### Appendix C.1: Review of Published Studies to Characterize Relative Risks

from Different Sources of Fecal Contamination in Recreational Water, EPA

822

- R

- 09

- 001EPA 822-R-09-001



## REVIEW OF PUBLISHED STUDIES TO CHARACTERIZE

RELATIVE RISKS FROM DIFFE RENT SOURCES OF FECAL

CONTAMINATION IN RECREATIONAL WATER

U.S. Environmental Protection Agency

Office of Water Health and Ecological Criteria Division

February 2009[this page intentionally left blank]U.S. Environmental Protection Agency

February 2009 i 

## D ISCLAIMER

This document has been reviewed in accordance with U.S. Environmental Protection Agency policy and approved for publication. Mention of trade names or commercial products does not

constitute endorsement or recommendation for use.[this page intentionally left blank]U.S. Environmental Protection Agency

February 2009 iii 

## A CKNOWLEDGMENTS

Questions concerning this document or its app lication should be addressed to the EPA Work Assignment Manager:

John Ravenscroft USEPA Headquarters Office of Science and Technology, Office of Water 1200 Pennsylvania Avenue, NW

Mail Code: 4304T Washington, DC 20460

Phone: 202-566-1101

Email: ravenscroft.john@epa.gov

This literature review was managed under EPA Contract EP-C-07-036 to Clancy Environmental Consultants, Inc. The following individuals c ontributed to the development of the report:

Lead Writer: Jeffery Soller Soller Environmental

Leiran Biton ICF International

Alexis Castrovinci ICF International Jennifer Clancy Clancy Environmental Consultants Mary Clark ICF International Martha Embrey ICF International

Mark Gibson ICF International Kelly Hammerle ICF International

Ami Parekh ICF International

Katherine Sullivan ICF International

Elizabeth Zelasko ICF International

Jennifer Welham ICF International[this page intentionally left blank]U.S. Environmental Protection Agency

February 2009 v 

## T ABLE OF 

## C ONTENTS

A CKNOWLEDGMENTS

.............................................................................................................................. ................... iii

T ABLES AND F IGURES

.............................................................................................................................. ................... vii

A CRONYMS

.............................................................................................................................. ..................................... ix

E XECUTIVE S UMMARY

.............................................................................................................................. ................... 1

I. B ACKGROUND AND I NTRODUCTION .................................................................................................................... 5

I.1 Background: Cont ext and Purpose .............................................................................................. .............. 5

I.2 Introduc tion

.................................................................................................................. .............................. 6

II. M ETHODS

.............................................................................................................................. ............................. 10

III. R ESULTS : R ECREATIONAL W ATER E PIDEMIOLOGICAL S TUDIES .................................................................. 12

III.1 Overview of Recreational Wate r Epidemiological Studies ...................................................................... 1 2

III.2 Descriptions of Key Recreational Water Epidemiological Studies .......................................................... 14

III.2.1 Selected Recreational Wa ter Epidemiological Studies Base d on Human Sources of Fecal

Contamination ................................................................................................................. ............ 14

III.2.2 Selected Recreational Water Epidemiology Studies Based on Nonwastewater Effluent

Sources of Fecal Contamination ................................................................................................ .. 24

IV. O UTBREAK R EPORTS FOR R ECREATIONAL AND D RINKING W ATERS ............................................................. 31

IV.1 Waterborne Disease Surveillance and Outbre ak Reporting in th e United States ..................................... 31

IV.2 Summary of CDC Surveillance Re ports on Drinki ng Wate r ................................................................... 31

IV.3 Summary of Selected Drinking Water Outbreaks Repo rted in the United States and Internationally ..... 32

IV.4 Descriptions of Drinking Water Outbreaks with Animal Related-Pathogen Sources .............................. 42

IV.5 Summary of Selected Recr eational Water Outbreaks .............................................................................. 43

IV.6 Summary of Selected Recreational Water Outb reaks Reported in th e United States and

Internatio nally ............................................................................................................... ........................... 57

IV.7 Descriptions of Recreational Water Outbreak s with Animal Related-Pathogen Sources ........................ 57 IV.7.1 Environmental Sampling Including Animal Sources .................................................................. 57

IV.7.2 Environmental Sampling no t Including Animal Sources ............................................................ 62

V. C OMPILATION OF D ATA AND S UMMARY ........................................................................................................... 63

VI. R EFERENCES

.............................................................................................................................. ........................ 68

A PPENDIX A: L ITERATURE S EARCH S TRATEGY AND R ESULTS ............................................................................. A-1[this page intentionally left blank]U.S. Environmental Protection Agency

February 2009 vii 

## T

ABLES AND 

## F IGURES

Table I.2.1. Representative Fecal Indicator Bacteria an d Zoonotic Pathogen Densities in Human and Animal Feces and Sewage .................................................................................................................... ................................................ 8

Table III.1.1. Recreational Water Epidemiology Studies In cluded in Reviews by Prüss (1998), Wade et al. (2003),

and Zmirou et al. (2003) ...................................................................................................... ........................................ 13

Table III.1.2a. Recently Completed Recreational Wate rs Epidemiological Studies—Some of Which Address Nonpoint Sources of Fecal Contam ination ....................................................................................... ........................... 15

Table III.1.2b. Ongoing Recreational Waters Epidemio logical Studies—Some of Which Address Nonpoint Sources

of Fecal Cont amination ........................................................................................................ ....................................... 16

Table IV.2.1. Select Waterborne Dis ease Outbreaks Associated with Drinking Water in the United States Reported by the CDC (199 9 to 2004) ..................................................................................................... .................................... 34

Table IV.3.1. Select Waterborne Disease Ou tbreaks Associated w ith Drinking Water ............................................. 38

Table IV.5.1. Select Waterborne Disease Outbreaks As sociated with Recreational Water in the United States Reported by the CD C (1999 to 2004) ............................................................................................ .............................. 45

Table IV.6.1. Select Waterborne Disease Ou tbreaks Associated with Recreationa l Water ........................................ 58[this page intentionally left blank]U.S. Environmental Protection Agency

February 2009 ix 

## A CRONYMS

AWQC

BEACH Act ambient water quality criteria

Beaches Environmental Assessment and Coastal Health Act

CCDR

CDC Canada Communicable Disease Report

U.S. Centers for Disease Control and Prevention

CFU

CI colony forming unit

confidence interval

DNA

EC

EEC

EPA

GI deoxyribonucleic acid European Commission European Economic Community U.S. Environmental Protection Agency

Gastrointestinal

HUS

MMWR

MPN

NM hemolytic uremic syndrome Morbidity and Mortality Weekly Report most probably number

nonmotile

NOAEL no-observed-adverse-effect-level

NRC National Research Council

PCR QMRA polymerase chain reaction Quantitative microbial risk assessment

SCCWRP

U.S. Southern California Co astal Water Research Project

United States

WHO

WSAA World Health Organi zation (United Nations)

Water Services Association of Australia[this page intentionally left blank]U.S. Environmental Protection Agency

February 2009 1 

## E XECUTIVE 

## S UMMARY

Introduction

The overall goal of the current ambient water quality criteria for bacteria in the United States is to provide public health protection from gastroen teritis (gastrointestinal [GI] illness) associated with exposure to fecal contamin ation during water-contact recrea tion. Because fecal matter can be a major source of pathogens in ambient water, and because it is not practical or feasible to monitor for the full spectrum of all pathogens that may occur in wa ter, water quality criteria are specified throughout the world in te rms of fecal indicator organism densities. For decades, these fecal indicator organisms have served as surr ogates for potential pathogens and subsequent

health risks in both recreati onal and drinking waters.

The U.S. Environmental Protection Agency’s (EPA) recommended recreational water quality

criteria do not differentiate betw een fecal sources of pathogens. Thus, EPA’s regulatory premise concerning recreational water quality has been that nonhuman-derived human pathogens in fecally contaminated waters are as hazardous as their human-derived c ounterparts. The World Health Organization’s (WHO) recommended appr oach for classifying the water quality of recreational waters is based on the premise that the measure of microbiological indicators of fecal contamination can be “interpreted” using evidence of the presence or absence of human fecal contamination. This approach assumes that in general, sources other than human fecal

contamination are less of a risk to human health. WHO indicated in their 2003 report Health Based Monitoring of Recreational Waters: The Feasibility of a New Approach (The “Annapolis

Protocol” ) that “due to the species barrier, the density of pathogens of public health importance is generally assumed to be less in aggregate in animal excreta than in human excreta and may therefore represent a significantl y lower risk to human health.”

Ultimately, the critical question is whether exposu re to different fecal sources from recreational waters translates to significant differences in the risk of human infection or disease severity. The purpose of this white paper is to describe the existing knowledgebase ava ilable to characterize

the relative risks of human illness from various sources of fecal contamination in recreational waters. Information related to human exposures to pathogens in fecally contaminated recreational and drinking waters was obtained by searching the scientific literature for epidemiological studies related to exposure to recreational waters and reports of outbreak investigations from both recr eational and drinking waters.

Recreational Water Epidemiological Studies

Numerous epidemiological investigations have been conducted since th e 1950s to evaluate the

association between illness risk to recreational water users and the density of suitable fecal

indicators. These studies have been conducted in Australia, Canada, Egypt, France, Hong Kong, Israel, the Netherlands, New Z ealand, Spain, South Africa, Un ited States, and the United Kingdom. Importantly, most of these studies in vestigated waters that were impacted or influenced by wastew ater effluent.U.S. Environmental Protection Agency

February 2009 2 Taken as a whole, the weight of evidence from these studies in dicates that fecal indicator bacteria are able to predict GI and respirator y illnesses from exposure to recreational waters. However, as indicated above, most of these studies investigated waters that were impacted or influenced by wastewater effluent , and close inspection of this base of information reveals that

few studies addressed sources of contamination other than wastewater efflue nt in the investigated waters. Prior to 1999, only three peer-reviewed pub lications addressed this topic substantially (Calderon et al., 1991; Cheung et al., 1990; McBride et al., 1998). In the last few years, researchers have conducted several additional ep idemiological studies focusing on waters not predominately impacted by wastewater effluent. Additionally, the Southe rn California Coastal Water Research Project (SCCWRP) is also conduc ting a series of epidemiological studies that investigate recreational water with various contamin ation sources other than wastewater effluent.

Review of the epidemiological studies that address recreational water predominantly impacted by sources other than wastewater effluent indicates that the resu lts are equivocal. For example, Colford et al. (2007) found that the incidence of swimmer illness was not a ssociated with any of

the traditional fecal indicators at a marine beach with primarily avian contamination. This result is substantially different than those studies described above on wa stewater impacted waterbodies. Whereas, a study from New Zealand (McBride et al., 1998) indicated that illness risks posed by

animal versus human fecal material were not substantially different.

Outbreak Reports for Recreati onal and Drinking Waters

In the United States, formal surveillance data on the occurrence and causes of waterborne disease outbreaks are collected through collaboration between EPA, the Council of State and Territorial Epidemiologists, and the U.S. Centers for Diseas e Control and Prevention (CDC). The goals of the surveillance program include characterizing the epidemiology of outbreaks, identifying the agents causing outbreaks as well as trends and risk factors, identifying deficiencies in providing safe drinking water, encouraging health offici als to investigate outbreaks, and fostering government and international agency collabor ation on waterborne disease prevention. The number of outbreaks reported is a significant underestimate of the actual number of outbreaks that occur, as the actual numbers reported vary depending on issues such as a lack of laboratory capability. Thus, the extent of underestimation is unknown overall. Even with these problems, surveillance studies provide the best informati on available on waterborne disease outbreaks and

such data are critical to adequately characterizing microbial hazards.

In reviewing outbreak information for recrea tional and drinking water waters, several overarching points emerged. One is that the pat hogen source in the majority of drinking waterrelated outbreaks remains unknown. The source of pathogens in drinking water outbreaks in many cases could have been humans or animals. Most reports, however, offered little detail, leaving a critical information gap for the purposes of this review. Nevertheless, several outbreak investigation studies were able to link pathogens isolated from patients with water samples and/or animals using laboratory analysis. Other reports used circumstantial evidence to link animal waste to outbreaks; however, although comp elling, laboratory results were not available

to confirm the contamination source. The animal sources linked to outbreaks included beavers, cats/cougars, deer, elk, pigs, cattle, and chicke ns/poultry, and the corresponding animal-related human pathogens in these outbreaks were Giardia intestinalis

, Cryptosporidium spp., E. coliU.S. Environmental Protection Agency

February 2009 3 O157:H7, Campylobacter spp., Toxoplasma gondii , and S. typhimurium . Given that outbreaks are known to be a notoriously poor measure of th e actual number of in fections and illnesses caused by waterborne pathogens, those investigati ons that link pathogens isolated from patients and/or water samples with animals provide un equivocal evidence that human illnesses can and do occur from animal-based contamination. Unfortunately, the drinking water outbreak literature does not substantially enhance the curr ent ability to quantitative ly differentiate risks from animal- versus human-related pathoge n sources for recreational water exposures.

The recreational water outbreak literature (Craun et al., 2005) indicates that of the 259

recreational water outbreaks that occurred in the United States between 1970 and 2000, only approximately half included any information about possible sources of the contamination or the sources contributing to it. Approxi mately 18 percent of the total outbreaks were associated with animals, likely etiologic agents included E. coli spp., Schistosomes spp., and Leptospira spp. E.

coli was associated with cattle, deer, or duck feces; Schistosomes spp. were associated with snails; and Leptospira spp. were associated with rat urine. Similar to the drinking water outbreak compilation, the recreational water outbreak litera ture does not appear to substantially enhance the current state of knowledge on quantitatively characterizing risks from animal-related pathogen sources compared with human s ources for recreational water exposures.

Interpretation of Results

Given that relatively few investigations worldwid e have evaluated the risk to human health from recreational exposure to waters primarily imp acted by sources of contamination other than wastewater effluent, and that the potential range of those sources is broad, the findings from this

literature review ar e not surprising.

Although information on differentiating human versus animal sources of pathogens is lacking, several research organizations and countries have suggested novel approaches for addressing risks from nonhuman sources (e.g., Wa ter Services Association of Au stralia). For example, New Zealand, where about 80 percent of total no tified illnesses are zoonotic and potentially waterborne, has recently updated its recreational wa ter quality criteria to address the issue of animal-source waterborne contamination by basing its freshwater guidelines principally on the risks associated with campylobacteriosis using E. coli concentrations as an indicator (Till and McBride, 2004).

In summary, both human and animal feces in r ecreational waters continue to pose threats to human health. Although the public health importance of waterborne zoonotic pathogens is being increasingly recognized, it is still not well char acterized. Policy makers and researchers have

often assumed that the human health risk fr om pathogens associated with domestic and agricultural animal and wildlife f eces is less than the risk from human feces, in large part because viruses are predominately host-specific. This literature review illustrates a lack of detailed and unequivocal information concerning the relative risks of human illness resulting from exposure to various sources of fecal contamin ation in recreational waters. Because of their retrospective nature, waterborne disease outbreak investigations rarely produce th e data needed to draw conclusions about the impact of a pathog en source. Finally, the ability to measure howU.S. Environmental Protection Agency

February 2009 4 the infectivity and virulence of known waterborne zoonotic pathogens are affected when passaged through animal hosts remains in its infancy.U.S. Environmental Protection Agency

February 2009 5 

## I. B ACKGROUND AND 

## I NTRODUCTION

I.1 Background: Context and Purpose

Since the U.S. Environmental Protection Agency (hereafter EPA or the Agency) last published recreational water quality criteria in 1986, significant advances have occurred, particularly in the areas of molecular biology, micr obiology, and analytical chemistry. EPA believes that these new

scientific and technical advances need to be considered and evaluated for feasibility and applicability in the development of new or revised Clean Water Act (CWA) Section 304(a)

criteria for recreation. The Beaches Environm ental Assessment and Co astal Health (BEACH) Act of 2000 (which amended the CWA) required EPA to conduct new studies and issue new or revised criteria, specifically for Great Lakes States and coastal marine waters. To this end, EPA has been conducting research and assessing releva nt information to provide the scientific

foundation for new or revised criteria.

To address the BEACH Act requirement, EPA has engaged a range of stak eholders representing the general public; public interest groups; state, local, and m unicipal governments; industry; and wastewater treatment professionals. In March 2007, EPA convened 43 nati onal and international technical, scientific, and implem entation experts from academia, numerous states, public interest groups, EPA, and other federal agencies at a form al workshop to discuss the state of the science on recreational water quality research and implementation (USEPA, 2007). The workshop outcome included a suggestion to incorporate th e ability to differentiate sources of fecal

contamination and determine the relative human heal th risk from these sources into the new or

revised criteria.

Based on the feedback from the larger gro up of stakeholders an d detailed input and

recommendations from the scientific community, the Agency developed a Critical Path Science Plan for Development of New or Revise d Recreational Water Quality Criteria . A key question the science plan asks is what is the risk to hum an health from swimming in water contaminated with human fecal matter as comp ared to swimming in water c ontaminated with nonhuman fecal matter? Human and animal feces both can pote ntially contain pathogens that cause human illness. However, while some human pathogens are host-specific (i.e., human enteric viruses), other human pathogens can be shed by both humans and animals. In other words, all enteric pathogens of humans are infect ious to other humans, while re latively few of the enteric pathogens of animals are infectious to human s (zoonotic pathogens). Understanding which human pathogens are associated with which s ource of fecal contamination would allow the Agency to recommend better (more appropriate) water quality criteria in those situations.

EPA’s current recommended criteria treat the human health risk from various sources of fecal contamination as equivalent based on health ri sks from fecal contamination originating from publicly owned treatment works, which represen t the highest relative risks to swimmers. Because health risks from other sources (e. g., poorly treated or untreated human waste, nonhuman fecal matter, and mixed sources, such as urban stormwater runoff) were not well

understood at the time the 1986 criteria were de veloped, the approach was to protect human health regardless of the source. However, EPA recognizes that the health risk from fecal sources other than publicly owned treatmen t works may be different and th at recent scientific advancesU.S. Environmental Protection Agency

February 2009 6 may now allow the Agency to better characteri ze the relative risks to human health from

different sources of fecal contam ination. Specifically, the Agency is interested in understanding what human illnesses are caused by swimming in waters contaminated with human fecal matter from various sources, including human sources (wastewater effluent and untreated human fecal matter), nonhuman fecal matter (ranging from wildlife sources to agricultural inputs), and mixed sources, such as urban stormwater runoff.

The purpose of this white paper is to descri be the existing knowledge base available to

characterize the relative risks of human illness fr om various sources of fecal contamination in

recreational waters. An overvie w of recreational water epidemio logy studies and results from illness outbreak investigations are discussed in an attempt to demonstrate any differential risk to human health that may exist from various sources of fecal contamination.

I.2 Introduction

The overall goal of the current ambient water qua lity criteria (AWQC) for bacteria in the United States (USEPA, 1986) is to provide public health protection from gastro enteritis (GI illness) associated with exposure to fecal contamination during water cont act recreation. Because fecal matter can be a major source of pathogens in ambi ent water, and because it is not practical or

feasible to monitor for th e full spectrum of all pathogens that may occur in water, water quality criteria are specified throughout the world in te rms fecal indicator organism densities (USEPA, 1986; WHO, 2003). These fecal indicator organisms have been used for decades as surrogates for potential pathogens and subsequent health risks in both recreational and drinking waters (NRC, 2004).

The Agency used prospective c ohort epidemiological studies of wastewater effluent-impacted recreational waters (USEPA, 1986) to develop the 1986 AWQC for recreat ional water. The results of those epidemiological studies provide quantitative relationships between fecal indicator density in recreational waters ( E. coli and enterococci for freshwater s and enterococci for marine waters) and GI illness levels for those indivi duals exposed to recreational waters (USEPA, 1986). Using randomized controlled trials, Ka y et al. (1994) showed fecal streptococci (enterococci 1 ) to be predictive of gastroenteriti s (GI illness) among bathers in the United Kingdom. Fleischer et al . (1996) reported that exposure to fecal streptococci also could predict acute febrile respiratory illnesses. These studies formed the basis of the guidelines recommended by the World Health Organization (WHO, 2003). In addition, detailed reviews conducted by Wade et al. (2003) and Prüss (1998) strongly suppor t the findings that increased enterococci (or fecal streptococci) concentrations predict GI illne ss risk (Lepesteur et al., 2006).

Internationally, many countries still rely on fecal and total coliforms as a basis for their recreational water quality criteri a, standards, or guidelines (s ee WHO, 1999). Other countries rely on measurements of enterococci, E. coli , or both for their recreatio nal waters, most based on criteria recommendations provi ded by WHO (2003) and/or on EP A’s epidemiological studies

that led to the 1986 criteria.

1 The terms fecal streptococci, ente rococci, intestinal enterococci, and Enterococcus are often used to refer to essentially the same environmental and fecal species of b acteria (see NRC, 2004 for further information). Thus, for convenience, this white paper uses the term enterococci unless otherwise noted.U.S. Environmental Protection Agency

February 2009 7 EPA’s recommended recreational wa ter quality criteria do not differentiate between fecal sources of pathogens. Thus, EP A’s regulatory premise concerning water quality has been that nonhuman derived human pathogens when present in fecally contaminated waters are as

hazardous as their human-derived counterparts (Schaub, 2004). This presumption is supported by scientific literature that confirms that there are many wa terborne zoonotic bacteria and protozoa common to both humans and to vari ous types of animal populations (especially mammalian species). The literature also suggests, however, that in certain instances there may be attenuation of the infectivity, virulence, and disease severity to humans from animal-derived (“passaged”) human pathogens. Mo reover, “[w]e must also recogn ize that more than half the

bacteria in the human intestine and more than 99 percent of environmental bacteria have not

been cultured or characterized...This is almost certainly also true for the broad array of domestic and wild animals in our environment” (Bolin et al., 2004).

WHO’s recommended approach for classifying the water quality of recreational waters relies on combining microbiological monitoring results fo r fecal indicators and a sanitary inspection (WHO, 2003). This approach is based on the premise that the measure of microbiological

indicator of fecal contamination can be “interpreted” using evidence of the presence or absence of human fecal contamination; the approach also presumes that in general, sources other than human fecal contamination present a lesser risk to human health (WSSA, 2003). WHO indicated that “due to the species barrier, the density of pathogens of public health importance is generally assumed to be less in aggregate in animal ex creta than in human excreta and may therefore represent a significantly lower ri sk to human health” (WHO, 1999).

WHO highlighted this issue of potential differential risks be tween human and nonhuman sources in its recent report on zoonoses (WHO, 2004), whic h noted that the inab ility to distinguish

human from animal fecal contamination has led resource managers and regulators to treat all fecal contamination as equally hazardous to human health. The report further indicated the following (Till and McBride, 2004):

• This approach frequently results in the clos ure of beaches and she llfish harvesting areas that are affected by stormwat er runoff that carries fecal indicator bacteria of nonhuman origin.

• The true risk of exposure to waters contaminated by anim als is not well characterized.

