United States

EnvironmentalProtection

Agency

EPA-600/1-84-004

Aug. 1984

Research and Development 

EPA Health Effects

Criteria for Fresh

Recreational Waters

Note: This electronic version was prepared from the original document using

optical character recognition software.
EPA-600 / 1-84-004

August 1984

Health Effects Criteria

for

Fresh Recreational Waters

by

Alfred P. Dufour

Toxicology and Microbiology Division

U.S. Environmental Protection Agency

Cincinnati, OH 45268

HEALTH EFFECTS RESEARCH LABORATORY

OFFICE OF RESEARCH AND DEVELOPMENT

U.S. ENVIRONMENTAL PROTECTION AGENCY

RESEARCH TRIANGLE PARK, NC 277711
ii

NOTICE

This document has been subject to the U.S. Environmental Protection Agency’s

peer and administrative review and approved for publication. Mention of trade

names or commercial products does not constitute endorsement or recommendation

for use.
iii

FOREWORD

The many benefits of our modern, developing, industrial society are accompanied

by certain hazards. Careful assessment of the relative risk of existing and new manmade environmental hazards is necessary for the establishment of sound regulatory

policy. These regulations serve to enhance the quality of our environment in order to

promote the public health and welfare and the productive capacity of our Nation's

population.

The complexities of environmental problems originate in the deep interdependent

relationships between the various physical and biological segments of man's natural

and social world. Solutions to these environmental problems require an integrated

program of research and development using input from a number of disciplines. The

Health Effects Research Laboratory, Research Triangle Park, NC and Cincinnati, OH

conducts a coordinated environmental health research program in toxicology,

epidemiology and clinical studies using human volunteer subjects. Wide ranges of

pollutants known or suspected to cause health problems are studied. The research

focuses on air pollutants, water pollutants, toxic substances, hazardous wastes,

pesticides and nonionizing radiation. The laboratory participates in the

developmentand revision of air and water quality criteria and health assessment

documents on pollutants for which regulatory actions are being considered. Direct

support to the regulatory function of the Agency is provided in the form of expert

testimony and preparation of affidavits as well as expert advice to the Administrator

to assure the adequacy of environmental regulatory decisions involving the protection

of thehealth and welfare of all U.S. inhabitants.

This report provides an assessment of the relationship between microbiological

indicators of water quality and illness that may have resulted from swimming. The

data base resulted from a series of in-house and extramural epidemiologicalmicrobiological research projects designed to develop the criterion for fresh waters.

The development and periodic reevaluation of such criteria is mandated by Section

304(a)l of Public Law 92-500: Federal Water Pollution Control Act Amendments of

1972; Clean Water Act of 1977.

 F. Gordon Hueter, Ph.D.

Director

 Health Effects Research Laboratory
iv

ABSTRACT

A criterion for the quality of the bathing water, based upon swimming-associated

gastrointestinal illness, was developed from data obtained during a multi-year

freshwater epidemiological-microbiological research program conducted at bathing

beaches near Erie. Pennsylvania and Tulsa, Oklahoma. Three bacterial indicators of

fecal pollution were used to measure the water quality. E. coli, enterococci and fecal

coliforms. A good correlation was observed between swimming-associated gastrointestinal symptoms and either E. coli or enterococci densities in the water. Fecal

coliform densities showed little or no correlation to gastrointestinal illness rates in

swimmers. In general, high gastrointestinal illness rates were associated with high

densities of fecal indicator bacteria. A comparison of the freshwater results with the

results obtained from studies at marine bathing beaches indicated that a separate

criterion should be used with each type of bathing water.
v

CONTENTS

Number Page

 

 Forward . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . iii

 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . iv

 Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vi

 Tables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii

 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . viii

 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

 2. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

 3. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

Swimming-Associated Outbreaks of Disease . . . . . . . . . . . . . . . . . . . . . . 3

Retrospective Epidemiological Studies . . . . . . . . . . . . . . . . . . . . . . 5

