacted to varying degrees by human fecal pollution (i.e., human sewage). Recreational areas that are not impacted by human or ruminant fecal pollution, such as those only impacted by wildlife/birds, may contain fewer human pathogens. At these sites, higher levels of indicator bacteria may be present before the risk of gastrointestinal illness (GI) exceeds the acceptable level of risk. Microbial source tracking methods, along with environmental health and safety surveys, can be used to determine the probable source(s) of fecal contamination to help characterize the potential associated human health risks (see Box 1). Recreational waters that have a very low risk of human or ruminant fecal contamination may benefit from the development of alternative criteria on a site-specific basis.
2.0 Application of the guidelines
Monitoring fecal indicators provides valuable information on water quality changes that may be occurring at the beach, and provides a measure for public health decisions. However, water quality monitoring results should not be the sole measure used for determining the acceptability of an area for recreational activities. Routine E. coli or enterococci monitoring should be included as part of a preventive risk management approach to protect the health of recreational water users. Public health decisions should also balance the potential increased health risks with the enjoyment and exercise that is associated with these activities. Further guidance can be found in the guideline technical documents on Understanding and Managing Risks in Recreational Waters and Microbiological Methods (Health Canada, in publication-a,b).
The guideline values recommended in this document are single-sample beach action values (BAV) for both culture-based (E. coli and enterococci) and PCR-based (enterococci) monitoring methods. Jurisdictions may choose to implement culture-based methods, PCR-based methods, or both, depending on their recreational water quality monitoring plan. Quantitative and digital PCR-based methods have the advantage of providing same-day results for decision making purposes, if water quality samples can be collected and received by the laboratory in a timely fashion.
The BAV guidelines are based on the water quality distributions observed in supporting epidemiological studies and calculated by the United States Environmental Protection Agency (US EPA) (see section 6 and US EPA, 2012). They are recommended for making day-to-day beach management decisions. If E. coli or enterococci values exceed the BAV, this should trigger further actions by the responsible authorities. The actions required will depend on site-specific considerations, such as the sources of fecal contamination and the extent of the exceedance. Actions may include issuing a swimming advisory, immediate resampling of the site(s), and conducting a shortened EHSS. Further information on EHSS can be found in Health Canada (in publication-b). A swimming advisory may be particularly warranted if the responsible authority determines that the area is prone to impacts from human sewage (and therefore likely enteric pathogens), that the beach is poorly characterized and therefore the source of the fecal indicator bacteria is unknown, or that there is evidence of illness in the community suspected to be associated with the recreational area.
At beaches where the fecal sources impacting the water quality are unknown, beach managers may use various methods to test for human and ruminant fecal sources (see Box 1). In recreational waters where the indicator bacteria are not from human or ruminant sources, the appropriate regulatory authority can assess whether developing alternative criteria may be beneficial for informing and supporting beach management decisions at these sites.
Decisions regarding the frequency of monitoring, the number of samples to be collected, the areas to be monitored, the choice of indicators, and the monitoring program design will be made by the appropriate regulatory and management authorities. Further guidance can be found in the guideline technical documents on Understanding and Managing Risks in Recreational Waters and Microbiological Methods (Health Canada, in publication-a,b).
Box 1: An approach to determining the source(s) of fecal bacteria in a recreational area
Multiple lines of evidence should be used to identify the source(s) of fecal pollution impacting recreational waters. Much can be learned from environmental health and safety surveys and from expanding E. coli surveillance in the immediate area around a beach or recreational water location. Techniques like smoke or dye cross-connection testing of wastewater infrastructure or microbial source tracking methods may assist in identifying likely fecal input sources or unsuspected sources of fecal inputs.
These techniques have been used to identify sources of fecal inputs at beaches across Canada. For example, multiple lines of evidence were used to identify the cause of frequent beach postings at Bluffers Park Beach in Toronto, Ontario (Edge et al., 2018). Beach observations, expanded E. coli surveillance, and microbial source tracking results consistently indicated the importance of reducing local impacts from bird fecal droppings and runoff from a parking lot and marsh inland of the beach. A bird management program and a berm engineered to reduce parking lot and marsh runoff led to immediate water quality improvements. The beach was subsequently awarded a Blue Flag certification (https://www.blueflag.global/all-bf-sites). Studies in Alberta (Beaudry, 2019) and Ontario (Staley et al., 2018) applied advances in microbial source tracking (quantitative and digital PCR techniques) to identify sewage cross-connections into stormwater systems and bird excreta as the important fecal sources in some recreational waters.
It is important to recognize however, that the predominant source of fecal matter may not be the most important source of human-infectious pathogens. Hence, if birds are the predominant source of fecal pollution, it is still critical to ensure that there is no human or ruminant fecal contamination. This is key because of the higher likelihood that these latter two sources may contribute the majority of human-infectious pathogens even when they contribute as little as 15% to 20% of the fecal load (Schoen et al., 2011; Soller et al., 2015).
3.0 E. coli as an indicator of fecal presence
Indicators can be used for various purposes as part of a recreational water quality management plan. Fecal indicators signal the likely presence of fecal pollution. Common fecal indicators include E. coli and enterococci, as well as source-specific fecal indicators, such as the HF183 Bacteroides genetic marker for detecting human sewage (Harwood et al., 2014). E. coli or enterococci are used as the primary indicators of fecal pollution in fresh waters, with enterococci the preferred indicator for marine waters. Source-specific fecal indicators are used when microbial source tracking is recommended.
3.1 Description
E. coli is a member of the coliform group of bacteria and part of the family Enterobacteriaceae. It is a facultative anaerobic, Gram-negative, non-spore-forming, rod-shaped bacterium that can ferment lactose. Coliform bacteria are also often defined by their ability to express the enzymes β-galactosidase and β-glucuronidase. E. coli is found in high numbers in the intestinal tract and feces of humans and warm-blooded animals. It can also be found in numerous cold-blooded animal species (Tenaillon et al., 2010; Gordon, 2013; Frick et al., 2018). Some strains of E.coli can adapt to live independently of fecal material and become naturalized members of the microbial community in environmental habitats. Naturalized strains can grow and maintain their population if favourable conditions exist. (Ashbolt et al., 1997; Ishii and Sadowsky, 2008; Jang et al., 2017).
E. coli is present in human feces at a concentration of approximately 107to 109 cells per gram and comprises about 1% of the total biomass in the large intestine (Edberg et al., 2000; Leclerc et al., 2001). In two separate studies, it was detected in 94% and 100% of the human subjects tested (Finegold et al., 1983; Leclerc et al., 2001). These values are significantly higher than those reported for other members of the coliform group and were matched or exceeded only by enterococci and certain species of anaerobic bacteria (Bacteroides, Eubacterium). E. coli comprises about 97% of the coliform organisms in human feces, with Klebsiella spp. comprising 1.5% and Enterobacter and Citrobacter spp. together comprising another 1.7%. In raw sewage, E. coli generally declines relative to other coliforms, representing less than 30% of coliforms at sewage plant influents (Ashbolt et al., 2001). Nonetheless, there are stress-resistant E. coli that appear to persist, if not grow, within sewage treatment works and are released in treated effluent (Zhi et al., 2016). Sewage effluents may also contribute antibiotic resistant bacteria in surface waters downstream of wastewater treatment plants (Day et al., 2019; Logan et al., 2020). In animal feces, E. coli numbers can vary considerably, but typically fall within the range from 103-109 cells per gram (Ashbolt et al., 2001; Tenaillon et al., 2010; Yost et al., 2011; Ervin et al., 2013). In domestic animals, E. coli has been shown to represent between 90% and 100% of all coliforms in feces (Dufour, 1977).
Although the vast majority of E. coli types are harmless, some strains of this bacterium can cause GI, as well as more serious health complications (e.g., hemorrhagic colitis, hemolytic uremic syndrome, kidney failure) and urinary tract infections. Nonetheless, even during outbreaks, fecal concentrations of the typical non-pathogenic E. coli will be greater in water sources than those of the pathogenic strains (Degnan, 2006; Soller et al., 2010a).
E. coli can be rapidly and easily enumerated in recreational waters and epidemiological studies have demonstrated a link between E. coli in fresh waters and the risk of GI among swimmers (Dufour, 1984; Wade et al., 2003; Wiedenmann et al., 2006; Marion et al., 2010). In Canada, most recreational water quality guidelines for natural fresh waters use E. coli as an indicator for making public health decisions. Enterococci are also beginning to be used more frequently.
3.2 Occurrence in the aquatic environment
Once shed from a human/animal host, survival of E. coli in the recreational water environment is dependent on many factors, including temperature, exposure to sunlight, available nutrients, water conditions such as pH and salinity, and competition from and predation by other microorganisms (Korajkic et al., 2015). Numerous authors have reported on the ability of beach sand, sediments, and aquatic vegetation to prolong the survival, replication, and accumulation of fecal microorganisms (Whitman and Nevers, 2003; Whitman et al., 2003; Ishii et al., 2006; Olapade et al., 2006; Kon et al., 2007a; Hartz et al., 2008; Byappanahalli et al., 2009; Heuvel et al., 2010; Verhougstraete et al., 2010; Whitman et al., 2014; Devane et al., 2020). These environments are thought to provide more favourable conditions of temperature and nutrients than the adjacent waters and to offer protection from certain environmental stressors such as sunlight. As mentioned earlier, some strains of E. coli can become naturalized and grow in environmental habitats (Power et al., 2005; Byappanahalli et al., 2006; Ishii et al., 2006; Kon et al., 2007b; Byappanahalli et al., 2012b). While these findings change the perception that E. coli is exclusively associated with recent fecal wastes, it is accepted that E. coli is predominantly of fecal origin and remains a valuable indicator for determining recreational water quality.
3.3 Association with pathogens
The occurrence of fecal pathogens in recreational waters, including enteric bacteria, enteric viruses and parasitic protozoa, is strongly dependent on the fecal sources that impact the swimming area. The presence and numbers of fecal pathogens in the environment can be sporadic and highly variable. Therefore, monitoring for fecal indicators is used in place of directly monitoring for pathogens. The presence of E. coli in water indicates the potential for the presence of fecal pathogens that could result in an increased health risk to swimmers.
The association between E. coli and individual enteric pathogens is highly variable. Several early studies found similar survival rates for E. coli and enteric bacterial pathogens (Rhodes and Kator, 1988; Korhonen and Martikainen, 1991; Chandran and Mohamed Hatha, 2005). In addition, one study reported that the probability of detecting Salmonella or Shiga-toxin producing E. coli (STEC) steadily increased as the concentration of E. coli increased, although no single sample could provide absolute assurance of the presence or absence of these pathogens (Yanko et al., 2004). Other studies have reported increased odds of detecting enteric pathogens (Campylobacter, Cryptosporidium, Salmonella and E. coli O157:H7) when densities of E. coli exceed 100 cfu/100 mL (Van Dyke et al., 2012; Banihashemi et al., 2015; Stea et al., 2015). In agricultural watersheds across Canada, Edge et al. (2012) generally found that higher numbers of waterborne pathogens were associated with higher levels of E. coli. However, they cautioned against using low levels of E. coli to infer no waterborne pathogen occurrence. Numerous studies have also reported on the lack of a correlation between E. coli concentrations and the presence of enteric viruses and protozoa in surface waters, reflecting different fecal sources and long persistence of these pathogens over fecal indicator bacteria (Griffin et al., 1999; Denis-Mize et al., 2004; Hörman et al., 2004; Dorner et al., 2007; Edge et. al., 2013; Prystajecky et al., 2014). Overall, although E. coli does not reliably predict the presence of specific fecal pathogens (Wu et al., 2011; Edge et al., 2013; Lalancette et al., 2014; Banihashemi et al., 2015; Krkosek et al., 2016), it can be used to indicate an increased potential for pathogens to be present.
4.0 Enterococci as an indicator of fecal pollution
Like E. coli, enterococci are used as a primary indicator of fecal pollution. Elevated numbers detected in either fresh or marine waters indicate the potential presence of fecal material and thus the possible presence of fecally sourced pathogenic bacteria, viruses and protozoa.
4.1 Description
Enterococci are members of the genus Enterococcus. The genus was created to include the more fecal-specific species of the genus Streptococcus, formerly considered as group D streptococci. In practice, the terms enterococci, fecal streptococci, Enterococcus and intestinal enterococci have been used interchangeably (Bartram and Rees, 2000). Enterococci are gram-positive, round-shaped bacteria that meet the following criteria: growth between temperatures of 10 °C and 45 °C, resistance to heat exposure at 60 °C for 30 minutes, growth in the presence of 6.5% sodium chloride and at pH 9.6, and the ability to reduce 0.1% methylene blue (Bartram and Rees, 2000; APHA et al., 2017). They are also often defined by their ability to express the enzyme β-glucosidase.