• Studies that have attempted to define the risk associated with swimming in animalcontaminated water have not given a clear indi cation that there is an excess illness rate related to this type of exposure.

• These equivocal results do not lead to the conc lusion that all fecally contaminated waters

should be treated alike.

• New research to define the risk posed by anim al fecal wastes to users of water resources and indicator systems that identify animal contamination of surf ace waters are needed.

Ultimately, the merit of an AWQC approach that treats animal and human sources of pathogens and indicators differently or somehow disc ounts animal sources depends on both the

characterization of relevant differences betw een human and animal fecal material and the availability of technology that can accurately and reliably differe ntiate between their sources. These issues are of concern to the developmen t of new or revised r ecreational AWQC becauseU.S. Environmental Protection Agency

February 2009 8 the normal microbial composition of animal feces is different from human feces and can change dramatically over time and space, es pecially in recreati onal waters (Table I.2.1) (Boehm et al., 2002; Dorner et al., 2007; NRC, 2004). Moreover, the critical question is whether these differences in fecal sources resulting from r ecreational water-related exposures translate to significant differences in the risk of hu man infection or disease severity.

Table I.2.1. Representative Fecal Indicator Ba cteria and Zoonotic Pathogen Densities in Human and Animal Feces and Sewage*

Indicator Observed Density Source

Bacteria

Fecal coliforms 10 8 -10 9 /gram feces Infected person

Fecal coliforms 4.9 x 10 10 organisms/day Canada geese

Fecal coliforms 1.4 x 10 8 -2.4 x 10 9
organisms/day Chicken

Fecal coliforms 5.4 x 10 9 organisms/day Cows

Fecal coliforms 4.2 x 10 8 organisms/day Horses

Fecal coliforms 8.9 x 10 9 -1.1 x 10 10
organisms/day Pigs

Fecal coliforms 1.8 x 10 9 -1.2 x 10 10
organisms/day Sheep

Fecal coliforms 5 × 10 9 organisms/day Dogs and cats

Fecal coliforms 10 5 -10 7
(MPN)/100 mL most probable number Sewage

Fecal coliforms 4.2 x 10 6 organisms/100 mL Combined sewer overflow

Fecal coliforms 9.6 x 10 2 -4.3 x 10 6
organisms/100 mL Urban runoff

Fecal coliforms 1.2 x 10 2 -1.3 x 10 6
organisms/100 mL Grazed pasture runoff

Fecal coliforms 1.35 x 10 6 -2.4 x 10 8
organisms/100 mL Feedlot runoff

Fecal coliforms 1.2 x 10 1 -1.43 x 10 4
organisms/100 mL Cropland runoff

E. coli 1.7 x 10 8 E. coli /gram Pigeons

E. coli 10 3 -10 4 colony forming units (CFU)/100 mL Stormwater

Enterococci 4.0 x 10 5 enterococci/day Pigeons

Enterococci 10 2 -10 3 enterococci/mL;

5.4 x 10 5 enterococci/100 mL SewageU.S. Environmental Protection Agency

February 2009 9 Indicator Observed Density Source

Pathogens

Bacteria

E. coli O157:H7 10 2 -10 6 per gram feces Calves

Pseudomonas aeruginosa 2.3 x 10 5 MPN/100 mL Sewage

Salmonella 0.2-11,000 MPN/100 mL Sewage

Protozoa

Protozoan parasites 10 6 -10 7 /gram feces Infected person

Cryptosporidium oocysts 370 ± 197 oocysts/gram feces

1.2 x 10 5 -3.9 x 10 5 organisms/ day Canada geese

Cryptosporidium oocysts 13.7/mL Slaughterhouse (cattle)

Cryptosporidium oocysts 1.4 x 10 4 -3.96 x 10 4 /L Treated effluent (activated sludge)

Cryptosporidium oocysts 4.0 x 10 0 -1.6 x 10 1 /L Treated effluent (activated sludge and sand filtration)

Cryptosporidium oocysts 3-13,700/1,000 mL Sewage

Giardia cysts 450 cysts/gram feces; 3.1 x 10 5
cysts/day Canada geese

Giardia cysts 2-200,000/1000 mL Sewage

Viruses

Enteric viruses 10 3 -10 12 /gram feces Infected person

Adenovirus 1-10,000/100 mL Sewage

Enterovirus 0.05-100,000/100 mL Sewage

Reovirus 0.1-125/100 mL Sewage

Rotavirus 0.1-85,000/100 mL Sewage

Caliciviruses 10 6 /gram (10 13 /day) Gray whales**

* Although marine mammal caliciviruses are not kn own to be human pathogens, they have been being investigated as potential sources of emerging zoonoses (Smith et al., 1998).

Source: Adapted from: Protocol for Developing Pathogen TMDLs (USEPA, 2001), Impacts and Control of CSOs and SSOs: Report to Congress (USEPA, 2004), and Waterborne Zoonoses: Identification, Causes, and Control (WHO, 2004).U.S. Environmental Protection Agency

February 2009 10 

## II. M ETHODS

As indicated previously, the primary purpose of this white paper is to describe the existing knowledge base available to characterize the rela tive risks of human illness from various sources of fecal contamination in recreational waters. The paper specifically covers human illness resulting from water-related exposures to f ecal material from human and nonhuman sources. Although the ultimate use of this information is to support the development of new or revised water quality criteria and/or standards for recreational waters, this review encompasses both recreational and drinking water exposures.

Information related to human exposures to pat hogens in fecally contaminated recreational and drinking waters was obtained by se arching the scientific literature for epidemiological studies related to exposure to recreational waters and reports of outbreak inve stigations from both recreational and drinking waters. Appendix A details the specific search strategies and databases employed.

This literature review combines disparate info rmation to infer potential differences in risk

between various sources of contamination an d the limitations in e ach class of study are important. For example, in epidemiological studies conducte d on recreationa l waters, the amount of water ingested duri ng recreation is ofte n not known. In many cases, studies also include multiple potential sources of waterbody contamination. Furthermore, outbreaks are a notoriously poor measure of the actual number of infections a nd illnesses caused by waterborne pathogens (Craun, 2004). The timel y investigation of a waterbor ne outbreak by the appropriate professionals who have access to adequate laborat ory resources can provide information about an outbreak’s mode of transmission, the etiologic ag ent, and sources of c ontamination. However, many outbreaks are not recognized or investigated, and even in recognized outbreaks, not all cases of disease are repo rted; the likelihood of reporting is dependent on many factors, including pubic awareness of waterborne illnesses (such as media coverage of an event), the local requirements for reporting, and the availability of laboratory facilities (Craun et al., 2005).

Often, gaps in data result in an incomplete pi cture of the incident—esp ecially in recreational water, where water testing may occur days or weeks after the outbreak started. In many recreational water outbreaks, by the time an outbr eak is discovered and the etiologic agent is isolated, it is too late to provide meani ngful data regarding th e source of disease.

An example of the difficulty of linking illness with its source in recreational water occurred during an outbreak of E. coli -related illness in the Netherlands (Cransberg et al., 1996). Four children hospitalized in one town with hemolytic uremic syndrome prompted a search for a single source of illness. The results of the inve stigation pointed to a shallow lake where the ill children had all been swimming during a 5-da y period. Pulsed-field electrophoresis of E. coli isolates of patients and family members showed an identical pattern: no E. coli DNA could be detected in filter-concentrated lake water samples using polymerase chain reaction (PCR). However, water samples were not taken until two weeks after the exposures.U.S. Environmental Protection Agency

February 2009 11 The principal methodology employed for th is white paper is provided below:

• Summarize the recreational water epidemio logy studies that have been published

worldwide.

• Provide a brief description of the most infl uential recreational wate r epidemiology studies as well as those that investigated waters imp acted with sources other than wastewater and

wastewater effluent.

• Summarize waterborne disease outbreaks asso ciated with drinking water in the United States reported by the CDC from 1999 to 2004.

• Summarize select waterborne disease outbreaks associated with drinking water from

other countries and from the United States before 1999.

• Summarize waterborne disease outbreaks associated with recreational water in the United States reported by the CDC from 1999 to 2004.

• Summarize select waterborne disease outbreak s associated with recreational water from

other countries and from the United States before 1999.

• Provide brief descriptions of reported dri nking water and recreational outbreaks with animal-related pathogen sources.

• Compile the information described above and determine the weight of evidence available to demonstrate any differential risk to human infection, disease sever ity, or both resulting from exposure to fecal material from human or animal sources in recreational water.U.S. Environmental Protection Agency

February 2009 12 

## III. R ESULTS ECREATIONAL ATER PIDEMIOLOGICAL TUDIES

III.1 Overview of Recreational Water Epidemiological Studies

Since the 1950s, numerous epidemiological studies have been conducted throughout the world to

evaluate the association between recreationa l water quality and adverse health outcomes, including GI symptoms; eye infections; skin comp laints; ear, nose, and throat infections; and respiratory illness (Prüss, 1998; Sinton et al., 1998; Wade et al., 2003; Zmirou et al., 2003). Although most of these studies i nvestigated wastewater effluent -impacted marine and estuarine

waters alone or in combination with freshwater , several investigated freshwater recreational environments or nonwastewater effluent-impacted wa ters. These studies indicate that the rates of some adverse health outcomes are higher in swimmers compared with nonswimmers (Prüss, 1998).

Several groups of researchers have compiled in formation and generated broad and wide-ranging inferences from these epidemiological studies. Below is a brief overview of the meta-analyses conducted by Prüss (1998), Wade et al. (2003), and Zmirou et al. (2003); Table III.1.1 provides an overview of the epidemiological st udies included in these reviews.

• Prüss (1998) conducted a systematic review following discussions between the WHO Regional Office for Europe a nd WHO Headquarters to init iate development of new guidelines for recreational use of the water environment. The comprehensive review of 22 published studies on sewage pollution of recreational water and health outcomes concluded that the epidemiological basis ha d been laid to develop WHO guidelines on fecal pollution based on a causal association between GI illness symptoms and increased bacterial indicator density (i.e., ente rococci for marine, enterococci and E. coli for fresh)

in recreational waters.

• A meta-analysis of 18 published studies (Zmirou et al., 2003) was conducted by researchers at the National Institute for Public Health Surveillance at the request of the French Ministry of Health to help provide a scientific basis for establishing new standards for the microbial quality of marine and fresh recreational waters to replace the 30 year-old European Union bathing wa ter quality guidelines (EEC, 1976). The researchers provided four major results: (1) increased concentrations of fecal coliforms

or E. coli and enterococci in both fres h and marine recreational waters are associated with increased risks of acute GI illness, with ente rococci eliciting four to eight times greater

excess risks than fecal coliforms or E. coli at the same concentrations; (2) GI illness risks

associated with enterococci occur at lowe r concentration in marine versus fresh recreational waters; (3) increased concentrations of total coliforms have little or no association with GI illness risk; and (4) no evidence exists of a threshold of indicator density below which there would be no GI illness risk to bathers.

• Wade et al. (2003) conducted a systematic review and meta-ana lysis of 27 published studies was to evaluate the evidence linking specific microbial indi cators of recreational water quality to specific health outcomes under nonoutbreak (endemic) conditions. Secondary goals included id entifying and describing criti cal study design issues and 

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February 2009 13 Table III.1.1. Recreational Water Epidemiolo gy Studies Included in Reviews by Prüss (1998), Wade et al. (2003), and Zmirou et al. (2003)

First Author Year Location Water Type Study Design Review Article

Alexander et al. 1992 UK Marine Cohort Wade, Zmirou

Bandaranayake 1995 New Zealand Marine Cohort Prüss

Brown 1987 UK Marine Cohort Zmirou

Cabelli 1983 USA Marine Cohort Wade, Prüss, Zmirou

Cabelli 1983 Egypt Marine Cohort Wade, Prüss

Calderon et al. 1991 USA Fresh Cohort Wade

Cheung et al. 1990 Hong Kong Marine Cohort Wade, Prüss, Zmirou

Corbett et al. 1993 Australia Marine Cohort Wade, Prüss, Zmirou

Dufour 1984 USA Fresh Cohort Wade, Prüss, Zmirou

Fattal et al. 1986 Israel Marine Cohort Wade, Prüss, Zmirou

Ferley et al. 1989 France Fresh Cohort Wade, Prüss, Zmirou

Fewtrell et al. 1992 UK Fresh Event Wade, Zmirou

Fewtrell 1994 UK Marine Cohort Wade, Zmirou

Fleisher et al. 1993 UK Marine Randomized trial Wade

Fleisher et al. 1996 UK Marine Randomized trial Prüss

Foulon et al. 1983 France Marine Cross-sectional Wade

Haile et al. 1996, 1999 USA Marine Cohort Wade, Prüss, Zmirou

Kay et al. 1994 UK Marine Randomized trial Wade, Prüss, Zmirou

Kueh et al. 1995 Hong Kong Marine Cohort Wade, Prüss

Lee et al. 1997 UK Fresh Event Wade

Lightfoot 1989 Canada Fresh Cohort Wade, Prüss

Marino et al. 1995 Spain Marine Cohort Wade

McBride et al. 1998 New Zealand Marine Cohort Wade

Medema et al. 1995 The Netherlands Fresh Event Wade

Medical Research Council 1995 South Africa Marine Cohort Prüss

Mujeriego 1982 Spain Marine Cohort Prüss

Philipp et al. 1985 UK Marine Event Wade, Zmirou

Pike 1994 UK Marine Cohort Wade, Prüss, Zmirou

Prieto et al. 2001 Spain Marine Cohort Wade

Seyfried et al. 1985 Canada Fresh Cohort Wade, Prüss, Zmirou

Stevenson 1953 USA Fresh Cohort Wade, Prüss, Zmirou

UNEP / WHO 1991a Israel Marine Cohort Prüss

UNEP / WHO 1991b Spain Marine Cohort Prüss

van Asperen et al. 1998 The Netherlands Fresh Event Wade, Zmirou

van Dijk 1996 UK Marine Cohort Prüss

von Schirnding et al. 1992 South Africa Marine Cohort Wade, Zmirou

and evaluating the potential for health effect s at or below the curr ent regulatory criteria (USEPA, 1986). The researcher s concluded that (1) enterococci and to a lesser extent E.

coli are adequate indicators (pre dictors) of GI illness in ma rine recreational waters, but fecal coliforms are not; (2) the risk of GI illn ess is considerably lower in studies with

enterococci and E. coli densities below those establis hed by EPA (1986), thus providing support for their regulatory use; (3) E. coli is a more reliable and consistent predictor of GI illness than enterococci or other indicators in fresh recreational waters; and (4) basedU.S. Environmental Protection Agency

February 2009 14 on heterogeneity analyses, st udies that used a nonswim ming control group and that

focused on children found elevated GI illness risks.

In addition, Sinton et al. (1998) reported on differentiating the re lative health risks associated

with human and animal fecal material. Illness risk associated with ba thing in water polluted primarily with human fecal material was revi ewed based on studies from the United States (Cabelli, 1983a; Dufour, 1984), Canada (Seyfrie d et al., 1985a,b), Israel (Fattal et al., 1983, 1986, 1987), Egypt (Cabelli, 1983b; El-Sharkawi a nd Hassan, 1979), Spain (Mujeriego et al., 1982), France (Ferley et al., 1989; Foulon et al ., 1983); the United Kingdom (Brown et al., 1987; Jones et al., 1989, 1991), Hong Kong (Holmes, 1989), and Australia (C orbett et al., 1993; Harrington et al., 1993). Most of these studies showed a positive correlation between GI illness and fecal indicator density; there was little equi valent evidence from waters polluted primarily with animal feces. The only study specifically de signed to address swimming-associated illness in animal-impacted waters was that of Cald eron et al. (1991) who found no statistically significant association between GI illness and fecal indicator bacter ia densities. Based on this observation, Sinton and colleagues (1998) concluded that reliable epidemiological evidence was lacking, and that other sources of information were needed to identify and apportion human and animal fecal inputs to natural waters.

Since the publication of Sinton’ s review article in 1998, a number of additional epidemiologicalstudies have been conducted, some of which further address the issue of nonwastewater effluentcontaminated recreational waters . Completed and ongoing studie s are summarized in Tables III.1.2a and III.1.2b, respectively; however, a comprehensive peer -reviewed summary of that information has not, to date, been published.

The following section provides brief summar ies of the epidemiological studies on nonwastewater effluent sources of contamination along with those studies on human sources that have most commonly been used as the basis for water quality criteria or standards throughout the

world.

III.2 Descriptions of Key Recreational Water Epidemiological Studies

III.2.1 Selected Recreational Water Epidemiologica l Studies Based on Human Sources of

Fecal Contamination

United States and Egypt (Cabelli, 1983a) Cabelli (1983a) conducted epidemiological studies in the following four locations: Coney Island and Rockaway beaches in New York, New York; Alexandria beaches in Egypt; Lake Pontchartrain in New Orleans, Louisiana; a nd Boston Harbor in Boston, Massachusetts. The goals of the studies were to develop health effect s and recreational water quali ty criteria for EPA.

The author used similar methods for each loca tion. The studies consis ted of two interviews—

one interview at the beach where individuals were recruited and a seco nd phone interview 7 to 10 days later. Beach interviews occurred only on weekends and were limited to individuals who had swam on one or two weekend days. Mid-we ek swimmers were excluded from the study.U.S. Environmental Protection AgencyFebruary 200915Table III.1.2a. Recently Completed RecreationalWaters Epidemiological Studies—Some ofWhich Address Nonpoint Sources of FecalContaminationReferenceLocationStudyDesignContamination Sourceand IndicatorsHealth Effect(s)HealthCorrelation1nConclusionsColford et al.,2005, 2007UnitedStatesCohortNonpoint source: dominant sourceavian; bacterial indicators viatraditional and nontraditionalmethods,Bacteroides, viruses14 healthoutcomesevaluatedincluding GI andskin rashNegative8,800Risk of illness was not correlated with levels of the traditionalwater quality indicators used in the study. Of particular note,the state water quality thresholds for bacterial indicators(similar to the 1986 AWQC for bacteria) were not predictive ofswimming-related illnesses. Similarly, no correlation wasfound between increased risk of illness and increased levels ofmost nontraditional water quality indicators measured in thestudy. Diarrhea and skin rash were increased in swimmerscompared with nonswimmers.Wade et al.,2006UnitedStatesCohortWastewater effluent- impactedwaters; enterococci andBacteroidesmeasured viaquantitative polymerase chainreaction (qPCR)Gastro-enteritisPositive5,717Swimmers attwo beaches had a higher incidence of GI illnesswhen compared to nonswimmers. A statistically significantrelationship was observed between an increased rate of GIillness and enterococci at the Lake Michigan beach, and apositive trend for enterococci at the Lake Erie beach wasnoted. The association between enterococci and increasedrisk of GI illness was significant when results for the twobeaches were combined. A positive trend was observed at theLake Erie beach forBacteroides, but no trend was observed atthe Lake Michigan beach.Wiedenmannet al., 2006GermanyRandomizedcontrolWastewater-impacted waters andwaters impacted by waterfowl andswimmers.E. coli, intestinalenterococci,C. perfringens,somatic coliphage, andPseudomonas aeruginosaAcute febrileinfection, ear, eye,skin, urinary tract,three definitions ofGIPositive2,196Data were not analyzed for differences in health outcomesfrom exposure to animal versus human fecal contamination.Authors recommended no observed adverse effect levels(NOAELs) for water quality as follows: 100E. coli, 25 intestinalenterococci, 10 somatic coliphages, or 10C. perfringensper100 mL. The authors further concluded that a NOAELapproach would be a more robust method to the complexprocess of setting standards.Dwight et al.,2004UnitedStatesCrosssectionalsurveyNonpoint source; compared urbanto rural runoffDiarrhea;vomiting, sorethroatPositive1,873Urban participants reported almost twice as many symptomsoverall as the rural participants during the first year and slightlymore during the second year of the study. In both study years,risk increased across almost every symptom category by anaverage of about 10% for each additional 2.5 hours of waterexposure per week. The study did not measure water qualityat the various sites.Lepesteur etal., 2006AustraliaCohortEvaluated for fecal streptococci;source recreational users andrunoffRespiratory illnessand GI illnessPositive340Risk of respiratory illness was highest in the 11–15 year oldage group, where vigorous activity such as jumping andenergetic swimming was observed. The authors suggestedfurther exposure-related research.1The health correlation represents the correlationbetween the health effect observed and the indicator.U.S. Environmental Protection AgencyFebruary 200916Table III.1.2b. Ongoing Recreational Waters Epidemiological Studies—Some of Which Address NonpointSources of Fecal ContaminationStudyLocationStudyDesignPathogen/PathogenSourceHealthEffect(s)HealthCorrelation1nConclusionsSouthernCalifornia CoastalWater ResearchProject(SCCWRP)StudiesUnitedStatesCohort,prospective30 differentmicrobial indicatorsincluding rapidmethods and newmicrobial indicators20 differentepidemiologicaloutcomesNotapplicable(N/A)N/ASCCWRP is conducting a series of epidemiology studies inSouthern California to examine the risk of swimming-related illnessfrom nonpoint source polluted waters. The studies are beingconducted at three different beaches. The fecal contamination atthese beaches is estimated tobe mostly human at one beach,primarily nonhuman at the second beach, and a mixture of humanand nonhuman at the third beach. Water samples will be collectedat multiple locations and times and evaluated with over 30microbiological indicators. The indicators to be tested includetraditional fecal indicator bacteria, rapid methods, new microbialindicators, microbial source tracking tools, and viruses. SCCWRPhopes that these studies will helpto determine the relative risk ofcontracting an illness from swimming at nonpoint source beachesand whether the risk of illness underthese conditions correlateswith traditional indicator density and/or new indicators or methods.VirobatheEuropeanUnionLaboratorymethodevaluationAdenovirus andnorovirusGastroenteritisN/AN/AVirobathe is a project aimed at detection of viruses in recreationalwaters and is investigating molecular methods for direct viralpathogen enumeration (adenovirus and norovirus). The final reportis currently being reviewed by the European Commission (EC)EpibatheEuropeanUnionRandomizedcontrolUnknownUnknownN/AN/AEpibathe is a consortium of European research institutions carryingout an EC-funded project to explore the relationship betweenmicrobial indicators and health outcomes to define appropriateguideline levels. The objective is to develop the dose-responserelationships between fecal indicator density (E. coliandenterococci) and self-reported minor disease outcomes (e.g.,gastroenteritis, skin irritation, eye ailments, and earinfections/symptoms) in Mediterranean bathing waters andfreshwater bathing sites in a new member state. Studies arecurrently being conducted in Spain and Hungary and a parallelstudy is under consideration in the United States (Florida). Theconsortium is expected to report to the EC in late 2008.1The health correlation represents the correlation between the health effect observed and the indicator.U.S. Environmental Protection Agency

February 2009 17 Interviews occurred on days with minimal tidal effects and during time periods of peak beach usage (from 11 am to 5 pm). For the studie s based in the United St ates, a total of 26,676 participants were interviewed, while 23,080 particip ants were interviewed in Egypt. Swimmers

were defined as individuals w hose upper body orifices were expos ed to water. Nonswimmers who attended the same beach were the control population for the study.