Prospective Epidemiological Studies . . . . . . . . . . . . . . . . . . . . . . 6

Water Quality Standards for Bathing Beaches l924-l980 . . . . . . . . . . . . . . . . 7

 4. Freshwater Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

Experimental Design . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

Lake Erie Study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

Keystone Lake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

 5. Development of a Criterion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

Criteria for Freshwater Bathing Areas . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

 6. Marine Versus Freshwater Criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
vi

FIGURES

Number Page

 

 1 Estimated Regression Lines for Highly Credible and Total

Gastrointestinal Symptom Rates on E. coli Densities . . . . . . . . . . . . . . . . 22

 2 Estimated Regression Lines for Highly Credible and Total

Gastrointestinal Symptom Rates on Enterococci Densities . . . . . . . . . . . . 22

 3 Estimated Regression Lines for Highly Credible and Total

Gastrointestinal Symptom Rates on Fecal Coliform Densities . . . . . . . . . 23

 4 Criterion for Estimating Swimming-Associated Gastrointestinal

Illness Rate from the Geometric Mean Density of E. coli per

100 ml in Freshwater Samples . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

 5 Criterion for Estimating Swimming-Associated Gastrointestinal

Illness Rate from the Geometric Mean Density of Enterococci per

100 ml in Freshwater Samples . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24

 6 Criterion for Estimating the Geometric Mean E. coli Density

per 100 ml from an Acceptable Risk Level of Swimming-Associated

Gastrointestinal Illness. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

 7 Criterion for Estimating the Geometric Mean Enterococci Density

per 100 ml from an Acceptable Risk Level of Swimming-Associated

Gastrointestinal Illness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

 8 Data Summary of Highly Credible Gastrointestinal Symptom

Rates and Indicator Densities from Marine and Freshwater Studies . . . . . . 28

 9 Marine and Freshwater Criteria for Swimming-Associated

Gastrointestinal Illness and Water Quality Using Enterococci to

Measure the Water Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29

 10 Marine and Freshwater Criteria for Swimming-Associated

Gastrointestinal Illness and Water Quality Using E. coli to

Measure the Water Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
vii

TABLES

Number Page

 

 1 Outbreaks of Disease Associated with Swimming in Natural Waters . . . . . 3

 2 Follow-up Success Rate for Beach Contacts at Lake Erie, 

Pennsylvania, 1979, 1980 and 1982 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

 3 Symptom Rates by Category for Swimmers and Nonswimmers at 

Lake Erie Beaches,1979-1982 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

 4 Bacterial Indicator Densities at Lake Erie, Pennsylvania 

Bathing Beaches, 1979, 1980 and 1982. . . . . . . . . . . . . . . . . . . . . . . . . . . 15

 5 Follow-up Success Rate for Beach Contacts at Keystone Lake, 

Oklahoma, 1979-1980 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

 6 Symptom Rates by Category for Swimmers and Nonswimmers at

Keystone Lake Beaches, 1979-1980 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

 7 Indicator Densities at Keystone Lake Bathing Beaches, 1979-1980 . . . . . . 17

 8 Summary of Microbiological and Epidemiological Results from

Lake Erie and Keystone Lake Bathing Beach Studies . . . . . . . . . . . . . . . . 19

 9 Summary of Regression Statistics Related to SwimmingAssociated Illness and Water Quality Indicators . . . . . . . . . . . . . . . . . . . . 20

 10 Summary of Statistics Related to Marine and Freshwater

Criteria for Highly Credible Swimming-Associated Illness

 and Water Quality Indicators, E. coli and Enterococci . . . . . . . . . . . . . . . . 29
viii

ACKNOWLEDGMENTS

The author gratefully acknowledges the work and cooperation of Prof. Stanley

Zagorski, Dr. Richard Gammon and Dr. Gerald Kraus of Gannon University, Erie,

Pennsylvania, and Drs. James Robertson, Donald Parker, Garry McKee and David

Shadid of the University of Oklahoma, Oklahoma City, Oklahoma. 