The genus Enterococcus is thought to comprise more than 30 species classified into 5 to 6 major groups (E. faecalis, E. faecium, E. avium, E. gallinarum, E. italicus, and E. cecorum) (Svec and Devriese, 2009; Byappanahalli et al., 2012a). E. faecalis and E. faecium occur in significant quantities in both human and animal feces and are the species most frequently encountered in polluted aquatic environments (Bartram and Rees, 2000). Other species commonly isolated from fecal material, but in lower numbers include E. durans, E. hirae, E. gallinarum, and E. avium (Pourcher et al., 1991; Moore et al., 2008; Staley et al., 2014). Enterococci are present in high concentrations in human and animal feces, with concentrations reported on the order of 106/g to 107/g (Sinton, 1993; Edberg et al., 2000). Human fecal microbiota studies reported by Leclerc et al. (2001) demonstrated that Enterococcus species were present in 100% of the subjects tested.
Enterococci have been used to indicate fecal contamination in fresh and marine waters and have been associated with the risk of GI among swimmers (Cabelli, 1983; Kay et al., 1994; Pruss, 1998; WHO, 1999; Wade et al., 2003, 2006, 2008; Napier et al., 2017).
4.2 Occurrence in the aquatic environment
Enterococci have been detected in water samples from diverse environmental habitats (Yamahara et al., 2009; Byappanahalli et al., 2012a; Staley et al., 2014). They are also routinely isolated from marine and fresh recreational waters known to be impacted by human and animal fecal pollution sources. In general, enterococci tend to be present at concentrations approximately onefold to threefold lower than those of E. coli in feces and municipal wastes (Sinton, 1993; Edberg et al., 2000). Compared with other indicator organisms (e.g., E. coli, thermotolerant coliforms), enterococci may have greater resistance to certain environmental stresses in recreational waters, such as conditions of sunlight and salinity. They have also demonstrated greater resistance to wastewater treatment practices, including chlorination, and prolonged survival in marine and freshwater sediments (Davies et al., 1995; Desmarais et al., 2002; Ferguson et al., 2005). The source of the enterococci may also affect their persistence, with enterococci from cattle out-persisting those from sewage (Korajkic et al., 2013). Enterococci has also been reported to survive and grow in organic-rich environments, such as on mats of the green algae species Cladophora (Byappanahalli et al., 2003; Whitman et al., 2003; Verhougstraete et al., 2010) and in some environmental habitats (e.g., sand, sediments, soils) (Ran et al., 2013; Staley et al., 2014).
As in the case of E. coli, the existence of environmental habitats as potential sources of enterococci is a challenge when interpreting monitoring data (Whitman et al., 2003; Byappanahalli et al., 2012a), but it is accepted that enterococci detected in water samples are predominantly of fecal origin and they remain a valuable indicator for determining recreational water quality.
4.3 Association with pathogens
Direct correlations between indicator concentrations and the concentration of any specific pathogen should not be expected. Within a watershed, indicators and pathogens may come from multiple different sources, and once discharged into water sources, they experience different dilution, transport, and inactivation rates (Wilkes et al., 2009). Although individual studies have occasionally observed a correlation between the presence of enterococci and the detection of a specific pathogen, the relationships are generally weak (Brookes et al., 2005, Wilkes et al., 2009). One study, a survey of surface waters collected from various watersheds in southern California, showed a good predictive ability with PCR detection of STEC and enterococci using culture-based methods (Yanko et al., 2004). It was reported that above an enterococci concentration of 100 most probable number (MPN)/100 mL, the probability of detection of STEC was approximately 60% to 70%. Like E. coli, enterococci are not predictive of the presence of viruses and protozoa (Griffin et al., 1999; Schvoerer et al., 2000, 2001; Jiang et al., 2001, Jiang and Chu, 2004).
The presence or absence of enterococci in an individual sample should not be interpreted to mean that specific enteric pathogenic microorganisms are also present or absent in the same sample. Enterococci are regarded as general indicators of fecal contamination and are routinely monitored, as epidemiological studies have shown that increased concentrations in recreational areas indicate an increased risk of adverse health impacts.
5.0 Alternative indicators of fecal pollution
No single organism is able to fill all of the roles of what might be considered a perfect indicator of recreational water quality—one that models all of the known pathogens, provides information on the degree and source of fecal pollution and communicates the potential risk of illness for recreational water users. This would require multiple indicators, each with unique characteristics that enable them to perform specific roles (Ashbolt et al., 2001). Although E. coli and enterococci are the indicators routinely used for monitoring recreational beaches, there are limitations to the information provided by these organisms (see section 3.0 and 4.0). Other microorganisms have been widely discussed as alternative indicators to fill some of the missing roles. These include Bacteroides spp., spores of Clostridium perfringens, male-specific and somatic coliphages (bacteriophages infecting E. coli) and bacteriophages infecting Bacteroides fragilis. A summary of the characteristics of the recommended and potential indicator organisms is presented in Table 3.
The potential roles of these alternative indicators vary. For example, enteric viruses represent the most significant health risk in many recreational waters impacted by human fecal sources, and although E. coli and enterococci are good indicators of fecal contamination, they alone may not be adequate indicators of human enteric pathogenic viruses. Alternative indicators, such as the coliphages, bacteriophages of Bacteroides spp., or human sewage markers (Nelson et al., 2018; Boehm et al., 2020), can provide additional information on the potential human health risks associated with a beach area. In addition, the fecal sources may not be known at many beaches and therefore less will be understood of the potential health risks. As suggested in section 2.0, the use of microbial source tracking markers from organisms such as the Bacteroides spp. can help provide valuable information on the sources of fecal contamination (Boehm et al., 2018). They may also help determine whether site-specific alternative guideline values would be beneficial. Risk-based threshold values have been proposed for fecal markers (e.g., HF183) that target Bacteroides spp. (Boehm et al., 2018; Boehm and Soller, 2020). Further information on microbial source tracking and understanding and managing risks in recreational areas can be found in Health Canada (in publication-b).
Characteristics |
Indicator organism |
|||||
---|---|---|---|---|---|---|
Recommended |
Potential |
|||||
E. coli |
Enterococci |
C. perfringens |
Bacteroides spp. |
Coliphages |
Bacteriophages of Bacteroides spp. |
|
Brief description |
Gram-negative, non-spore forming bacteria |
Gram-positive, non-spore forming bacteria; comprised of >30 species, E. faecalis and E. faecium more frequent in aquatic environments |
Gram-positive, spore-forming, anaerobic bacteria |
Gram-negative, non-spore-forming, anaerobic bacteria; dominant species - B. fragilis, B. vulgatus, B. distasonis and B. thetaiotaomicron |
Two main types (1) somatic – diverse group that can infect various members of Enterobacteriaceae family, and (2) male-specific (F+) coliphages |
Bacteriophage host strains most often used are for B. fragilis and B. thetaiotaomicron; CrAssphage is a member of this group of bacteriophages |
Includes members that are not human pathogens |
Yes |
Yes |
Yes |
Yes |
Yes |
Yes |
Includes human pathogenic members |
Yes |
Yes |
Yes |
No |
No |
No |
Found within the intestinal tract of humans and warm-blooded animals. |
107–109 cfu/g feces in humans; 103–109 cfu/g feces in animals |
human and animals feces contain 103–107 cfu/g |
In humans: 103–108 cells/g feces; |
1011 cells/g feces (except in some birds) |
In humans: 101–104 PFU/g feces; animals: <10–107 PFU/g feces; raw sewage 106 PFU/g, |
In human feces: 10–102 PFU/g feces, variable isolation; sewage: < 10–105 phages/100 mL; not detected in animals |
Present in waters with recent fecal contamination at higher numbers than enteric pathogens |
Yes |
Yes |
Dependent upon source of contamination |
Insufficient data |
Dependent upon source of contamination. |
Dependent upon source of contamination |
Capable of growth in the aquatic environment. |
Yes, under specific conditions |
Yes, under specific conditions |
No |
No |
Somatic may grow if host bacteria is growing in the environment; F+ not likely to grow; appreciable regrowth is not expected for either |
No |
Capable of surviving longer than pathogens. |
Similar to bacterial pathogens |
Similar to bacterial pathogens |
Yes |
Insufficient data |
Similar to enteric viruses |
Similar to enteric viruses |
Applicable to fresh, estuarine and marine waters |
YesFootnote 1 |
Yes |
Yes |
Yes |
Yes |
Yes |
Exclusively associated with animal and human feces. |
No |
No |
No |
Insufficient data. |
Yes |
Yes |
Association between GIand the indicator |
Yes |
Yes |
Yes, although association weak in some studies |
Weak associations, more studies with human-specific marker (HF183) needed |
Yes |
No |
Host-specific characteristics for microbial source tracking |
No |
No |
No |
Yes |
Maybe (for F+ coliphages) |
Maybe (some cross-reactivity reported) |
Rapid, easy, inexpensive, culture-based method available |
Yes |
Yes |
Yes |
No |
Yes |
No |
Well-established molecular method available |
Yes |
Yes |
No |
Yes |
||
Currently suggested role: |
Primary indicator |
Primary indicator |
Secondary indicator (e.g., sewage inputs) |
Microbial source tracking; secondary indicator |
Secondary indicator (human fecal inputs); microbial source tracking |
Secondary indicator (human fecal inputs) |
References |
Dufour, 1984; Edberg et al., 2000; Solo-Gabriele et al., 2000; Ashbolt et al., 2001; Leclerc et al., 2001; Wade et al., 2003; Marion et al., 2010; Byappanahalli et al., 2012b; Ervin et al., 2013 |
Bartram and Rees, 2000; Edberg et al., 2000; Ashbolt et al., 2001; Wade et al., 2003; Wade et al., 2006; Wade et al., 2008; Verhougstraete et al., 2010; Byappanahalli et al., 2012a; Ervin et al., 2013; Staley, et al., 2014 |
Fujioka and Shizumura, 1985; Ashbolt et al., 2001; Lipp et al., 2001; Hörman et al., 2004; Fernandez-Miyakawa et al., 2005; Wiedenmann et al., 2006; Carman et al., 2008; Mueller-Spitz et al., 2010; Wade et al., 2010; Viau et al., 2011; Vierheilig et al., 2013; Jacob et al., 2015 |
Bernhard and Field, 2000a, 2000b; Wade et al., 2006; Hong et al., 2008; Ballesté and Blanch, 2010; Wade et al., 2010; McQuaig et al., 2012; Cao et al., 2016; Lloyd-Price et al., 2016; Hughes et al., 2017; Napier et al., 2017 |
Cole et al., 2003; Muniesa et al., 2003; Luther and Fujioka, 2004; Nappier et al., 2006; Colford et al., 2007; Wade et al., 2010; Lee and Sobsey, 2011; Wu et al., 2011; Haramoto et al., 2012; Plummer et al., 2014; US EPA, 2015; Griffith et al., 2016; Jofre et al., 2016; Benjamin-Chung et al., 2017; Jebri et al., 2017; Nappier et al., 2019 |
Puig et al., 1999; Mocé-Llivina et al., 2005; Payan et al., 2005; McLaughlin and Rose, 2006; Ebdon et al., 2012; Harwood et al., 2013; McMinn et al., 2014; Sirikanchana et al., 2014; Stachler and Bibby, 2014; Diston and Wicki, 2015; McMinn et al., 2017; Dias et al., 2018; Korajkic et al., 2020 |
|
6.0 Epidemiological studies for primary contact activities
Over the last several decades, numerous epidemiological studies have been conducted in fresh and marine water recreational environments primarily to investigate an association between E. coli/enterococci fecal indicators and GI. Most of these studies have been conducted at beaches with known sources of human fecal contamination. Fewer studies have been conducted on recreational beaches impacted by non-point sources of fecal pollution (see Table 4). Non-point source impacted areas, particularly those with only non-human impacts, may present a lower level of risk to recreational water users at the established guideline levels. Additional studies at non-point source impacted beaches are needed. Studies at sites with both point and non-point sources are important for understanding the variability in the levels of risk to human health and the utility of fecal indicator organisms as part of managing recreational water quality. A smaller number of studies have focused on other health endpoints, such as respiratory or skin ailments. The most recent studies have been broadened to include a range of indicators (e.g., coliphages, fecal source markers such as HF183) and qPCR detection methods. Several reviews of the available epidemiological studies have also been published (Pruss, 1998; US EPA, 2002; Wade et al., 2003; Fewtrell and Kay, 2015).
The previous edition of this guideline document, published in 2012, reviewed the epidemiological studies published prior to 2009. Since that time, additional epidemiological studies and statistical reanalyses of older datasets have been conducted (Table 4), and the definition used to characterize GI has been expanded. The guideline values for primary contact recreation in this document consider all the studies published in Table 4 and balance the potential health risks and the benefits of recreational water use in terms of physical activity and enjoyment.