Water samples were collected at two to three locations along the beach, typically three to four samples were collected during the peak beach usage. Water samples were analyzed for

Salmonella

, Enterobacter-Citrobacter

, Klebsiella , fecal coliforms, and staphylococci. Results were analyzed using regression analysis.

In the New York study, two beaches were sampled. The Coney Island beach was considered “barely acceptable” in terms of pollution leve ls, whereas the Rockaways beach was deemed “relatively unpolluted.” The aut hor found statistically significant differences in the rate of GI symptoms in swimmers compared to nonswimm ers at the Coney Island, but not Rockaways beach. The author also found a higher rate of respiratory symptoms in swimmers at Rockaways beach. The symptom rate for GI illness for swimmers at Coney Island was 10 out of 1,000 swimmers compared to 2 out of 1,000 swimme rs for Rockaways beach. There the author

determined that measurable health effects coul d occur on beaches that met existing recreational guidelines and standards. When examining the relationship of the indicator densities to GI symptoms, the author found that enterococci densities provided the best correlation; E. coli was the second best indicator.

The author was unable to find a beach that was both heavily affected with close point-source sewage discharges and used by a large number of people. Instead, several beaches with combined sewer outfalls in Alexandria, Egypt me t those requirements. The author found that swimmers in more heavily polluted beaches experi enced more symptoms than swimmers at less polluted beaches. Rates of GI symptoms appeared to follow Enterococcus and E. coli densities. However, the rates of illness were not as high as expected despite higher pollution levels than the New York study.

The author then conducted a focused study on visitors to the beach that were from Cairo. In that study, the rates of illnes s for swimmers was higher than for nonswimmers and there was more inverse relationship at the least polluted beach for time spent swimming and rate of illness compared to the other beaches. Th e rate of illness for visitors from Cairo was similar to the New York study.

The Lake Pontchartrain study was located near the mouth of Bayou St. John in a brackish area with limited tidal activity. The au thors found statistically different rates of illness for swimmers versus nonswimmers in symptoms of vomiti ng, diarrhea, stomachache, earache, and skin irritations. In general, the GI symptom rates we re higher in children than adults. The authors also found that enterococci appeared to be a better indicator of illness than E. coli , stormwater runoff appeared to be less harmful than sewage sources, and enterococci and E. coli may overstate risks of illness.U.S. Environmental Protection Agency

February 2009 18 The Boston Harbor study took place on two b eaches in 1978 and attempted to confirm the observation that significant health effects can be observed when ther e are low indicato r densities. Although the author did not find statistically differe nt illness in GI symptoms between swimmers and nonswimmers, the beach with the most polluti on had a greater difference in the rate of illness between swimmers and nonswimmers, ev en if not statistica lly significant.

Overall, the Cabelli (1983a) studi es found that there was an incr eased risk in GI illness from swimming in waters in increasingl y polluted seawater. Enterococci also appeared to be a better indicator for illness from swimming in seawater than E. coli or other fecal indicators.

United States (Dufour, 1984) Dufour (1984) conducted a series of epidemio logical studies to id entify whether a model developed by EPA to predict health effects base d on marine water qualit y could also apply to freshwater, including identifying a water quality indicator that best describes the relationship

between health effects and freshw ater quality and determining whet her the marine water criterion was applicable to freshwater. The studies were conducted at two U.S. beaches, Lake Erie in Erie, Pennsylvania (29,976 partic ipants) and Keystone Lake in Tulsa, Oklahoma (16,363 participants).

The Lake Erie studies were conducted in 1979, 1980, and 1982 on beaches considered to have good or excellent microbial water quality. One s ite was located approximately three-quarters of a mile northwest of a sewage outfall for the City of Erie. The Keystone Lake studies were conducted in the summers of 1979 and 1980, and the beaches demonstrated variable water quality for bacteria. The two beach sites at Keys tone Lake were located 3 and 5 miles from an outfall for wastewater treatment facility. In 1979, the treatment plant released an average of 120,000 gallons of unchlorinated sewage per day into the lake. In 1980, this practice was discontinued, and sewage passed through a settling lagoon, an aeration basin, and was chlorinated before being released into the lake.

Water samples were tested for E. coli and enterococci (includes Streptococcus faecalis and Streptococcus faecium ). Fecal coliforms were also monitored for two years during the Keystone Lake studies and in two years of the Lake Erie studies. Statistical analyses examined the relationship between the occurrence of GI illn ess in swimmers compared with a nonswimming control group. Because of the small population of nonswimmers, the nonswimming control group was pooled from an entire season of beachgoe rs to form a single control population. To evaluate their relationship, the incidence of illness between swimmers and nonswimmers and the indicator bacteria density at th e time of swimming were used. The model controlled for age as a confounding factor. A regr ession analysis determin ed whether there was a direct relationship between swimming-associated GI illness and microbial water quality. A correlation analysis determined which water quality indicator show ed the strongest relationship to a swimmingrelated illness.

Researchers conducted surveys at the beaches on weekends when the beaches were more crowded and monitored water quality at the time of swimming activity. There were two phases

of beach interviews

— the first as beachgoers were leaving the beach area and a second follow-up telephone interview 8 to 10 days after swimming. Follow-up interviews were only conducted onU.S. Environmental Protection Agency

February 2009 19 beachgoers who had not gone swimming the five days prior to the initial interview. For the study, swimming was defined as having all orifices immersed in water. Interviewers asked beachgoers during the initial inte rview about sex, age, race a nd ethnicity; whether a person swam; length of time and time of day in the wate r; illness symptoms they may have had in the previous week; and the reason, if a nonswimmer, why they did not enter the water. Follow-up interviewers asked the beachgoers about any illn ess symptoms that occurred since swimming at

the beach.

In the Lake Erie studies, both si tes met local and state standards for water quality. In general, symptom rates for swimmers were higher than nons wimmers in all categories; however, most symptoms were not statistically significant. Statistically significant differences between swimmers and nonswimmers were found in symptoms related to enteric di seases and tended to occur at the beach with poorer water quality.

In the Keystone Lake study, symptoms for enteric diseases tended to be higher in swimmers than nonswimmers. In 1979, there was only one other group of symptoms (fever, headaches lasting greater than three hours, and backache) that s howed significant differences between swimmers and nonswimmers. In 1980, statistical differen ces between swimmers and nonswimmers were found at one or both sampling locations with sympto ms for GI, respiratory, and other illnesses.

United Kingdom (Fleisher and Kay, 2006; Fleisher et al., 1993, 1996, 1998) Fleisher and Kay (2006) and Fleisher et al. (1993, 1996, 1998) repor ted the results of randomized intervention trials at separate marine bathing locations to identify the potential dose-response relationships among swimmers exposed to marine waters contaminated with domestic sewage and the potential risk of nonenteric illness (e.g., acute febrile respiratory illness, ear, eye, and skin ailments). Fleisher et al. (1996, 1998) re ported the final results of the four randomized intervention trials conducted at four separate marine bathing locations and incorporated the results on two of the locations, which were presen ted preliminarily in Flei sher et al. (1993). Fleisher and Kay (2006) analyzed the data pr esented in Fleisher et al. (1993, 1996, 1998) and Kay et al. (1994) to identify and quantify any risk perception biases that may have affected the

observed association between skin ailments and exposure to mari ne waters contaminated with domestic sewage at one of the study locations. The Fleisher et al. (1998, 1996, 1993) studies are included in the meta-analyses of Prüss (1998), Wade et al. (2003), a nd Zmirou et al. (2003).

The four separate trials took pl ace at four different locations during the summers of 1989 through 1992. The study population consisted of 1,216 adults (>18 years of age) that were recruited from populations located near the study locations duri ng the 3 weeks prior to the exposure day. No recruits participated in more than one study cohort, and study part icipants were blinded to the outcome illness being studied. Study recruits part icipated in an extensive interview and medical examination no more than two days prior to the da y of exposure. Research ers gathered data on a number of potential confounding factors (e.g., age, sex, general health, illness in previous three weeks, medications taken, water contact activities, other c onfounding factors).

Study participants were randomized into ba thers (548 participants) and nonbathers (668 participants) who were unaware of their status until they arrive d at the study lo cation beach. Bathers entered into a defined area in the water, remained in the water for at least 10 minutes,U.S. Environmental Protection Agency

February 2009 20 and completely immersed their heads in the wate r at least 3 times. Nonbathers remained on the beach in a designated area. On the day of expos ure, study participants were interviewed again about their health and dietary habits and any water contact activities experienced between the

initial interview and the day of exposure. Furthermore, one week following the exposure period, study participants were medically examined and interviewed extensively again for data on their health, diet, water contact activity, and other potential risk factor s. Lastly, study participants were mailed a questionnaire to fill out with any other symptoms of illness and exposure to

recreational water.

In addition, the water quality of the bathing ar ea was sampled in 30-minute increments during the exposure period at various desi gnated locations (sampled every 20 m at surf, mid [1 m deep], chest depth [1.3 to 1.4 m deep], and 30 cm be low the surface). These water samples were analyzed via standard methods for the following indicators: total and fecal coliforms, fecal streptococci, and P. aeruginosa . Total staphylococci were also counted at three of the study sites. The sampling results were assigned to each individual bather within 15 minutes of exposure and within a maximum of 10 m of the place of exposure.

Linear trend, chi-square, and multiple logistic regression analyses were used to estimate the dose-response relationship between the microbiological water qual ity results and occurrence of gastroenteritis, acute febrile respiratory infect ion, and eye and ear ailments. The statistical analyses controlled for the e ffects of confounding factors, whic h included nonexposure-related

variables associated with the incidence of these outcome illnesses. The results from participants who did not take part in the follow-up interviews or who reported illnesses of interest on the actual exposure day were excluded.

Fleisher et al. (1998) indicated that bathers had statis tically significant (p< 0.05) higher rates of gastroenteritis and ear and eye ai lments as compared to nonbathers. Moreover, bathers exposed

to ≥ 60 fecal streptococci per 100 mL had a statistically si gnificant (p<0.001) hi gher rate of acute febrile respiratory infection re lative to nonbathers. In addition, the authors reported that approximately 34.4 to 65.8 percent of illnesses re ported by the study cohort could be associated with bathing in marine waters contaminated with domestic sewage . Fleisher et al. (1996) also noted that fecal strept ococci exposure of ≥ 60 per 100 mL was predic tive of acute febrile respiratory infection and indica ted that a fecal coliform expos ure of 100/100 mL was predictive

of ear ailments. No indicator was found to predict eye aliments, although the risk of eye ailments was higher for bathers versus nonbathers. There was no statistically significant doseresponse relationship found for skin ailments. Fl eisher and Kay (2006) not ed that the observed difference in skin ailments associated with exposure between bathers and nonbathers at one of the four study locations may be attri butable to “risk perception bias.”

Based on the results of these studies, the authors concluded that future epidemiological studies should incorporate the same study de sign to help control for the la rge disparity observed in risk estimates reported in previously published epidemiological studies. Additionally, Fleisher et al. (1996) noted that these study results demonstrated that a single indicator would not be sufficient to establish water quality standards aimed at prot ecting public health. Fleisher et al. (1998)

concluded that illness associated with bathing in contaminated (marine) recreational waters is aU.S. Environmental Protection Agency

February 2009 21 significant threat to public health, and further studie s to assess the severity of illnesses associated with bathing in recreational wa ters contaminated with domes tic sewage should be conducted.

United Kingdom (Kay et al., 1994) Kay et al. (1994) conducted the first randomized control study to evaluate the heath effects associated with swimming in coastal waters. Th is study is included in th e meta-analyses of Prüss (1998), Wade et al. (2003), and Zmirou et al. (2003). The 4-year study took place at four different locations during the summers fr om 1989 through 1992. This study builds on the preliminary results from two of the locations that were published in Fleisher et al. (1993). Although this study also uses the same study population that was used in the Fleischer and Kay (2006) and Fleisher et al. pa pers (1996, 1998), it focuses specifi cally at the dose-response relationship between gastroenteriti s and exposure to marine water of varying microbial quality.

Linear trend and multiple logistic regression anal yses were used to estimate the dose-response relationship between the occurrence of gastroenteritis and microbiol ogical water quality (exposure). The statistical anal ysis controlled for confounding factors, such as nonexposurerelated variables associated with gastroenteritis.

The results indicated that of the indicators meas ured, only fecal streptococci demonstrated a statistically significant dose-res ponse relationship with gastroen teritis. The model used for bathers exposed to more than 32 fecal stre ptococci/100 mL demons trated a significant relationship with the risk of ga stroenteritis, whereas the model utilized for bathers exposed to less than 32 fecal streptococc i/100 mL did not show a significant relationship. The latter relationship was independent of nonwater-r elated predictors of gastroenteritis.

Based on their results, the authors concluded that although none of the other microbiological indicators illustrated a significan t relationship between measured concentrations and occurrence of gastroenteritis, the relationshi p between fecal streptococci concentration measured at chest depth and gastroenteritis is robust. However, the biological basis unde rlying this significant relationship is not known. The authors sugge sted that whatever causes gastroenteritis “copartitions” in seawater with fecal streptoco cci. The authors’ findi ngs also suggest that coliforms seem to have little value as indicators of gastroenteritis risk from sewage pollution of coastal waters and that fecal streptococci conc entrations are a better microbiological indicator.

Spain (Prieto et al., 2001) Prieto et al. (2001) conducted a cohort study to determine whether water polluted with sewage posed a danger to a bather’s health and to dete rmine the best microbiologi cal indicator to predict illness. The study took place during the summer of 1998 on four beaches in northern Spain and included 1,805 participants. Water samples were co llected 3 days a week at 10 am in the area of the beaches that usually had the highest bather density. Water samples were tested for total coliforms, fecal coliforms, fecal streptococci, S. aureus , and P. aeruginosa

.

The epidemiological study consisted of two surv eys—one survey at the beach and a follow-up survey within seven days of the beach interview. The surveys focused on family groups. Once an individual was selected for an interview, all other family members were interviewed. The interviews occurred on the same days that water samples were collected and timed so that a dailyU.S. Environmental Protection Agency

February 2009 22 average of 15 people were interviewed. During th e follow-up interview, individuals were asked about a series of symptoms and additional personal information.

For the statistical analyses, study participan ts were divided into swimmer and nonswimmer categories. The authors conducte d a bivariate analysis to exam ine the relationship of bathing,water quality, and illness. A multivariate analysis was carried out to determine the doseresponse relation between indicator bacteria densities and their re lation to health problems.

Water quality at the four beaches exceeded the European Community Directive guide standards for total coliforms (39.8 percent of samples), fecal coliforms (57.1 percent of samples), and fecal streptococci (in 37.9 percent of the samples). In the follow-up interv iews, 7.5 percent of participants reported symptoms. The rate of these symptoms wa s significantly greater (p=0.011) for “holidaymakers” (9.9 percent) and “day tr ippers” (8.4 percent) than for residents (5.8 percent). The study did not find a significant diffe rence in the incidence rate of each symptom between swimmers and nonswimmers, nor did the au thors find a difference in the incidence of these symptoms between swimmers who submer ged their head and those who did not.

The rate of symptoms did increase with the con centration of total coliforms. Gastrointestinal symptom incidence increased with total coliforms and fecal stre ptococci and was significantly higher in swimmers than nonswimmers.

United States (Wade et al., 2006) Wade et al. (2006) conducted a prospective co hort study of beachgoers at two beaches in the Great Lakes area—one beach on Lake Michigan in Indiana and the second beach on Lake Erie in Cleveland, Ohio. Both beaches were impacted by effluent from wastewater treatment plants. First, beachgoers were recruited at beaches on the weekends and holidays during the summer of 2003. Each participating beachgoer completed and returned the questionnaire prior to leaving the beach. The questionnaire asked for info rmation on demographics, swimming and other beach activities, consumption of raw or undercooked meat or runny eggs, chronic illnesses, allergies, exposure to an imals, and other related health symp toms or encounters with sick people in the previous 48 hours. Second, following a 10 to 12 day period, a telephone interview was conducted to gather information about health sy mptoms experienced since the beach visit, as well as on other water-related activities, contact with animals, and consumption of high-risk

foods.

Water samples were also collected three times a day on each study day and analyzed for

Bacteroides and enterococci. The water samples were an alyzed via a modified version of PCR. This new method provides a faster assessment of water quality. Respiratory and GI illness and ear, eye, and skin rash symptoms were eval uated. The authors only reported the GI illness

results. Swimmers at both beaches had a higher incidence of GI illness compared to nonswimmers. A statistically significant relationsh ip was observed between increased rate of GI illness and enterococci at the Lake Michigan beach, while a positive trend for enterococci at the

Lake Erie beach was noted. The association betw een enterococci and increased risk of GI illness was significant when results for the two beaches were combined. In terms of Bacteroides , a positive trend was observed at the Lake Erie beach, but no trend was observed at the LakeU.S. Environmental Protection Agency

February 2009 23 Michigan beach. In addition, the association be tween enterococci and GI illness strengthened with increasing exposure.

Australia (Lepesteur et al., 2006) Lepesteur et al. (2006) conducted an epidemiol ogical study examining the relationship between incidence of disease and exposure to fecal contam ination in recreational water. The study area was the Peel Harvey estuary at Mandurah Bridge beach located 70 km south of Perth in Western Australia. Water circulation is influenced by tidal currents, wind, and river flow. The water recreational area was relatively sm all—approximately 500 sq. m.

The surveys were conducted in th e afternoons with water samples collected each day and tested for fecal streptococci. Social surveys were conducted at the beach and through follow-up interviews by telephone two week s later. A total of 119 groups or families and 340 individuals participated in the study. The interviews includ ed questions related to frequency of beach visits, length of stay and days of visit, age of user s, and beach activities. Exposure to recreational waters consisted of any visit to the estuary over 30 minutes th at involved swimming, paddling, and playing in wet sand.

During the initial interview, participants were asked to provide information on their current health status. The follow-up interview asked who swam and whether anyone became ill during the two-week period since the initial interview. Evidence of GI and respiratory illnesses was recorded. Two or more symptoms were consider ed an incident of illness. Confounding factors such as food and drink intake, age, sex, history of diseases, pregnanc y, additional bathing, jellyfish sting, travel, and period of exposure to sun were identified during the follow-up interview. For the analysis, the authors adjust ed background illness rates using age-dependent probability factors. The odd ratios with 95 percen t confidence intervals were used to quantify the magnitude of effect of exposure to recr eational waters for different age groups.

The water showed evidence of fecal contamina tion year-round with increased concentrations caused by recreational users during the bathing season. Increased fecal indicator densities were also associated with rainfall. Most survey participants conducted a number of recreational activities at any visit to the beach, with 76 percent identifying swimming as one of their activities. The average number of expos ures was 17 per person per season.

Respiratory illness comprised most of the re ported symptoms, with GI illness being less common. The authors observed a relationship be tween excess respiratory illness and exposure to fecal streptococci. The highest odds ratio was ob served in the 11 to 15 year-old age range. The authors attributed this result to greater exposur e to water combined w ith vigorous activity.U.S. Environmental Protection Agency

February 2009 24 III.2.2 Selected Recreational Water Epidemiol ogy Studies Based on Nonwastewater

Effluent Sources of Fecal Contamination

United States (Calderon et al., 1991) Calderon et al. (1991) followed the health status and swimming ac tivities of volunteer participants. This study is included in the meta -analysis of Wade et al. (2003). The study site was a small pond (3 ac) located in a semirural a nd largely forested community in Connecticut. An intense sanitary survey of the surrounding wate rshed indicated that no human sources of fecal contamination impacted the stream that fed the pond, and there were no point sources of microbial pollution.

Water samples were analyzed for E. coli , enterococci, fecal coliforms, P. aeruginosa , and staphylococci. A total of 104 families participated in the study. Swimming was defined as a day in which an individual swam in the pond, and during swimming activity, completely submerged their head and body beneath the surface of the water. There were 1,310 exposure-days accumulated by swimmers and 8,356 person-days for nonswimmers.

Water quality data were collected on 49 days of the study. The geometric mean E. coli density

was 51 CFU/100 mL. Rain occurred on 16 of th e 49 days of the study. The geometric mean

densities of E. coli and fecal coliforms were determined to be over two times greater on rainy days than on dry days; levels of enterococci were four times higher on rain days than dry days. The densities of staphylococci and Pseudomonas were about the same during rainy and dry periods.

The symptomatic GI illness rate in swimmers was 22.9 per 1,000 person-days, whereas, in nonswimmers, the rate was 2.6 per 1,000 person-days. Gastrointestinal illness was also strongly associated with swimming when adjusted for ag e. However, no association was found between high fecal indicator bacteria densities and GI illness in sw immers or between swimmer illness and high-volume rain days. The authors suggest ed that swimming-associated illness may have been due to etiological agents that were transmitted from swimmer-to-swimmer via bathing

water.

The data from this study indicate that illness in swimmers was not statistically associated with densities of commonly used fecal indicator bact eria in a recreational water whose source was

rainwater runoff from a forested watershed. Th ese results led the authors to conclude that currently recommended bacterial indicators (i.e., E. coli and enterococci for fresh recreational waters per USEPA, 1986) are “...ineffective for predicting potential health effects associated with water contaminated by nonpoint sources of fecal pollution.”

Hong Kong (Cheung et al., 1990; Holmes, 1989) Cheung et al. (1990) and Holmes (1989) describe d a prospective cohort study that was conducted in two phases in the summers of 1986 and 1987. The first phase involved four popular beaches and tested the epidemiological techniques used in the second phase (main study) that incorporated results from nine beaches. The main study was undertaken to provide data for deriving health-related bathing water quality stan dard specific to the conditions of Hong Kong. Six of the beaches in the main study were pr edominately impacted by human sewage, two wereU.S. Environmental Protection Agency

February 2009 25 impacted by livestock wastes (mainly pig excret a), and one was impacted by a combination of sewage and livestock waste. Each phase invo lved two parts, epidem iological studies using beachgoer interviews and follow- up telephone interviews and wate r testing for microbiological quality. Beachgoers (33,083) were recruited to pa rticipate in the study during the weekends and asked for contact information and any informa tion on potential prestudy illness or swimming activities. The following day, te lephone interviews were conducte d to obtain information from these recruits on water exposure and any type of food eaten while at the beach. This information allowed the researchers to categorize the participants as swimmers or nonswimmers. Additionally, 7 to 10 days after the follow-up telephone interview, the study participants were interviewed again via telephone to gather info rmation on any poststudy, mid-week swimming activities, any illness, any perceived symptoms, and the duration of any perceived symptoms.

