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Introduction and Historical Background

INTRODUCTION

The first outbreak of a waterborne disease to be scientifically documented in modern Western society occurred in London, England, in 1854. This early epidemiology study by John Snow, a prominent local physician, determined that the consumption of water from a sewage-contaminated public well led to cholera (Snow, 1854a,b). This connection, decades before the germ theory of disease would be hypothesized and proven, was the first step to understanding that water contaminated with human sewage could harbor microorganisms that threaten public health. Since then, epidemiology has been the major scientific discipline used to study the transmission of infectious diseases through water (NRC, 1999a).

In the late nineteenth century and throughout the twentieth century, sanitary practices were established in the UnhÚed States regarding the handling and disposal of sewage, while filtration and chlorination systems were increasingly used to disinfect drinking water. Through these historical efforts and owing to ongoing advances in water and wastewater treatment and source water protection, the United States has secured and maintains one of the cleanest and safest supplies of drinking water in the world. Starting in 1920, national statistics on waterborne disease outbreaks caused by microorganisms, chemicals, or of unknown etiology have been collected by a variety of researchers and federal agencies (Lee et al., 2002). These data demonstrate that several outbreaks still occur every year in this country. Moreover, epidemiologists generally agree that these reported outbreaks represent only a fraction of the total that actually occur because many go undetected or unreported (NRC, 1999a). Thus, continued vigilance to protect the public from waterborne disease remains a necessity.



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Indicators for Waterborne Pathogens 1 Introduction and Historical Background INTRODUCTION The first outbreak of a waterborne disease to be scientifically documented in modern Western society occurred in London, England, in 1854. This early epidemiology study by John Snow, a prominent local physician, determined that the consumption of water from a sewage-contaminated public well led to cholera (Snow, 1854a,b). This connection, decades before the germ theory of disease would be hypothesized and proven, was the first step to understanding that water contaminated with human sewage could harbor microorganisms that threaten public health. Since then, epidemiology has been the major scientific discipline used to study the transmission of infectious diseases through water (NRC, 1999a). In the late nineteenth century and throughout the twentieth century, sanitary practices were established in the UnhÚed States regarding the handling and disposal of sewage, while filtration and chlorination systems were increasingly used to disinfect drinking water. Through these historical efforts and owing to ongoing advances in water and wastewater treatment and source water protection, the United States has secured and maintains one of the cleanest and safest supplies of drinking water in the world. Starting in 1920, national statistics on waterborne disease outbreaks caused by microorganisms, chemicals, or of unknown etiology have been collected by a variety of researchers and federal agencies (Lee et al., 2002). These data demonstrate that several outbreaks still occur every year in this country. Moreover, epidemiologists generally agree that these reported outbreaks represent only a fraction of the total that actually occur because many go undetected or unreported (NRC, 1999a). Thus, continued vigilance to protect the public from waterborne disease remains a necessity.

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Indicators for Waterborne Pathogens For more than 100 years, U.S. public health personnel have relied extensively on an indicator organism approach to assess the microbiological quality of drinking water. These bacterial indicator microorganisms (particularly “coliforms,” described later) are typically used to detect the possible presence of microbial contamination of drinking water by human waste. More specifically, fecal indicator bacteria provide an estimation of the amount of feces, and indirectly, the presence and quantity of fecal pathogens in the water. Over the long history of their development and use, coliform test methods have been standardized, they are relatively easy and inexpensive to use, and enumeration of coliforms has proven to be a useful method for assessing sewage contamination of drinking water. In conjunction with chlorination to reduce coliform levels, this practice has led to a dramatic decrease in waterborne diseases such as cholera and typhoid fever. Furthermore, the use of bacterial indicators has been extended to U.S. “ambient” waters in recent decades—especially freshwater and marine-estuarine waters used for recreation. However, an increased understanding of the diversity of waterborne pathogens, their sources, physiology, and ecology has resulted in a growing understanding that the current indicator approach may not be as universally protective as was once thought. In this regard, several limitations of bacterial indicators for waterborne pathogens have been reported and are discussed throughout this report. To protect public health, it is important to have accurate, reliable, and scientifically defensible methods for determining when water is contaminated by pathogens and to what extent. Furthermore, recent and forecasted advances in microbiology, biology, and analytical chemistry make it timely to assess the current paradigm of relying predominantly or exclusively on traditional bacterial indicators for waterborne pathogens in order to make judgments concerning the microbiological quality of water to be used for recreation or as a source for drinking water supply. Committee and Report This report was prepared by the National Research Council (NRC) Committee on Indicators for Waterborne Pathogens—jointly overseen by the NRC’s Board on Life Sciences and Water Science and Technology Board. The committee consists of 12 volunteer experts in microbiology, waterborne pathogens (bacteriology, virology, parasitology), aquatic microbial ecology, microbial risk assessment, water quality standards and regulations, environmental engineering, biochemistry and molecular biology, detection methods, and epidemiology and public health. The report’s conclusions and recommendations are based on a review of relevant technical literature, information gathered at four committee meetings, a public workshop on indicators for waterborne pathogens (held on September 4, 2002), and the collective expertise of committee members. The committee was formed in early 2002 at the request of the U.S. Environ-