Source Water |
Main Conclusions |
References |
---|---|---|
Fresh water – impacted by human sewage (and other non-point sources) |
|
Dufour, 1984; Ferley et al., 1989; Van Asperen et al., 1998; Wade et al., 2006; Wiedenmann et al., 2006; Wade et al., 2008 |
|
Dorevitch et al., 2015Footnote * |
|
Fresh water – impacted by non-point sources (e.g., urban runoff, agriculture; forested watershed), minimal risk of human sewage impacts |
|
Marion et al., 2010 |
|
Calderon et al., 1991; |
|
Marine water – impacted by human sewage (and other non-point sources) |
|
Cabelli, 1983; Cheung et al., 1990; Alexander et al., 1992; Corbett et al., 1993; Kay et al., 1994; Prieto et al., 2001; US EPA, 2010; Wade et al., 2010; Colford et al., 2012; Yau et al., 2014; Lamparelli et al., 2015; Griffith et al., 2016; Benjamin-Chung et al., 2017 |
|
von Schirnding et al., 1992; Harrington et al., 1993; Marino et al., 1995; McBride et al., 1998; Colford et al., 2012; Papastergiou et al., 2012 |
|
Marine water – impacted by non-point sources (e.g., urban runoff, agriculture; forested watershed), minimal risk of human sewage impacts |
|
Colford et al., 2007; Fleisher et al., 2010; Sinigalliano et al., 2010; Arnold et al., 2013 |
|
6.1 Definition of gastrointestinal illness and associated risk of illness
In earlier studies, the association between illness and indicator values was based on a definition of GI that included symptoms of highly credible gastrointestinal illness (HCGI). HCGI was defined as either vomiting, diarrhea with a fever, or stomach ache/nausea with a fever (Cabelli, 1983). However, many enteric viruses do not present with fever, and recent studies have shown that enteric viruses are a significant cause of GI among bathers (Sinclair et al., 2009; Soller et al., 2016). For that reason, in more recent studies a broader definition of GI is used that includes illness with or without fever (see section 6.2.1). This broader definition means more cases of GI would be recorded at a recreational area compared to cases of HCGI. Therefore, it has been necessary to determine the number of cases of GI that is equivalent to the human health risk of HCGI. Recent epidemiological studies in the United States showed that the risk of illness at fresh and marine water beaches was similar at comparable levels of enterococci, and this risk of illness was similar to the freshwater illness rates from previous studies (8 HCGI per 1000 exposed) (US EPA, 2012). Using data on the rates of GI and HCGI in non-swimmers from the available epidemiological studies, it was calculated that a factor of 4.5 must be applied to the rate of HCGI to determine the rate of GI upset without a fever that corresponds to the same human health risk (Wymer et al., 2013). Using this factor, the risk of illness in fresh and marine waters at the guideline values in this document are equivalent to 36 GI per 1000 exposed people.
6.2 Human sewage impacted beaches
Epidemiological studies have been conducted worldwide at recreational beaches that are impacted by raw and treated human sewage. Table 4 provides an overview of various studies conducted to date and their main conclusions with respect to the link between fecal indicators and GI.
6.2.1 U.S. studies
In the United States, numerous studies have been conducted to support the development of the US EPA's recreational water quality criteria. In the 1980s, two large studies—one in fresh waters and one in marine waters—found statistically significant rates of GI among swimmers and were able to derive regression equations to relate increasing indicator organism concentrations to increased risk of HCGI (Cabelli, 1983; Dufour, 1984). For symptoms unrelated to GI, no statistically significant differences were observed (Cabelli, 1983; Dufour, 1984). These studies were used to support the US EPA's 1986 recreational water quality criteria and are the basis for the risk of illness in previous editions of the Health Canada guideline. Between 2003 and 2007, there were seven additional epidemiological studies at four freshwater and three marine beaches under the National Epidemiologic and Environmental Assessment of Recreational (NEEAR) Water Study (US EPA, 2010). These studies monitored sites for enterococci using qPCR and culture-based methods. E. coli data are not available for the seven study sites. These studies were used to develop the US EPA's 2012 recreational water quality criteria (see Table 6) (US EPA, 2012) and have been used as the basis for the updated values in this document (see section 6.5). Two main findings from the NEEAR studies were, first, that enterococci qPCR results had a stronger association with GI than the enterococci culture-based methods, and second, unlike the earlier epidemiological studies, no linear regression equation fit the NEEAR culture-based data. A linear regression equation could be fit to the qPCR enterococci data. Since qPCR detects DNA (as opposed to viability), the enterococci signal may persist longer in the water sources and give a better relationship with risk of illness. The lack of linear regression using culture-based methods may be due to the fact that the wastewater discharges impacting the recreational water quality areas were disinfected, as opposed to the earlier studies, where the wastewater was less treated (US EPA, 2012). However, a cut-point analysis showed that the rate of GI between swimmers and non-swimmers was significantly different when the geometric mean concentration of enterococci exceeded 30 or 35 cfu/100 mL, corresponding to a risk level of 32 or 36 GI per 1000 bathers, respectively. As discussed in section 6.1, 36 GI is equivalent to 8 HCGI. For enterococci qPCR, a regression model was possible using the NEEAR studies. Using the regression model, geometric mean concentrations of 300 and 470 cce of enterococci per 100 mL provide the level of health protection comparable to that of the culture-based guideline (US EPA, 2012). As E. coli were not measured during these studies, the equivalent thresholds for E. coli concentrations were determined using the regression analysis from Dufour (1984). Geometric mean concentrations of 100 and 126 cfu of E. coli per 100 mL would correspond to the same risk levels of 32 or 36 GI per 1000 bathers, respectively. This approach was possible because the rates of illness in the NEEAR studies for both fresh and marine water were similar to the illness rates observed in fresh water in the earlier epidemiological studies. Using the NEEAR study data, the US EPA's 2012 criteria also included accompanying statistical threshold values (STVs) (see Table 6). The STVs approximate the 90th percentile of the distribution of the water quality results and should not be exceeded by more than 10% of the samples used to calculate the associated geometric mean. Using the same water quality distribution, BAVs corresponding to the 75th percentile are included for use in beach management decisions (see Table 6) (US EPA, 2012). These BAVs are the basis for the guideline values in this document (see section 6.5).
6.2.2 European studies
In Europe, numerous epidemiological studies have also been conducted to investigate links between illness and indicator organisms. Randomized controlled trials were conducted in marine waters in the United Kingdom in the 1990s (Kay et al., 1994; Fleisher et al., 1996). These studies reported significant dose-response relationships between fecal streptococci and the incidence of both GI and respiratory illness among swimmers. Possible thresholds for an increased risk of gastroenteritis at a concentration of 32 fecal streptococci/100 mL (Kay et al., 1994) and an increased risk of respiratory illness at a concentration of 60 fecal streptococci/100 mL (Fleisher et al., 1996) were reported. At freshwater swimming areas in Germany, Wiedenmann et al. (2006) conducted a randomized controlled prospective cohort study. The authors reported a relationship between the observed rates of illness and measured concentrations of E. coli, enterococci, Clostridium perfringens and somatic coliphages. No-observed-adverse-effect levels (NOAELs) were reported for several definitions of gastroenteritis, ranging from 78 to 180 E. coli/100 mL and from 21 to 24 enterococci/100 mL. The authors proposed guidelines by combining all of the data derived from the different definitions of GI investigated and suggested values of 100 E. coli/100 mL, 25 enterococci/100 mL, 10 somatic coliphages/100 mL and 10 C. perfringens/100 mL. Although the authors propose a value of 100 E. coli/100 mL, it is important to note that the NOAEL reported for GI that most closely fits the criteria of HCGI was 180 E. coli/100 mL and that the definition that most closely fits the broadened GI definition (i.e., fever is not required) was 167 E. coli/100 mL. In addition, the quartile and quintile breakdown of the data for the United Kingdom's definition of GI indicated that the rates of swimmer illness compared to those of the control group were not statistically significant until E. coli concentration ranges approached or exceeded 245 E. coli/100 mL and until enterococci concentration ranges approached or exceeded 68 enterococci/100 mL. In a separate study, concentrations of E. coli needed to exceed a geometric mean of 355 E. coli/100 mL before the risk of gastroenteritis was significantly higher in swimmers compared to non-swimmers (Van Asperen et al., 1998).
Another large randomized control study in Europe, Epibathe, was conducted over two summers (2006 and 2007) and investigated both marine beaches (Spain) and freshwater beaches (Hungary) to determine links between health endpoints (GI, respiratory, skin ailments) and the concentration of either E. coli or enterococci (Epibathe report, 2009). Across all study locations, the risk of GI was higher in bathers than in non-bathers. Also, the risk of becoming ill was higher in marine waters than in fresh waters at similar levels of indicator organisms. This may be due to the shorter lifespan of enterococci in marine waters compared to pathogens (Epibathe report, 2009). All beaches investigated met the "excellent" water quality criteria as defined in the EU bathing directive (see Table 6). Both the marine and freshwater beaches lacked strong evidence of positive dose-response relationships between E. coli or enterococci and GI. However, the illness levels at both beaches were quite low in comparison to previous studies and therefore, although they enrolled a high number of participants, the study had very low statistical power. To give the study more power, the Epibathe results were combined with previous results from the United Kingdom (marine waters) and Germany (fresh waters) (Kay et al., 1994; Fleisher et al., 1996; Wiedenmann et al., 2006) and a meta-analysis and regression analysis were conducted. Although the meta-analysis was unable to find any dose-response relationship, it did show an increased risk of illness in bathers versus non-bathers. The logistic regression, on the other hand, showed an increased risk of GI in marine waters when the enterococci concentrations exceeded 28 cfu/100 mL. No link between organism numbers and illness was found in fresh waters with enterococci, but E. coli concentrations exceeding 336 cfu/mL at the freshwater sites were linked with an increased risk of GI in bathers.
6.3 Non-point source impacted beaches
6.3.1 Epidemiological studies
There have been a limited number of epidemiological studies at beaches impacted only by non-point sources of contamination (i.e., no human sewage outfalls so minimal risk of human feces) (see Table 4). An early study by Calderon et al. (1991) investigated a freshwater beach with no human contamination sources; only non-point source pollution (from a forested watershed) was impacting the beach. No link between the risk of GI and the concentrations of E. coli or enterococci could be found. However, there was a relationship between high bather density, total staphylococci counts and risk of illness. Marion et al. (2010) conducted a beach cohort study at a freshwater inland lake in the United States with only non-point source contamination. Municipal wastewater discharges were permitted in tributaries but not directly into the reservoir. E. coli was the only indicator bacteria measured. The results showed that the odds of contracting a GI were 3.2-fold greater for beachgoers entering the water compared to those who did not. The risk of GI was also significantly higher for individuals who consumed food at the beach. The study also suggested an increased risk of GI or HCGI with E. coli concentrations in the highest two quartiles (i.e., > 11.3 to 59 cfu/100 mL and > 59 to 1551 cfu/100 mL). Although the increase was not always statistically significant, the trend is suggestive of increased odds of illness. A large study in Florida (Fleisher et al., 2010; Sinigalliano et al., 2010) investigated marine non-point source contaminated beaches. The authors used a prospective randomized exposure study where participants were randomly assigned to water exposure or beach-only exposure. The study reported an increased risk of health impacts in bathers compared to the beach-only exposure group, but did not find any link between enterococci concentrations and GI. They did, however, report an association between skin ailments and enterococci concentrations.
6.3.2 Quantitative microbial risk assessment studies
Quantitative microbial risk assessment (QMRA) has been used in numerous research studies to better understand the potential health impacts from human pathogens in recreational settings and to investigate the relative risks from different sources of fecal pollution. Modelling has generally shown that human and ruminant fecal pollution poses the highest risk of human health impacts, while fecal pollution from other animals poses a lower risk (Schoen and Ashbolt, 2010; Soller et al., 2010b, 2015). These studies estimate that at similar levels of E. coli or enterococci, the risk to human health from other animals (e.g., gulls, pigs, chickens) ranges from 10 to 6000 times lower than the risks associated with municipal sewage. These data support the recommendation that site-specific alternative recreational criteria be developed by jurisdictional or management authorities for recreational areas at very low risk of human pathogens. In Canada, this approach has been used by the Province of Alberta in its most recent safe beach protocol (Government of Alberta, 2019). Further information on QMRA, including its use for developing MST targets of health significance (Boehm et al., 2018; Boehm and Soller, 2020), can be found in the recreational water quality technical guideline document on Understanding and Managing Risks in Recreational Water Quality (Health Canada, in publication-b).
6.4 Non-swimming primary contact activities
While most epidemiological studies have focused on swimming as the exposure route, there are many other primary contact activities, some of which have undergone limited investigation. In fresh water, a few epidemiological studies have investigated the health effects associated with whitewater canoeing and rafting (Fewtrell et al., 1992; Lee et al., 1997). In marine recreational waters, several epidemiological studies have investigated the health effects of surfing (Harrington et al., 1993; Gammie and Wyn-Jones, 1997; Dwight et al., 2004; Stone et al., 2008; Tseng and Jiang, 2012). The conclusions of these studies are that GI is the most frequently reported —but not the only—adverse health outcome of these types of activities and that factors related to the risk of illness include the water quality and the frequency of immersion and water ingestion.
6.5 Rationale for primary contact guidelines
The goal of the primary contact guidelines set out in this document is to protect the health of Canadians during recreational activities. Numerous studies have shown that individuals have an increased risk of illness when engaging in primary contact recreational activities in comparison to non-participants (see section 6). A risk management approach, which includes using the fecal indicator guideline values provided in this document, aims to keep the health risk to a level that is deemed acceptable. The guideline values correspond to a potential risk of 36 GI for every 1000 people engaged in primary contact activities.