The author also is indebted to Mr. Leland McCabe, Dr. Morris Levin, Dr. William

Watkins, Ms. Cynthia Thomas and the staff of the HERL Marine Field Station,

Kingston, Rhode Island for their many contributions. 

A special acknowledgment is reserved for Dr. Victor Cabelli who directed the EPA

Recreational Water Quality Program until his retirement from government service in

1978. His dedicated work and steadfast guidance were, in large part, responsible for

the program reaching its goal, the development of a water quality criteria for

recreational waters.
1

SECTION 1

 

INTRODUCTION

The current EPA recommended criteria for bathing waters is that given in Quality Criteria

for Water (I) which states:

“Based on a minimum of five samples taken over a 30-day period, the fecal coliform

bacterial level should not exceed a log mean of 200 per 100 ml, nor should more than

10 percent of the total samples taken during any 30-day period exceed 400 per 100 ml”

This criterion, which is used by 95% of the states and territories of the United States (2),

was first proposed by the National Technical Advisory Committee (NTAC) to the Federal

Water Pollution Control Administration in 1968 (3). The NTAC used epidemiological data

collected by the United States Public Health Service (USPHS) from 1948-1950(4) to develop

the criteria for recreational bathing waters. The criterion was closely examined in 1972 by

a committee of the National Academy of Sciences - National Academy of Engineers (NASNAE) and they concluded that the epidemiological data base used to develop the NTAC

criterion was too limited to be scientifically defendable (5). The NAS-NAE committee

decided not to recommend a criterion for recreational bathing waters based on the paucity

of epidemiological information available.

In 1972, the Environmental Protection Agency (EPA) initiated a long-term recreational

water quality research program that was to examine the relationship between water quality

and swimming-associated acute infectious disease. The first phase of the program, from 1972

to 1978, was conducted at multiple marine bathing beaches in New York, Louisiana and

Massachusetts. The result of these studies was a marine recreational water criterion which

described a direct linear relationship between swimming-associated gastroenteritis and water

quality which was indexed by the density of enterococci in the water (6).

From 1978 to 1982, the EPA recreational water quality research program was directed at

freshwater bathing areas. This report will describe and summarize the results of freshwater

beach studies conducted in Pennsylvania and Oklahoma, and will present two fresh

recreational water criteria, which relate swimming-associated gastroenteritis to water quality,

characterized with either one of two bacterial indicators, enterococci or E. coli. It will be

shown that the model developed for the marine criterion, i.e., a direct linear relationship, has

been validated by the freshwater studies and, lastly, the results of the marine studies will be

compared to those of the freshwater results to show that a single criterion cannot be used for

marine and fresh bathing waters.

The material presented in this report is a natural extension of the information given in

“Health Effects Water Quality Criteria for Marine Recreational Water”(6). Many references

will be made to that report, since the rationale for the marine studies and the study design

have been used in the freshwater studies. Whenever possible the data presentations in this

report will be in such a manner that the results can be compared directly to those of the

marine studies. Although most of the information pertinent to developing a water quality

criterion are included in the organization of this report, there are certain elements that have

been omitted, which can be found in the marine water quality report, such as the two

sections which relate to water quality indicators and the limitations associated with the use

of criteria developed with bacterial water quality indicators of enteric origin.
2

SECTION 2

 

CONCLUSIONS

The results of the freshwater bathing beach studies conducted at two sites over a

three-year period lead to the following conclusions.

1. Swimming-associated gastrointestinal illness is related to the quality of the

bathing water. A direct linear relationship was observed between highly credible

gastrointestinal illness and bacterial densities of two indicators of fecal

contamination, enterococci and E. coli.

2. The relationship between the rate of swimming-associated illness and bacterial

indicator density was almost identical for two of the indicators examined, E. coli

and enterococci. Thus, either indicator can be used to measure the potential for

swimming-associated illness in bathing waters. Fecal coliforms showed no

relationship to the rate of swimming-associated gastrointestinal illness.