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Indicators for Waterborne Pathogens mental Protection Agency (EPA) Office of Water to report on candidate indicators and/or indicator approaches (including detection technologies) for microbial pathogen contamination in U.S. recreational waters (excluding coastal marine water and marine-estuarine water) and source water (including groundwater) for drinking water.1 It is important to note that the committee’s charge, as outlined in its statement of task (see Box ES-1), was slightly but substantively altered after its first meeting and subsequent discussions with EPA, most notably to include coastal and marine-estuarine recreational waters that were originally excluded. As a result, it was agreed that the committee’s report would give less space and emphasis to the importance and public health impacts of waterborne pathogens; place less emphasis on defining currently known waterborne pathogen classes and anticipating those emerging waterborne pathogens that are likely to be of public health concern (although Appendix A provides a brief summary discussion and table of new and [re]emerging waterborne pathogens); exclude consideration of blue-green algae and their toxins; and not specifically consider how the use of candidate indicators might allow for determination of an appropriate level of water treatment needed to protect public health. It is also important to state that although an assessment of suitable indicators for shellfish waters is beyond the scope of this report, some discussion of shellfish experience is included because of the (especially historical) interrelatedness of the various microbial indicator standards and their development. Lastly, this report does not address public swimming and wading pools that are regulated by state and local health departments whose disinfection practices vary widely from place to place. This chapter provides an introduction to the public health importance of waterborne pathogens; a brief summary of key federal laws, regulations, and programs concerning microbial water quality monitoring and especially the use of indicator organisms; the historical development and current use of microbial indicators for waterborne pathogens; and the current status of waterborne disease outbreaks and endemic disease. The chapter ends with a summary of its contents and conclusions. Chapter 2 provides an overview of health effects assessment as related to the current and future use of indicators of waterborne pathogens to help protect public heath. Chapter 3 focuses on the ecology and evolution of waterborne pathogens and indicator organisms by major classes (i.e., viruses, bacteria, protozoa). Chapter 4 assesses the development and uses of indicators and indicator approaches according to their applications and attributes, while Chapter 5 reviews some emerging and innovative approaches for measuring indicator organisms and waterborne pathogens. Lastly, Chapter 6 provides a recommended 1   For the purposes of this report, surface water sources for drinking water and recreational waters can be considered a subset of U.S. “ambient waters” and “waters of the United States” (see footnote 2). As such and per the statement of task, unless noted otherwise all discussion of “water” in this report refers to source water for drinking water (including groundwater) and freshwater, coastal, and marine-estuarine recreational waters.

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Indicators for Waterborne Pathogens phased monitoring framework for selection and use of indicators, along with examples of how to use such a framework. Relevant Laws and Regulations It is beyond the scope of this report to systematically review and discuss all federal, state, or local laws, regulations, and programs that concern the microbiological quality of source water for drinking water and ambient recreational waters. Regarding the latter, state and local governments have primary authority for maintaining the quality and safety of recreational waters (both freshwater and marine). However, given their nationwide application, importance to this report, and direct relevance to the committee’s charge, a brief discussion of the Safe Drinking Water Act (SDWA), Clean Water Act (CWA), Beaches Environmental Assessment and Coastal Health (BEACH) Act of 2000, and several related regulations and programs follows (see also Tables 1-1 and 1-2). Safe Drinking Water Act The SDWA, enacted in 1974 and administered by EPA, is the most important and comprehensive law designed to protect the public from man-made or naturally occurring contaminants in drinking water. It has been amended regularly, including significant changes in 1986 and 1996. Prior to passage of the TABLE 1-1 Microbiological and Other Indicators Used Under EPA’s Drinking Water Regulationsa,b Rule or Program Indicator Use URLs and Notes Total Coliform Rule Total coliforms (TC) Determine treatment efficiency and distribution system integrity http://www.epa/gov/safewater/tcr/tcr.html   Fecal coliforms (FC) Escherichia coli Determine or verify presence of fecal contamination if PWSs obtain sample(s) positive for TC   Surface Water Treatment Rule (SWTR), as amended by the following rules Turbidity Measure of filter efficiency and source water quality http://www.epa.gov/safewater/mdbp/ieswtrfr.pdf Disinfectant residual Nondetection of a disinfectant residual indicates a distribution system problem  