The guideline values provided in this document for primary contact activities (referred to as BAVs) are adopted from US EPA (2012), based on epidemiological studies conducted in the United States (see section 6.2). These studies reported GI associations with enterococci concentrations for both culture- and PCR-based methods, with the PCR-based methods having a stronger association with the risk of GI. Based on this research, the guideline values in this document now include the use of PCR-based methods for monitoring water quality. The use of PCR-based methods can provide more rapid results for beach management decisions, particularly at high use beaches where monitoring is conducted daily.
The BAVs shown in Tables 1 and 2 represent the 75th percentile value of the water quality distribution as reported in US EPA (2012). Use of the 75th percentile value, as opposed to the 90th or 95th percentile values, which is used in other jurisdictions, is a conservative approach and therefore should not be interpreted as a "never to exceed" value. The BAVs should be used to trigger activities to investigate water quality issues, issue beach notifications (when necessary) and initiate corrective actions (where applicable). The 75th percentile value for enterococci also aligns with the previous single-sample maximum for this indicator, maintaining a consistent level of public health protection with the 2012 guidelines for enterococci. The BAVs for E. coli are lower than in the 2012 guidelines, but are based on the same epidemiological studies as the enterococci values.
Although the BAVs are recommended for making day-to-day beach management decisions, the overall suitability of an area for recreational use, including an analysis of the long-term trends in water quality, can be assessed using the geometric mean of the sample results. For example, geometric means can be used to compare water quality over numerous years to determine whether the quality of the water is changing or remaining stable. The greater the number of samples included in the calculation of the geometric mean, the more reflective it will be of the water quality. The geometric mean of the water quality distributions used for the BAVs, which were calculated by the US EPA (2012), are shown in Table 5. Exposure to water at beaches with these geometric mean values for water quality will result in the same predicted risk as exposure to water with the corresponding BAV provided in Tables 1 and 2.
Fecal Indicator Bacteria |
Culture-based Methods |
PCR-based Methods |
---|---|---|
E. coli |
126 Footnote cfu/100 mL |
|
Enterococci |
35 Footnote cfu/100 mL |
470 Footnote cce/100 mL |
|
Although this guideline technical document recommends generally applicable BAVs, regulatory authorities are encouraged to consider developing site-specific alternative values for areas that are at a low risk for human fecal contamination. QMRA data indicates that the risk of human pathogens varies with the source of the fecal matter, with human and ruminant sources being higher risk (see section 6.3.2). The epidemiological studies used as the basis for the BAVs were conducted in recreational areas with known human fecal sources. In the absence of human fecal sources, the BAVs may represent a risk lower than 36 illnesses per 1000 individuals. Therefore, the appropriate regulatory authorities may choose to develop alternative site-specific values, to help balance the benefits of engaging in recreational activities with the potential associated health risks associated with these activities.
6.6 Guidelines used by other countries/organizations
The guideline values for fecal indicator organisms established by various other government and multinational organizations worldwide are presented in Table 6. These values are applicable to both fresh and marine waters (unless otherwise indicated).
Country/ organization | Indicator | Guideline Values | Basis of the Guideline Values | Reference | |
---|---|---|---|---|---|
US EPA |
NGI -36Footnote a |
NGI – 32Footnote a |
Cabelli, 1983; Dufour, 1984; NEEAR Studies: US EPA, 2010; Wade et al., 2006, 2008, 2010 |
US EPA, 2012 |
|
E. coli - Using culture methods |
GMFootnote b: 126 cfu/100 mL BAVFootnote c: 235 cfu/100 mL STVFootnote d: 410 cfu/100 mL |
GMFootnote b: 100cfu/100 mL BAVFootnote c: 190cfu/100 mL STVFootnote d: 320cfu/100 mL |
|||
Enterococci- Using culture methods Using qPCR methodsFootnote e |
GMFootnote b: 35 cfu/100 mL BAVFootnote c: 70 cfu/100 mL STVFootnote d: 130 cfu/100 mL GMFootnote b: 470 cce/100 mL BAVFootnote c: 1000 cce/100 mL STVFootnote d: 2000 cce/100 mL |
GMFootnote b: 30cfu/100 mL BAVFootnote c: 60cfu/100 mL STVFootnote d: 110cfu/100 mL GMFootnote b: 300 cce/100 mL BAVFootnote c: 640 cce/100 mL STVFootnote d: 1280 cce/100 mL |
|||
WHOFootnote * |
Intestinal enterococciFootnote f |
95th percentile/100 mL: A: ≤40 B: 41-200 C: 201-500 D: >500 |
Kay et al., 1994; Fleisher et al., 1996; Kay et al., 2001 |
WHO, 2003 |
|
AustraliaFootnote * |
Intestinal enterococciFootnote f |
95th percentile/100 mL: A: ≤ 40 B: 41–200 C: 201–500 D: > 500 |
Kay et al., 1994; Fleisher et al., 1996; Kay et al., 2001 |
NHMRC, 2008 |
|
European Union |
Fresh Water Intestinal enterococci |
95th percentile/100 mL: Excellent: 200/100 mL Good: 400/100 mL 90th percentile/100 mL: Sufficient: 330/100 mL |
Kay et al., 1994; Wiedenmann et al., 2006 |
EU, 2006 |
|
E. coli |
95th percentile/100 mL: Excellent: 500/100 mL Good 1000/100 mL 90th percentile/100 mL: Sufficient: 900/100 mL |
||||
European Union |
Marine Water Intestinal enterococci |
95th percentile/100 mL: Excellent: 200/100 mL Good: 400/100 mL 90th percentile/100 mL: Sufficient: 330/100 mL |
Kay et al., 1994; Wiedenmann et al., 2006 |
EU, 2006 |
|
E. coli |
95th percentile/100 mL: Excellent: 500/100 mL Good 1000/100 mL 90th percentile/100 mL: Sufficient: 900/100 mL |
||||
|
7.0 Water intended for secondary contact recreational activities
The Guidelines for Canadian Recreational Water Quality are intended to be protective for those activities that involve intentional or incidental immersion in natural waters. Recreational activities that have been traditionally considered secondary contact activities (e.g., canoeing, kayaking, fishing) involve different exposures from those associated with primary contact uses. A recent meta-analysis found a significant increase in GI associated with primary contact activities (swimming, sports-related water activities), but a non-significant increase in risk with secondary contact activities (minimal contact) (Russo et al., 2020). Secondary contact activities are presumed to result in a lower ingestion of water and therefore a lower risk of GI. Although secondary contact activities are associated with lower risk, inadvertent immersion can result in whole body contact, and splashing can lead to a variety of water exposure scenarios. Illnesses affecting the skin and perhaps the mucous membranes of the eyes and ears may be of relatively greater importance for secondary contact uses (US EPA, 2002). Inhalation may also be an important route of exposure during primary and secondary contact activities in areas where splash, spray or aerosols are generated.
7.1 Exposure
There has been limited research on the differences in exposures between primary and secondary contact activities. A study by Dorevitch et al. (2011) estimated that the average volume of water ingested during secondary contact activities was approximately 3 to 4 mL/h, in comparison to primary contact activities with ranges between 10 and 40 mL/h (Dorevitch et al., 2011; Dufour et al., 2017; US EPA, 2019). In addition to swallowing a lower volume of water, only 1% of the individuals engaged in secondary contact activities reported swallowing water (compared to 51% of primary contact participants) (Dorevitch et al., 2011). This translates into fewer individuals being exposed during secondary contact activities. In a follow-up analysis of the Dorevitch study (2011), data on numerous human pathogens were collected and QMRA was utilized to estimate the likely health effects for fishing, canoeing, and boating. The waterway analyzed was a man-made canal system where primary contact activities were prohibited but secondary contact activities were allowed. The risk assessment model results estimated the health risks from these activities to be lower than the acceptable illness risk associated with the US EPA's primary contact recreational water guidelines (Rijal et al., 2011). This is consistent with an earlier study that found no significant risk of GI in individuals engaged in canoeing or rowing (Fewtrell et al., 1994). In contrast, a companion prospective cohort epidemiological study compared the health impacts of secondary contact recreation activities on the same man-made waterway (where the water quality does not meet guidelines for primary contact recreation) to the health impacts of secondary contact activities on a lake with acceptable water quality for primary contact activities. An increased risk of GI (13.7–15.1 illnesses per 1000 exposures) was found in both water types (Dorevitch et al., 2012). This risk is higher than that calculated by Rijal et al. (2011) using their risk assessment model, which had several limitations associated with the pathogen datasets. Although the risk of illness was similar for the canal system and for the general-use area, the exposures for these sites were different. Recreators in the man-made canal system were less likely to report head/face submersion than their counterparts in the general-use waters. There were also more individuals fishing in the general-use waters, which is associated with a longer exposure time compared to canoeing and kayaking. Fishing has been reported elsewhere as a significant contributor to the overall risk of GI owing to the extended potential exposure time and possible routes of exposure other than ingestion (e.g., hand-to-mouth transfer of pathogens) (Sunger et al., 2015).
7.2 Recommendations
To date, there are insufficient epidemiological data available to derive health-based fecal indicator limit values for secondary contact recreational activities. However, because a lower degree of water exposure occurs at most times during the majority of secondary contact recreational activities, separate secondary contact water quality values may be developed using the primary contact guidelines combined with the lower water exposure. This approach may be considered reasonable and acceptable to local and regional authorities where a secondary contact designation is desired.
When contemplating the establishment of separate fecal indicator values for water areas used entirely for secondary contact recreation, a clear understanding of the types of activities that would fit under this description is required. The World Health Organization (WHO), in its Guidelines for Safe Recreational Water Environments: Volume 1—Coastal and Fresh Waters (WHO, 2003), has proposed a scheme for the classification of recreational water activities according to their degree of water exposure. The following descriptions (adapted from WHO, 2003), may be used as an initial guide when determining whether a specific recreational activity would be considered primary or secondary contact:
- Primary contact: Recreational activity in which the whole body or the face and trunk are frequently immersed or the face is frequently wetted by spray, and where it is likely that some water will be swallowed. Inadvertent immersion, through being swept into the water by a wave or slipping, would also result in whole body contact. Examples include swimming, surfing, waterskiing, whitewater canoeing/rafting/kayaking, windsurfing and subsurface diving.
- Secondary contact: Recreational activity in which only the limbs are regularly wetted and in which greater contact (including swallowing water) is unusual. Examples include rowing, sailing, canoe touring, and fishing.
Even if these classification criteria are used, it remains a significant challenge to discern which activities constitute primary contact and which constitute secondary contact. The classification of certain recreational water activities will be clear, whereas that of others may be less obvious and more open to interpretation. Activities considered potential candidates under a secondary contact use designation should be evaluated on a case-by-case basis.
Other factors to consider before assigning a secondary contact use designation to a recreational water area include the following:
- The water area should first be subject to an assessment of existing uses, water quality and the potential for improvement as well as any other relevant factors, such as health or environmental considerations.
- The secondary contact designation should not be applied where an assessment has shown primary contact recreation to be a significant use.
- Where the water area has a shared use (e.g., swimming and canoeing), it is the primary contact values that should apply.
- When an area is posted as suitable only for secondary contact recreational uses, communication material should clearly convey that accidental immersion (through falls, canoe spills, etc.) can lead to whole body exposure; under such circumstances, water ingestion may result in an increased risk of illness.
- Users should be reminded to take the precautions necessary to ensure that these types of exposures are avoided as much as possible; the skill of the person performing the activity may strongly influence the degree of water exposure.
Where, on the basis of an assessment of the available information, it is determined that a water area is intended to be used specifically for secondary contact recreation (i.e., where primary contact is not an existing use), a direct multiplier based on the assumed ratio difference between the primary contact exposure volume and the desired secondary exposure scenario volume can be applied to the fecal indicator guideline values. For example, using average ingestion volumes, the ratio between low ingestion activities, such as boating, fishing, and canoeing/kayaking without capsizing (3.8 mL/h; Dorevitch et al., 2011), and swimming (10 mL/h to 40 mL/h; Dorevitch et al., 2011; Dufour et al., 2017; US EPA, 2019) is approximately 3 to 8. The choice of multiplier should consider the sources of fecal contamination in the waters, as human fecal sources are more likely to contain human pathogens than other non-point sources of contamination. For example, in a water system that is impacted by human or ruminant fecal sources, the responsible authority may want to apply the conservative assumption of 3 times higher than the primary guideline value. This would result in a BAV of 705 cfu E. coli/100 mL for the secondary contact values. Any value calculated would represent a risk management decision based on a thorough assessment of the expected exposure scenarios and potential health risks for the recreational water user. In considering both the potential health risks and the benefits of recreational water use, it was concluded that this is a tolerable and reasonable approach to protect users engaged in a voluntary activity. For other parameters in the Guidelines for Canadian Recreational Water Quality, insufficient information is available to develop secondary contact guidelines, and the primary contact values and associated guidance provided in the Guidelines should therefore be used. The development of secondary contact values should not be used as a mechanism for downgrading the status of an area in response to poor water quality issues. This is particularly important where an assessment has shown that the primary contact guideline values could be achieved.