3. The criterion developed for marine bathing waters is not applicable to fresh

bathing water. At equivalent indicator densities, the swimming-associated illness

rate was approximately three times greater in seawater swimmers relative to that

in freshwater swimmers.
3

SECTION 3

 

BACKGROUND

Swimming-Associated Outbreaks of Disease

The history of disease outbreaks and illness associated with poor quality bathing water

has been described in many reviews on this subject (7,8,9). A listing of the most

frequently referenced literature on swimming-associated illness is given in Table I. This

table is instructive in the sense that it shows that some factors assumed to be important

in past considerations of the hazards related to swimming in polluted water may have

little relevance today. For instance, it is obvious that reports of disease in swimmers

caused by Salmonella species began to decline in the 1940's and none were reported after

the Australian outbreak which occurred in 1958. Two factors probably contributed to the

decrease in Salmonella related illness in swimmers. First, there was the steady increase

in the number of sewage treatment plants practicing disinfection, especially in large

population centers, and second, there was a widespread use of newly discovered

antibiotics which greatly aided in limiting the spread of disease and, thereby, the number

of ill individuals in the discharging population. Another obvious point is the lack of

swimming-associated outbreaks caused by poliovirus. Although strong evidence relating this

virus to disease contracted by swimming has never been presented, many of the early studies
4

on the effect of polluted water on swimmers were probably stimulated by the anxiety

created by the then incurable disease caused by poliovirus.

After the 1958 outbreak of salmonellosis in Australia (10) there was a long period

when no outbreaks of swimming-associated illness were reported in the literature. This

lull was broken in 1973 when Hawley et al., (11) reported an outbreak of illness,

apparently swimming related, caused by Coxsackie B virus. Most of the reports from

1973 to the present have dealt mainly with viral mediated swimming-related disease.

The exception to the viral etiology of swimming-associated illness was the outbreak

attributed to Shigella sonnei which occurred downstream from Dubuque, Iowa on the

Mississippi River in 1976(12). This pathogen differs from most of the bacterial species

associated with illness in swimmers in that it has a low infective dose. As few as ten

ingested Shigella have caused illness in a significant percentage of volunteers (13).

A notable characteristic of the early outbreaks and those which have occurred more

recently is the lack of good data describing the quality of the water. It is almost

characteristic of outbreaks that they do not occur coincidental to measuring the quality

of the water. This was true in the Michigan (14), Dubuque, Iowa (12), South Carolina

(15) and Perth, Australia (10) outbreaks. In all of these incidents the water quality was

usually examined before or subsequent to, but not during the outbreaks.

The Michigan outbreak, for instance, occurred one week after the water had been

analyzed and one week before the next planned sampling of the water (14). ln the

Dubuque outbreak the water quality was not examined until one week after the illnesses

were first observed (12). Bryan noted that coliforms were present in the South Carolina

lake water where the Hepatitis A outbreak occurred, but densities were not reported

(15). The Australian outbreak was similar to other outbreaks in that it was only after the

onset of cases of illness that the water quality was examined and high concentrations

of fecal coliforms were observed.

Investigators in both the Vermont and Beccles, England outbreaks did not examine

the water for water quality indicators. They did, however, isolate the etiologic agent

from water samples obtained from swimming waters where patients had been bathing.

Three outbreaks apparently were associated with swimming in grossly polluted water.

The Walmer, England outbreak report clearly implicated sewage from a nearby outfall

as the source of the typhoid fever among army recruits (7). The often cited somewhat

obscure reports linking typhoid fever with bathing in polluted harbor water in New York