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Indicators for Waterborne Pathogens Rule or Program Indicator Use URLs and Notes Interim Enhanced SWTR Heterotrophic plate count Measure of drinking water quality in distribution system http://www.epa.gov/OGWDW/mdbp/ieswtr.html Long-Term 1 ESWTR TC FC Measure of source water quality (for unfiltered PWSs) http://www.epa.gov/safewater/mdbp/lt1eswtr.html Information Collection Rule (1996-1998) Cryptosporidium Giardia Total culturable viruses TC FC Results provided information to facilitate development of the Long-Term 2 ESWTR http://www.epa.gov/safewater/icr.html Applicable for PWSs serving ≥ 100,000 persons to provide treatment data and monitor disinfection by-products and source water quality parameters Long-Term 2 ESWTR (proposed rule) Cryptosporidium E. coli Determine minimum treatment level needed by surface water system www.epa.gov/safewater/lt2/st2eswtr.html Groundwater Rule (final rule expected in late 2004) E. coli Enterococci Coliphage Determine presence of fecal contamination in source groundwater http://www.epa.gov/safewater/gwr/gwrprop.pdf GWR does not apply to privately owned wells that serve <25 person (e.g., household wells) Drinking Water Contaminant Candidate List (CCL) Virulence-factor activity relationships (under consideration) Assess potential pathogenicity (virulence) of waterborne pathogens as recommended in Classifying Drinking Water Contaminants for Regulatory Consideration (NRC, 2001) www.epa.gov/safewater/ccl/ccl_fr.html www.epa.gov/safewater/ndwac/mem_ccl_cp.html First CCL published in 1998 as required by the SDWA Amendments of 1996, includes 10 pathogens and groups of related pathogens (EPA,1998a) aAs of August 11, 2003. bRefer to actual rules (URLs) for a description of the monitoring requirements. SOURCES: EPA, 2002d; Lee et al., 2002.

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Indicators for Waterborne Pathogens TABLE 1-2 Microbiological and Other Indicators Used Under Select CWA Regulations and Related Programs Activity or Program Indicator Use URLs and Notes Ambient Water Quality Criteria for Bacteria Freshwater: Escherichia coli Enterococci Marine water: Enterococci Determine presence of fecal contamination in ambient and recreational waters http://www.epa.gov/ost/pc/ambientwqc/bacteria1986.pdf Beaches Environmental Assessment and Coastal Health Act of 2000 E. coli Enterococci Proposed rapid methods such as Bioluminometer Fiber optics System flow cytometry Rapidly determine presence of fecal contamination in freshwater and marine recreational waters http://www.epa.gov/ORD/WebPubs/beaches/ Shellfish Program Total coliforms (TC) Fecal coliforms (FC) E. coli Help ensure shellfish waters are adequately protected from microbial contamination http://www.epa.gov/waterscience/shellfish/ Biosolids (Treated Sewage Sludge) Program FC Salmonella Enteric viruses Viable helminth ova Adequacy of sludge treatment practices to protect human and environmental health http://www.epa.gov/owmitnet/mtb/biosolids/ See also (NRC, 2002) http://cfpub.epa.gov/npdes/ National Pollutant Discharge Elimination System (NPDES Permitting Program) TC FC Fecal streptococci Ensure ambient water quality standards are maintained despite pollutant discharges   305(b) Water Quality Assessment Report Program Varies by state Determine if waters meet state-determined ambient water quality standards http://www.epa.gov/owow/monitoring/guidelines.html http://www.epa.gov/owow/tmdl/2002wqma.html See also Table 1-3 303(d) Impaired Waters List and Total Maximum Daily Load (TMDL) Program Varies by state Determine if waters meet state-determined ambient water quality standards http://www.epa.gov/ http://www.epa.gov/owow/tmdl/ http://www.epa.gov/owow/tmdl/pathogen_all.pdf http://www.epa.gov/owow/tmdl/examples/pathogens.html http:///www.epa.gov/owow/tmdl/2002wqma.html   SOURCE: EPA, 2002d.