Water samples were collected on the weekend days from 3 sampling points (50 to 150 m apart and 1 m in depth) at each beach in the study and in locations of high bather density. The water samples were analyzed for the following microbial indicators: fecal coliforms, E. coli, Klebsiella spp., fecal streptococci/enterococci, staphylococci, P. aeruginosa

, Candida albicans

, and total fungi. The beaches were categorized as “relat ively unpolluted” and “barely acceptable” for each of the microbial indicators analyzed.

Study results suggest that overall perceived sy mptom rates were higher for swimmers than nonswimmers, and the rates of GI illness, ear, eye, skin symptoms, respiratory illness, fever, and

total illness were significantly higher for swimmers as compared to nonswimmers. Furthermore, swimming-associated symptom rates for GI, ski n, and respiratory symptoms, and total illness were significantly higher at barely acceptabl e beaches compared to relatively unpolluted beaches, indicating that the perceived symptoms were pollution-related. The authors concluded

that E. coli is the best indicator of health effects—mainly gastroenteritis and skin symptoms— associated with swimming at beaches in Hong K ong. Staphylococci was al so correlated with ear symptoms and respiratory and total illness. A linear relationship was established between the geometric mean of E. coli densities and combined gastroenteritis and skin symptom rates for individual beaches. However, no significant relationship between E. coli and gastroenteritis or skin symptom rates, nor staphylococci and ear or sore throat symptoms, could be established.

United States (Haile et al., 1999) Haile et al. (1999) conducted the first large epidemiological study of persons who swim in marine recreational waters contaminated by urba n runoff. This study is included in the metaanalyses of Wade et al. (2003) and Zmirou et al. (2003). The exposures of interest were swimming distances from st orm drains, levels of bacterial i ndicators (total coliforms, fecal coliforms, enterococci, and E. coli ) and presence of human enteri c viruses. The study assessed persons who immersed their heads in ocean wa ter at three beaches in Santa Monica Bay,

California.

The study included 15,492 subjects, 13,278 of whom were contacted for follow-up health interviews and 10,459 of whom were ultimately included in the analysis. Distance from the storm drain where participants sw am was noted (0, 1 to 50, 51 to 100, or 400+ yds). During the follow-up telephone interview, the occurrence of the following health outcomes was noted: fever, chills, eye discharge, earache, ear discharge, skin rash, infected cuts, nausea, vomiting,U.S. Environmental Protection Agency

February 2009 26 diarrhea, diarrhea with blood, st omach pain, coughing, coughing w ith phlegm, nasal congestion,

and sore throat.

The statistical analysis addressed, (1) are there different risks of specific outcomes among subjects swimming at different di stances from a storm drain? and (2) are risks of specific outcomes associated with levels of specifi c bacterial indicators or enteric viruses?

The results of the study indicated that the risks of several health outcomes were higher for people

who swam at storm drain locations compared to those who swam va rious distances from a drain. Other relevant findings include th e following: (1) statistically significant increases in fever, chills, ear discharge, cough and phlegm, and respiratory disease in people who swam at a storm

drain than those who swam 400+ yds from a drain; (2) the in crease in “hig hly credible gastrointestinal symptoms” (i.e., GI illness with vomiting and fever as used in USEPA, 1986) was not statistically significant for those who swam at a drain compared to those who swam 400+ yds from a drain; and (3) no dose-response relationship was associated with swimming closer to a storm drain and illness (one would ex pect a gradient of increasing risk of illness to swimmers the closer they are to a storm drain). Furthermore, swimmers reported adverse health outcomes more often on days when the water samples were positive for viruses, suggesting assays for viruses may be informative for predic ting risk. Notably, the risk of highly credible gastrointestinal illness for t hose swimming at a storm drain lo cation was estimated to be 0.018 (i.e., 18 in 1,000 bathers), which is effectively identic al to the current tolera ble GI illness rate of 0.019 in marine waters (USEPA, 1986). However, Haile and colleagues noted that causal effects may be higher than reported because both distan ce from a storm drain and detections of fecal indicator bacteria are proxies for the presence of water borne pathogens.

Based on the results, the authors concluded that “t here may be increased risk of a broad range of

adverse health effects associated with swimming in ocean water subject to urban runoff....Consequently, the prospect that untreated storm drain r unoff poses a health risk to swimmers is probably relevant to many beaches subject to such runoff, including areas on the East, West, and Gulf coasts of No rth America, as well as numerous beaches on othe r continents.”

Other researchers have concurre d with the Haile study conclusi ons; for example, Grant et al. (2004) stated that “contamination of the surf z one by dry weather runoff apparently increases the

risk that marine recreational bathers will co ntract diarrhea and other acute illnesses.”

New Zealand (McBride et al., 1998) McBride et al. (1998) conducted a cohort study us ing a modified prospective cohort (“Cabelli protocol”) epidemiological study de sign to ascertain the association, if any, be tween illness rates among beachgoers and the degree of fecal contamina tion of marine water from either human or animal sources. This study is included in the me ta-analyses of Wade et al. (2003). It was conducted at seven popular bathing beaches du ring the summer of 1995. Three categories of beaches were selected, two control beaches (c onsidered minimal impact ), two rural beaches (animal waste impacted), and three oxidation pond beaches (human waste-impacted). On each of the 107 interview days, groups of bathers and nonbathers were interviewed at each beach using a standard questionnaire to obtain basic field data, eligibility, demographic information, foods eaten in the past three days that could influence outcome, and contact information. Three to five days following the initial interview, study participants were contac ted to distinguish beachU.S. Environmental Protection Agency

February 2009 27 swimmers and paddlers from nonswimmers and for information regarding illness and onset of symptoms. A swimming-associated illness risk was calculated by comparing illness risks between people who swam or paddled in the water (1,577 total) an d nonexposed individuals (2,307 total).

Additionally, water quality samples were taken on the same day as the initial interview and analyzed for fecal coliforms, E. coli , and enterococci. Samples were taken approximately 10 cm below the water surface, twice per day, from the adult chest and knee depth, and generally from three locations spaced evenly along the beach. Water samples were collected on days when significant bathing occurred, regardless of weather.

Log-linear modeling of the results demonstrated a statistically significant association between illness and enterococci concentration, with the most significant associations observed among paddlers and long-duration swimmers (i.e., swimmi ng more than 30 minutes). No significant relationships were found between the other f ecal indicators a nd health risks. Furthermore, no significant differences in illness risks were found between the human- and animal-impacted beaches, although illness risks at bot h types of beaches were significantly higher than the control

beaches.

The researchers concluded that the overall st udy results were affected by unexpectedly low levels of indicator organisms at the impacted beache s. In addition to requ iring a greater range of fecal contamination at study beaches, the research ers concluded that any future studies designed to strengthen the current study conclusions would re quire larger (sufficient) numbers of bathers at the study locations.

Germany (Wiedenmann et al., 2006) Wiedenmann et al. (2006) performed randomized controlled studies at fi ve public freshwater bathing sites (four lakes and one river site) in Germany that had complied with current European

standards for at least the three previous bathing seasons. These studies were conducted to obtain a greater scientific basis for the definition of re creational water quality st andards. Sources of fecal contamination potentially impacting the waterbodies included treated and untreated municipal sewage, agricultural runoff, and cont amination from water fowl. Data were not analyzed for differences in health outcomes from exposure to animal versus human fecal

contamination.

A total of 2,196 participants were recruited from the local population. Afte r a pilot study at one of the five locations that included only adults, the study was expanded to include children aged 4 years and up for the other four locations. Approximately two to three days before exposure, participants were interviewed a nd administered a brief medical ex amination. Volunteers deemed unfit for participation were excluded from the study.

On the day of exposure, study pa rticipants were randomized into equal groups of bathers and nonbathers. After arriving at their designated lo cations, study participants were interviewed a second time for information on symptoms occurring after the first intervie w and diet from the preceding two to three days. Bathers were expose d for 10 minutes in designated areas and had toU.S. Environmental Protection Agency

February 2009 28 immerse their head at least three times. Followi ng their exit from the wa ter, bathers weres asked to report whether they had acci dentally swallowed water.

During the exposure period, water samples for micr obiological analysis were collected at 20- minute intervals and analyzed for E. coli , enterococci, C. perfringens , somatic coliphages, aeromonads, and pyocyanine-positive P. aeruginosa . Furthermore, one week following the exposure period, study participants were medically examined and interviewed again. Three weeks later, study participants were mailed a questionnaire to complete.

Data were analyzed for the following disease out comes: acute febrile respiratory infection, common cold, ear and eye ailments, skin infecti ons or symptoms, urinary tract infections, and three definitions of gastroente ritis that were based on th e responses obtained from the questionnaires. Dose-response effects with no -observed-adverse-effect -levels (NOAELs) were

determined for the three different definitions of gastroenteritis and four fecal indicator organisms, E. coli , enterococci, C. perfringens , and somatic coliphages. Relative risks for bathing in waters with leve ls above NOAELs compared with nonbathing ranged from 1.8 (95 percent CI, 1.2 to 2.6) to 4.6 (95 percent CI , 2.1 to10.1), depending on the definition of gastroenteritis that was used. Additionally, swallowing water as compared to not swallowing water resulted in significantly higher attributable risks abov e NOAELs than below NOAELs. Moreover, swallowing water below NOAELs did not result in any significant effect compared with nonbathing, while swallowing water above NOA ELs always produced a significant effect. Based on the results of this study, the authors concluded that the NOAELs for water quality

should be as follows: 100 E. coli , 25 enterococci, 10 somatic coliphages, or 10 C. perfringens per 100 mL. The authors further concluded that a NOAEL approach would be a more robust method to the complex process of setting standards.

United States (Colford et al,. 2005, 2007) Colford et al. (2005) conducted an epidemiological study in Mission Ba y, California, where historically, nearly 20 percent of the routine bacterial samples failed state water quality standards, but the dominant fecal source appears to be nonhuman. Microbial source tracking in Mission Bay has indicated that human fecal sources are minor contributors to overall microbial loading. Moreover, Mission Bay has an unusually long hydraulic residence time compared to other coastal systems, which likely affects the age and viability of waterborne fecal material.

The study focused on whether (1) water contact increased the risk of illness during the two weeks following exposure to water, (2) there were associations between illness and measured levels of traditional indicators of water quality among those individuals w ith water contact, and (3) there were associations between illness and measured levels of nont raditional (a lternative) indicators of water quality among thos e individuals with water contact.

Nearly 8,800 participants were recruited for th is cohort study from the 6 most popular swimming beaches in Mission Bay on weekends and holiday s during the summer of 2003. Each participant provided their current state of h ealth and degree of water exposure during their day at the beach. On the same day, water quality was monitore d for traditional feca l indicator bacteria (enterococci, fecal coliforms, total coliforms). Pa rticipants provided their current state of health and degree of water exposure during their day at the beach. On the same day, water quality wasU.S. Environmental Protection Agency

February 2009 29 monitored for traditional fecal indicator bacter ia (enterococci, fecal coliforms, and total coliforms). A subset of samples was also meas ured for nontraditional or alternative indicators,

such as Bacteroides and viruses (somatic and male-s pecific phages, adenoviruses, and noroviruses). This subset was also tested with new methods for measuring traditional indicators, such as chromogenic substrate or quantitative PCR.

Ten to fourteen days later, the participants were contacted by phone and interviewed about symptoms of illness that occurred since their visit to the beach, including GI illnesses (diarrhea, nausea, stomach pain, cramps, vomiting, and highl y credible GI illness [using two definitions]); respiratory illnesses (cough, cough with phlegm, na sal congestion or runny nose, sore throat, and significant respiratory illness); de rmatologic outcomes (skin rash a nd infected cuts or scrapes); and nonspecific symptoms (fever, chills, eye irritati on, earache, ear discharg e, and eye irritation or redness). Multivariate analyses assessed relationships between health outcomes and degree of

water contact or levels of wa ter quality indicators. These analyses were adjusted for confounding covariates such as age, gender, and ethnicity.

Of the measured health outcome s, only skin rash and diarrhea consistently were significantly elevated in swimmers compared to nonswimmers. For diarrhea, this risk was strongest among children 5 to 12 years old. However, illness risk was not correlated with levels of the traditional water quality indicators used in the study. Of particular note, th e state water quality thresholds for bacterial indicators (sim ilar to the 1986 AWQC for bacter ia) were not predictive of swimming-related illnesses. Similarly, no co rrelation was found between increased risk of

illness and increased levels of most nontraditional water quality indicators m easured in the study. Although a significant associ ation was observed between the leve ls of male-specific coliphage and highly credible GI illness, nausea, cough, a nd fever, these associations were based on far fewer participants. Thus, the researchers ur ged caution in extra polating these results.

The researchers concluded that the results of the study suggest the need for further evaluation of

traditional indicators in circumstances where n onpoint sources of microbial pollution are the

dominant fecal contributors to recreational waters.

United States (Dwight et al., 2004) Dwight et al. (2004) compared ra tes of reported health symptoms among surfers in urban North Orange County, California and rural Santa Cruz County, California during the winters of 1998 and 1999 to determine whether symptoms were asso ciated with exposure to urban runoff. Two cross-sectional surveys of 1,873 su rfers were conducted. Surfers were selected as the study population because of their regular exposure to coas tal waters. Data were gathered on reported health symptoms (diarrhea, vomiting, and sore th roat) experienced during the previous three

months.

Logistic regression was used to estimate adjust ed odds ratios compari ng symptom reporting rates between the two counties, stratified by year. The model included county, water exposure, gender, age, occupation, educational level, annual income, political outlook, and level of concern about water quality.U.S. Environmental Protection Agency

February 2009 30 The results indicate that the urba n participants (North Orange C ounty) reported almost twice as many symptoms overall compared to the rural part icipants (Santa Cruz County) during the first year and slightly more during the second year. In both study years, risk increased across almost every symptom category by an average of about 10 percent for each additi onal 2.5 hour s of water exposure per week. The study did not meas ure water quality at the various sites.

Based on the results, the author s concluded that discharging unt reated urban runoff onto public beaches can pose health risks. Furthemore, large-scale epidemiological studies are needed to further characterize the health risks of people exposed to urban runoff in coastal waters.

United States (SCCWRP 2007-ongoing) The SCCWRP is conducting a series of epidem iological studies to examine the risk of swimming-related illness from waters polluted by nonpoint sources of pollution. The studies are being conducted at three diverse beaches with contamination ranging from mostly human (untreated or poorly treated), to primarily nonhuman (likely avia n), or a mixture of human and nonhuman fecal sources. Water samples at the va rious beaches will be collected at multiple

locations and times and tested for over 30 differe nt microbiological indicato rs. These indicators are grouped into five categories and include the following: (1) traditional fecal indicator bacteria; (2) rapid methods; (3) new, alternative microbial indi cators; (4) microbial source tracking tools; and (5) viruses.

The studies are based on a prospective cohort design. Swimmers will be interviewed at the beach to determine their eligibility to participat e in the study and contacted 10 to 14 days later for a follow-up interview. During the second in terview, study participan ts will be asked to describe illness symptoms that have occurred since the initial interview. The SCCWRP hopes that these studies will help evaluate the relative risk of contracting an illness from swimming at beaches polluted with nonpoint sources. Furtherm ore, the researchers hope to determine whether

the risk of illness under these conditions correlates with traditional indicato r densities and/or new

indicators or methods.U.S. Environmental Protection Agency

February 2009 31 

## IV. O UTBREAK 

## R EPORTS FOR 

## R ECREATIONAL AND 

## D RINKING


## W ATERS

IV.1 Waterborne Disease Surveillance and Outbrea k Reporting in the United States

In the Unites States, formal surveillance data on the occurrence and causes of waterborne disease outbreaks are collected through collaboration between EPA, the Council of State and Territorial Epidemiologists, and CDC. The goals of the surveillance program include characterizing the epidemiology of outbreaks, identifying the agents causing outbreaks as well as trends and risk factors, identifying deficiencies in providing safe drinking water, encouraging health officials to investigate outbreaks, and fostering government and international agency collaboration on waterborne disease prevention (L iang et al., 2006). State, territo rial, and local public health departments are responsible for investigating a nd reporting outbreaks to CDC. Because this reporting is voluntary and originat es with the investigating agency, it is called “passive”

surveillance.

The number of outbreaks reported is a signif icant underestimate of the actual number of outbreaks that occur; the actual number repo rted varies depending on the issues mentioned above, and the extent of underestimation is unknown overall. However, CDC is collaborating with EPA to prepare an estimate of how many wa terborne illnesses occur in the United States (Craun and Calderon, 2006; Messner et al., 2006). The adequacy of this approach depends on good surveillance data and reasonable estimates for under-reporting cases.

CDC defines an outbreak as at least two people who are linked by location of exposure to water, time, and illness (Liang et al., 2006). Evidence mu st implicate water as the probable source of the outbreak, which is often difficult. CDC uses a classification system to rank the strength of the data available based on an outbreak investig ation. The classification system is two-pronged, based on epidemiological and water quality data , and ranges from Cla ss I, which indicates adequate epidemiological and water quality data, to Class IV, which indicates that epidemiologic data was available, although limited, but that th e water quality data wa s either absent or inadequate. CDC weights epidemiologic data more heavily and will include an outbreak that does not include any water quality informati on, provided the epidemiological evidence is sufficient (Liang et al., 2006).

Despite the problems noted above, surveillance studi es provide the best information available on

waterborne disease outbreak s, and such data are critical to adequately characterizing microbial hazards (Embrey, 2002).

IV.2 Summary of CDC Surveillance Reports on Drinking Water

CDC systematically tracks the following water-relat ed parameters in their reports: type of water system (e.g., community, individual, noncommun ity, and bottled); water source (e.g., well, spring, and pond); and the water treatment defi ciency (e.g., source wa ter contamination, treatment deficiency, and distribution deficiency). The classification for deficiencies is further broken down by point of contamination and whether or not the water was treated or meant to beU.S. Environmental Protection Agency

February 2009 32 ingested. Although the report narrative occasionally mentions evidence of a sewage leak or other pathogen origin, based on standard reporting parameters, it is impossible to determine systematically whether the source of contam ination was of human or animal origin.

Craun et al. (2006) summarized CD C statistics on waterborne dise ase since the first year that

data were collected in 1920 to 2002, including outbreaks cause d by chemical and microbial contamination of drinking and recreational wate r. During that time, over 880,000 illnesses have been reported, including over 1,000 deaths—mainly due to typhoid fever before 1940. In terms of microbial etiologies, Giardia and Cryptosporidium have been the most frequently identified from 1990 to 2002, which the authors attribute to th eir high infectivity a nd imperviousness to many conventional water treatment practices. Addtionally, reports have identified a wider variety of pathogens in recent years, in cluding newly emerging pathogens, such as Cyclospora

. Although laboratory testing has improved drama tically, many etiologies of outbreaks of

waterborne disease are still undetermined.

The deficiencies linked with wa terborne disease outlets have also changed. Water treatment deficiencies have become a much less important cause (probably due to strengthened regulations and better water treatment practices), while di stribution system problems have increased in importance. Further, the proportion of outbreak s associated with surface water sources of drinking water has decreased, while the proportion of outbreaks associated with groundwater has stayed constant. Because the predominant pat hogens and causes identified in outbreaks have changed over the years, it is likel y that new regulations or better enforcement of water treatment regulations, as well as advances in both treatment and laborator y detection methodologies, will affect future surveillance reports.

Starting in its 2002 report, CDC began disaggre gating details of individual outbreaks and including data on water quality parameters when available. Table IV.2.1 below summarizes CDC data on individual drinking water-related disease outbreaks from the last three reports covering outbreaks from 1999 to 2004 (Blackburn et al., 2004; Lee et al., 2002; Liang et al., 2006). Outbreaks that may have been related to animal contamination are shaded gray.

IV.3 Summary of Selected Drinking Water Outbre aks Reported in the United States and Internationally

To augment the results reported by CDC, a comp rehensive literature se arch using the U.S. National Library of Medicine’s PubMed system was conducted (see Appendix A for further information). Search terms included “drinking AND water AND outbreak,” which resulted in 495 hits and “waterborne AND outbreak,” which produced 448 hits. The results from these

searches were combined and the result was incl uded in our review if the abstract showed evidence that the etiologic agent was detected in the source water (Table IV.3.1). Although this is a higher bar than what CDC uses to eval uate outbreak evidence, the large quantity of international articles with questionable outbreak investigation methods required a more stringent

standard for inclusion in the review.