(16) and New Haven (17), on the other hand, did not clearly establish the association

between swimming activity and disease. The New York report indicated an unusual

increase in the number of reported cases of typhoid in the summer of 1932. The cases

were sporadic and did not constitute an outbreak. Neither water nor milk was implicated

as a common source of the etiologic agent. The report stated that, “From all the data at

hand it is very probable that most of the increase (in typhoid fever) may be charged to

bathing in polluted harbor waters condemned by the Department of Health” The report

also states that, “It should be noted that in Brooklyn, up to the age of twenty, the

infections among males are nearly double the number among females, a fact which lends

support for the belief that bathing in polluted waters has played an important part in the

increased prevalence of typhoid fever.” The 1921 report by Ciampolini (17) on the incidence

of typhoid in New Haven was more detailed, but similar to the New York report in that an

excess of cases was noted in an area of the city near the harbor. A total of 32 cases was

reported from January to December and none of these could be attributed to drinking water

or food. Many of the cases were due to person-to-person contact. Only nine of the cases

were thought to be due to bathing. The nine cases lived in close proximity to the

harbor, and all had a common history of bathing at some time or other in the harbor

which had been shown some years before to be grossly polluted with sewage.

Thus in both the New York and New Haven typhoid outbreaks, swimming activity was
5

perceived as being marginally associated with an excess of cases but not the sole cause

of the outbreak attributable to a single source, such as polluted harbor water. 

In contrast to the outbreaks discussed above, the Coxsackie A16 outbreak-reported 

by Denis et al (18) was quite thorough with respect to its description of the quality of

the water at the time of the incident. Not only was the etiological agent isolated from

the lake water but E. coli, group D streptococci and Pseudomonas aeruginosa also were

detected and enumerated.

The nature of disease outbreaks is such that the relationship between an illness and

a common source of an etiological agent is clearly defined because of some coherent

characteristic of the affected group such as a common affiliation or activity. Thus,

disease outbreaks are instructive in the sense that they establish relationships such as

that between swimming-associated illness and water quality which probably would not

have been discovered had the members of the group not had some type of common

characteristic. Most of the above outbreaks fit this description in that the affected

individuals belonged to a group, such as army recruits or boy scouts, or they were taking

part in a common activity such as camping or picnicking. The occurrence of disease in

these groups was instrumental in showing that recreational activity in poor quality water

was a reasonable means by which pathogens could be disseminated from point sources

of pollution to susceptible individuals. However, disease outbreaks are not very useful

for establishing the relationship between the incidence of disease and some measure of

water quality because the water quality is seldom measured at the time of the outbreak.

Thus, the study of outbreaks serves a valuable purpose, but in order to establish water

quality criteria or guidelines for recreational waters, a more purposeful, directed means

of obtaining health effects information must be used. Epidemiological studies provide

a rational means for obtaining the desired information. 

Retrospective Epidemiological Studies 

Only three studies have been published which attempted to assess the health risks of

swimming by identifying cases of a specific illness and then determining if that illness

was somehow related to swimming activity. The first such study was reported by the

Public Health Laboratory Service (19) in 1959. They described an intensive effort over

a five-year period to identify patients with enteric fever whose illness might be

associated with a history of swimming. Attempts were made to see if the frequency of

enteric illness in coastal areas differed significantly from those in the national

population. The assessment of whether or not a case of paratyphoid or typhoid fever was

related to swimming was made on the basis of(l) the organism causing the disease being

the same type as that found in the bathing water, (2) other common sources of infection

being excluded, (3) the accidental swallowing of a good deal of water, (4) the bathing

waters being highly polluted and (5) a bathing episode prior to the onset of the illness

that was consistent with the time interval of the incubation period. Using these criteria,

no evidence could be found that seaside residents had a higher rate of enteric disease

than the nation as a whole. In all, between 1954 and 1959, only 10 cases of enteric fever

were found whose histories suggested a swimming-associated infection and of these ten

cases only four satisfactorily fit the criteria. These four cases were associated with

beaches known-to be grossly contaminated with untreated sewage. It is interesting to

note that the minimal findings of this study frequently have been interpreted to mean

that swimming in contaminated water does not pose a health risk until the quality

of the water is judged to be unsatisfactory based on aesthetic grounds. The second

retrospective study on the risks associated with swimming also was reported by

Moore (20). In this study, the case-control method was used to determine if the

swimming experiences of children with diagnosed poliomyelitis differed from those

of children the same sex and age who did not have the disease. This was

accomplished by carefully recording the swimming experiences for the three weeks
6

prior to the onset of illness for each patient and for each control individual at the time they

were selected. One hundred and fifty matched pairs were selected during a two-year period.