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Indicators for Waterborne Pathogens SDWA, the only enforceable federal drinking water standards were for waterborne pathogens in water supplies used by interstate carriers such as buses and trains. Interested readers should refer to Safe Water from Every Tap: Improving Water Service to Small Communities (NRC, 1997) for an overview of the development of drinking water supply regulations in the United States to include the SDWA, or to Pontius and Clark (1999) for a more thorough discussion of the SDWA and its subsequent amendments. Under the SDWA, microbial contamination is regulated primarily under the Total Coliform Rule (TCR) and the Surface Water Treatment Rule (SWTR), both originally promulgated in 1989 (EPA, 1989a,b, 1990). Under the TCR, all public water systems (PWSs) are required to routinely collect total coliform samples at sites that are considered representative of water throughout the distribution system. The SWTR covers all drinking water systems using surface water or groundwater systems that rely on surface water, requiring them to disinfect their water, while most must also filter (unless they meet EPA-stipulated filter avoidance criteria). The SWTR is intended to protect the public from exposure to the intestinal protozoan parasite Giardia lamblia and viruses through a combination of removal (filtration) and inactivation (disinfection) (EPA, 1989a). In 1998, EPA promulgated the Interim Enhanced Surface Water Treatment Rule (IESWTR; EPA, 1998c), which builds on the SWTR and includes more stringent requirements related to the performance of filters used in drinking water treatment to protect against the protozoan parasite Cryptosporidium and other pathogens for systems that serve more than 10,000 persons. Similarly, EPA promulgated and finalized the Long-Term 1 Enhanced Surface Water Treatment Rule (LT1ESWTR) requiring PWSs that serve less than 10,000 persons (EPA, 2002a) to meet more stringent filtration requirements. In addition, EPA recently proposed a Long-Term 2 Enhanced Surface Water Treatment Rule (LT2ESWTR) that will provide additional protection against Cryptosporidium and will apply to all systems using surface water or groundwater under the influence of surface water (EPA, 2003b). All PWSs will be assigned to a water treatment category (“bin”) based on Cryptosporidium concentrations in their source water; the category determines how much additional treatment is required. In 2000, EPA proposed the Ground Water Rule (GWR) in response to the SDWA Amendments of 1996 that mandate the development of regulations for the disinfection of groundwater systems as necessary to protect public health (EPA, 2000b). The GWR had not yet been finalized as this report neared publication in early 2004. Table 1-1 summarizes these and other existing and proposed rules and programs concerning the use of pathogens under the auspices of the SDWA and EPA. Clean Water Act Growing public awareness of and concern for controlling water pollution nationwide led to enactment of the Federal Water Pollution Control Act (FWPCA;

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Indicators for Waterborne Pathogens originally enacted in 1948) Amendments of 1972. Together with the Clean Water Act of 1977 and the Water Quality Act of 1987—both of which amended and reauthorized the FWPCA—it provides the foundation for protecting the nation’s surface waters. Collectively, they are referred to as the Clean Water Act, and that usage is maintained throughout this report. The CWA is of central importance to this report in that it is a comprehensive statute intended to restore and maintain the chemical, physical, and biological integrity of the waters of the United States.2 To accomplish this, the CWA sought to attain a level of water quality that “provides for the protection and propagation of fish, shellfish, and wildlife, and provides for recreation in and on the water” by 1983 and to eliminate the discharge of pollutants into navigable waters by 1985. Primary authority for implementation and enforcement of the CWA rests with the EPA. In addition to measures authorized before 1972, the CWA authorizes water quality programs; requires federal effluent limitations for wastewater discharges to surface waters and publicly owned treatment works (i.e., municipal sewage treatment plants) and ambient water quality standards;3 requires permits for discharge of pollutants4 into waters of the United States; provides enforcement mechanisms; and authorizes funding for wastewater treatment works construction grants and state revolving loan programs, as well as funding to states and tribes for their water quality programs. Provisions have also been added to address water quality problems in specific regions and specific waterways, and the CWA has been amended almost yearly since its inception. Due consideration must be given to the improvements necessary to conserve these waters for the protection and propagation of fish and 2   As defined in the CWA, “waters of the United States” applies only to surface waters, rivers, lakes, estuaries, coastal waters, and wetlands. However, not all surface waters are legally waters of the United States, and the exact division between waters of the United States and other waters can be difficult to determine. In addition, it is important to note that the CWA does not deal directly with groundwater or water quantity issues; see http://www.epa.gov/r5water/cwa.htm or http://www.epa.gov/watertrain/cwa/ for further information about the CWA. 3   Ambient water quality standards (AWQSs) are determined by each state (collectively includes territories, American Indian tribes, the District of Columbia, and interstate commissions of the United States) and consist of (1) designated beneficial uses (e.g., aquatic life support, drinking water supply, primary contact recreation); (2) narrative and numeric criteria (ambient water quality criteria, or AWQC; discussed later) for biological, chemical, and physical parameters to meet designated use(s); (3) antidegradation policies to protect existing uses; and (4) general policies addressing implementation issues (e.g., low flows, variances). State water quality standards have become the centerpiece around which most surface water quality programs revolve; for example, they serve as the benchmark for which monitoring data are compared to assess the health of waters and to list impaired waters under CWA Section 303(d) (discussed later). 4   As authorized by the CWA (Section 402), the National Pollutant Discharge Elimination System (NPDES) Permitting Program controls water pollution by regulating point sources (e.g., discrete conveyances such as pipes or man-made ditches) that discharge pollutants into waters of the United States.