The summary of reports from outside the United States and U.S. reports older than 1999 that may provide useful information, but need to be in terpreted within their c ontext. For example,U.S. Environmental Protection Agency

February 2009 33 countries in Northern Europe (Finland, Norway, and Sweden) of ten have municipal water supply systems that use unchlorinated groundwater in areas of sparse populati on (Hanninen et al., 2003), which makes the water supply susceptible under certain common conditions —every outbreak but one reported in Finland between 1998 and 1999 occurred in undisinfected groundwater (Miettinen et al., 2001). Also, several giardiasis outbreaks were associat ed with beavers, but none has been reported in the past 15 years. In the 1980s, researchers considered beavers to be a primary source of zoonotic Giardia in the environment; however, r ecent research suggests that the importance of animals as a risk factor for human infections is unclear (Hunter and Thompson, 2005; Lane and Lloyd, 2002). The outbreak s that are possibly related to animal

sources are shaded in Table IV.3.1.U.S. Environmental Protection AgencyFebruary 200934Table IV.2.1. Select Waterborne Disease Outbreaks Associated with Drinking Waterin the United States Reported by the CDC (1999 to2004)*ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceLiang et al., 2006MontanaS. typhimurium70WellColiforms detected; disinfection malfunction;cross-connectionPossibly poultryLiang et al., 2006WashingtonCampylobacterspp. (spp.)110WellColiforms detected; untreated source; crossconnectionUnknownLiang et al., 2006OhioC. jejuni,spp.Shigella57PondColiforms andE. colidetected; etiologic agentsnot detected; untreated sourceUnknownLiang et al., 2006WisconsinC. jejuni20WellColiformsandE. colidetected; untreated sourceUnknownLiang et al., 2006IllinoisUnidentified180WellE. colidetected; chlorinated sourceUnknownLiang et al., 2006PennsylvaniaNorovirus70PondColiforms detected; cross-connection withuntreated, unpotable waterProbably snowmelt and/orseptic systemLiang et al., 2006New YorkC. jejuni,Entamoebaspp.,Giardiaspp.27WellBroken sewer line swamped the well headSewageLiang et al., 2006OhioC. jejuni,C. lari,Cryptospordiumspp., andHelicobactercanadensis82WellCryptosporidiumspp. detected; cross-connectionwith untreated, unpotable waterUnknownLiang et al., 2006PennsylvaniaUnidentified174WellColiforms detected; sewage pipe break noted;chlorination unit brokenSewageBlackburn et al.,2004ArizonaNaegleria fowleri(meningoencephalitis)2(2 deaths)WellColiforms andN. fowleridetected; untreatedsourceUnknownBlackburn et al.,2004IndianaCryptosporidiumspp.10WellFiltration system bypassed intentionally; welllocated in a high-density septic tank areaPossibly sewageBlackburn et al.,2004New YorkGiardia intestinalis6Well/springPower outage resulted innegative pressure inthe distribution systemPossibly sewageBlackburn et al.,2004AlaskaC. jejuni,Yersiniaenterocolitica12WellColiforms detected; undisinfected source;documented contamination with surface waterSurface waterU.S. Environmental Protection AgencyFebruary 200935ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceBlackburn et al.,2004WisconsinC. jejuni13WellC. jejunidetected; untreated source; documentedcontamination with surface water; well locatednear a chicken coopPossibly chickenfecesBlackburn et al.,2004ArizonaNorovirus71(1 death)WellUnsanitary water dispensing and ice makingdocumentedUnknownBlackburn et al.,2004ConnecticutNorovirus142WellColiforms andE. colidetected; heavy rainsprobably caused surface water infiltration;untreated sourceUnknownBlackburn et al.,2004KansasNorovirus86WellColiformsdetected; untreated sourceUnknownBlackburn et al.,2004; Anderson etal., 2003WyomingNorovirus230(1 hospitalization)WellColiforms and norovirusdetected; wells locatednear septic tanks or outhouses; overloadedseptic system documentedSewageBlackburn et al.,2004PennsylvaniaUnknown19WellNo chlorine residual detectedUnknownLee et al., 2002FloridaG. intestinalis2WellInadequate chlorine documented; pigsmaintained near wellPossibly pigfecesLee et al., 2002MinnesotaG. intestinalis12WellColiforms detected; cross-connection withsewage pipe documentedSewageLee et al., 2002New MexicoG. intestinalis4RiverInadequate or nonexistent filtrationUnknownLee et al., 2002ColoradoG. intestinalis27RiverGiardiadetected; treatment malfunctiondocumentedUnknownLee et al., 2002FloridaG. intestinalis2WellColiforms detected; cross-connection with animaltroughs; inadequate chlorinePossibly animalfecesLee et al., 2002New HampshireG. intestinalis5WellFiltration system malfunction; nonexistentdisinfectionUnknownLee et al., 2002FloridaC. parvum5WellSystem break documented; lowresiduallevels of chlorineUnknownLee et al., 2002MissouriS. typhimurium124(17 hospitalizations)WellInadequatechlorinationUnknownLee et al., 2002New YorkC. jejuni,E. coliO157:H7781(71 hospitalizations;2 deaths)WellE. coliO157:H7 detected; nonexistentdisinfection; heavy rains; cross-connection withseptic system; possible cross-connection withmanure storageProbablysewage; possiblyanimal fecesLee et al., 2002TexasE. coliO157:H722WellInadequate chlorinationUnknownU.S. Environmental Protection AgencyFebruary 200936ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceLee et al., 2002IdahoE. coliO157:H74CanalColiforms detected (100/100mL); untreatedsourcePossiblyagricultural runoffLee et al., 2002IdahoC. jejuni15WellColiforms detected; potential surface water andagricultural runoff documentedPossiblyagricultural runoffLee et al., 2002UtahC. jejuni, E. coliO157:H7,E. coliO111102IrrigationwaterC. jejunidetected; nonpotable sourceUnknownLee et al., 2002CaliforniaE. coliO157:H75CreekFiltered sourcePossibly humanfeces; possiblydeer fecesLee et al., 2002OhioE. coliO157:H729(9 hospitalizations)SurfaceColiforms detected; possible cross-connectionwith animal-contaminated source documentedPossibly animalfecesLee et al., 2002MultistateSalmonella Bareilly84Spring/wellColiforms andE. colidetected; adequatetreatment documentedUnknownLee et al., 2002New MexicoSmall roundstructured virus70SpringColiforms detected; proximity to latrine and septicsystem documentedPossibly sewageLee et al., 2002West VirginiaNorwalk-like virus123WellColiforms detected; sewage contaminationdocumentedSewageLee et al., 2002KansasNorwalk-like virus86WellColiforms detected; improper well constructiondocumentedUnknownLee et al., 2002CaliforniaNorwalk-like virus147WellColiforms detected; untreated sourceUnknownLee et al., 2002FloridaUnknown4WellColiforms detected; improper well constructiondocumented; untreated sourceUnknownLee et al., 2002FloridaUnknown3WellColiforms detected; cross-connection withirrigation well documentedUnknownLee et al., 2002FloridaUnknown6SurfaceCross-connection with irrigation welldocumented; irrigation well proximate to acommercial septic system and garbage containerUnknownLee et al., 2002FloridaUnknown3WellNo chlorine residual detected; well proximate to achicken coopPossibly chickenfecesLee et al., 2002CaliforniaUnknown31WellColiforms detected; untreated sourceUnknownLee et al., 2002WashingtonUnknown46CreekUntreated sourceUnknownLee et al., 2002WashingtonUnknown68WellColiforms detected; horse manure detected atthe siteUnknownU.S. Environmental Protection AgencyFebruary 200937ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceLee et al., 2002FloridaUnknown71WellColiforms detected;Cryptosporidiumoocystsdetected; well contamination with lake waterdocumentedUnknownLee et al., 2002FloridaUnknown2WellColiforms detected; heavy rainfall and unsanitarywell conditions documented; untreated sourceUnknownLee et al., 2002CaliforniaUnknown63IrrigationColiforms detected; nonpotable sourceUnknown* Outbreaks that may have been related to animal contamination are shaded gray.U.S. Environmental Protection AgencyFebruary 200938Table IV.3.1. Select Waterborne Disease Outbreaks Associated with Drinking Water*ReferenceLocationEtiologic AgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceAlamanos et al.,2000GreeceShigella sonnei288(91hospitalizations)WellS. sonneidetected with same resistance profile as clinicalisolates; coliforms and fecal streptococci detected; sourcenot regularly disinfected; nostructural or functional welldamaged noted; well situated near a milk factoryUnknownAmvrosieva etal., 2001BelarusEchovirus 30(aseptic meningitis;gastroenteritis)460River and wellEchovirus 30 and otherenteroviruses detected in drinkingwater and source water;UnknownAmvrosieva etal., 2006BelarusEchovirus 30,echovirus 6,coxsackievirus B5(meningitis;encephalitis;herpangina;myocarditis)1,351Surface reservoirEtiologic agents detected in surface and finished waterUnknownAtherton et al.,1995EnglandCryptosporidium125ReservoirOocysts detected; heavy rain; filter at treatment works hadreceived maintenanceUnknownBell et al., 1995;Bowie et al.,1997; IsaacRenton et al.,1998CanadaToxoplasma gondii(retinochoroiditis;toxoplasmosis;lymphadenopathy)100(plus 12 congenitalcases)Well/reservoirT. gondiioocysts undetected; however, source water isunfiltered and chloraminated, which would not removeoocysts. Multiple epidemiological measures indicated themunicipal water supply as the outbreak source; cats trappednear reservoir were seropositive; heavy rainProbably feline feces(domestic/feral/wild)Brown et al.,2001BermudaNorwalk-like virus448Rainwater catchmentColiforms, Norwalk-like virus, andE. colidetected; watersupply deficiencies documentedProbably sewageCCDR, 2000;Bruce-GreyOwen SoundHealth Unit,2000CanadaE. coliO157:H7,Campylobacterspp.1,346(65 hospitalizations, 6deaths)WellColiforms andE. coliO157:H7 detected;Campylobacterspp. andE. coliO157:H7 detected in animal manure ofadjacent farms (cattle isolatesidentical to human isolates);heavy rain and flooding; chlorinated sourceProbably cattle fecesCDC, 1996Idaho, U.S.S. sonnei82WellColiforms detected, butS. sonneitests negative; heavy rain;poorly draining sewage documentedPossibly sewageCDC, 1998aTajikistanS. typhii8,901(95 deaths)River/ground mix4–400+ CFU/100 mL fecal coliforms detected at tap; majortreatment failures; low pressure resulted in cross-connectionwith wastewater; inadequate chlorination; multipledistribution system failuresUnknownDworkin et al,1996Washington,U.S.C. parvum86WellsColiformsandC. parvumpresumptive oocysts detected;untreated source; treated wastewater from an irrigationsystem leaking into well documented; cattle grazing nearwell documented;Treated wastewaterGlaberman etal., 2002NorthernIrelandC. parvumgenotype)(bovine129Municipalsupply(otherwise unknown)UnknownUnknownU.S. Environmental Protection AgencyFebruary 200939ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceGlaberman etal., 2002NorthernIrelandC. parvum(human genotype)117Municipalsupply(otherwise unknown)UnknownSewageGlaberman etal., 2002NorthernIrelandC. parvum(human genotype)230Municipalsupply(otherwise unknown)C. parvumdetectedWastewaterGoldstein et al.,1996Nevada, U.S.C. parvum78(20 deaths in immunocompromised patientswith cryptosporidiosis)River/lakeNo coliforms or oocystsdetected in source or finished waterduring study; presumptive oocysts detected intermittentlyafter study; municipal supply receives filtration anddisinfection; no malfunctions detectedUnknownHafliger et al.,2000SwitzerlandNorwalk-like virus1,750+WellColiforms, enteroviruses, and Norwalk-like virusesdetected; identical genotypes of clinical and water samplesdocumented; wastewater system defect documentedSewageHanninen et al.,2003FinlandC. jejuni400WellColiforms (1 CFU);C. jejuni;andwell source and tap water; heavyE. coli(1 CFU) detected inprecipitationSurface waterHanninen et al.,2003FinlandC. jejuni1,000WellColiforms (1–66 CFU);E. coli(1–630 CFU); enterococci (3–1,080 CFU) andC. jejunidetected in well source andinfiltrating surface water;C. colifound in porcine fecalsamples; the variety of strains ofCampylobacterspp. foundand proximity to a farm indicated animal fecalcontamination; heavy precipitation; undisinfected sourcePossibly animal fecesHayes et al.,1989Georgia, U.S.Cryptospridium13,000SurfaceCryptosporidiumoocysts detected; oocysts detected incattle feces; filtered and chlorinated source; suboptimalflocculation and filtration noted; sewage overflowdocumented; heavy precipitationPossibly cattle fecesor sewageHowe et al.,2002EnglandC. parvum58Spring/reservoirC. parvumdetected (0.1–0.9 oocysts/L); genotyping ofoocysts suggested animal source; disinfected but unfilteredsource; spring collection chambers in poor repair; cattlefeces on top of spring covers documented; manure spreadon field within 5 m of one well head; heavy rainProbably cattle fecesIsaac-Renton etal., 1994CanadaG. duodenalis124CreekG. duodenaliscysts detected in water and beavers; beaveractivity noted near water intake; beaver, water, and casecysts of the same karotype; unfiltered sourceBeaver fecesIstre et al., 1984Colorado, U.S.G. lamblia(intestinalis)20CreekG. lambliacysts detected; treatment malfunction resulted ininadequate chlorination; other treatment deficienciesdocumented; two beaver dams proximate to water intake;heavy snowfallPossibly beaver fecesKent et al.,1988Massachusetts,U.S.G. lamblia(intestinalis)703Surface reservoirColiforms detected (1–41 CFU/100 mL);G. lambliacystsdetected (7–80/100 gal); disinfected but unfiltered source;malfunction in chlorinator documented; beaver activitydocumented;G. lambliacysts detected in beaver fecesPossibly beaver fecesKukkula et al.,1999FinlandNorwalk-like virus1,700–3 ,000(estimated)LakeColiforms (38–48 CFU/100mL) in tap water detected;Norwalk-like virus detected; filtered and disinfected source;inadequate chlorination documentedUnknownU.S. Environmental Protection AgencyFebruary 200940ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceKuusi et al,2004FinlandC. jejuni463(9 of 113 casesquestioned were hospitalized)Wells/reservoirsColiforms andC. jejunidetected; untreated source; heavyprecipitation and infiltration of surface water into wellsnoted; wells and reservoirs accessible to people andanimalsUnknownLicence et al.,2001ScotlandE. coliO157:H76SpringColiforms,E. coliandE. coliO157:H7 detected in water andsheep feces; untreated source; sheep and deer grazingnear source; human, water, and sheep samplesindistinguishableSheep fecesMacKenzie etal., 1995Wisconsin, U.S.C. parvum403,000 (estimated)LakeC. parvumoocysts detected (0.7–13.2 oocysts/100 L);filtered and disinfected source; increased turbidity; heavyprecipitation/runoffPossibly cattle feces;possibly sewageMaurer andSturcheler,2000SwitzerlandC. jejuni, S sonnei,enteropathogenicE. coli, small roundstructured viruses1,607–2,213(estimated)WellEnteroviruses, small round structured virus detected;sewage pump failure documentedSewageMelby et al.,1991NorwayC. jejuni680Lake/riverColiforms andC. jejunidetected (different serotype fromhuman isolates); untreated source; sheep grazing nearbynoted; sheep infected withcampylobacternotedPossibly sheep fecesNavin et al.,1985Nevada, U.S.G. lamblia(intestinalis)324Wells/river/reservoirGiardiacysts detected in source and treated water (10cysts/3,800L) supply and a beaver in the reservoir waterdistribution site; source waterdisinfected but not filteredPossibly beaver fecesNygard et al.,2003SwedenNorovirus200WellNorovirus detected; untreated source; sewage overflowdocumentedProbably sewageO’Reilly et al,2007; Fong etal., 2007Ohio, USAC. jejuni, norovirus,G intestinalis,S. typhimurium1,450(21 hospitalizations)Well/lakeColiforms (0.1–90 CRI/100 mL);E. coli(0.1–4.0 CFU/100mL); enterococci (0.1–6.6 CFU/100 mL);Arcobacterspp.;coliphages; enteric viruses;C. jejuni; Salmonellaspp.,adenovirus,Cryptosporidiumspp.,andGiardiaspp.detected (all well water samples); heavy rain; irregularsewage disposal noted; geology noted to be prone tocontaminate aquifer; possible cross-connection with LakeErieProbably sewageOlsen et al.,2002Wyoming, USAE. coliO157:H7157(4 hemolytic uremicsyndrome cases)SpringColiforms detected; untreated source; surface watercontamination documented; risk of animal contaminationnoted; heavy rain and runoff; deer and elk feces near springdocumented (but negative forE. coliO157:H7)Possibly deer and elkfecesParshionikar etal., 2003;Gelting et al.,2005; Andersonet al., 2003Wyoming, USANorovirus84WellColiforms andnorovirus detected; overloaded wastewaterdisposal system noted; heavy precipitation; chlorinatormalfunctionSewageRamakrishna etal., 1996IndiaV. choleraeO139475Wells/surfacereservoirsColiforms (10–1,800 MPN/L) andV. cholerae O139detected; chlorination had been discontinuedUnknownU.S. Environmental Protection AgencyFebruary 200941ReferenceLocationEtiologicAgentNumber of CasesWater SourceWater Quality/Environmental InformationPathogenSourceStirling et al.,2001CanadaC. parvum1,907(50 hospitalizations)RiverC. parvumoocysts detected (no coliforms detected);disinfected and filtered source water; treatment deficiencydocumented which resulted in increased turbidity; chlorineresidual levels normalUnknownSwerdlow et al.,1992PeruV. choleraeO116,400(6.673hospitalizations;71 deaths)WellsColiforms (1–1,800/100 mL),V. choloraeO1 detected;untreated source; low water pressure and poor water lineintegrity notedUnknown* Outbreaks that may have been related to animal contamination are shaded gray.U.S. Environmental Protection Agency

February 2009 42 IV.4 Descriptions of Drinking Water Outbreaks with Animal Related-Pathogen Sources

Information in the two outbreak summary tables (Tables IV.2.1 and IV.3.1) indicates that the pathogen source in the majority of drinking water-related outbreaks remains unknown. The majority of outbreaks in both tables occurred in groundwater sources, and often, surface water contamination of the spring or well is the extent of the impli cation. Although the source of pathogens in surface water could be humans or animals, surface water that is subject to agricultural runoff would have a cl oser link to animal pathogens. However, most reports provide little detail regarding pathogen s ource, leaving a critical informa tion gap for the purposes of this

paper.

In this review of drinking water outbreaks, seve ral studies have linked pathogens isolated from patients with water samples, animals, or both (e.g., CCDR 2000; Howe et al., 2002; Licence et al., 2001). The suspected animal sources include b eavers, cats/cougars, deer , elk, pigs, cattle, and chickens/poultry. The animal-related pathogens in these outbreaks were Giardia intestinalis

, Cryptosporidium spp., E. coli O157:H7, Campylobacter spp., Toxoplasma gondii , and S. typhimurium. In addition, Krewski and colleagues ( 2002) describe waterbor ne disease outbreaks

in British Columbia from 1980 to 2000. Of the 24 outbreaks in the records, the suspected source of the pathogen (mostly Giardia and Campylobacter ) was an animal in 21 outbreaks; however, the largest of those outbreaks was caused by Cryptosporidium of human origin. A summary of 288 Canadian drinking water outbreaks re ported between 1974 and 2001 linked 44 (or 15 percent) with animal sources (S chuster et al., 2005); about half of the 25 outbreaks linked to private water supplies in England and Wales listed animals as po ssible contributing factors (Said et al., 2003).

Furthermore, in some studies, investigator s hypothesize about the contamination based on circumstantial evidence. For example, Lee et al. (2002) described a Giardia outbreak where pigs

were housed near a well while Ol sen et al. (2002) noted deer and elk feces near a spring that was the source of water causing an E. coli O157:H7 outbreak in Wyoming. As laboratory methods have become increasingly sophisticated, more i nvestigators are using mo lecular techniques to track pathogen sources. Most i nvestigating agencies do not have the resources to perform such in-depth testing. As these techniques beco me more common and affordable, however, investigators will likely use them more often to shed light on outbreak causes. Three studies are

summarized below to illustrate how advanced la boratory methods can link outbreaks with animal

sources.

• An outbreak of E. coli O157 resulted from drinking fr om an untreated, private supply sourced from a spring located in an area wher e deer and sheep grazed (Licence et al., 2001). Water samples taken one week before th e first illness had elevated coliforms (11 CFU/100 mL) and E. coli (15 CFU/100 mL) showing fecal contamination. After the outbreak, E. coli O157 isolates collected from patient stool, water, and sheep feces were all identical based on pulsed fi eld gel electrophoresis analysis. Interestingly, the six cases were tourists to the area, while the perman ent residents who were also exposed to the contaminated water did not experience any GI symptoms. The authors concluded that low levels of contamination may have provided some level of immunity.U.S. Environmental Protection Agency

February 2009 43 • Researchers also used pulsed field gel electrophoresis to link Giardia isolates from water, beavers, and stool samples from cases fr om an outbreak in British Columbia (IsaacRenton et al., 1994). A creek used as the dr inking water source was chlorinated, but not filtered. The source water was found to be heavily contaminated with Giardia cysts, and

an infected beaver was livin g near the water intake. Wh en the animal was removed, water samples continually tested negative for Giardia cysts.

• A well documented and highly publicized outbreak that was linked to an animal source occurred in Walkerton, Ontario from May to June, 2000. In that municipal water system outbreak, E. coli O157:H7 and Campylobacter spp. were implicated in 1,346 reported cases of gastroenteritis, including 65 hosp italizations, 27 cases of hemolytic uremic syndrome, and six deaths (CCDR, 2000). On e particular well was implicated as the source of contamination based on microbiologica l testing and a history of susceptibility to surface water influence. In addition, hydr ological modeling indicated that the well could have been contaminated by an adjacen t farm—especially under the record-breaking rain conditions present before the outbreak. Subsequent microbiological testing supported

this model. The Investigative Report of the Walkerton Outbreak of Waterborne

Gastroenteritis (Bruce-Grey-Owen Sound Health Un it, 2000) reported that “The molecular subtyping and phage-typing of the E. coli O157:H7 and the Campylobacter spp. isolates from this farm were identical to those found in the ma jority of the human cases. While investigators could not prove the pathogens were present prior to the outbreak, the evidence suggested the pathogens likely originated from cattle manure on this farm.” Other testing of deer feces was negative for E. coli

.

Finally, in another outbreak in British Columbia, T. gondii was implicated (Bowie et al., 1997). The cysts were never detected in the water s ource; however, the author s concluded that the strength of the epidemiologica l and environmental data was indisputable. Although rarely implicated as a waterborne pathogen, T. gondii can have devastating se quelae in fetuses whose mothers are infected—especially in the first part of pregnancy. Toxoplasmosis can also be fatal in immunocompromised people. Felines are the definitive hosts in the Toxoplasma life cycle, and the cysts they excrete are extremely hardy a nd long-lived in the environment. In this outbreak, cats and cougars were impli cated as the source of the pathogen.

IV.5 Summary of Selected Recreational Water Outbreaks

The CDC tracks waterborne disease and outbreaks from drinking water and recreational water,

with the latter includi ng recreational water outbre aks since 1978. CDC’s an alysis of recreational water includes swimming pools, wading pools, sp as, waterslides, interactive fountains, wet decks, and fresh and marine bodies of water; it does not include recreati onal waters associated with cruise ships.

A summary by Craun et al. (2005) that analyzed the recreational water outbreaks in the United

States between 1970 and 2000 illustra tes the difficulties associated with addressing all the data gaps in an outbreak investig ation. During that period, CDC r eceived reports of 259 outbreaks

associated with recreational water. Over two-thir ds were associated with either bacteria or protozoa; over 15 percent had unid entified etiologies and only 7 pe rcent were viral. However, CDC estimates that approximately 80 percent of th e annual illnesses overall in the United StatesU.S. Environmental Protection Agency

February 2009 44 due to known pathogens are of viral origin (M ead et al., 1999). The trend in the number of outbreaks that are reported annua lly has increased dramatically since 1990, probably due to a combination of better reporting practices and the occurrence of more outbreaks.

Of the 259 recreational water outbreaks report ed, only half included any information about possible sources of the contamin ation or contributing factors. In untreated recreational water outbreaks, feces or ill bathers in the water, bath er overcrowding, and the presence of children in diapers accounted for 90 percent of the assumed sources; however, Craun et al. (2005) did not

indicate that these attributions were anything more than assumpti ons and were not reinforced by laboratory analysis, other than measures of microbi al indicators. Further, most of the related assumptions were based on eyewitness reports such as adults seen rinsing diapers in the water and the measure of bather density was subjective. Craun et al. estimated that 18 percent of the

outbreaks were associated with animals and 21 percent were associated with sewage contamination—although the propor tion actually confirmed by la boratory analysis is unknown. Some animal-associated outbreaks may have been cl assified based on the etiological agent itself. For example, because the source of Leptospira is animal urine and leptospirosis is not spread from person-to-person, any waterborne outbreaks of leptospirosis can be assumed to have an animal source (CDC, 2005). Alth ough most cases of leptospirosi s occur in Hawaii, a large

outbreak in 1998 of tria thletes in Illinois an d Wisconsin caused 375 illnesses and 28 hospitalizations (CDC, 1998b).