8.0 References
Alexander, L.M., Heaven, A., Tennant, A. and Morris, R. (1992). Symptomatology of children in contact with sea water contaminated with sewage. J. Epidemiol. Community Health, 46(4): 340-344.
APHA, AWWA and WEF (2017). Standard methods for the examination of water and wastewater. 23rd edition. Washington (DC): American Public Health Association, American Water Works Association and Water Environment Federation.
Arnold, B.F., Schiff, K.C., Griffith, J.F., Gruber, J.S., Yau, V., Wright, C.C., Wade, T.J., Burns, S., Hayes, J.M., McGee, C., Gold, M., Cao, Y., Weisberg, S.B. and Colford, J.M.,Jr (2013). Swimmer illness associated with marine water exposure and water quality indicators: Impact of widely used assumptions. Epidemiology, 24(6): 611-623.
Ashbolt, N.J., Dorsch, M.R., Cox, P.T. and Banens, B. (1997). Blooming E. coli, what do they mean? In: Kay, D. and Fricker, C. (eds.). Coliforms and E. coli: Problem or solution? London (UK): The Royal Society of Chemistry, Cambridge, pp 78-85.
Ashbolt, N.J., Grabow, W.O.K. and Snozzi, M. (2001). Indicators of microbial water quality. In: Fewtrell, L. and Bartram, J. (eds.). Water quality—Guidelines, standards and health: Assessment of risk and risk management for water-related infectious disease. London (UK): IWA Publishing, on behalf of the World Health Organization, pp. 289-315.
Ballesté, E. and Blanch, A.R. (2010). Persistence of Bacteroides species populations in a river as measured by molecular and culture techniques. Appl. Environ. Microbiol., 76(22): 7608-7616.
Banihashemi, A., Van Dyke, M.I. and Huck, P.M. (2015). Detection of viable bacterial pathogens in a drinking water source using propidium monoazide-quantitative PCR. J. Water Supply Res. Technol. Aqua, 64(2): 139-148.
Bartram, J. and Rees, G. (eds.). (2000). Monitoring bathing waters: A practical guide to the design and implementation of assessments and monitoring programmes. New York (NY): E & FN Spon,
Beaudry, M. (2019). From nuisance to resource: Understanding microbial sources of contamination in urban stormwater-impacted bodies of water intended for water reuse activities. M.Sc. thesis. University of Alberta.
Benjamin-Chung, J., Arnold, B.F., Wade, T.J., Schiff, K., Griffith, J.F., Dufour, A.P., Weisberg, S.B. and Colford, J.M. (2017). Coliphages and gastrointestinal illness in recreational waters: Pooled analysis of six coastal beach cohorts. Epidemiology, 28(5): 644-652.
Bernhard, A.E. and Field, K.G. (2000a). Identification of nonpoint sources of pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes. Appl. Environ. Microbiol., 66(4): 1587-1594.
Bernhard, A.E. and Field, K.G. (2000b). A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides-Prevotella genes encoding 16S rRNA. Appl. Environ. Microbiol., 66(10): 4571-4574.
Boehm, A. B., Soller, J. A. and Shanks, O. C. (2015). Human-associated fecal quantitative polymerase chain reaction measurements and simulated risk of gastrointestinal illness in recreational waters contaminated with raw sewage. Environ. Sci. Technol. Lett., 2 (10): 270-275.
Boehm, A.B., Graham, K.E., Jennings, W.C. (2018). Can we swim yet? Systematic review, meta-analysis, and risk assessment of aging sewage in surface waters. Environ. Sci. Technol., 52(17): 9634-9645.
Boehm, A.B. and Soller, J.A. (2020). Refined ambient water quality thresholds for human-associated fecal indicator HF183 for recreational waters with and without co-occurring gull fecal contamination. Microb. Risk Anal., 16:100139.
Brookes, J.D., Hipsey, M.R., Burch, M.D., Linden, L.G., Ferguson, C.M. and Antenucci, J.P. (2005). Relative value of surrogate indicators for detecting pathogens in lakes and reservoirs. Environ. Sci. Technol., 39(22): 8614-8621.
Brown, K.I., Graham, K.E., Soller, J.A. and Boehm, A.B. (2017). Estimating the probability of illness due to swimming in recreational water with a mixture of human- and gull-associated microbial source tracking markers. Environ. Sci.: Process. Impacts, 19: 1528-1541.
Byappanahalli, M.N., Fowler, M., Shively, D. and Whitman, R. (2003). Ubiquity and persistence of Escherichia coli in a midwestern coastal stream. Appl. Environ. Microbiol., 69(3): 4549-4555.
Byappanahalli, M.N., Whitman, R.L., Shively, D.A., Sadowsky, M.J. and Ishii, S. (2006). Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environ. Microbiol., 8(3): 504-513.
Byappanahalli, M.N., Sawdey, R., Ishii, S., Shively, D.A., Ferguson, J.A., Whitman, R.L. and Sadowsky, M.J. (2009). Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds. Water Res., 43(3): 806-14.
Byappanahalli, M.N., Nevers, M.B., Korajkic, A., Staley, Z.R. and Harwood, V.J. (2012a). Enterococci in the environment. Microbiol. Mol. Biol. Rev., 76(4): 685-706.
Byappanahalli, M.N., Yan, T., Hamilton, M.J., Ishii, S., Fujioka, R.S., Whitman, R.L. and Sadowsky, M.J. (2012b). The population structure of Escherichia coli isolated from subtropical and temperate soils. Sci. Total Environ., 417-418: 273-279.
Cabelli, V.J. (1983). Health effects criteria for marine recreational waters. U.S. Environmental Protection Agency, Document No.: EPA-600/1-80-031, Cincinnati, OH.
Calderon, R.L., Mood, E.W. and Dufour, A.P. (1991). Health effects of swimmers and nonpoint sources of contaminated water. Int. J. Environ. Health Res., 1(1): 21-31.
Cao, Y., Raith, M.R. and Griffith, J.F. (2016). A duplex digital PCR assay for simultaneous quantification of the Enterococcus spp. and the human fecal-associated HF183 marker in waters. J. Vis. Exp., (109): e53611.
Carman, R.J., Sayeed, S., Li, J., Genheimer, C.W., Hiltonsmith, M.F., Wilkins, T.D. and McClane, B.A. (2008). Clostridium perfringens toxin genotypes in the feces of healthy North Americans. Anaerobe, 14(2): 102-108.
Chandran, A. and Mohamed Hatha, A.A. (2005). Relative survival of Escherichia coli and Salmonella typhimurium in a tropical estuary. Water Res., 39(7): 1397-1403.
Cheung, W.H., Chang, K.C., Hung, R.P. and Kleevens, J.W. (1990). Health effects of beach water pollution in Hong Kong. Epidemiol. Infect., 105(1): 139-162.
Cole, D., Long, S.C. and Sobsey, M.D. (2003). Evaluation of F+ RNA and DNA coliphages as source-specific indicators of fecal contamination in surface waters. Appl. Environ. Microbiol., 69(11): 6507-6514.
Colford, J.M., Schiff, K.C., Griffith, J.F., Yau, V., Arnold, B.F., Wright, C.C., Gruber, J.S., Wade, T.J., Burns, S., Hayes, J., McGee, C., Gold, M., Cao, Y., Noble, R.T., Haugland, R. and Weisberg, S.B. (2012). Using rapid indicators for Enterococcus to assess the risk of illness after exposure to urban runoff contaminated marine water. Water Res., 46(7): 2176-2186.
Colford, J.M.,Jr, Wade, T.J., Schiff, K.C., Wright, C.C., Griffith, J.F., Sandhu, S.K., Burns, S., Sobsey, M., Lovelace, G. and Weisberg, S.B. (2007). Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology, 18(1): 27-35.
Corbett, S.J., Rubin, G.L., Curry, G.K. and Kleinbaum, D.G. (1993). The health effects of swimming at Sydney beaches. the Sydney beach users study advisory group. Am. J. Public Health, 83(12): 1701-1706.
Day, M.J., Hopkins, K.L., Wareham, D.W., Toleman, M.A., Elviss, N., Randall, L., Teale, C., Cleary, P., Wiuff, C., Doumith, M., Ellington, M. J., Woodford, N. and Livermore, D.M. (2019). Extended-spectrum β-lactamase-producing Escherichia coli in human-derived and foodchain-derived samples from England, Wales, and Scotland: An epidemiological surveillance and typing study. Lancet Infect. Dis. 19 (12): 1325-1335.
Davies, C.M., Long, J.A., Donald, M. and Ashbolt, N.J. (1995). Survival of fecal microorganisms in marine and freshwater sediments. Appl. Environ. Microbiol., 61(5): 1888-1896.
Degnan, A.J. (2006). Chapter 10. Escherichia coli. In: Waterborne pathogens (M48): AWWA manual of water supply practices. 2nd ed. Denver (CO): American Water Works Association. pp. 103-106.
Denis-Mize, K., Fout, G.S., Dahling, D.R. and Francy, D.S. (2004). Detection of human enteric viruses in stream water with RT-PCR and cell culture. J. Water Health, 2(1): 37-47.
Desmarais, T.R., Solo-Gabriele, H. and Palmer, C.J. (2002). Influence of soil on fecal indicator organisms in a tidally influenced subtropical environment. Appl. Environ. Microbiol., 68(3): 1165-1172.
Devane, M.L., Moriarty, E., Weaver, L., Cookson, A. and Gilpin, B. (2020). Fecal indicator bacteria from environmental sources; strategies for identification to improve water quality monitoring. Water Res., 185: 116204.
Dias, E., Ebdon, J. and Taylor, H. (2018). The application of bacteriophages as novel indicators of viral pathogens in wastewater treatment systems. Water Res., 129: 172-179.
Diston, D. and Wicki, M. (2015). Occurrence of bacteriophages infecting Bacteroides host strains (ARABA 84 and GB-124) in fecal samples of human and animal origin. J. Water Health, 13(3): 654-661.
Dorevitch, S., Panthi, S., Huang, Y., Li, H., Michalek, A.M., Pratap, P., Wroblewski, M., Liu, L., Scheff, P.A. and Li, A. (2011). Water ingestion during water recreation. Water Res., 45(5): 2020-2028.
Dorevitch, S., Pratap, P., Wroblewski, M., Hryhorczuk, D.O., Li, H., Liu, L.C. and Scheff, P.A. (2012). Health risks of limited-contact water recreation. Environ. Health Perspect., 120(2): 192-197.
Dorevitch, S., DeFlorio-Barker, S., Jones, R.M. and Liu, L. (2015). Water quality as a predictor of gastrointestinal illness following incidental contact water recreation. Water Res., 83: 94-103.
Dorner, S.M., Anderson, W.B., Gaulin, T., Candon, H.L., Slawson, R.M., Payment, P. and Huck, P.M. (2007). Pathogen and indicator variability in a heavily impacted watershed. J. Water Health, 5(2): 241-257.
Dufour, A.P. and Cabelli, V.J. (1976). Characteristics of Klebsiella from textile finishing plant effluents. J. Water Pollut. Control Fed., 48(5): 872-879.
Dufour, A.P. (1977). Escherichia coli: The fecal coliform. Am. Soc. Test. Mater. Spec. Tech. Publ., 635(45): 58.
Dufour, A.P. (1984). Health effects criteria for fresh water recreational waters. United States Environmental Protection Agency, Document Number: EPA 600/1-84-004, Cincinnati, Ohio.
Dufour, A.P., Behymer, T.D., Cantu, R., Magnuson, M. and Wymer, L.J.(2017). Ingestion of swimming pool water by recreational swimmers. J. Water Health, 15(3): 429-437.
Dwight, R.H., Baker, D.B., Semenza, J.C. and Olson, B.H. (2004). Health effects associated with recreational coastal water use: Urban versus rural California. Am. J. Public Health, 94(4): 565-567.
Ebdon, J.E., Sellwood, J., Shore, J. and Taylor, H.D. (2012). Phages of Bacteroides (GB-124): A novel tool for viral waterborne disease control? Environ. Sci. Technol., 46(2): 1163-1169.
Edberg, S.C., Rice, E.W., Karlin, R.J. and Allen, M.J. (2000). Escherichia coli: The best biological drinking water indicator for public health protection. Symp. Ser. Soc. Appl. Microbiol., (29): 106S-116S.
Edge, T.A., El-Shaarawi, A., Gannon, V., Jokinen, C., Kent, R., Khan, I.U., Koning, W., Lapen, D., Miller, J., Neumann, N., Phillips, R., Robertson, W., Schreier, H., Scott, A., Shtepani, I., Topp, E., Wilkes, G. and van Bochove, E. (2012). Investigation of an Escherichia coli environmental benchmark for waterborne pathogens in agricultural watersheds in Canada. J. Environ. Qual., 41(1): 21-30.