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Indicators for Waterborne Pathogens aquatic life and wildlife, recreational purposes, and the withdrawal of water for public water supply, agricultural, industrial, and other purposes. Not surprisingly, EPA conducts a wide variety of programs and activities related to the monitoring of indicators for waterborne pathogens under the CWA as summarized in Table 1-2. It is important to note, however, that many of these listed programs and activities lie outside the committee’s charge. Regarding the attainment of water quality standards, Section 305(b) of the CWA requires states and other jurisdictions (e.g., American Indian tribes, District of Columbia) to assess and submit to EPA the health of their waters and the extent to which their water quality standards are being met every two years. In 2002, EPA released the 2000 National Water Quality Inventory (NWQI; EPA, 2002c)—the thirteenth installment in a series that began in 1975. These NWQI reports (commonly called “305(b) reports”), as the biannual culmination of the 305(b) process, are considered by EPA to be the primary vehicle for informing Congress and the public about general water quality conditions in the United States5 (EPA, 1997). As such, the reports characterize water quality, identify widespread water quality problems of national significance, and describe various programs implemented to restore and protect U.S. waters. Notably, states use bacterial indicators—although specific indicators, methods, and sampling practices vary from state-to-state—to determine whether waters are safe for swimming and drinking (i.e., support designated beneficial uses). Table 1-3 summarizes select findings from the 2000 NWQI report (EPA, 2002c) related to the identification of surface waters impaired by pathogens (predominantly bacteria). In addition to establishing water quality standards, and similar to Section 305(b) of the CWA, Section 303(s) of the CWA requires states to identify waters not meeting ambient water quality standards and include them on their 303(d) list of impaired waters. Section 303(d) also requires states to define the pollutants and sources responsible for the degradation of each listed water, establish total maximum daily loads (TMDLs6) necessary to attain those standards, and allocate responsibility to sources for reducing their pollutant releases. The CWA further requires that water quality standards be maintained once obtained and that EPA must approve or disapprove all lists of impaired waters and TMDLs established by states (NRC, 2001). If a state submission is inadequate, EPA must establish the list or the TMDL. Consistent with the latest NWQI report (EPA, 2002c), in 2000 EPA released 5   Although positive advances have been made in recent NWQI reports, groundwater data collection under 305(b) is still too undeveloped to allow comprehensive national assessments of groundwater quality (EPA, 2002c). 6   A TMDL can be defined as the sum of the allowable loads of a single pollutant from all contributing point and nonpoint sources that includes a margin of safety to ensure the waterbody can be used for all the purposes the state has designated. The calculation must also account for seasonal variation in water quality.

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Indicators for Waterborne Pathogens TABLE 1-3 Selected Findings and Results from the 2002 National Water Quality Inventory Waterbody Type Total Sizea Amountb Assessed (% of Total) Coastal resources: Ocean shoreline waters 58,618 miles 3,221 miles (6%) Rivers and streams 3,692,830 miles 699,946 miles (19%) Coastal resources: Estuaries 87,369 sq. miles 31,072 sq. miles (36%) Coastal resources: Great Lakes shoreline 5,521 miles 5,066 miles (92%) Lakes, reservoirs, and ponds 40,603,893 acres 17,339,080 acres (43%) aUnits are miles for rivers and streams; acres for lakes, reservoirs, and ponds; and square miles for coastal resources (estuaries, Great Lakes shoreline, and ocean shoreline waters). bIncludes waterbodies assessed as not attainable for one or more designated uses (i.e., total number of waterbody units assessed as good and impaired do not necessarily add up to total assessed). Atlas of America’s Polluted Waters (EPA, 2000a), which states that about 21,000 river segments, lakes, and estuaries encompassing more than 300,000 river and shore miles and 5 million lake acres have been reported as impaired by states and that the second leading cause of impairments (behind sedimentation or siltation) is “pathogens.”7 As for the 305(b) reports, states rely primarily on bacterial indi- 7   Although the reported terminology for “pathogens” varies considerably and in many cases is unspecified, it includes primarily variations in coliforms but also includes Escherichia coli and enteric viruses (EPA, 2000a).

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Indicators for Waterborne Pathogens Impairedc (% of Assessed) Impaired by Pathogens (Bacteria; % of Impaired) Top Five Leading Pollutants and Causes of Impairmentd 434 miles (14%) 384 miles (88.5%) Pathogens (bacteria) Oxygen-depleting substances Turbidity Suspended solids Oil and grease 269,258 miles (39%) 93,431 miles (34.7%) Pathogens (bacteria) Siltation Habitat alteration Oxygen-depleting substances Nutrients 15,676 sq. miles (51%) 4,754 sq. miles (30%) Metals Pesticides Oxygen-depleting substances Pathogens (bacteria) Priority toxic organic chemicals 3,955 miles (78%) 102 miles (9.3%) Priority toxic organic chemicals Nutrients Pathogens (bacteria) Sedimentation or siltation 7,702,370 acres (45%) Not reported Nutrients Metals Siltation Total dissolved solids Oxygen-depleting substances cPartially or not supporting one or more designated uses. dFor states and jurisdictions that report this type of information (i.e., often a subset of the total number of states and jurisdictions that assess and report on various waterbodies; see EPA, 2002e for further information). SOURCE: Adapted from EPA, 2002c. cators rather than specific pathogens to assess whether waters are achieving their standards and to develop TMDLs. Indeed, EPA estimates that from 3,800 to 4,000 TMDLs will have to be completed per year to meet typical 8- to 13-year dead-lines imposed on the process (NRC, 2001). It is beyond the scope of this report to discuss the 303(d) TMDL process in any detail. Rather, please refer to the 2001 NRC report Assessing the TMDL Approach to Water Quality Management, which reviews the program at the request of Congress and provides many recommendations for its comprehensive improvement. For example, based on that report, EPA