A summary of the CDC’s surveillance reports since 2000 is provided below:

• During 2001 to 2002 (Yoder et al., 2004), the la rgest number of recreational water outbreaks occurred since repor ting began in 1978. In total, 65 outbreaks were reported, with 30 involving gastroenteritis. Fifty pe rcent of the outbreaks i nvolving gastroenteritis

were associated with Cryptosporidium in treated drinking water, followed by E. coli (25 percent) and then noroviru s (25 percent) in freshwater.

• Results from 2003 to 2004 indicate that 26 st ates and Guam reported a total 62 outbreaks associated with recreational water (excluding Vibrio cases) (Dziuban et al., 2006). Of the 62 cases, 20 were confirmed as bacterial, 15 as parasitic, and 6 as viral. For the remaining cases, the etiologic agents were chemical- or toxin-mediated or were not identified. Primary illnesses resulting from these outbreaks included gastroenteritis, dermatitis, and acute respiratory illness. Other illnesses included amebic meningoencephalitis, meningitis, leptospirosis, otitis externa, and mixed illnesses. In addition, 16 states reported a total of 142 Vibrio cases associated with recreational water.

Data for the Vibrio cases were analyzed separately to avoid substantially altering total

waterborne disease outbreak num bers when compared with previous reports. Of the

Vibrio cases, 70 resulted in hospitalization and 9 patients died. The most frequently

isolated Vibrio species was V. vulnificus ; others included V. parahaemolyticus

, V. cholerae

, V. damsela

, V. fluvialis , nonspeciated Vibrio , and mixed Vibrio . Nearly all

Vibrio cases were exposed to recreati onal water in a coastal state.

CDC data on recreational water-related disease outbreaks from the last three reports covering 1999 to 2004 (Dziuban et al., 2006; Lee et al., 2002; Yoder et al., 2004) are summarized in

Table IV.5.1. Individual studies identified in the scien tific literature also are included in theU.S. Environmental Protection AgencyFebruary 200945Table IV.5.1. Select WaterborneDisease Outbreaks Associated with RecreationalWater in the United States Reported by the CDC(1999 to2004)*ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceWheeler etal., 20072California2004CryptosporidiumAcutegastrointestinalillness (AGI)315Water parkCryptosporidiumoocystsdetected in backwash and onsand filters;CryptosporidiumorGiardianot detected fromthe county park lake and threewells; fecal coliform notdetected in well-waterUnknownDziuban etal., 20063California2004CryptosporidiumAGI336PoolCryptosporidiumoocystsdetected in backwash;CryptosporidiumorGiardianotdetected from the county parklake and three wells; fecalcoliform not detected in wellwaterUnknownDziuban etal., 2006Colorado2004CryptosporidiumAGI6PoolUnknownUnknownDziuban etal., 2006Florida2004NorovirusAGI42WaterslideUnknownChild with diarrheaDziuban etal., 2006Georgia2004CryptosporidiumAGI14PoolUnknownUnknownDziuban etal., 2006Guam2004Leptospiraspp.Leptospirosis3RiverUnknownUnknownDziuban etal., 2006Idaho2004NorovirusAGI140PoolUnknownUnknownDziuban etal., 2006Illinois2004P. aeruginosaSkin, acuterespiratory infection(ARI)16Pool, spaUnknownUnknownDziuban etal., 2006Illinois2004P. aeruginosaSkin5SpaUnknownUnknown2Also referenced in Dziuban et al. (2006)3See Wheeler et al. (2007) for additional informationU.S. Environmental Protection AgencyFebruary 200946ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceDziuban etal., 2006Illinois2004CryptosporidiumAGI37Pool, wadingpoolUnknownUnknownDziuban etal., 2006Illinois2004CryptosporidiumAGI8PoolUnknownUnknownDziuban etal., 2006Minnesota2004NorovirusAGI9LakeUnknownUnknownDziuban etal., 2006Missouri2004Giardia intestinalisAGI9LakeUnknownUnknownDziuban etal., 2006NorthCarolina2004P. aeruginosaSkin41SpaUnknownUnknownDziuban etal., 2006Ohio2004C. hominisAGI160Pool, wadingpool,interactivefountainAlthough bothCryptosporidiumoocysts andGiardiacysts were identified inthe pool water, onlyCryptosporidiumoocysts wereisolated from clinicalspecimens.UnknownDziuban etal., 2006Ohio2004P. aeruginosaEar, skin119Pool, spaPseudomonasdetectedHigh bather loadDziuban etal., 2006Oregon2004P. aeruginosaSkin2SpaUnknownUnknownDziuban etal., 20064Oregon2004NorovirusAGI39LakeUnknownUnknownDziuban etal., 2006Vermont2004NorovirusAGI70PoolUnknownUnknownDziuban etal., 2006Wisconsin2004P. aeruginosaSkin, AGI22Pool, spaUnknownUnknownDziuban etal., 2006Wisconsin2004CryptosporidiumAGI6PoolUnknownUnknownDziuban etal., 2006Arkansas2003CryptosporidiumAGI4PoolUnknownUnknownDziuban etal., 2006Connecticut2003Echovirus 9Neurological36PoolUnknownHigh bather load4See Keen et al. (1994) for additional informationU.S. Environmental Protection AgencyFebruary 200947ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceDziuban etal., 2006Connecticut2003Microbe-resistantStaphylococcusinfectionSkin10SpaUnknownUnknownDziuban etal., 2006Georgia2003S. sonneiAGI13LakeFecal coliform detectedBathersDziuban etal., 2006Idaho2003CryptosporidiumAGI4LakeUnknownUnknownDziuban etal., 2006Illinois2003P. aeruginosaSkin52SpaPseudomonasdetectedPotted plantDziuban etal., 2006Iowa2003Cryptosporidium; G.intestinalisAGI63WadingpoolUnknownUnknownDziuban etal., 2006Kansas2003C. hominisAGI617Pools, wadingpoolsUnknownLikely children whocontinued to swimwhile ill with diarrheaDziuban etal., 2006Maryland2003S. sonnei;P.shigelloidesAGI65LakeFecal coliform andE. colidetectedDiapers, dumpingwasteDziuban etal., 20065Mass.2003G. intestinalisAGI149PoolNotconductedUnknownDziuban etal., 2006NorthCarolina2003N. fowleriNeuro1LakeUnknownUnknownDziuban etal., 2006Ohio2003P. aeruginosaSkin17Pool,spaUnknownUnknownDziuban etal., 2006Ohio2003P. shigelloidesAGI3LakeUnknownUnknownDziuban etal., 2006Oregon2003S. sonneiAGI56InteractivefountainFecal coliform andE. colidetectedUnknownDziuban etal., 2006Wyoming2003P. shigelloidesAGI2ReservoirUnknownUnknownKatz et al.,20066Mass.2003G. intestinalisAGI149PoolNot conductedChildrens’ pool5See Katz et al. (2006) for additional information6Also referenced by Dziuban et al. (2006)U.S. Environmental Protection AgencyFebruary 200948ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceIwamoto etal., 20057Georgia,2003S. sonneiGastroenteritis17LakeFecal coliform detected (160fecal coliform bacteria per 100mL);Shigellanot detectedFecal contaminationof lake water by aninfected swimmerYoder et al.,2004Alaska2002P. aeruginosaSkin110Pool/spaP. aeruginosadetectedUnknownYoder et al.,2004Alaska2002P. aeruginosa(suspected etiologybased on clinicalsyndrome andsetting)Skin3Pool/spaUnknownUnknownYoder et al.,2004Colorado2002P. aeruginosaSkin12Pool/spaP. aeruginosadetectedUnknownYoder et al.,2004Florida2002N. fowleriMeningoencephalitis1LakeUnknownUnknownYoder et al.,2004Florida2002N. fowleriMeningoencephalitis1LakeUnknownUnknownYoder et al.,2004Georgia2002Cryptosporidiumspp.Gastroenteritis3Wading poolUnknownFecal accidentYoder et al.,2004Georgia2002N. fowleriMeningoencephalitis1RiverUnknownUnknownYoder et al.,2004Iowa2002P. aeruginosa(suspected etiologybased on clinicalsyndrome andsetting)Skin24Pool/spaUnknownUnknownYoder et al.,2004Maine2002E. coliO157:H7Gastroenteritis9WadingpoolUnknownUnknownYoder et al.,2004Maryland2002P. aeruginosa(suspected etiologybased on clinicalsyndrome andsetting)Skin3SpaUnknownUnknownYoder et al.,2004Mass.2002Cryptosporidiumspp.Gastroenteritis767PoolUnknownUnknown7Also referenced in Dziuban et al. (2006)U.S. Environmental Protection AgencyFebruary 200949ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceYoder et al.,2004Minnesota2002NorovirusGastroenteritis11LakeUnknownUnknownYoder et al.,2004Minnesota2002NorovirusGastroenteritis36PoolUnknownUnknownYoder et al.,2004Minnesota2002Cryptosporidiumspp.Gastroenteritis52Indoor poolUnknownUnknownYoder et al.,2004Minnesota2002Cryptosporidiumspp.Gastroenteritis41PoolUnknownUnknownYoder et al.,2004Minnesota2002Cryptosporidiumspp.Gastroenteritis16PoolUnknownUnknownYoder et al.,2004Ohio2002P. aeruginosaSkin18SpaP. aeruginosadetectedUnknownYoder et al.,2004Ohio2002P. aeruginosaSkin31Pool/spaP. aeruginosadetectedUnknownYoder et al.,2004Oregon2002Avian schistosomes(suspected etiologybased on clinicalsyndrome andsetting)Skin19LakeUnknownUnknownYoder et al.,2004Texas2002CryptosporidiumhominisGastroenteritis54WadingpoolThe species ofCryptosporidiumthat infectshumans and monkeysDiaper-aged childrenYoder et al.,2004Wisconsin2002NorovirusGastroenteritis15PoolUnknownUnknownYoder et al.,2004Wisconsin2002NorovirusGastroenteritis44LakeE. colidetectedBathers or dumpingsewage from boatsYoder et al.,2004Wyoming2002Cryptosporidiumspp.Gastroenteritis3LakeUnknownUnknownYoder et al.,2004Wyoming2002G. intestinalisGastroenteritis2RiverUnknownHuman or animalcontaminationCauser etal., 20058Illinois2001CryptosporidiumGastroenteritis358PoolCryptosporidiumoocystsdetectedFecal accident bypark visitor8Also referenced in Yoder et al. (2004)U.S. Environmental Protection AgencyFebruary 200950ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceYoder et al.,Colorado2001S. sonneiGastroenteritis33InteractiveUnknownUnknown2004fountainYoder et al.,Florida2001P. aeruginosaSkin34PoolUnknownUnknown2004(suspected etiologybased on clinicalsyndrome andsetting)Yoder et al.,2004Florida2001P. aeruginosaSkin53SpaP. aeruginosadetectedUnknownYoder et al.,Florida2001P. aeruginosaSkin7SpaUnknownUnknown2004(suspected etiologybased on clinicalsyndrome andsetting)Yoder et al.,20049Illinois2001CryptosporidiumhominisGastroenteritis358PoolCryptosporidiumoocystsdetected; the species ofCryptosporidiumthat infectshumans and monkeysFecal accident bypark visitorYoder et al.,2004Iowa2001S. sonneiGastroenteritis45WadingpoolUnknownUnknownYoder et al.,Maine2001P. aeruginosaSkin21SpaUnknownUnknown2004(suspected etiologybased on clinicalsyndrome andsetting)Yoder et al.,Maryland2001P. aeruginosaSkin8SpaUnknownUnknown2004(suspected etiologybased on clinicalsyndrome andsetting)Yoder et al.,Minnesota2001E. coliO157:H7Gastroenteritis20LakeFecal coliform detectedGeese2004Yoder et al.,Minnesota2001NorovirusGastroenteritis40LakeUnknownUnknown20049See Causer et al. (2005)for additional informationU.S. Environmental Protection AgencyFebruary 200951ReferenceLocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater SourceWater QualityInformationPathogen SourceYoder et al.,2004Minnesota2001E. coliO26:NMGastroenteritis4LakeUnknownUnknownYoder et al.,2004Minnesota2001P. aeruginosaSkin6SpaP. aeruginosadetectedUnknownYoder et al.,2004Nebraska2001Cryptosporidiumspp.Gastroenteritis157PoolsUnknownUnknownYoder et al.,2004Nebraska2001Cryptosporidiumspp.Gastroenteritis21PoolUnknownUnknownYoder et al.,2004Nebraska2001P. aeruginosa(suspected etiologybased on clinicalsyndrome andsetting)Skin9Pool/spaUnknownUnknownYoder et al.,2004, 2004Oklahoma2001N. fowleriMeningoencephalitis1LakeUnknownUnknownYoder et al.,2004Penn.2001P. aeruginosaSkin2SpaP. aeruginosadetectedUnknownYoder et al.,2004Penn.2001P. aeruginosa(suspected etiologybased on clinicalsyndrome andsetting)Skin42SpaUnknownUnknownYoder et al.,2004Penn.2001Bacillusspp.Skin20SpaBacillusdetectedUnknownYoder et al.,2004Penn.2001Staphylococcusspp.(suspected etiologybased on clinicalsyndrome andsetting)Skin3SpaUnknownUnknownYoder et al.,2004SouthCarolina2001E. coliO157:H7Gastroenteritis45LakeFecal coliforms detectedFecal contaminationYoder et al.,2004, 2004Texas2001N. fowleriMeningoencephalitis1LakeUnknownUnknownYoder et al.,2004, 2004Texas2001N. fowleriMeningoencephalitis1LakeUnknownUnknownU.S. Environmental Protection AgencyFebruary 2009 52Reference LocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater Source Water Quality Information Pathogen SourceYoder et al.,2004, 2004Texas 2001N. fowleriMeningoencephalitis1 Lake Unknown UnknownYoder et al.,2004, 2004Texas 2001N. fowleriMeningoencephalitis1 Lake Unknown UnknownYoder et al.,2004Washington 2001P. aeruginosaSkin 3 SpaP. aeruginosadetected UnknownYoder et al.,2004Wisconsin 2001P. aeruginosa(suspected etiologybased on clinicalsyndrome andsetting)Skin 7 Spa Unknown UnknownYoder et al.,2004Wyoming 2001Cryptosporidiumspp.Gastroenteritis 2Flow-throughpool/hot springUnknown UnknownMathieu etal., 200410Ohio 2000C. parvumGastroenteritis749suspectedcases;144laboratoryconfirmedPoolC. parvum(both the humanand bovine genotypes)detected in water and sandfilter samplesFecal accidentsLee et al.,2002Alaska 2000P. aeruginosaSkin 29 Pool/hot tubP. aeruginosadetected High bather loadLee et al.,2002Arkansas 2000P. aeruginosaSkin 26 Pool/hot tub Unknown UnknownLee et al.,2002California 2000N. fowleriMeningoencephalitis1 Mudhole Unknown UnknownLee et al.,2002California 2000Schistosomes(suspected etiologybased on clinicalsyndrome andsetting)Skin 6 Pond Unknown Unknown10Also referenced in Lee et al. (2002)U.S. Environmental Protection AgencyFebruary 2009 53Reference LocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater Source Water Quality Information Pathogen SourceLee et al.,2002California 2000Schistosomes(suspected etiologybased on clinicalsyndrome andsetting)Skin 4 Pond Unknown UnknownLee et al.,2002Colorado 2000C. parvumGastroenteritis 112 Pool Unknown UnknownLee et al.,2002Florida 2000C. parvumGastroenteritis 3 Pool Unknown Fecal materialLee et al.,2002Florida 2000C. parvumGastroenteritis 5 Pool Unknown Ill childLee et al.,2002Florida 2000C. parvumGastroenteritis 19 Pool Unknown UnknownLee et al.,2002Florida 2000C. parvumGastroenteritis 5 Pool UnknownFecal accidents by illchildLee et al.,2002Florida 2000N. fowleriMeningoencephalitis1 Unknown Unknown UnknownLee et al.,2002Florida 2000P. aeruginosa(suspected etiologybased on clinicalsyndrome)Skin 6 Hot tub Unknown UnknownLee et al.,2002Georgia 2000C. parvumGastroenteritis 36 Pool Unknown UnknownLee et al.,2002Guam 2000LeptospirainterrogansLeptospirosis 21 Lake Unknown UnknownLee et al.,2002Maine 2000P. aeruginosaSkin 9 Hot tub/pool Unknown UnknownLee et al.,2002Maine 2000P. aeruginosaSkin 11 Hot tubP. aeruginosadetected UnknownLee et al.,2002Minnesota 2000C. parvumGastroenteritis 220 Lake UnknownWashing babieswhile changingdiapersLee et al.,2002Minnesota 2000S. sonneiGastroenteritis 15 Lake/pond Unknown UnknownLee et al.,2002Minnesota 2000C. parvumGastroenteritis 7 Pool Unknown UnknownU.S. Environmental Protection AgencyFebruary 2009 54Reference LocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater Source Water Quality Information Pathogen SourceLee et al.,2002Minnesota 2000C. parvumGastroenteritis 6 PoolC. parvumnot detected UnknownLee et al.,2002Minnesota 2000S. sonneiGastroenteritis 25 LakeShigellanot detected Fecal accidentsLee et al.,2002Minnesota 2000C. parvumGastroenteritis 4 Pool Unknown UnknownLee et al.,2002Minnesota 2000P. aeruginosaSkin 16 Hot tub Unknown UnknownLee et al.,2002Missouri 2000Shigella flexneriGastroenteritis 6 Wading pool Unknown UnknownLee et al.,2002Nebraska 2000C. parvumGastroenteritis 225 Pools Unknown Fecal accidentsLee et al.,200211Ohio 2000C. parvumGastroenteritis 700 Pool UnknownHigh bather load;multiple fecalaccidentsLee et al.,2002SouthCarolina2000C. parvumGastroenteritis 26 Pool Coliforms not detected UnknownLee et al.,2002Texas 2000N. fowleriMeningoencephalitis1 Lake Unknown UnknownLee et al.,2002Washington 2000P. aeruginosa(suspected etiologybased on clinicalsyndrome)Skin 10 Pool/hot tub Unknown UnknownLee et al.,2002Wisconsin 2000 Norwalk-like virus Gastroenteritis 9 Pool Unknown UnknownBruce et al.,200312Washington 1999E. coliO157:H7Gastroenteritis, 3cases of hemolyticuremic syndrome37 LakeE. coliO157:H7 detectedPossible fecalaccident.; noagricultural sourcesidentifiedLee et al.,2002Arkansas 1999P. aeruginosaSkin 10 PoolP. aeruginosadetected UnknownLee et al.,2002Colorado 1999P. aeruginosaSkin 19 Hot tubP. aeruginosadetected Unknown11See Mathieu et al. (2004) for additional information12Also referenced in Lee et al. (2002)U.S. Environmental Protection AgencyFebruary 2009 55Reference LocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater Source Water Quality Information Pathogen SourceLee et al.,2002Colorado 1999P. aeruginosa(suspected etiologybased on clinicalsyndrome)Skin 5 Hot tub Unknown UnknownLee et al.,200213Connecticut 1999E. coliO121:H19 Gastroenteritis 11 LakeE. coliand shiga toxins notdetected in lake; total andfecal coliforms detected(results differ slightly from thatstated in McCarthy paper)Toddler with severediarrheaLee et al.,2002Florida 1999Campylobacter jejuniGastroenteritis 6 Pool Unknown UnknownLee et al.,2002Florida1999S. sonnei,C. parvumGastroenteritis 38InteractivefountainColiforms detected; fecalcoliforms not detectedUnknownLee et al.,2002Florida 1999C. parvumGastroenteritis 6 Pool Unknown UnknownLee et al.,2002Florida 1999E. coliO157:H7 Gastroenteritis 2 Ditch water Unknown UnknownLee et al.,2002Florida 1999N. fowleriMeningoencephalitis1 Pond Unknown UnknownLee et al.,2002Idaho 1999 Norwalk-like virus Gastroenteritis 25 Hot springs Unknown UnknownLee et al.,2002Mass. 1999G. intestinalisGastroenteritis 18 Pond Total coliforms detected UnknownLee et al.,2002Minnesota 1999C. parvumGastroenteritis 10 Pool Unknown UnknownLee et al.,2002Nebraska 1999E. coliO157:H7 Gastroenteritis 7 Wading pool Unknown UnknownLee et al.,2002New York 1999 Norwalk-like virus Gastroenteritis 168 Lake Unknown Feces13See McCarthy et al. (2001)for additional informationU.S. Environmental Protection AgencyFebruary 2009 56Reference LocationYear ofOutbreakEtiologic AgentPredominantIllness/SymptomsNumberof CasesWater Source Water Quality Information Pathogen SourceLee et al.,2002Oregon 1999Schistosomes(suspected etiologybased on clinicalsyndrome andsetting)Skin 2 Lake Unknown UnknownLee et al.,2002Vermont 1999P. aeruginosa(suspected etiologybased on clinicalsyndrome)Skin 9 Hot tub Unknown UnknownLee et al.,200214Washington 1999E. coliO157:H7 Gastroenteritis 36 LakeE. coliO157:H7 detected UnknownLee et al.,2002Wisconsin 1999C. parvumGastroenteritis 10 Pool Unknown UnknownLee et al.,2002Wisconsin 1999E. coliO157:H7 Gastroenteritis 5 Lake/pondTotal and fecal coliformdetected by did not exceedregulatory levels; one sampletested forE. coliO157:H7 wasnegativeUnknownSamadpouret al., 200215Washington1999E. coliO157:H7Gastroenteritis36LakeE. coliO157:H7 detected inhuman and duck fecesPossible humanfeces, but duck fecescould have helpedto sustaincontamination for alonger period of timeMcCarthy etal., 200116Connecticut 1999E. coliO121Gastroenteritis;hemolytic uremicsyndrome11 LakeE. colinot detected in lakewater;E. colidetected in waterfrom storm drain; Shiga toxin–producing strain not detected(results differ slightly fromthose reported in Lee et al.,2002)Toddler with severediarrhea* Outbreaks that may have been related to animal contamination are shaded gray.14See Bruce et al. (2003) and Samadpour etal. (2002) for additional information15Also referenced in Lee et al. (2002)16Also referenced in Lee et al. (2002)U.S. Environmental Protection Agency

February 2009 57 table (see Appendix A). Outbreaks caused by Legionella spp. were not included in the table because they are not relevant to the analys is. Table IV.5.1 is sorted by outbreak year (descending order) followed by author and year, and then location (alphabetically). Outbreaks that may have been related to animal contamination are shaded gray.

IV.6 Summary of Selected Recreational Water Outb reaks Reported in the United States and Internationally

To augment the results reported by the CDC, a comprehensive literature search was conducted (see Appendix A for further detail). Studies for which the Abstracts from the literature identified were reviewed, and studies were included if the ab stract showed evidence th at the etiologic agent

was detected in the source water were included in Table IV.6.1. As mentioned previously, this is a higher bar than what the CDC uses to evalua te outbreak evidence, but the large number of international articles with questionable outbreak investigation methods required a more stringent

standard for inclusion. The articles are cross-referenced to the CDC table accordingly. The table is sorted by outbreak year (descending orde r) followed by study author (alphabetically) and location (alphabetically). Outbre aks that may have been related to animal contamination are shaded gray.