Edge, T.A., Khan, I.U.H., Bouchard, R., Guo, J., Hill, S., Locas, A., Moore, L., Neumann, N., Nowak, E., Payment, P., Yang, R., Yerubandi, R. and Watson, S. (2013). Occurrence of waterborne pathogens and Escherichia coli at offshore drinking water intakes in Lake Ontario. Appl. Environ. Microbiol., 79(19): 5799-5813.
Edge, T.A., Hill, S., Crowe, A., Marsalek, J., Seto, P., Snodgrass, B., Toninger, R. and Patel, M. (2018). Remediation of a beneficial use impairment at Bluffer's Park Beach in the Toronto Area of Concern. Aquat. Ecosyst. Health Manag., 21: 285-292.
Epibathe (2009). Activity report for EU framework 6 specific targeted research projects. Project reference 022618.
Ervin, J.S., Russell, T.L., Layton, B.A., Yamahara, K.M., Wang, D., Sassoubre, L.M., Cao, Y., Kelty, C.A., Sivaganesan, M., Boehm, A.B., Holden, P.A., Weisberg, S.B. and Shanks, O.C. (2013). Characterization of fecal concentrations in human and other animal sources by physical, culture-based, and quantitative real-time PCR methods. Water Res., 47(18): 6873-6882.
EU (2006). Directive 2006/7/EC of the European parliament and of the council of 15 February 2006 concerning the management of bathing water quality and repealing directive 76/160/EEC. Official Journal of the European Union, European Union.
Ferguson, D.M., Moore, D.F., Getrich, M.A. and Zhowandai, M.H. (2005). Enumeration and speciation of enterococci found in marine and intertidal sediments and coastal water in southern California. J. Appl. Microbiol., 99(3): 598-608.
Ferley, J.P., Zmirou, D., Balducci, F., Baleux, B., Fera, P., Larbaigt, G., Jacq, E., Moissonnier, B., Blineau, A. and Boudot, J. (1989). Epidemiological significance of microbiological pollution criteria for river recreational waters. Int. J. Epidemiol., 18(1): 198-205.
Fernandez-Miyakawa, M.E., Pistone, C.V., Uzal, F.A., McClane, B.A. and Ibarra, C. (2005). Clostridium perfringens enterotoxin damages the human intestine in vitro. Infect. Immun., 73(12): 8407-8410.
Fewtrell, L., Kay, D., Salmon, R., Wyer, M., Newman, G. and Bowering, G. (1994). The health effects of low contact water activities in fresh and estuarine waters. Water Environ. J., 8: 97-101.
Fewtrell, L., Jones, F., Kay, D., Wyer, M.D., Godfree, A.F. and Salmon, B.L. (1992). Health effects of white-water canoeing. Lancet, 339(8809): 1587-1589.
Fewtrell, L. and Kay, D. (2015). Recreational water and infection: A review of recent findings. Curr. Environ. Health Rep., 2(1): 85-94.
Finegold, S.M., Sutter, V.L. and Mathison, G.E. (1983). Normal indigenous intestinal flora. In: Hentges, D.J. (ed.). Human intestinal microflora in health and disease. New York (NY): Academic Press. pp. 3-31.
Fleisher, J.M., Kay, D., Salmon, R.L., Jones, F., Wyer, M.D. and Godfree, A.F. (1996). Marine waters contaminated with domestic sewage: Non-enteric illnesses associated with bather exposure in the United Kingdom. Am. J. Public Health, 86(9): 1228-1234.
Fleisher, J.M., Fleming, L.E., Solo-Gabriele, H.M., Kish, J.K., Sinigalliano, C.D., Plano, L., Elmir, S.M., Wang, J.D., Withum, K., Shibata, T., Gidley, M.L., Abdelzaher, A., He, G., Ortega, C., Zhu, X., Wright, M., Hollenbeck, J. and Backer, L.C. (2010). The BEACHES study: Health effects and exposures from non-point source microbial contaminants in subtropical recreational marine waters. Int. J. Epidemiol., 39(5): 1291-1298.
Frick, C., Vierheilig, J., Linke, R., Savio, D., Zornig, H., Antensteiner, R., Baumgartner, C., Bucher, C., Blaschke, A.P., Derx, J., Kirschner, A.K.T., Ryzinska-Paier, G., Mayer, R., Seidl, D., Nadiotis-Tsaka, T., Sommer, R., Farnleitner, A.H. (2018). Poikilothermic animals as a previously unrecognized source of fecal indicator bacteria in a backwater ecosystem of a large river. Appl. Environ. Microbiol. 84 (16), art. no. e00715-18.
Fujioka, R.S. and Shizumura, L.K. (1985). Clostridium perfringens, a reliable indicator of stream water quality. J. Water Pollut. Control Fed., 57(10): 986-992.
Gammie, A.J. and Wyn-Jones, A.P. (1997). Does hepatitis a pose a significant health risk to recreational water users? Water Sci. Technol., 35(11): 171-177.
Gordon, D.M. (2013). The ecology of Escherichia coli. In: Donnenberg, M.S. (ed.). Escherichia coli: Pathotypes and principles of pathogenesis. 2nd edition. London (UK): Academic Press. pp. 3-20.
Government of Alberta (2019). Alberta safe beach protocol. July 2019. Available at: https://open.alberta.ca/publications/9781460145395.
Griffin, D.W., Gibson, C.J.,3rd, Lipp, E.K., Riley, K., Paul, J.H.,3rd and Rose, J.B. (1999). Detection of viral pathogens by reverse transcriptase PCR and of microbial indicators by standard methods in the canals of the Florida Keys. Appl. Environ. Microbiol., 65(9): 4118-4125.
Griffith, J.F., Weisberg, S.B., Arnold, B.F., Cao, Y., Schiff, K.C. and Colford, J.M. (2016). Epidemiologic evaluation of multiple alternate microbial water quality monitoring indicators at three California beaches. Water Res., 94: 371-381.
Haramoto, E., Otagiri, M., Morita, H. and Kitajima, M. (2012). Genogroup distribution of F-specific coliphages in wastewater and river water in the Dofu basin in Japan. Lett. Appl. Microbiol., 54(4): 367-373.
Harrington, J.F., Wilcox, D.N., Giles, P.S., Ashbolt, N.J., Evans, J.C. and Kirton, H.C. (1993). The health of Sydney surfers: An epidemiological study. Water Sci. Technol., 27(3-4): 175-181.
Hartz, A., Cuvelier, M., Nowosielski, K., Bonilla, T.D., Green, M., Esiobu, N., McCorquodale, D.S. and Rogerson, A. (2008). Survival potential of Escherichia coli and enterococci in subtropical beach sand: Implications for water quality managers. J. Environ. Qual., 37(3): 898-905.
Harwood, V.J., Boehm, A.B., Sassoubre, L.M., Vijayavel, K., Stewart, J.R., Fong, T.T., Caprais, M.P., Converse, R.R., Diston, D., Ebdon, J., Fuhrman, J.A., Gourmelon, M., Gentry-Shields, J., Griffith, J.F., Kashian, D.R., Noble, R.T., Taylor, H. and Wicki, M. (2013). Performance of viruses and bacteriophages for fecal source determination in a multi-laboratory, comparative study. Water Res., 47(18): 6929-6943.
Harwood, V.J., Staley, C., Badgley, B.D., Borges, K. and Korajkic, A. (2014). Microbial source tracking markers for detection of fecal contamination in environmental waters: Relationships between pathogens and human health outcomes. FEMS Microbiol. Rev., 38(1): 1-40.
Health Canada. (in publication-a). Guidelines for Canadian Recreational Water Quality: Guideline Technical Document – Microbiological Methods. Water and Air Quality Bureau, Healthy Environments and Consumer Safety Branch, Health Canada, Ottawa, Ontario.
Health Canada. (in publication-b). Guidelines for Canadian Recreational Water Quality: Guideline Technical Document – Understanding and Managing Risks in Recreational Water Quality. Water and Air Quality Bureau, Healthy Environments and Consumer Safety Branch, Health Canada, Ottawa, Ontario.
Health Canada (2012). Guidelines for Canadian Recreational Water Quality, 3rd ed. Water, Air and Climate Change Bureau, Healthy Environments and Consumer Safety Branch, Health Canada, Ottawa, Ontario. (Catalogue No H129-15/2012E).
Heuvel, A.V., McDermott, C., Pillsbury, R., Sandrin, T., Kinzelman, J., Ferguson, J., Sadowsky, M., Byappanahalli, M., Whitman, R. and Kleinheinz, G.T. (2010). The green alga, Cladophora, promotes Escherichia coli growth and contamination of recreational waters in Lake Michigan. J. Environ. Qual., 39(1): 333-344.
Hong, P., Wu, J. and Liu, W. (2008). Relative abundance of Bacteroides spp. in stools and wastewaters as determined by hierarchical oligonucleotide primer extension. Appl. Environ. Microbiol., 74(9): 2882-2893.
Hörman, A., Rimhanen-Finne, R., Maunula, L., von Bonsdorff, C.H., Torvela, N., Heikinheimo, A. and Hanninen, M.L. (2004). Campylobacter spp., Giardia spp., Cryptosporidium spp., noroviruses, and indicator organisms in surface water in southwestern Finland, 2000-2001. Appl. Environ. Microbiol., 70(1): 87-95.
Hughes, B., Beale, D.J., Dennis, P.G., Cook, S. and Ahmed, W. (2017). Cross-comparison of human wastewater-associated molecular markers in relation to fecal indicator bacteria and enteric viruses in recreational beach waters. Appl. Environ. Microbiol., 83(8): e00028-17.
Huntley, B.E., Jones, A.E. and Cabelli, V.J. (1976). Klebsiella densities in waters receiving wood pulp effluents. J. Water Pollut. Control Fed., 48: 1766-1771.
Ishii, S., Ksoll, W.B., Hicks, R.E. and Sadowsky, M.J. (2006). Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl. Environ. Microbiol., 72(1): 612-621.
Ishii, S. and Sadowsky, M.J. (2008). Escherichia coli in the environment: implications for water quality and human health. Microbes Environ. 23(2): 101-108.
Jacob, P., Henry, A., Meheut, G., Charni-Ben-Tabassi, N., Ingrand, V. and Helmi, K. (2015). Health risk assessment related to waterborne pathogens from the river to the tap. Int. J. Environ. Res. Public. Health, 12(3): 2967-2983.
Jang, J., Hur, H.G., Sadowsky, M.J., Byappanahalli, M.N., Yan, T. and Ishii, S. (2017). Environmental Escherichia coli: Ecology and public health implications-a review. J. Appl. Microbiol., 123(3): 570-581.
Jebri, S., Muniesa, M. and Jofre, J. (2017). General and host-associated bacteriophage indicators of fecal pollution. In: Rose, J.B. and Jiménez-Cisneros, B. (eds.). Global water pathogens project. East Lansing (MI): UNESCO.
Jiang, S., Noble, R. and Chu, W. (2001). Human adenoviruses and coliphages in urban runoff-impacted coastal waters of southern California. Appl. Environ. Microbiol., 67(1): 179-184.
Jiang, S.C. and Chu, W. (2004). PCR detection of pathogenic viruses in southern California urban rivers. J. Appl. Microbiol., 97(1): 17-28.
Jofre, J., Lucena, F., Blanch, A.R. and Muniesa, M. (2016). Coliphages as model organisms in the characterization and management of water resources. Water (Switzerland), 8(5): 199
Kay, D., Jones, F., Wyer, M.D., Fleisher, J.M., Salmon, R.L., Godfree, A.F., Zelenauch-Jacquotte, A. and Shore, R. (1994). Predicting likelihood of gastroenteritis from sea bathing: Results from randomised exposure. The Lancet, 344(8927): 905-909.
Kay, D., Bartram, J., Prüss, A., Ashbolt, N., D. Wyer, M.D., Fleisher, J.M., Fewtrell, L., Rogers, A. and Rees, G. (2004). Derivation of numerical values for the World Health Organization guidelines for recreational waters, Water Res., 38(5): 1296-1304.
Kon, T., Weir, S.C., Howell, E.T., Lee, H. and Trevors, J.T. (2007a). Genetic relatedness of Escherichia coli isolates in interstitial water from a Lake Huron (Canada) beach. Appl. Environ. Microbiol., 73(6): 1961-1967.
Kon, T., Weir, S.C., Trevors, J.T., Lee, H., Champagne, J., Meunier, L., Brousseau, R. and Masson, L. (2007b). Microarray analysis of Escherichia coli strains from interstitial beach waters of Lake Huron (Canada). Appl. Environ. Microbiol., 73(23): 7757-7758.
Korajkic, A., McMinn, B.R., Harwood, V.J., Shanks, O.C., Fout, G.S. and Ashbolt, N.J. (2013). Differential decay of enterococci and Escherichia coli originating from two fecal pollution sources. Appl. Environ. Microbiol., 79(6): 2488-2492.
Korajkic, A., Parfrey, L.W., McMinn, B. R., Baeza, Y.V., Van Teuren, W., Knight, R. and Shanks, O.C. (2015). Changes in bacterial and eukaryotic communities during sewage decomposition in Mississippi River water. Water Res., 69: 30-9.