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Indicators for Waterborne Pathogens FIGURE 1-3 Number of waterborne disease outbreaks by illness and water type in the United States: 1989-2000 (n = 278). *AGI denotes acute gastrointestinal illness of unknown etiology. **PAM denotes primary amoebic meningoencephalitis (see Chapter 3 for further information). SOURCE: Outbreak data through 2000 from the CDC’s National Waterborne Diseases Outbreak Surveillance System. unknown etiology are most likely to be associated with groundwater sources because these outbreaks are widely thought to be caused predominantly by viruses, which are difficult to identify in clinical specimens and even more so in water samples (NRC, 1999a). Gastrointestinal outbreaks of known viral etiology were also more likely to occur in groundwater systems. Surprisingly, gastrointestinal illnesses of parasitic origin also were somewhat more likely to be associated with groundwater systems, probably because some of these systems are actually groundwater under the influence of surface water. Gastrointestinal outbreaks of drinking water supplies from bacteria and viruses were rare in surface water systems since these microorganisms are readily killed by conventional treatment practices. While gastrointestinal outbreaks associated with bacteria were most commonly reported in ambient recreational waters, outbreaks of dermatitis and cases of primary amoebic meningoencephalitis were associated only with recreational water. The “other” illness category includes one outbreak each of leptospirosis, legionellosis, and keratitis in ambient waters and one outbreak associated with algae in a surface water system. The outbreak data summarized in Figures 1-1 through 1-3 demonstrate that the association between various pathogens and human health effects differs depending on the type of water system involved. If indicators for waterborne patho-

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Indicators for Waterborne Pathogens gens are to be used to predict the likelihood of water contamination with potential ensuing health effects, it is unlikely that a single indicator will suffice for these different routes of exposure. For these and other reasons, epidemiologic studies are needed to establish the causal link between the presence and density of an indicator and the associated health effects under a variety of environmental conditions. Surveillance for waterborne disease outbreaks and epidemiologic study designs are discussed further in Chapter 2. Endemic Waterborne Disease In 1991, Payment and colleagues reported the results of the first randomized intervention trial (i.e., in which investigators control the conditions of exposure) to evaluate whether the consumption of tap water that met current Canadian microbiological standards was associated with an increased risk of gastrointestinal disease. They compared illness rates in households drinking tap water and households drinking reverse osmosis-filtered water, which were considered pathogen free (Payment et al., 1991). The trial estimated that 35 percent of the reported gastrointestinal illness among persons drinking tap water was associated with its consumption. In 1997, Payment and colleagues conducted a follow-up intervention trial to confirm the previous results and to attempt to determine the source(s) of the illnesses (Payment et al., 1997). This second study attributed 14-40 percent of gastrointestinal illness to consumption of tap water meeting current Canadian water treatment standards. These two studies are described in more detail in Chapter 2. Researchers’ interest in the possible contribution of drinking water that met current treatment standards to the incidence of gastrointestinal illness was heightened as a result of the Payment studies and the continuing occurrence of waterborne disease outbreaks in the United States and elsewhere. As noted previously, Congress responded with new mandates in the 1996 SDWA amendments, and CDC and EPA entered into an interagency agreement in 1997 in response to the congressional mandate to conduct studies and develop a national estimate of endemic waterborne disease. The SDWA amendments were interpreted to mean that the focus of efforts should be directed at municipal drinking water. The amendments did not specify which waterborne diseases were to be studied, and after conducting several workshops, the two agencies determined that the health outcome that would be studied in this initial effort would be gastrointestinal disease. Based on this interagency agreement, CDC has funded cooperative agreements with academic institutions to conduct two pilot intervention trials of home water treatment in households and one full-scale intervention trial along with several related “nested” epidemiology studies to help maximize the benefit of the large-scale trial. Each of these studies is reviewed in Chapter 2 along with related (including three community intervention trials conducted by EPA) studies of en-