The results of the study indicated that the frequency of swimming during the three weeks

preceding the onset of symptoms, in the index case, was no greater in patients than it was

in controls. The conclusion reached was that a history of swimming is not related to

contracting poliomyelitis. This study and the previous one seriously challenged the premise

that swimming in contaminated waters posed a significant health problem.

A third study of this type was conducted by D'Alessio et al. in the Madison, Wisconsin

area in 1977 (21). They examined the swimming histories of 679 well children and 216 ill

children. Enteroviruses were isolated from 119 of the ill children. Statistical analysis of these

data indicated that the risk of enteroviral disease was 3.4 times greater in children who swam

exclusively at beaches than in nonswimmers. The risk was 10.6 times greater in children

who swam exclusively at beaches if they were less than four years old. These positive

findings should be accepted with some skepticism because, as the authors point out,

swimming was not rigidly defined and, therefore, person-to-person contact cannot be entirely

ruled out as a means of transmission.

In general, when little is known about etiologic factors, retrospective studies are useful

for discovering underlying factors associated with specific disease. This usefulness does not

extend much beyond identifying associations between specific etiologic agents and exposure

factors, which is similar to what is accomplished by examining outbreaks of disease.

Furthermore, this type of study gives no information about the incidence rates in exposed and

non-exposed individuals, both of which are critical elements for determining the importance

of certain exposure factors. Retrospective studies have been used in spite of these recognized

limitations, mainly because they are much less expensive than studies where an exposed

group is identified along with a demographically similar control group and both are followed

for a period of time to assess the proportions of a response in each group, i.e., prospective

studies.

Prospective Epidemiological Studies

The first attempts to show a relationship between swimming-associated health

effects and water quality using a prospective epidemiological study design were carried

out in the late 1940's and early 1950's by the US PHS (4). The studies were conducted

at two freshwater sites, one on Lake Michigan at Chicago, Illinois and another on the

Ohio River at Dayton, Kentucky, and at two marine sites on Long Island Sound at New

Rochelle and Mamaraneck, New York. Essentially the same experimental design was

used in each of the three studies. At each location, an attempt was made to select two

beach sites, one with a high coliform density and one with a low coliform density. At the

New York and Chicago locations beaches were available that had fairly homogeneous

populations nearby and which fit the water quality requirements of the study design. At

the Ohio River location two beaches were not available and, therefore, the population

which frequented the public swimming pool was used as the study group swimming in

water with low coliform densities. Swimming activity and the occurrence of

gastrointestinal, respiratory or “other” symptoms were recorded on a “calendar” given

to each participant at the beginning of the study. The “calendars” were collected when

the study ended. Statistically significant illness rates were determined by comparing the

observed rates in swimmers to an age-adjusted expected rate calculated using the rates

observed in the total study population. The coliform densities at the study sites were

monitored daily. Swimming-associated gastroenteritis was not observed at the marine

sites or at the Lake Michigan site. However, the Ohio River study showed that

gastrointestinal illness was observed more frequently than expected in river swimmers,

based on the illness experience of all members of the study population, when the median coliform
7

density was about 2300 per 100 ml. This study established the first experimental link

between gastrointestinal illness in swimmers and bathing water contaminated with

fecal material. The design of the USPHS studies has been criticized on a number of

issues (22.23). The most frequent criticisms address the poor definition of swimming

activity and the fact that swimming days were not related directly to water quality

measurements. The use of the “calendar” system was also faulted because it allowed

for possible memory lapses between the swimming episode and the collection of data.