IV.7 Descriptions of Recreational Water Ou tbreaks with Animal Related-Pathogen

Sources

Information from the two outbreak summary tabl es (Tables IV.5.1 and IV.6.1) indicates that the pathogen source in the majority of recreational wate r-related outbreaks re mains unknown. All of

the outbreak studies that cited an animal source we re based in natural water sources that include lakes, streams, a swimming area with water fe d by a brook, and a canal. The etiologic agents

were E. coli spp. (n=5), Schistosomes spp. (n=2), and Leptospira spp. (n=1). E. coli was associated with cattle , deer, or duck feces; Schistosomes spp. was associated with snails; and Leptospira spp. was associated with rat urine. Five studies identified animal sources as part of their environmental investigati on. Three additional studies cite d animal-related pathogens as a potential source; however, environmental sampli ng was not conducted to support this claim. Summaries of these studies are provided below.

IV.7.1 Environmental Sampling Including Animal Sources

Cornwell, Southwest England (cattle feces) In 2004, seven children were infected with E. coli O157:H7 after playing in a stream located in Cornwell, southwest England (Ihekweazu et al., 2006). Environmental samples from the stream and cattle grazing on the surroundin g fields above the stream were analyzed; both the water and cattle feces were found to be positive for E. coli O157:H7. Stool samples from all seven cases

were confirmed E. coli phage type 21/28, though none of the environmental isolates were phage type 21/28, including the cattle fece s. Regardless, cattle feces, according to the study authors,

remains the most likes source of stream contamin ation. Heavy rainfall occurring two days prior

to the outbreak increased the likelihood that cattle feces we re the potentia l source of

contamination since the fecal matter could have b een washed into the str eam. Another potential source of contamination was sewage from overflow drains located around the stream.U.S. Environmental Protection AgencyFebruary 2009 58Table IV.6.1. Select Waterborne Disease Outbreaks Associated with Recreational WaterReference LocationYear ofOutbreakEtiologicAgentPredominantIllnessNumberof CasesWaterSourceWater Quality InformationPathogenSourceCCDR, 2005BritishColumbia,Canada2004E. coliO157:H7Gastroenteritis10(8 (confirmed;2 probable)PoolElevated fecal indicators detected(sample 1: 2,200 fecal coliforms/100 mL,1500E. coli/100 mL; sample 2: 16,000fecal coliforms/100 mL, 14,400E. coli/100 mL); E. coliO157:H7 not detectedOverloaded andblocked stormsewerIhekweazu etal., 2006Cornwall,U.K.2004E. coliO157ConfirmedE.coliO157 phagetype 21/287StreamE. coli O157detected in stream and incattle feces in the catchment area of thestream; none of the environmentalisolates were phage type 21/28Cattle feces and/orsewage overflowVerma et al.,2007Trafford, U.K. 2004E. coliO157Gastroenteritisand hemolyticuremicsyndrome(HUS)8 GI and 2HUSPoolE. coliO157 not detected; blockage tochlorine system notedUnknownJones et al.,2006SouthwestEngland,U.K.2003CryptosporidiumGastroenteritis 63 PoolColiform detected (2,100 coliforms, 40E.coliper cu mm)UnknownLouie et al.,2004Surrey,Canada2003C. parvumCryptosporidiosis33 PoolC. parvumdetected Fecal accidentsEnk et al.,2003MinasGerais, Brazil2002SchistosomamansoniAcuteschistosomiasis17Pool(waterprovided bynearbybrook)Schistosoma mansonidetected in nearbysnailsSnailsHoebe et al.,2004TheNetherlands2002 Norovirus Gastroenteritis 90 PoolColiform bacteria detected (>1,000organisms/mL); enterococci detected(3,500 organisms/100 mL);E. colidetected (7,700 organisms/100 mL);norovirus detectedLikely children inwater fountainTate et al.,2003U.K. 2002P.aeruginosaFolliculitis 35 PoolP. aeruginosanot detected in water, butdetected on inflatable toyInfected batherBruneau etal., 2004MontrealCentre,Canada2001E. coliO157:H7Gastroenteritis 4 Beach6-162 fecal coliforms/100mL detected.Three strains ofE. coliO157:H7 foundFecal accidents (bychildren or adults)U.S. Environmental Protection AgencyFebruary 2009 59Reference LocationYear ofOutbreakEtiologicAgentPredominantIllnessNumberof CasesWaterSourceWater Quality InformationPathogenSourceHauri et al.,2005Kassel,Germany2001 Echovirus 30Asepticmeningitis215 PondAn echovirus 30 sequence obtained fromone pond water sample showed a 99%nucleotide and 100% amino-acidhomology with patient isolates. Weeklytesting for total coliforms, fecal coliforms,enterococci,Staphylococcus aureusnever exceed European Union bathingguidelinesLikely human fecesMaunula etal., 2004Helsinki,Finland2001Norovirus;astrovirusGastroenteritis 242 PoolFecal contamination not detected 2weeks prior to outbreak;E. colidetectedin outlet well 2 weeks after outbreak;norovirus and astrovirus detected.Norovirus detected in outlet well as muchas 8 months after incidentUnknownPerra et al.,2002Rochefort,France2001Leptospiraspp.Leptospirosis5(3 confirmedand 2possible)CanalE. colidetected (between 100 and2,000/100 mL); 130 rats trapped;prevalence of seropositive rodents was30.8%Rodent urineFeldman etal., 2002California,U.S.1999E. coliO157:NMGastroenteritis7(3 confirmedand 4possible)LakeTotal and fecal coliform counts spiked 2weeks prior to outbreakPossibly from fecesfrom humans,cattle, or deerLévesque etal., 2002Quebec City,Canada1999SchistosomesCercarialdermatitis53LakeFecal coliforms and fecal streptococcidetected but at very low levels;P.aeruginosanot detected;Staphylococcusaureusdetected by at levels are found ingood quality surface water in CanadaOcellate cercaria and non-ocellateisolated detected in snailsSnailsFields et al.,2001Wisconsin,U.S.1998L. micdadeiPontiac Fever 45 Spa/poolHeterotrophic bacteria detected;L.micdadeidetectedUnknownFiorillo et al.,2001Alberta,Canada1998P.aeruginosaPseudomonashot-footsyndrome40 PoolP. aeruginosadetected in inlets, the floor,and a drain to the poolUnknownLim et al.,2004Minnesota,U.S.1998CryptosporidiumGastroenteritis 26 PoolCryptosporidiumnot detected UnknownU.S. Environmental Protection AgencyFebruary 2009 60Reference LocationYear ofOutbreakEtiologicAgentPredominantIllnessNumberof CasesWaterSourceWater Quality InformationPathogenSourceMorgan et al.2002Illinois, U.S. 1998Leptospiraspp.Leptospirosis 98 LakeOne of the 27 lake water samplesdetected a pathogenicLeptospiraspp.;however, no organism was isolated. Twosamples were culture positive; however,both isolated organisms were saprophyticLeptospiraspp.Likely runoff due tounusually rainyseason, howeveranimal reservoirwith epidemic strainwas not foundCransberg etal., 1996TheNetherlands1993E. coliO157:H7Hemolyticuremicsyndrome4LakeO157:H7-DNA not detected, but samplingoccurred ~2 weeks after date of exposurePossibly human orcattle fecesJoce et al.,1991Doncaster,U.K.1988CryptosporidiumGastroenteritis 79 PoolCryptosporidiumoocysts detected inlearner pool;Cryptosporidiumoocysts notdetected in main pool; rotavirus detectedin learner poolSewage from mainsewerPorter et al.,1988New Jersey,U.S.1985GiardiaGastroenteritis 9 PoolColiform not detected; standard bacterialplate counts of 1-2 per mL detectedFecal accidentSorvillo et al.,1988California,U.S.1985ShigellasonneiGastroenteritis 68Humanmade lakeHigh fecal coliform detectedDirect bather con-taminationKhabbaz etal., 1983Georgia, U.S. 1981P.aeruginosaSkin 75 Pool(s)P. aeruginosaserotype 0:9 detected UnknownReid andPorter, 1981U.K. 1980P.aeruginosaOtitis externa 18 PoolP. aeruginosadetected in swabs fromvarious places around pool and vacuumbag used to clean poolUnknownBaron et al.,1982Michigan,U.S.1979NorwalkagentAGI 121 LakeFecal coliform detected but withinacceptable range (<200 colonies per 100mL of water)UnknownKappus et al.,1982Ohio, U.S. 1977NorwalkagentAGI 103 PoolModerate numbers of fecal coliformdetected; total coliform (1/100 mL), fecalcoliform (1/100 mL), and fecalstreptococci (4/100 mL to 9/100 mL)detected in samples sent to EPA; poolchlorinator was not functioning at time ofoutbreakUnknownRosenberg etal., 1976Iowa, U.S. 1974S. sonneiGastroenteritis 31 RiverFecal coliform detected (mean=17,500organisms per 100 mL);Shigella sonneidetectedLikely sewagetreatment plantU.S. Environmental Protection Agency

February 2009 61 Minas Gerais, Brazil (snails)

Seventeen cases of acute schistosomiasis occurre d in Minas Gerais, Brazi l in 2002 (Enk et al., 2003). Affected individuals bathed in a swimmi ng pool at a holiday resort. Water in the pool was provided from a nearby stream . Environmental sampling from the stream included a survey of site snails (mollusks), which tested positive for Schistosoma mansoni

.

Quebec City, Canada (snails) In August 1999, 53 cases of cercarial dermatitis were associated with a recr eational tourist lake in Quebec City, Quebec Canada (Lévesque et al., 2002). Water samples showed low concentrations of fecal pollution. Pseudomonas aeruginosa was not dete cted, though Staphylococcus aureus was detected at levels correspond ing to good quality surface water in Canada. Snails were analyzed for schistosomes , and two forms of furco cercaria type cercariae

were identified. The snails were located in only in one location, which is where 42 of the 53

cases occurred.

Rochefort, France (rodent urine) Five cases of leptospirosis were diagnosed in Rochefort, France in 2001 among teenagers who had swum in the Genouillé canal (Perra et al., 2 002). Water samples revealed moderate quality according to France’s swimming water criteria ( E. coli between 100 to 2,000/100 mL). An environmental survey also included trapping rodent s and conducting a serological status analysis. Results of this analysis showed that the prev alence of seropositive rodents was 30.8 percent, 23.1 percent, 4.6 percent, and 3.8 percent for total antigens, L. icterohaemorrhagiae

, L. saxkoebing

, and L. australis

, respectively. Consequently, rodent urine was believed to be the primary source

of contamination.

Washington, U.S. (duck feces) In 1999, an outbreak of E. coli O157:H7 occurred at a state lake in Vancouver, Washington (Samadpour et al., 2002). The number of cases wa s not reported; however, the CDC summary of

recreational water outbreaks in 1999 and 2000 reported an E. coli O157:H7 outbreak that also

occurred at a state lake in Vancouver and had 396 cases. Envi ronmental sampling occurred a month after the outbreak and consisted of 108 samp les, including water, soil, sand, sediment, and animal fecal matter (cow, coyote, deer, duck, and rabbit). E. coli O157:H7 was recovered from both the water and the duck fecal sample s. Water samples tested positive for Stx

, eaeA , and hly genes by a PCR technique; duck fecal samples tested positive for Stx and eaeA genes. These virulence factors ( Stx

, eaeA , and hly genes) were also found in patient stool samples. Additionally, the study used a pulsed-field gel el ectrophoresis to compare duck feces and water; all isolates resulted in the same restriction fragment patterns. According to the authors, regardless of the evidence, duck feces could s till not be confirmed as the primary fecal

contamination source. Ducks and the lake c ould have been transiently infected by the contaminated water, so the initial source of cont amination could be human feces or anther animal feces. Also, the delay between the outbreak an d the sampling may support the notion that duck feces were not the original source.U.S. Environmental Protection Agency

February 2009 62 IV.7.2 Environmental Sampling not Including Animal Sources

California, U.S. (cattle or deer feces)

An outbreak of seven cases of E. coli O157:nonmotile (NM) occurred at a lake in California during August 1999 (Feldman et al., 2002). Potentia l sources of contamination were fecal matter from cattle or deer based on the presence of a he rd of cattle on the opposite bank of the river and the observation by a park manager of numerous deer in the area. Fecal matter from these animals, however, was not analyzed for E. coli O157:NM.

Minnesota, U.S. (geese feces) According to the CDC summary of recreationa l water outbreaks in 2002 and 2001, there was an

outbreak of E. coli O157:H7 at a lake beach in which 20 cases were identified (Yoder et al., 2004). A brief case description in dicated that an environmental investigation re vealed a high

level of fecal coliforms. According to local officials, the la rge number of geese that occupied the beach during the summer may have contributed to the elevated overall fecal coliform (and thus potentially E. coli O157:H7) levels.

The Netherlands (cattle feces) In 1993, four cases of hemolytic uremic syndrome in children were reported in the Netherlands (Cransberg et al., 1996). All f our affected individuals bathed in a shallow recreational lake within a 5-day period. E. coli O157:H7 was isolated in the stoo l of two of the patients. Water samples were taken 16 days after the latest date of patient contaminati on; however, no O157:H7

DNA was detected in filter-concentr ated lake water after using P CR enhancement. According to the study authors, the contamination source could ha ve been human- or cattle-based. Cattle feces were identified as a plausible source because the wa ter in the lake is derived from ditches, which

drain their water from meadows with cattle. Cattle feces, however, were not analyzed for

O157:H7.U.S. Environmental Protection Agency

February 2009 63 

## V. C OMPILATION OF 

## D ATA AND 

## S UMMARY

Numerous epidemiological investigations have been conducted since th e 1950s to evaluate the association between the density of suitable fecal indicators and the risk of illness to recreational

water users. Reviews of these st udies are provided in Prüss (1998); Sinton et al. (1998); Wade et al. (2003); and Zmirou et al. (2003). Taken as a whole, the weight of evidence from these studies indicates that fecal indicator bacteria (fecal streptococcus / Enterococcus , in particular) are able predict GI and respiratory illnesses from exposure to recrea tional waters (Prüss, 1998; Wade et al., 2003; Zmirou et al., 2003). This broad base of information stems from studies conducted in the following countries (NZME, 2003):

• Australia (Corbett et al ., 1993; Harrington et al. 1993)

• Canada (EHD, 1980; Lightfoot, 1989; Seyfried et al., 1985a,b)

• Egypt (Cabelli, 1983b; El-S harkawi and Hassan, 1979)

• France (Ferley et al., 1989; Foulon et al., 1983)

• Hong Kong (Cheung et al., 1990; Kueh et al., 1995)

• Israel (Fattal et al., 1986, 1987, 1991)

• Netherlands (Medema et al., 1995, 1997)

• New Zealand (McBride et al., 1998)

• South Africa (von Schir nding et al., 1992, 1993)

• Spain (Mariño et al., 1995; Mujeriego et al., 1982)

• United Kingdom (Alexander et al., 1992; Balarajan et al ,. 1991; Fewtrell et al., 1992, 1994; Fleisher et al. 199 6; Kay et al., 1994)

• United States (Cabelli et al., 1983a ; Dufour, 1984; Stevenson, 1953)

However, as indicated above, most of these studies investigated waters that were impacted or influenced by wastewater efflue nt, and close inspection reveal s that few studi es addressed

sources of contamination other than wastewater e ffluent in the investigat ed waters.In fact, prior to 1999, the only peer-reviewed publi cations that substantially addr essed this topic were Cheung et al. (1990), Calderon et al. (1991), and McBride et al. (1998). In recent years, researchers have conducted several additional epidemiological st udies focusing on waters not predominately impacted by wastewater effluent, including Haile et al. (1999); Dwight et al. (2004); Wiedenmann et al. (2006); and Colford et al . (2007). Additionally, the SCCWRP is also conducting a series of epidemiologi cal studies that investigate r ecreational water with various

contamination sources other than wastewater effl uent. Section III.2 provided a brief overview of

each of these studies.

Review of the epidemiological studies that address recreational water predominantly impacted by fecal contamination sources other than wastewater effluent indicates that the results are equivocal. On one hand, Colford et al. (2007) found that the incidence of swimmer illness was not associated with any of the tr aditional fecal indicators at a marine beach with primarily avian contamination. Similarly, Calderon et al. (1991) found no statistically significant association

between swimmers’ illness risk and animal fecal contamination in a freshwater pond. On the other hand, McBride (1993) suggested that if more swimmers had been included in the CalderonU.S. Environmental Protection Agency

February 2009 64 et al. (1991) study, achieving st atistically significan t results would have been possible. Furthermore, the marine bathing study in New Zealand (McBride et al. 1998) indicated that illness risks posed by animal versus human fecal material were not substantially different; however, the study’s limited range of beach contamination precluded the development of a

detailed statistical model of health risks versus indi cator density.

In the first study to be conducted in waters direc tly impacted by urban runoff, Haile et al. (1999) reported rates of illnesses in Southern California similar to those conducted in waters contaminated with domestic sewage. However, this nonpoint runoff sour ce was known to have human sources of fecal contamination (Colford et al., 2007). Similarly, Dwight and colleagues (2004) found that surfers exposed to Southern California urban runoff had higher illness rates than surfers exposed to Northern California rural runoff. The results from the Hong Kong marine water study (Cheung et al., 1990) and the German freshwater stud y (Wiedenmann et al., 2006) are more difficult to interpret regardi ng risks from human versus nonhuman sources because in both studies, the analyses combined the results from sites with different predominant

contamination sources.

In reviewing outbreak information for dri nking water and recreational waters, several overarching points emerge. One is that the pathogen source in the majority of drinking waterrelated outbreaks remains unknown. The source of pathogens in drinking water outbreaks in many cases could have been humans or animal s; however, most reports offered little detail, leaving a critical information gap for the pur poses of this review. Keeping in mind the previously noted limitations of outbreak investig ations, it is noteworthy that several outbreak investigation studies were able to link pathogens isolated from patients with water samples, animals, or both using laboratory an alysis (e.g., CCDR 2000; Howe et al., 2002; Licence et al., 2001). Other reports used circumstantial evid ence to link animal waste to outbreaks, but although compelling, laboratory results were not av ailable to confirm the contamination source.

The animal sources linked to outbreaks included beavers, cats/cougars, deer, elk, pigs, cattle, and chickens/poultry, and the corr esponding animal-related pathoge ns in these outbreaks were

Giardia intestinalis

, Cryptosporidium spp., E. coli O157:H7, Campylobacter spp., Toxoplasma gondii , and S. typhimurium . In general, 14 percent of th e drinking water outbreaks reported by the CDC from 1999 to 2004 were possibly animal-re lated (Blackburn et al., 2004; Lee et al., 2002; Liang et al., 2006). In addition, about 15 pe rcent of Canadian outbreaks between 1974 and 2001 were linked to animal sources (Schuster et al., 2005) and about half of the outbreaks linked to private water supplies in England and Wales lis ted animals as possible factors (Said et al., 2003).

Given that outbreaks are known to be a notoriously poor measure of the actual number of

infections and illnesse s caused by waterborne pathogens (Cra un, 2004), those investigations that link pathogens isolated from patients, water samp les, or both with animals provide unequivocal

evidence that human illnesses can and do occur from animal-based contamination. Unfortunately, the drinking water outbreak literature does not substantially enhance the current ability to differentiate risks from animal- vers us human-related pathogen sources for recreational water exposures in a quantitative manner.U.S. Environmental Protection Agency

February 2009 65 The recreational water outbreak literature (Craun et al., 2005) indicates that of the 259

recreational water outbreaks that occurred in the United States between 1970 and 2000, only approximately half included any information a bout possible sources of the contamination or contributing factors to it. Over two-thirds of the outbreaks that did list possible sources were associated with either bacteria or protozoa; over 15 percent had unidentified etiologies; and 7 percent were viral. In untreated recreational water outbreaks (streams, lakes, etc.), feces or ill bathers in the water, bather ove rcrowding, and the presence of ch ildren in diapers accounted for the vast majority of the assumed sources; how ever, the report by Craun et al. (2005) did not indicate that laboratory analys es, other than microbial indicat or measures, supported these attributions. Their analysis estimated that 18 pe rcent of these outbreaks were associated with animals and that the likely etiologic agents included E. coli spp., Schistosomes spp., and Leptospira spp. E. coli was associated with cattle, deer, or duck feces; Schistosomes spp. were associated with snails; and Leptospira spp. were associated with rat urine. Similar to the drinking water outbreak compilation, the recreational water outbreak literature does not appear to enhance substantially the current state of knowle dge on quantitatively characterizing risks from animal-related pathogen sources compared with human sources for recreational water exposures.

Given that relatively few investigations worldwid e have evaluated the risk to human health from recreational exposure to waters primarily imp acted by sources of contamination other than wastewater effluent, and that the potential range of those sources is broad, the findings from this literature review are not surprising. In fact, the results of this literature review seem consistent with WHO’s (2004) report on zoonose s, which indicated the following:

• Inadequate information exists on differentiati ng human versus anim al strains of human pathogens, both in the field (e.g., pathogen typing and micr obial source tracking) and analytically (e.g., relative infec tivity and pathogenicity). Both of these areas are priorities for targeted research.

• Currently available surveillance data on both sporadic (endemic) and outbreak diseases

are of limited use in unders tanding the importanc e of zoonotic water borne infection. Surveillance for waterborne disease in genera l and waterborne zoonoses in particular has failed to provide a meaningful indication of the associated burden of disease, even in countries with established surveillance systems.

• The risk of exposure to animal-contaminated water is unknown. Studies to define the risk associated with swimming in animal-cont aminated water have not clearly indicated that this type of exposure results in an exce ss illness rate. These results of these studies do not support the premise that all fecally co ntaminated waters should be treated the

same. New research to define the risk of illness posed by an imal fecal wastes is needed (Till et al., 2004).

Furthermore, because pathogens can evolve rapidly depending on their previous host environments due to changing host factors and ot her mechanisms of phenotypic change, it is reasonable to suspect that zoono tic pathogens propagated in anim als would be different from pathogens from human sources. However, data remain incomplete on how zoonotic pathogens

are attenuated or increase inf ectivity or virulence when passaged through animal hosts.U.S. Environmental Protection Agency

February 2009 66 Although conclusive information on differentiating hum an versus animal sour ces of pathogens is lacking, several research organizations and countries have suggested novel approaches for addressing risks from nonhuma n sources (e.g., NZME, 2003; WSSA, 2003). For example, New Zealand, where about 80 percent of total no tified illnesses are zoonotic and potentially waterborne, has recently updated its recreational wa ter quality criteria to address the issue of animal-source waterborne contamination by basing its freshwater guidelines principally on the risks associated with campylobacteriosis using E. coli concentrations as an indicator (Till and McBride, 2004).