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Indicators for Waterborne Pathogens demic waterborne disease. In addition, questions regarding water consumption patterns and usage behavior were added to CDC’s yearly cross-sectional survey for FoodNet (CDC, 1996; see Chapter 2 for further information) beginning with the 1998-1999 cycle. As part of the BEACH Program, EPA will be conducting new epidemiologic studies intended to correlate water quality with human health effects. The health outcomes will include gastrointestinal disease as well nongastrointestinal health outcomes in eyes, ears, skin, and the respiratory system (Rebecca Calderon, EPA, personal communication, 2002). Beach site selection criteria will include point source contamination, range of exposures, population size, geographic variety, and historical microbial testing. A pilot study was conducted during summer 2002 at one freshwater recreational beach (Indiana Dunes National Lakeshore). The current projected time line includes full-scale studies at three beaches each summer from 2003 to 2005 for a total of nine beaches. Data analysis and report preparation are expected to be completed in 2006 (see Chapter 2 for further information). All of the aforementioned studies focus on health effects associated with water of varying quality. This water quality is measured using many methods and parameters. Because pathogens are difficult to detect in water, surrogates or indicators are often used in their stead. The following section describes the indicators for waterborne pathogens that are currently in use and provides an overview of the issues associated with the selection of appropriate indicators for waterborne pathogens. CURRENT INDICATORS FOR WATERBORNE PATHOGENS In the United States, predominantly bacterial indicators are used to determine (1) if drinking water sources are microbiologically safe, (2) if treatment of drinking water has been adequate, (3) if drinking water in the distribution system continues to be protected, and (4) if recreational and shellfish waters are microbiologically safe (see also Tables 1-1 and 1-2). Each of these test objectives has different requirements, and it is not likely that any one indicator or system of indicators can adequately meet all of these needs. For example, for recreational waters, shellfish waters, and source waters for drinking water, the question being addressed is the same, namely: Has this water been exposed to significant microbiological contamination? However, complexities of several kinds come into play. First, it is important to know something about the type and source of contamination, particularly if the contamination is of fecal or nonfecal origin. At the time the coliform index was conceived, contamination by human feces was clearly the central public health issue to be addressed. Since that time it has become clear that although contamination with human fecal matter is clearly of profound and continuing public health significance, human pathogens occur in other environ-

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Indicators for Waterborne Pathogens ments as well. For example, based on the preceding discussion it is clear that animal fecal matter can be of particular significance and that the widespread use of antibiotics for animal growth promotion, as well as for control of animal diseases, may constitute an important source of antibiotic-resistant pathogens (NRC, 1999b). Finally, some enteric waterborne pathogens have natural reservoirs in the environment where they can proliferate (see Chapter 3 for further discussion of these issues). Moreover, some nonenteric waterborne pathogens are capable of proliferating in waters under the right conditions, and human exposure to the high concentrations resulting from this proliferation can create human health risks. An example is Legionella pneumophila, which proliferates in warm waters containing sediments and nutrients (e.g., institutional hot water systems) and causes respiratory disease through inhalation of aerosolized water (Kaufman et al., 1981). The specific application and geographic location can also have an impact on selection of the most important indicator candidates. For example, some indicators will be more useful in temperate zones than in the subtropics, some will be more effective in surface water than in groundwater sources of drinking water, and some will be more useful in freshwaters than in marine recreational waters. Finally, a different set of indicator attributes will come into play when the effectiveness of treatment or the integrity of a drinking water distribution system is at issue (though the latter are excluded from explicit consideration in the committee’s charge). These and related issues are discussed and illustrated at length in this report, especially in Chapters 4 and 6. The timeliness of the indicator system is also more important in some applications than in others. For example, in the case of recreational waters, the results of current bacterial indicator tests are often tied directly and immediately to a decision to allow or restrict public access (see Chapter 4 for further information). It is essential that indicator systems used in such applications provide timely results because swimmers may be exposed to unacceptable levels of pathogens while the analysis is being conducted. Furthermore, beach contamination is often episodic and of short duration and a long turnaround on an indicator test runs the risk that the public is allowed access to unsafe waters, but denied access when the episode has already past (Boehm et al., 2002). Drinking water supplies generally face different requirements for indicators for waterborne pathogens. It is sometimes possible to use indicator measurements alone to divert or avoid a water supply during a contamination episode. However, it is more common to use indicators in conjunction with other measures (e.g., sanitary surveys) to assess the overall microbiological risk associated with a given water supply source and to address that contamination by removing its source and/or installing (additional) treatment systems to serve as a protective barrier. For assessments of this sort, the accuracy and specificity of the indicator system are more important than the timeliness of the result.