Korajkic, A., McMinn, B., Herrmann, M.P., Sivaganesan, M., Kelty, C.A., Clinton, P., Nash, M.S. and Shanks, O.C. (2020). Viral and bacterial fecal indicators in untreated wastewater across the contiguous United States exhibit geospatial trends. Appl. Environ. Microbiol., 86: e02967-19.
Korhonen, L.K. and Martikainen, P.J. (1991). Survival of Escherichia coli and Campylobacter jejuni in untreated and filtered lake water. J. Appl. Bacteriol., 71(4): 379-382.
Krkosek, W., Reed, V. and Gagnon, G.A. (2016). Assessing protozoan risks for surface drinking water supplies in Nova Scotia, Canada. J. Water Health, 14(1): 155-166.
Lalancette, C., Papineau, I., Payment, P., Dorner, S., Servais, P., Barbeau, B., Di Giovanni, G.D. and Prévost, M. (2014). Changes in Escherichia coli to Cryptosporidium ratios for various fecal pollution sources and drinking water intakes. Water Res., 55: 150-161.
Lamparelli, C.C., Pogreba-Brown, K., Verhougstraete, M., Sato, M.I.Z., de Castro Bruni, A., Wade, T.J. and Eisenberg, J.N.S. (2015). Are fecal indicator bacteria appropriate measures of recreational water risks in the tropics: A cohort study of beach goers in Brazil? Water Res., 87: 59-68.
Leclerc, H., Mossel, D.A., Edberg, S.C. and Struijk, C.B. (2001). Advances in the bacteriology of the coliform group: Their suitability as markers of microbial water safety. Annu. Rev. Microbiol., 55: 201-234.
Lee, H.S. and Sobsey, M.D. (2011). Survival of prototype strains of somatic coliphage families in environmental waters and when exposed to UV low-pressure monochromatic radiation or heat. Water Res., 45(12): 3723-3734.
Lee, J.V., Dawson, S.R., Ward, S., Surman, S.B. and Neal, K.R. (1997). Bacteriophages are a better indicator of illness rates than bacteria amongst users of a white water course fed by a lowland river. Water Sci. Technol., 35(11): 165-170.
Leonard, A.F.C., Zhang, L., Balfour, A.J., Garside, R., Hawkey, P.M., Murray, A.K., Ukoumunne, O.C. and Gaze, W.H. (2018). Exposure to and colonisation by antibiotic-resistant E. coli in UK coastal water users: Environmental surveillance, exposure assessment, and epidemiological study (Beach Bum Survey). Environ. Int., 114: 326-333.
Lipp, E.K., Kurz, R., Vincent, R., Rodriguez-Palacios, C., Farrah, S.R. and Rose, J.B. (2001). The effects of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary. Estuaries, 24(2): 266-276.
Lloyd-Price, J., Abu-Ali, G. and Huttenhower, C. (2016). The healthy human microbiome. Genome Medicine, 8(51): 11.
Logan, L.K., Zhang, L., Green, S.J., Dorevitch, S., Arango-Argoty, G.A., Reme, K., Garner, E., Aldstadt, J., Johhson-Walker, Y.J., Hayden, M.K., Weinstein, R.A. and Pruden, A. (2020). A pilot study of Chicago waterways as reservoirs of multidrug-resistant Enterobacteriaceae (MDR-Ent) in a high-risk region for community-acquired MDR-Ent infection in children. Antimicrobial Agents and Chemotherapy, 64(4): e02310-19.
Luther, K. and Fujioka, R. (2004). Usefulness of monitoring tropical streams for male-specific RNA coliphages. J. Water Health., 2(3): 171-181.
Marino, F.J., Morinigo, M.A., Martinez-Manzanares, E. and Borrego, J.J. (1995). Microbiological-epidemiological study of selected marine beaches in Malaga (Spain). Water Sci. Technol., 31(5): 5-9.
Marion, J.W., Lee, J., Lemeshow, S. and Buckley, T.J. (2010). Association of gastrointestinal illness and recreational water exposure at an inland U.S. beach. Water Res., 44(16): 4796-4804.
McBride, G.B., Salmond, C.E., Bandaranayake, D.R., Turner, S.J., Lewis, G.D. and Till, D.G. (1998). Health effects of marine bathing in New Zealand. Int. J. Environ. Health Res., 8(3): 173-189.
McLaughlin, M.R. and Rose, J.B. (2006). Application of Bacteroides fragilis phage as an alternative indicator of sewage pollution in Tampa Bay, Florida. Estuaries Coast., 29(2): 246-256.
McMinn, B.R., Korajkic, A. and Ashbolt, N.J. (2014). Evaluation of Bacteroides fragilis GB-124 bacteriophages as novel human-associated fecal indicators in the United States. Lett. Appl. Microbiol., 59(1): 115-121.
McMinn, B.R., Ashbolt, N.J. and Korajkic, A. (2017). Bacteriophages as indicators of fecal pollution and enteric virus removal. Lett. Appl. Microbiol., 65(1): 11-26.
McQuaig, S., Griffith, J. and Harwood, V.J. (2012). Association of fecal indicator bacteria with human viruses and microbial source tracking markers at coastal beaches impacted by nonpoint source pollution. Appl. Environ. Microbiol., 78(18): 6423-6432.
Mocé-Llivina, L., Lucena, F. and Jofre, J. (2005). Enteroviruses and bacteriophages in bathing waters. Appl. Environ. Microbiol., 71(11): 6838-6844.
Moore, D.F., Guzman, J.A. and McGee, C. (2008). Species distribution and antimicrobial resistance of enterococci isolated from surface and ocean water. J. Appl. Microbiol., 105(4): 1017-1025.
Mueller-Spitz, S.R., Stewart, L.B., Klump, J.V. and McLellan, S.L. (2010). Freshwater suspended sediments and sewage are reservoirs for enterotoxin-positive Clostridium perfringens. Appl. Environ. Microbiol., 76(16): 5556-5562.
Muniesa, M., Moce-Llivina, L., Katayama, H. and Jofre, J. (2003). Bacterial host strains that support replication of somatic coliphages. Antonie Van Leeuwenhoek, 83(4): 305-315.
Napier, M.D., Haugland, R., Poole, C., Dufour, A.P., Stewart, J.R., Weber, D.J., Varma, M., Lavender, J.S. and Wade, T.J. (2017). Exposure to human-associated fecal indicators and self-reported illness among swimmers at recreational beaches: A cohort study. Environ. Health, 16(Article Number 103): 1-15.
Nappier, S.P., Aitken, M.D. and Sobsey, M.D. (2006). Male-specific coliphages as indicators of thermal inactivation of pathogens in biosolids. Appl. Environ. Microbiol., 72(4): 2471-2475.
Nappier, S.P., Hong, T., Ichida, A., Goldstone, A., Eftim, S.E. (2019). Occurrence of coliphage in raw wastewater and in ambient water: A meta-analysis. Water Res., 153: 263-273.
Nelson, K.L., Boehm, A.B., Davies-Colley, R.J., Dodd, M.C., Kohn, T., Linden, K.G., Liu, Y., Maraccini, P.A., McNeill, K., Mitch, W.A., Nguyen, T.H., Parker, K.M., Rodriguez, R.A., Sassoubre, L.M., Silverman, A.I., Wigginton, K.R. and Zepp, R.G. (2018). Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches. Environ. Sci. Process Impacts, 20(8): 1089-1122.
NHMRC (2008). Guidelines for managing risks in recreational water. National Health and Medical Research Council, Australian Government, Canberra.
Olapade, O.A., Depas, M.M., Jensen, E.T. and McLellan, S.L. (2006). Microbial communities and fecal indicator bacteria associated with Cladophora mats on beach sites along Lake Michigan shores. Appl. Environ. Microbiol., 72(3): 1932-1938.
Papastergiou, P., Mouchtouri, V., Pinaka, O., Katsiaflaka, A., Rachiotis, G. and Hadjichristodoulou, C. (2012). Elevated bathing-associated disease risks despite certified water quality: A cohort study. Int. J. Environ. Res. Public Health, 9(5): 1548-1565.
Payan, A., Ebdon, J., Taylor, H., Gantzer, C., Ottoson, J., Papageorgiou, G.T., Blanch, A.R., Lucena, F., Jofre, J. and Muniesa, M. (2005). Method for isolation of Bacteroides bacteriophage host strains suitable for tracking sources of fecal pollution in water. Appl. Environ. Microbiol., 71(9): 5659-5662.
Plummer, J.D., Long, S.C., Charest, A.J. and Roop, D.O. (2014). Bacterial and viral indicators of fecal contamination in drinking water. American Water Works Association, 106(4): E200-E211.
Pourcher, A.-., Devriese, L.A., Hernandez, J.F. and Delattre, J.M. (1991). Enumeration by a miniaturized method of Escherichia coli, Streptococcus bovis and enterococci as indicators of the origin of fecal pollution of waters. J. Appl. Bacteriol., 70(6): 525-530.
Power, M.L., Littlefield-Wyer, J., Gordon, D.M., Veal, D.A. and Slade, M.B. (2005). Phenotypic and genotypic characterization of encapsulated Escherichia coli isolated from blooms in two Australian lakes. Environ. Microbiol., 7(5): 631-640.
Prieto, M.D., Lopez, B., Juanes, J.A., Revilla, J.A., Llorca, J. and Delgado-Rodriguez, M. (2001). Recreation in coastal waters: Health risks associated with bathing in sea water. J. Epidemiol. Community Health, 55: 441-447.
Pruss, A. (1998). Review of epidemiological studies on health effects from exposure to recreational water. Int. J. Epidemiol., 27(1): 1-9.
Prystajecky, N., Huck, P.M., Schreier, H. and Isaac-Renton, J.L. (2014). Assessment of Giardia and Cryptosporidium spp. as a microbial source tracking tool for surface water: Application in a mixed-use watershed. Appl. Environ. Microbiol., 80(8): 2328-2336.
Puig, A., Queralt, N., Jofre, J. and Araujo, R. (1999). Diversity of Bacteroides fragilis strains in their capacity to recover phages from human and animal wastes and from fecally polluted wastewater. Appl. Environ. Microbiol., 65(4): 1772-1776.
Ran, Q., Badgley, B.D., Dillon, N., Dunny, G.M. and Sadowsky, M.J. (2013). Occurrence, genetic diversity, and persistence of enterococci in a Lake Superior watershed. Appl. Environ. Microbiol., 79: 3067-3075.
Rhodes, M.W. and Kator, H. (1988). Survival of Escherichia coli and Salmonella spp. in estuarine environments. Appl. Environ. Microbiol., 54(12): 2902-2907.
Rijal, G., Tolson, J.K., Petropoulou, C., Granato, T.C., Glymph, A., Gerba, C., Deflaun, M.F., O'Connor, C., Kollias, L. and Lanyon, R. (2011). Microbial risk assessment for recreational use of the Chicago area waterway system. J. Water Health, 9(1): 169-186.
Rokosh, D.A., Rao, S.S. and Jurkovic, A.A. (1977). Extent of effluent influence on lake water determined by bacterial population distributions. J. Fish. Res. Board can., 34: 844-849.
Russo, G.S., Eftim, S.E., Goldstone, A.E., Dufour, A.P., Nappier, S.P. and Wade, T.J. (2020). Evaluating health risks associated with exposure to ambient surface waters during recreational activities: a systematic review and meta-analysis. Water Res., 176: 115729.
Schoen, M.E. and Ashbolt, N.J. (2010). Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. Environ. Sci. Technol., 44: 2286-2291.
Schoen, M.E., Soller, J.A. and Ashbolt, N.J. (2011). Evaluating the importance of fecal sources in human-impacted waters. Water Res., 45(8): 2670-2680.
Schvoerer, E., Bonnet, F., Dubois, V., Cazaux, G., Serceau, R., Fleury, H.J. and Lafon, M.E. (2000). PCR detection of human enteric viruses in bathing areas, waste waters and human stools in southwestern France. Res. Microbiol., 151(8): 693-701.
Schvoerer, E., Ventura, M., Dubos, O., Cazaux, G., Serceau, R., Gournier, N., Dubois, V., Caminade, P., Fleury, H.J. and Lafon, M.E. (2001). Qualitative and quantitative molecular detection of enteroviruses in water from bathing areas and from a sewage treatment plant. Res. Microbiol., 152(2): 179-186.
Sinclair, R.G., Jones, E.L. and Gerba, C.P. (2009). Viruses in recreational water-borne disease outbreaks: A review. J. Appl. Microbiol., 107(6): 1769-1780.
Sinigalliano, C.D., Fleisher, J.M., Gidley, M.L., Solo-Gabriele, H.M., Shibata, T., Plano, L.R.W., Elmir, S.M., Wanless, D., Bartkowiak, J., Boiteau, R., Withum, K., Abdelzaher, A.M., He, G., Ortega, C., Zhu, X., Wright, M.E., Kish, J., Hollenbeck, J., Scott, T., Backer, L.C. and Fleming, L.E. (2010). Traditional and molecular analyses for fecal indicator bacteria in non-point source subtropical recreational marine waters. Water Res., 44(13): 3763-3772.