In 1972 the United States Environmental Protection Agency (EPA) began a series

epidemiological-microbiological studies at marine bathing beaches that were designed

to eliminate some of the deficiencies of the earlier USPHS studies. The objectives of

the EPA study were to determine if there was a health risk associated with swimming

in polluted marine waters and what measure of water quality best relates to

swimming-associated illness, and to develop a criterion for swimming- associated

health effects and some measure of water quality if such a relationship existed. The

EPA epidemiological-microbiological studies were conducted in New York City, New

York, Lake Pontchartrain, Louisiana and Boston, Massachusetts (6). The results of the

marine water studies indicated an excess of gastrointestinal illness occurred in

swimmers relative to a nonswimming control group in water contaminated with fecal

material and that the swimming-associated gastroenteritis was linearly related to the

water quality, as measured with a bacterial indicator. Several indicators of fecal

pollution were examined to determine which one best described the relationship

between the quality of the water and the swimming-associated health effect.

Enterococci were showri to have the strongest relationship to swimming-associated

gastroenteritis. Fecal coliforms, the currently recommended bacterial indicator of

water quality, showed no correlation to the incidence of swimming-associated

gastroenteritis. The final report of the marine recreational water quality study

concluded that water quality standards or guidelines for marine bathing beaches be

based on a criterion which describes a direct linear relationship between bathing

water quality, measured with enterococci, and the incidence of swimming-associated

gastroenteritis. The utility of the criterion was that it could be used at any level of

government to set standards or guidelines. The local regulatory body could determine

an acceptable level of risk, based on community perceptions, desires and needs, and

translate that risk level to a water quality standard or guideline indexed by the

enterococcus group. The marine studies had, in fact, established a valid

epidemiological criterion or model which had been unavailable to groups of standard

setters in the previous sixty years. 

Water Quality Standards for Bathing Beaches I924-1980

The evolution of national guidelines and standards for bathing places in the United

States began with the formation of the American Public Health Association Committee

on Bathing Places (24). One of the committee's first actions was to survey physicians

and public health officials across the United States to determine if bathing places

might be considered as important for the transmission of infections. A majority of the

replies expressed the opinion that disease and even epidemics could be attributed to

bathing beach activity. The committee report for 1924, tentatively adopted a

Bacterium coli standard for swimming pools, but did not extend the standard to

natural bathing waters (25). In 1933, the committee considered natural bathing waters

in great detail but did not adopt a bacterial standard because they did not want to

propose arbitrary standards or measures that might promote public hysteria about the

dangers of outdoor bathing places (26). The reluctance to propose bacterial standards

for outdoor bathing places was again evident in the 1936 and 1940 reports of the

committee wherein classification schemes were discussed but actions were not

taken despite pressures to do so from various quarters (27,28). The basis for this

general reluctance of the committee to propose standards for outdoor bathing

places was the paucity of epidemiological evidence linking illness to bathing in
8

polluted water. The 1936 report noted “the committee is unconvinced that bathing places are

a major public health problem,” and the 1940 report reiterated this position by stating,

“Epidemiological evidence does not appear to warrant the conclusions that bathing places

constitute a major public health problem.” 

The committee did consider the means of classifying natural bathing waters. The 1933

report of the committee noted that California had proposed a standard of 10 B. coli per c.c.

and that New York City had a standard of 30 B. coli per c.c. (26). The State of Connecticut

also had proposed a system of classification based on B. coli densities per 100 ml. Waters

were classified A, B, C and D. Class A. 50 B. coli per 100 ml or less, was considered very

good and Class D, more than 1000 B. coli per 100 ml, was very poor. The 1936 report stated

it was reasonable to conclude that water having a B. coli density less than 1000 per 100 ml

is probably acceptable (27). As late as 1951 this observation of the APHA Committee on

Bathing Places appeared to be still reasonable (28). Streeter (29) summarized the bathing and

recreational standards of 11 states and regions. In 9 of the 11 standards, the limiting coliform

density was 1000 per 100 ml, either as an average or a maximum. Discher (8) listed the

current standards for all of the states in 1963 and 70% of them considered waters containing

less than 1000 coliforms per 100 ml acceptable.