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Indicators for Waterborne Pathogens SUMMARY AND CONCLUSIONS To protect public health, and as mandated in the SDWA and CWA, it is important to have accurate, reliable, and scientifically defensible methods for determining whether source waters for drinking water and recreational waters are contaminated by pathogens and to what extent. In this regard, the development and use of bacterial indicators for waterborne pathogens began more than a century ago, when contamination of drinking waters by enteric bacterial pathogens originating from human waste constituted a major public health threat. The use of bacterial indicators (predominantly coliforms) was later expanded and adopted for use in ambient, recreational, and shellfish waters and continues to focus on identification of fecal contamination, principally of human origin. As such, the current indicator approaches have become standardized; are relatively easy and inexpensive to use; and constitute a cornerstone of local, state, and federal monitoring and regulatory programs. Although these approaches have been extremely effective in reducing waterborne disease outbreaks caused by human enteric bacteria, it is now widely understood that bacteria are not the only pathogens of public health concern; fecal contamination is not the only significant potential source of waterborne microbial pathogens; and many human pathogens and indicator organisms occur in other environments. The number of reported disease outbreaks associated with drinking water peaked in the early 1980s, declined for more than 10 years, and increased from 1997 through 2000, although the number of persons affected has remained comparable to previous years. Recreational water outbreaks associated with ambient water did not show a specific trend. Better detection methods in clinical specimens as well as in water samples have increased the identification of pathogens, most notably viruses. Despite these improvements, the etiologic agent remains unknown for a large percentage of drinking water and recreational water outbreaks, making the selection and use of indicators for waterborne pathogens very complex. An increased understanding of the diversity of waterborne pathogens, their sources, physiology, and ecology has resulted in a growing understanding that the use of bacterial indicators may not be as universally protective as once thought. For example, the superior environmental survival of important waterborne viruses and protozoa raised serious questions about the suitability of relying on relatively short-lived coliforms as indicators of the microbiological quality of water. That is, while the presence of coliforms could still be taken as a sign of fecal contamination, the absence of coliforms could no longer be taken as assurance that water was uncontaminated. Thus, existing bacterial indicators and indicator approaches do not in all circumstances identify all potential waterborne pathogens. Indeed, the committee concludes that no single indicator organism or small set of indicators can successfully identify or predict the presence, let alone the source, of all classes of potential pathogens—especially emerging microor-

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Indicators for Waterborne Pathogens ganisms. Furthermore, recent and forecasted advances in microbiology, molecular biology, and analytical chemistry make it timely to assess the current paradigm of relying predominantly or exclusively on traditional bacterial indicators for waterborne pathogens to make judgments concerning the microbiological quality of source waters for drinking water and recreational waters. Nonetheless, indicator approaches will still be required for the foreseeable future since it is not practical or feasible to monitor for the complete spectrum of microorganisms that may occur in source waters for drinking water and recreational waters, and many known pathogens are difficult to detect directly and reliably in water samples. Lastly, improvements in the timeliness of indicator analysis (i.e., rapidity of results) are needed if exposure to pathogen-contaminated water is to be prevented or controlled in a timely manner that protects public health. REFERENCES Andrewes, F.W., and T.J. Horder. 1906. A study of the streptococci pathogenic for man. Lancet 2: 708-713. APHA (American Public Health Association). 1949. Standard Methods for the Examination of Water and Wastewater, 10th Edition. Washington, D.C. APHA. 1965. Standard Methods for the Examination of Water and Wastewater, 12th Edition. Washington, D.C. APHA. 1998. Method 9221(3) or Method 9222 (d) in Standard Methods for the Examination of Water and Wastewater, L. Clesceri, A. Greenberg, and A. Eaton, eds., 20th Edition. Washington, D.C. Ashbolt, N.J., W.O.K. Grabow, and M. Snozzi. 2001. Indicators of microbial water quality. Chapter 13 in Water Quality—Guidelines, Standards and Health: Assessment of Risk and Risk Management for Water-Releated Infectious Disease, L. Fewtrell and J. Bartram, eds., London: World Health Organization and IWA Publishing. Bartram, J., and G. Rees. 2000. Monitoring Bathing Waters: A Practical Guide to the Design and Implementation of Assessments and Monitoring Programmes. Geneva: World Health Organization. Barwick, R.S., D.A. Levy, G.F. Craun, M.J. Beach, and R.L. Calderon. 2000. Surveillance for waterborne-disease outbreaks—United States, 1997-1998. MMWR 49 (No. SS-4): 1-35. Bermudez, M., and T.C. Hazen. 1988. Phenotypic and genotypic comparison of Escherichia coli from pristine tropical waters. Applied and Environmental Microbiology 54: 979-983. Boehm, A., S. Grant, J. Kim, S. Mowbray, C. McGee, C. Clark, D. Foley, and D. Wellman. 2002. Decadal and shorter period variability of surf zone water quality at Huntington Beach, CA. Environmental Science and Technology 36(18): 3885-3892. Bonde, G.J. 1963. Bacteria indicators of water pollution. Teknisk Forlag, Copenhagen 221-226. Bonde, G.J. 1966. Bacteriological methods for the estimation of water pollution. Health Laboratory Science 3: 124. Bonde, G.J. 1975. Bacteria indicators of sewage pollution. Pp. 37-47 in Discharge of Sewage from Sea Outfalls: Proceedings of an International Symposium, A.L.H. Gameson, ed. New York: Pergamon Press. Bruce-Grey-Owen Sound Health Unit. 2000. The Investigative Report of the Walkerton Outbreak of Waterborne Gastroenteritis May-June, 2000. Ontario Ministry of Health. Owen Sound, Ontario. Budd, W. 1856. Outbreak of fever at clergy orphanage. Lancet: 15 November. Burman, N.P. 1961. Some observations on coli-aerogenes bacteria and streptococci in water. Journal of Applied Bacteriology 24: 368.

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