Sinton, L.W. (1993). Faecal streptococci as faecal pollution indicators: A review. Part II: Sanitary significance, survival and use. N. Z. J. Mar. Freshwater Res., 27: 117-137.
Sirikanchana, K., Wangkahad, B. and Mongkolsuk, S. (2014). The capability of non-native strains of Bacteroides bacteria to detect bacteriophages as fecal indicators in a tropical area. J. Appl. Microbiol., 117(6): 1820-1829.
Soller, J., Embrey, M., Tuhela, L., Ichida, A. and Rosen, J. (2010a). Risk-based evaluation of Escherichia coli monitoring data from undisinfected drinking water. J. Environ. Manage., 91(11): 2329-2335.
Soller, J.A., Schoen, M.E., Bartrand, T., Ravenscroft, J.E. and Ashbolt, N.J. (2010b). Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of fecal contamination. Water Res., 44: 4674-4691.
Soller, J., Bartrand, T., Ravenscroft, J., Molina, M., Whelan, G., Schoen, M., Ashbolt, N. (2015). Estimated human health risks from recreational exposures to stormwater runoff containing animal fecal material. Environ. Model. Softw., 72: 21-32.
Soller, J.A., Eftim, S., Wade, T.J., Ichida, A.M., Clancy, J.L., Johnson, T.B., Schwab, K., Ramirez-Toro, G., Nappier, S. and Ravenscroft, J.E. (2016). Use of quantitative microbial risk assessment to improve interpretation of a recreational water epidemiological study. Microb. Risk Anal., 1: 2-11.
Solo-Gabriele, H., Wolfert, M.A., Desmarais, T.R. and Palmer, C.J. (2000). Sources of Escherichia coli in a coastal subtropical environment. Appl. Environ. Microbiol., 66(1): 230-237.
Stachler, E. and Bibby, K. (2014). Metagenomic evaluation of the highly abundant human gut bacteriophage crAssphage for source tracking of human fecal pollution. Environ. Sci. Technol. Lett., 1: 405-409.
Staley, C., Dunny, G.M. and Sadowsky, M.J. (2014). Environmental and animal-associated enterococci. Adv. Appl. Microbiol., 87: 147-186.
Staley, Z.R., Boyd, R.J., Shum, P. and Edge, T.A. (2018). Microbial source tracking using quantitative and digital PCR to identify sources of fecal contamination in stormwater, river water, and beach water in a Great Lakes Area of Concern. Appl. Env. Microbiol., 84(20): e01634-18.
Stea, E.C., Truelstrup Hansen, L., Jamieson, R.C. and Yost, C.K. (2015). Fecal contamination in the surface waters of a rural and an urban-source watershed. J. Environ. Qual., 44(5): 1556-1567.
Stone, D.L., Harding, A.K., Hope, B.K. and Slaughter-Mason, S. (2008). Exposure assessment and risk of gastrointestinal illness among surfers. J. Toxicol. Environ. Health A., 71(24): 1603-1615.
Sunger, N. and Haas, C.N. (2015). Quantitative microbial risk assessment for recreational exposure to water bodies in Philadelphia. Water Environ. Res., 87(3): 211-222.
Svec, P. and Devriese, L.A. (2009). The genus Enterococcus. In: De Vos, P., Garrity, G.M., Jones, D., Krieg, N.R., Ludwig, W., Rainey, F.A., Schleifer, K.H. and Whitman, W.B. (eds.). Bergey's manual of systematic bacteriology. 2nd ed. New York (NY): Springer.
Tenaillon, O., Skurnik, D., Picard, B. and Denamur, E. (2010). The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol., 8(3): 207-217.
Tseng, L.Y. and Jiang, S.C. (2012). Comparison of recreational health risks associated with surfing and swimming in dry weather and post-storm conditions at southern California beaches using quantitative microbial risk assessment (QMRA). Mar. Pollut. Bull., 64(5): 912-918.
US EPA (2002). Implementation guidance for ambient water quality criteria for bacteria (May 2002 draft). EPA-823-B-02-003. Washington (DC): United States Environmental Protection Agency, Office of Water.
US EPA (2010). Report on 2009 National Epidemiologic and Environmental Assessment of Recreational Water Epidemiology Studies (NEEAR 2010 - Surfside & Boquerón). EPA-600-R-10-168.
US EPA (2012). Recreational water quality criteria. United States Environmental Protection Agency. Office of Water, 820-F-12-058.
US EPA (2015). Review of coliphages as possible indicators of fecal contamination for ambient water quality. United States Environmental Protection Agency, Office of Water, Document Number: 820-R-15-098.
US EPA (2019). Recommended human health recreational ambient water quality criteria or swimming advisories for microcystins and cylindrospermopsin. United States Environmental Protection Agency, Office of Water, Document Number: 822-R-19-001.
van Asperen, I.A., Medema, G., Borgdorff, M.W., Sprenger, M.J. and Havelaar, A.H. (1998). Risk of gastroenteritis among triathletes in relation to fecal pollution of fresh waters. Int. J. Epidemiol., 27(2): 309-315.
Van Dyke, M.I., Ong, C.S.L., Prystajecky, N.A., Isaac-Renton, J.L. and Huck, P.M. (2012). Identifying host sources, human health risk and indicators of Cryptosporidium and Giardia in a Canadian watershed influenced by urban and rural activities. J. Water Health, 10(2): 311-323.
Verhougstraete, M.P., Byappanahalli, M.N., Rose, J.B. and Whitman, R.L. (2010). Cladophora in the Great Lakes: Impacts on beach water quality and human health. Water Sci. Technol., 62(1): 68-76.
Viau, E.J., Goodwin, K.D., Yamahara, K.M., Layton, B.A., Sassoubre, L.M., Burns, S.L., Tong, H., Wong, S.H.C., Lu, Y. and Boehm, A.B. (2011). Bacterial pathogens in Hawaiian coastal streams—Associations with fecal indicators, land cover, and water quality. Water Res., 45(11): 3279-3290.
Vierheilig, J., Frick, C., Mayer, R.E., Kirschner, A.K., Reischer, G.H., Derx, J., Mach, R.L., Sommer, R. and Farnleitner, A.H. (2013). Clostridium perfringens is not suitable for the indication of fecal pollution from ruminant wildlife but is associated with excreta from nonherbivorous animals and human sewage. Appl. Environ. Microbiol., 79(16): 5089-5092.
Vlassoff, L.T. (1977). Klebsiella. Am. Soc. Test. Mater. Spec. Tech. Publ., 635: 275-288.
von Schirnding, Y.E., Kfir, R., Cabelli, V., Franklin, L. and Joubert, G. (1992). Morbidity among bathers exposed to polluted seawater. A prospective epidemiological study. S. Afr. Med. J., 81(11): 543-546.
Wade, T.J., Pai, N., Eisenberg, J.N. and Colford, J.M.,Jr (2003). Do U.S. environmental protection agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic review and meta-analysis. Environ. Health Perspect., 111(8): 1102-1109.
Wade, T.J., Calderon, R.L., Sams, E., Beach, M., Brenner, K.P., Williams, A.H. and Dufour, A.P. (2006). Rapidly measured indicators of recreational water quality are predictive of swimming-associated gastrointestinal illness. Environ. Health Perspect., 114(1): 24-28.
Wade, T.J., Calderon, R.L., Brenner, K.P., Sams, E., Beach, M., Haugland, R., Wymer, L. and Dufour, A.P. (2008). High sensitivity of children to swimming-associated gastrointestinal illness: Results using a rapid assay of recreational water quality. Epidemiology, 19(3): 375-383.
Wade, T.J., Sams, E., Brenner, K.P., Haugland, R., Chern, E., Beach, M., Wymer, L., Rankin, C.C., Love, D., Li, Q., Noble, R. and Dufour, A.P. (2010). Rapidly measured indicators of recreational water quality and swimming-associated illness at marine beaches: A prospective cohort study. Environ. Health, 9(Article Number 66): 1-14.
Whitman, R.L., Shively, D.A., Pawlik, H., Nevers, M.B. and Byappanahalli, M.N. (2003). Occurrence of Escherichia coli and enterococci in Cladophora (chlorophyta) in nearshore water and beach sand of Lake Michigan. Appl. Environ. Microbiol., 69(8): 4714-4719.
Whitman, R., Harwood, V.J., Edge, T.A., Nevers, M., Byappanahalli, M., Vijayavel, K., Brandao, J., Sadowsky, M.J., Alm, E.W., Crowe, A., Ferguson, D., Ge, Z., Halliday, E., Kinzelman, J., Kleinheinz, G., Przybyla-Kelly, K., Staley, C., Staley, Z. and Solo-Gabriele, H.M. (2014). Microbes in beach sands: Integrating environment, ecology and public health. Rev. Environ. Sci. Biotechnol., 13(3): 329-368.
Whitman, R.L. and Nevers, M.B. (2003). Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Appl. Environ. Microbiol., 69(9): 5555-5562.
WHO (1999). Health-based monitoring of recreational waters: The feasibility of a new approach (the "Annapolis protocol"). Outcome of an expert consultation, Annapolis, MD, co-sponsored by the U.S. Environmental Protection Agency. WHO/SDE/WDH/99.1, Geneva (CH): World Health Organization.
WHO (2003). Guidelines for safe recreational water environments, Volume 1: Coastal and fresh waters. Geneva (CH): World Health Organization.
Wicki, M., Auckenthaler, A., Felleisen, R., Karabulut, F., Niederhauser, I., Tanner, M. and Baumgartner, A. (2015). Assessment of source tracking methods for application in spring water. J. Water. Health, 13(2): 473-488.
Wiedenmann, A., Kruger, P., Dietz, K., Lopez-Pila, J.M., Szewzyk, R. and Botzenhart, K. (2006). A randomized controlled trial assessing infectious disease risks from bathing in fresh recreational waters in relation to the concentration of Escherichia coli, intestinal enterococci, Clostridium perfringens, and somatic coliphages. Environ. Health Perspect., 114(2): 228-236.
Wilkes, G., Edge, T., Gannon, V., Jokinen, C., Lyautey, E., Medeiros, D., Neumann, N., Ruecker, N., Topp, E. and Lapen, D.R. (2009). Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Res., 43(8): 2209-2223.
Wu, J., Long, S.C., Das, D. and Dorner, S.M. (2011). Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. J. Water Health, 9(2): 265-278.
Wymer, L.J., Wade, T.J. and Dufour, A.P. (2013). Equivalency of risk for a modified health endpoint: A case from recreational water epidemiology studies. BMC Public Health, 13(1).
Yamahara, K.M., Walters, S.P. and Boehm, A.B. (2009). Growth of enterococci in unaltered, unseeded beach sands subjected to tidal wetting. Appl. Environ. Microbiol., 75(6): 1517-1524.
Yanko, W.A., De Leon, R., Rochelle, P.A. and Chen, W. (2004). Development of practical methods to assess the presence of bacterial pathogens in water. Water Environment Research Foundation, Alexandria, VA.
Yau, V.M., Schiff, K.C., Arnold, B.F., Griffith, J.F., Gruber, J.S., Wright, C.C., Wade, T.J., Burns, S., Hayes, J.M., McGee, C., Gold, M., Cao, Y., Boehm, A.B., Weisberg, S.B. and Colford Jr., J.M. (2014). Effect of submarine groundwater discharge on bacterial indicators and swimmer health at Avalon beach, CA, USA. Water Res., 59: 23-36.
Yost, C.K., Diarra, M.S. and Topp, E. (2011). Animals and humans as sources of fecal indicator bacteria. In: Sadowsky, M.J. and Whitman, R.L. (eds.). The fecal bacteria. Washington (DC): American Society for Microbiology. p. 67.
Zhi, S., Banting, G., Li, Q., Edge, T.A., Topp, E., Sokurenko, M., Scott, C., Braithwaite, S., Ruecker, N.J., Yasui, Y., McAllister, T., Chui, L. and Neumann, N.F. (2016). Evidence of naturalized stress-tolerant strains of Escherichia coli in municipal wastewater treatment plants. Appl. Environ. Microbiol., 82(18): 5505-18.
Appendix A Abbreviations
- BAV
- Beach action value
- cce
- Calibrator cell equivalent
- cfu
- Colony-forming units
- E. coli
- Escherichia coli
- EHSS
- Environmental health and safety surveys
- GI
- Gastrointestinal illness
- GM
- Geometric mean
- HCGI
- Highly credible gastrointestinal illness
- MPN
- Most probable number
- MST
- Microbial source tracking
- NEEAR
- National epidemiologic and environmental assessment of recreational water
- NOAEL
- No-observed-adverse-effect level
- PCR
- Polymerase chain reaction
- QMRA
- Quantitative microbial risk assessment
- STEC
- Shinga-toxin producing E. coli
- STV
- Statistical threshold value
- UK
- United Kingdom
- US EPA
- United States Environmental Protection Agency
- WHO
- World Health Organization
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