In 1992, the New Zealand Department of Health issued provisiona l microbiological water quality guidelines for recreational waters, which advised that exposure to animal fecal microorganisms was much less of a risk than exposure to pa thogens of human origin. In 1998, Sinton et al. concluded that there was no reliable epidemiolo gical information on the relative risks to humans associated with human and animal fecal polluti on in water, but that the high ratio of grazing animals to humans in the country made animal fecal sources a greater health risk to humans than previously assumed. Because Campylobacter -related illness is of grea t public health concern in New Zealand, research has been especially focused on the dairy industry and its impact on microbial water quality (Till a nd McBride, 2004). Thus, although New Zealand’s current marine water guidelines (NZME, 2003) derive directly from W HO’s 2003 recommendations, the country bases its freshwater guidelines principally on the risks associated with campylobacteriosis (using E. coli concentrations as an indicator). Notably, Till and McBride (2004) stated that current inves tigations in New Zealand have fo cused on determining the source

of human Campylobacter infections in part because that information “...may help to shed light

on the relative health risk of animal versus human wastes.”

Based on the results of this detailed literature re view, it appears that: (1) insufficient information is available to support a robust a nd quantitative characterization of the relative risks of human illness from the range of various sources of feca l contamination in recreational waters, and (2) epidemiological studies are more likely to provide salient insights than outbreak investigations. Continued epidemiological work in this arena is consistent with ongoing in ternational efforts to understand and manage human health risks associ ated with exposure to waterborne zoonoses (Till and McBride, 2004).

Tools that complement epidemiology may help addr ess the characterization of the relative risks

of human illness from various sources of fecal c ontamination in recreational waters; for example, quantitative microbial risk a ssessment (QMRA) is one alternative that could supplement traditional epidemiological investigations to identify potential excess human health risks for defined pathways of particular pathogens (C arr and Bartram, 2004). Because QMRA has the potential to provide much greate r sensitivity in quantifying risk than epidemiological studies (Carr and Bartram, 2004), the potential synergy from using both methods could be helpful to manage risks of water-related in fectious diseases (see Bartram et al., 2001). To date, data gaps have limited the degree to which QMRA has b een used to inform public policy decisions and manage recreational waters. The greatest data defi ciencies appear to be a lack of dose-response and environmental occurrence data for many water borne zoonotic pathogens (Carr and Bartram, 2004; Till and McBride, 2004).U.S. Environmental Protection Agency

February 2009 67 In addition, more robust environmental testin g in recreational and dr inking water outbreak investigations using rapidly e volving molecular methods is anot her complementary tool that could supplement traditional epid emiological investigations in ch aracterizing the relative risks of human illness from the range of various sources of fecal contamination in recreational waters. A notable drawback to this approach is that state and lo cal health departments, who are responsible for investigating outbreaks, are unl ikely to have the tec hnical or financial resources to pursue this sort of testing, so extramural funding would likely be needed.

Finally, even if or when sufficient inform ation becomes available to support robust and quantitative characterization of the relative ri sks of human illness from the range of fecal contamination sources in recreational waters, a nu mber of issues will likely remain regarding the use of indicator organisms to predict human i llnesses from exposure to these waters. The

essential intent of fecal indicators is that they represent the overall “p athogenicity” of the water (NZME, 2003). Within this context, it is not surp rising that indicator orga nisms correlate well to some pathogens in some waters but correlate poorly in other cases (e.g., Ashbolt et al., 1993; Elliott and Colwell, 1985; Ferguson et al., 1996; Gr abow et al., 1989; Jiang et al., 2001). If new or revised water quality criter ia are to address quantitatively the various sources of fecal contamination of potential interest in recrea tional waters covering diverse geographic regions, the approach will likely require a set or toolbox of indicators (as measured by specific methods). Recent research documenting the ex treme variability in densities of traditional indicators over very short time periods (Boehm, 2007) underscore s the need for a variety of indicator/method combinations that address a range of c ontamination sources and geographic areas.

In summary, both human and animal feces in r ecreational waters continue to pose threats to human health. Although the public health importance of waterborne zoonotic pathogens is being increasingly recognized, it is still not well char acterized. Policy makers and researchers have

often assumed that the human health risk fr om pathogens associated with domestic and agricultural animal and wildlife f eces is less than the risk from human feces, in large part because viruses are predominately host-specific. This literature review illustrates a lack of detailed and unequivocal information concerning the relative risks of human illness from various

sources of fecal contamination in recreational waters. In additi on, the ability to measure how the infectivity and virulence of know n waterborne zoonotic pathogens are affected when passaged through animal hosts remains in it s infancy. Thus, the findings of this literature review support the perspectives set forth by WHO (2004) and i ndicate that addressing fecal contamination sources in recreational water quality criteria will require additional research to better define the risk posed by animal fecal matter.U.S. Environmental Protection Agency

February 2009 68 

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WHO. 2003. Guidelines for safe recreational wate r environments Volume 1 Coastal and Fresh Waters. World Health Organization (WHO): Geneva.

WHO. Cotruvo, J.A., Dufour, A., Rees, G., Bartra m, J., Carr, R., Cliver, D.O., Craun, G.F., Fayer, R., Gannon, V.P.J., ed. 2004. Waterborne zoonoses: identification, causes and control. World Health Organization (WHO) . IWA Publishing: London, UK.

Wiedenmann, A., Kruger, P., Di etz, K., Lopez-Pila, J.M., Sz ewzyk, R., 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. Environmenta l Health Perspectives 114(2): 228-236.

Yoder, J.S., Blackburn, B.G., Craun, G.F., Hill, V., Levy, D.A., Chen, N., Lee, S.H., Calderon, R.L., Beach, M.J. 2004. Surveillance for water borne-disease outbreaks associated with

recreational water

– United States, 2001-2002. Mortality and Morbidity Weekly Report CDC Surveillance Summaries 53(8): 1-22.

Zmirou, D., Pena, L., Ledrans, M., Letertre, A. 2003. Risks associated wi th the microbiological quality of bodies of fresh and marine water us ed for recreational purposes: summary estimates based on published epidemiological studies. Archives of Envir onmental Health 58(11): 703-711U.S. Environmental Protection Agency

February 2009 A-1 

## A PPENDIX 

## A

L ITERATURE 

## S EARCH 

## S TRATEGY AND 

## R ESULTS

The literature search strategy consisted of a number of combined approaches. Search terms and a synopsis of information needed were given to a professional librarian to search the online DIALOG databases. To supplement the DIALOG searches, individual au thors used free search engines on the internet to find ar ticles pertaining to specific in formation needed. Experts that participated in EPA’s Experts Scientific Wo rkshop on Critical Research Needs for the Development of New or Revised Re creational Water Quality Criteria 1 were contacted by email and requested to contribute literature they felt was important. The titles of literature cited in specific reports, books, review articles, and conference proceedings were evaluated for

relevance.

A.1 Initial Literature Search Strategy Conducted by Professional Librarian

Selection of DIALOG data base files used for this search:

File 155:MEDLINE(R) 1950-2007/Nov 12 (c) format only 2007 Dialog File 266:FEDRIP 2007/Sep Comp & dist by NTIS, Intl Copyright All Rights Res
File 245:WATERNET(TM) 1971-2007Jul
(c) 2007 American Water Works Association

File 144:Pascal 1973-2007/Oct W4

(c) 2007 INIST/CNRS File 117:Water Resources Abstracts 1966-2007/Aug

(c) 2007 CSA. File 40:Enviroline(R) 1975-2007/Sep (c) 2007 Congressional Information Service

File 110:WasteInfo 1974-2002/Jul

(c) 2002 AEA Techn Env. File 143:Biol. & Agric. Index 1983-2007/Oct
(c) 2007 The HW Wilson Co

File 6:NTIS 1964-2007/Nov W3 (c) 2007 NTIS, Intl Cpyrght All Rights Res
File 5:Biosis Previews(R) 1926-2007/Nov W2 (c) 2007 The Thomson Corporation

File 73:EMBASE 1974-2007/Nov 12
(c) 2007 Elsevier B.V.

Search strategies used for this search:

#1: Waterborne terms NEAR fecal terms

**S1 3210 WATERBORNE()(DISEASE? ? OR OUTBREAK? ? OR ZOONOT? OR ZOONOS?**

**OR EPIDEMIC? ? OR EPIDEMIOLOG?)**

**S2 43 WATERBORNE()(HEPATITIS OR ROTAVIRUS? OR NOROVIRUS?)**

**S3 232098 FECAL OR FECES FAECAL OR (LIVESTOCK OR BOVINE OR CATTLE)(S)**

1 Report from this workshop: http://www.epa.gov/waterscience/criteria/recreation/

.U.S. Environmental Protection Agency

February 2009 A-2 **CONTAMINATION**
**S4 1637 PATHOGEN()FECAL()SHEDDING OR PATHOGENS (S) SEWAGE OR RAW()**

**SEWAGE()CONTAMINATION**

**S8 207 S1 (S) S3**

**S9 250 S2 OR S8 S10 140 RD S9 (unique items--deduped; no year/language limits)** 

#2: Pathogen terms NEAR Sewage terms AND ( Waterborne or Recreational Water Terms)

**S4 1637 PATHOGEN()(FECAL OR FAECAL)()SHEDDING OR PATHOGENS (S) SEWAGE**

**OR RAW()SEWAGE()CONTAMINATION**

**S29 1282 S4 NOT (S9 OR S13 OR S16 OR S21) S30 717 RD S29 (unique items)** 

**S31 110 S30 AND (S11 OR S12 OR S1) (WATERBORNE/RECREATIONAL WATER**

**SETS)**

#3: (Remaining Pathogen terms OR I ndicator Terms) AND Selected Authors

**S34 592 S30 NOT (S31 OR S33) [REMAINING PATHOGEN RESULTS]**

**S35 2164 S7 NOT (S9 OR S13 OR S16 OR S33 OR S21 OR S31) [INDICATORS] S36 1078 RD S35 (unique items)** 

**S37 2011 AU=(ASHBOLT ? OR PAYMENT ? OR PRUSS ?)**

**S38 33410 S37 OR AU=(BYAPPANAHALLI? OR COLFORD ? OR DUFOUR ? OR**

**MCBRIDE ? OR GANNON ? OR CICMANEC? OR COTRUVO?)**

**S39 38 (S34 OR S36) AND (S37 OR S38) [AUTHORS ON THOSE 2 TOPICS]**

#4: (Remaining Pathogen terms OR Indica tor Terms) AND Waterborne or Recreational Water Terms)

**S5 462847 CLOSTRIDIUM OR BACTEROIDES OR TOTAL()(FECAL OR FAECAL)()**

**COLIFORM OR E()COLI OR ECOLI OR ENTEROCOCC? OR FECAL()**

**STREPTOCOCC? OR COLIPHAGE**

**S6 540854 INDICATOR? ?**

**S7 2551 S5 (5N) S6**

**S42 1611 (S34 OR S36) NOT S39**
**S43 243 S42 AND (S1 OR S11 OR S12) [combined w/waterborne/**
**recreational terms]**

Dates : 1985-present [2002-present is more crucial] Language : no restrictions

Descriptions of these files are available at http://library.dial og.com/bluesheets/

.U.S. Environmental Protection Agency

February 2009 A-3 Retrieve : titles and year

Format : MS Word

Additional information : Interested in international and domestic journals and government

reports.

Search terms : Fecal waterborne disease* (i.e., * allows for multiple endings) Waterborne zoono* (for zoono tic, zoonosis, zoonoses)

Waterborne outbreak* Waterborne disease epidemiology

Livestock contamination of water

Fecal load Pathogen fecal shedding Pathogens AND sewage Microbial quality of effluent Waterborne Hepatitis

Waterborne rotavirus*

Waterborne Norovirus* Raw sewage contamination

Clostridium AND indicator*

Bacteroides AND indicator* total fecal coliform, AND indicator*

E. coli and Indicator*

Enterococcus AND indicator*

fecal streptococcus AND indicator* coliphage AND indicator*

Key authors : Ashbolt N Payment P

Prüss A Byappanahalli M

Colford J

Dufour A

McBride GB

Gannon VPJ

Cicmanec JL

Cotruvo JA

Specific literature : WHO. (2004) Waterborne Zoonoses. http://www.who.int/wat er_sanitation_health/ diseases/zoonoses.pdf All MMWR supplements on waterbor ne illness (1983 to present) Airlie report (USEPA , 2007) referencesU.S. Environmental Protection Agency

February 2009 A-4 Objectives of this literature search :

• All epidemiological studies of waterborne illness due to ambient recreational exposures (any location)

• Morbidity and Mortality Weekly Report surveillance summaries and papers that evaluate

trends based on CDC data for waterborne illn esses due to recreational exposures (ambient and pools)

• Papers on outbreaks due to ambient recreational exposur es (not pools)

• References to illness resulting from waterborne exposure to fecal materials from a variety of sources (emphasis on animal-derived wa ste, including point and nonpoint sources)

• Prevalence of fecal indicators in humans and an imals (livestock and wild animals): (total and fecal coliform, E. coli

, Enterococcus , fecal streptococcus

, Bacteroides , coliphage (somatic and F+), and Clostridium) variation of quantities in fecal material (temporal and within a population)

o References for a Fecal Shedding Table (average for a species): columns – indicator and pathogen sheddi ng quantification, ra tio of indicator to pathogens (if

known or can be calculated without be ing misleading), primary literature citations; rows – species

• Variation and uncertainty in shedding data (how much and how frequently do infected animals shed pathogens in feces)

• magnitude and duration of fecal excretion of specific pathogens during illness

• Pathogen prevalence in herds or wild animals

• number of infected per herd

• geographic distribution of herds

• seasonal, temporal, event dr iven (calving) variation

• Pathogen prevalence in raw and treated sewa ge (mostly human source) – likely variation

• human point and nonpoint source contaminant levels quantified in receiving waters

A.2 Literature Search Strategy and Result s Specific to Epidemiological Studies

Conducted in Recreational Waters

The following terms were searched on the Web of Science:

• Recreational water + epidemiology + fecal matter

• Recreational water + epidemiology + nonpoint source

• Recreational water + epidemiology + point source

• Recreational water + epidemiology + animal fecal matter

• Recreational water + epidemiology + animal waste

• Recreational water + exposure to fecal matter

• Recreational water + epidemiological studies + microbiological indica tors of fecal matter

• Recreational water + epidemiology + fecal matter + European Union

• Recreational water + epidemiology + fecal matter + United Kingdom

A summary of the results of this litera ture search is provided in Table A.2.1U.S. Environmental Protection Agency

February 2009 A-5 Table A.2.1. Summary of Epidemiologica l Studies in Recreational Waters

Search Topic #
Citations Citations

Reviewed (Web

information only) #
Citations

of

Interest

Recreational water + epidemiology + fecal matter 50 Yes 1

Recreational water + epidemiology + nonpoint source 30 Yes 3

Recreational water + epidemiology + point source 30 Yes 3

Recreational water + epidemiology + animal fecal matter 20 Yes 1

Recreational water + epidemiology + animal waste 30 Yes 4

Recreational water + exposure to fecal matter 30 Yes 1

Recreational water + epidemiological studies + microbiological
indicators of fecal matter 40 Yes 5

Recreational water + epidemiology + fecal matter + European Union 40 Yes 2

Recreational water + epidemiology + fecal matter + United Kingdom 40 Yes 4

New + recreational waters + epidemiological studies + EU 60 Yes 10

The results of this literature revi ew were then combined into a lib rary with the relevant citations

from a reverse literature citation search on several of the key epidemiological studies (e.g., the Wade et al., 2003; Zimrou et al., 2003; Prüss 19 98; and Sinton et al., 1998 review articles), and duplicates were discarded. Additionally, publicat ions describing studies conducted in Europe were obtained for free from Dr. David Kay, one of the key investigators of epidemiological studies in Europe ( http://www.aber.ac.uk/iges/staff/kaydavid.shtml ). Furthermore, unpublished information on current and ongoing activities in the European Union was obtained through personal communications with Dr. Kay and a review of the rele vant activity’s website.

A.3 Literature Search Strategy and Results Specific to Outbreak Data

Drinking Water

The purpose of the literature s earch was to capture published articles on waterborne disease outbreaks that identified an etiological pathogen a nd linked it to a drinking water source. Due to the broad nature of the topic, many more pape rs have been published in the peer-reviewed literature related to drinking wate r outbreaks, and this literature search by no means represents all of them. The searches were performed on December 5 to 6, 2007.

A Google Scholar search of “w aterborne AND outbreak” resulted in 9,940 hits, and a search of “drinking AND water AND outbreak” resulted in 42,900 hits, which were not reviewed. A

search of Scirus scientific database of “wat erborne AND outbreak” resulted in 13,694 hits which

were not reviewed.

The following terms were searched on the Nationa l Library of Medicine’s PubMed database:

• water + outbreakU.S. Environmental Protection Agency

February 2009 A-6 • waterborne + outbreak

• drinking + wate r + outbreak

• zoono* + water + outbreak (title only)

A summary of the results of this litera ture search is provided in Table A.3.1.

Table A.3.1. Summary of Outbreak In vestigations in Drinking Water

Search Topic #
Citations Citations

Reviewed # Citations

of Interest

Water AND outbreak 3,344 No

Waterborne AND outbreak 448 Yes 118

Drinking AND water AND outbreak 497 Yes 146

Zoono* AND water AND outbreak 81 Yes 0

The results of the two searches that produced cita tions of interest were combined, and duplicates and articles in languages other than English we re discarded. The resulting list was narrowed to 55 articles, which were chosen based on an indicati on in the abstract that the etiological pathogen in the outbreak was actually detect ed in the drinking water source.

Recreational Water

For the literature search regarding recreati onal water outbreaks, the following terms were

searched on the U.S. National Librar y of Medicine’s PubMed system:

• (beach OR lake OR stream OR pond OR swim OR recreation) AND water AND (outbreak OR epidemic)

A summary of the results of this litera ture search is provided in Table A.3.2.

Table A.3.2. Summary of Outbreak Invest igations in Recreational Water

Search Topic #
Citations Citations

Reviewed #
Citations

of

Interest

(Beach OR lake OR stream OR pond OR swim OR recreation) AND water AND (outbreak OR epidemic) 52 Yes 40

Abstracts from the literature identified were review ed, and studies were incl uded if the abstract showed evidence that the etiologic agen t was detected in the source water.

A.4 Summary of Literature Search Results

This process resulted in a total order of 365 cita tions of which a total of 273 (75 percent) were received during the expedited writing process, not all of which could be reviewed. There areU.S. Environmental Protection Agency

February 2009 A-7 many more papers in the peer-reviewed literature and this by no means represents all of them. Of the articles reviewed, 182 citations were included in the white paper.

A.5. Supplemental Literature Search Strategy

In addition to the literature s earch conducted by the professional librarian several other resources

were consulted.

The flowing experts in the field were contact ed directly by email and asked to suggest

references:

Nicholas Ashbolt, USEPA Thomas Atherholt, New Jersey Depa rtment of Environmental Protection Michael Beach, Centers for Disease Control and Prevention Bart Bibler, Florida De partment of Health Alexandria Boehm, Stanfo rd University, California Rebecca Calderon, USEPA Jennifer Clancy, Clancy E nvironmental Consultants Jack Colford, University of California, Berkeley Elizabeth Doyle, USEPA Alfred Dufour, USEPA Lee Dunbar, Connecticut Department of Environmental Protection Lora Fleming, University of Miami School of Medicine and Rosenstiel School of Marine and Atmospheric Sciences, Florida Charles Hagedorn, Virginia Tech Joel Hansel, USEPA Lawrence Honeybourne, Orange County Health Care Agency, Santa Ana, California Donna Francy, U.S. Geological Survey Roger Fujioka, University of Hawaii, Manoa Toni Glymph, Wisconsin Depart ment of Natural Resources Mark Gold, Heal the Bay, California Paul Hunter, University of East Anglia, U.K. Dennis Juranek, Centers for Disease Control and Prevention (retired) David Kay, University of Wales, U.K. Sharon Kluender, Wisconsin State Laboratory of Hygiene Erin Lipp, University of Georgia Graham McBride, National Institute of Wa ter and Atmospheric Research, New Zealand Charles McGee, Orange County Sanitation District, California Samuel Myoda, Delaware Department of Natural Resources Charles Noss, USEPA Robin Oshiro, USEPA James Pendergast, USEPA Mark Pfister, Lake County Health Department, Illinois John Ravenscroft, USEPA Stephen Schaub, USEPA Mark Sobsey, University of North Carolina, Chapel HillU.S. Environmental Protection Agency

February 2009 A-8 Jeffrey Soller, Soller Environmental, California Michael Tate, Kansas Department of Health and Environment Peter Teunis, RIVM (National Institute of Pub lic Health and the Environment), Netherlands Gary Toranzos, University of Puerto Rico, Rio Piedras Timothy Wade, USEPA John Wathen, USEPA Stephen Weisberg, Southern Californi a Coastal Water Research Project David Whiting, Florida Department of Environmental Protection Richard Zepp, USEPA

In addition to contacting experts in the field, spec ific reports were obtained and the titles of the references cited in the reports were reviewed for relevance.

• NRC. 2004. Indicators for waterborne pa thogens. National Academies Press. Washington, DC. 315 pp.

• USEPA. 2007. Report of the experts scientif ic workshop on critical research needs for the development of new or revised recrea tional water quality criteria. EPA 823-R-07-006.

Available online at http://www.epa.gov/watersci ence/criteria/recreation

• References cited by the Natural Resources De fense Council reviewers of the EPA Critical

Path Science Plan

• Prüss (1998) Review of Epidemiological St udies on Health Effects from Exposure to

Recreational Water. International Journal of Epidemiology 27:1-9.

• Wade, T.J., Pai, N., Eisenberg, J.N., and Co lford, Jr., J.M. 2003. Do U.S. Environmental Protection Agency water quality guidelines for recreational waters prevent gastrointestinal illness? A systematic revi ew and meta-analysis. Environmental Health Perspectives 111(8):1102-1109.

• Zmirou, D., Pena, L., Ledrans, M., and Lete rtre, A. 2003. Risks associated with the microbiological quality of bodi es of fresh and marine water used for recreational purposes: Summary estimates based on publishe d epidemiological studies. Archives of Environmental Health 58(11): 703-711.

• Sinton, L.W., Finlay, R.K., Hannah, D.J. 1998. Di stinguishing human from animal fecal

contamination in water: A review. New Z ealand Journal of Marine and Freshwater

Research 32: 323-348.

• Boehm et al. 2008. A sea change ahead for recr eational water quality criteria (peer review in progress)

In addition, Clancy Environmental Consultant s, ICF International, Soller Environmental, WaltJay Consulting, and EPA’s Health and Ecologica l Criteria Division all maintain extensive

literature databases and reference lists from previously completed projects. All of those in house

resources were also sources of literature.