The 1000 coliform per 100 ml standard first used by many of the States was not derived

from a single line of evidence. Regulatory groups and some states independently established

their standards based on available state-of-the-art information. The California standard, for

instance, was arbitrarily set by the California Bureau of Sanitary Engineering over forty years

ago (30). The standard was not based on epidemiological evidence, but rather on the

perception that it related well with the drinking water standard of that time. that there was

no epidemiological evidence of health effects within the standard, that the 10 coliforms per

ml level could easily be attained and. lastly. that any 1ess stringent standard might result in

waters that would be aesthetically unacceptable. Connecticut, on the other hand, did not want

to set up a classification scheme that would be too arbitrary and, thus. they used a relative

scheme (31). They used coliform bacteria to index four classes of water. Class A, B, C and

D ranged from 0-50, 51-500, 501-1000 and over 1000, respectively. An extensive survey of

the Connecticut shoreline indicated that 92.8% of the samples contained less than 1000

coliforms per 100 ml (32,33,34). This classification agreed well with a sanitary survey

classification which showed that only 6.9% of the shoreline was designated as poor. The high

correlation led to the acceptance of waters having less than 1000 coliforms per 100 ml. Thus,

the standard in this case was based more on easy attainment in over 90% of the shoreline

rather than epidemiological data. Streeter (29) adopted a more analytical approach in arriving

at the 1000 coliform per 100 ml criteria. He used the coliform-Salmonella ratio developed by

Kehr and Butterfield (35), the number of bathers exposed, the approximate volume of water

ingested daily per bather and the average coliform density per ml of bathing water to develop

a bather risk factor. Streeter speculated that in water containing 1000 coliforms per 100 ml

there would be no great hazard for individual bathers, at least from Salmonella typhosa. It is

interesting to note that in spite of the use of different means for obtaining a standard measure

for water quality, either arbitrarily, practically, or analytically, the final results were

approximately the same. 

The coliform index was the bacteriologic standard of choice until 1968 when the NTAC to

the Federal Water Pollution Control Administration recommended that fecal coliforms, a

subgroup of the coliform group (now designated total coliforms), be used as the bacterial

indicator of water quality (3). The recommendations of the NTAC committee were based on

prospective epidemiological studies conducted by the USPHS in 1948, 1949 and 1950 (4).

These studies had indicated that gastrointestinal illness in swimmers was significantly higher

than in a control population when coliform densities averaged 2400 per 100 ml (median) on

the Ohio River and that multiple symptomatic illness (respiratory, gastrointestinal and
9

“other”) was significantly higher in swimmers than in nonswimmers when the geometric

mean coliform density was 2300 per 100 ml at a Chicago beach. The NTAC committee used

fecal coliform and total coliform density data collected on the Ohio River in the mid-1960's

to determine that the fecal coliform subgroup was approximately 18% of the total coliform

group. The committee reasoned that if a detectable health effect was observed at a coliform

density of 2300-2400/100 ml then the recommended water quality standard should include

a factor of safety. Eighteen percent of one-half of the coliform density at which a detectable

effect occurred was arbitrarily chosen as the appropriate level and, therefore, 200 fecal

coliforms per 100 mL became the recommended standard.

The recommended fecal coliform standard has been adopted by many states and

municipalities in spite of the fact that the 1972 NAS-NAE report on Water Quality Criteria

did not recommend guidelines for recreational water because of a paucity of valid

epidemiological data (5). The NAS-NAE committee was not alone in questioning the validity

of the USPHS studies which had been summarized by Stevenson in 1953 (4). Henderson (9)

and Moore (23) have discussed the inadequacy of the epidemiological studies used to support

the NIAC recommendation.

In 1972, the EPA recommended a recreational water quality standard similar to that

proposed by the NTAC (1). Although the Stevenson report (4) is referenced in the rationale

for the criterion, the relationship between the US PHS studies and the 200 fecal coliform per

100 ml standard was not described. Rather, the relationship between the frequency of

occurrence of Salmonella and density of fecal coliforms was emphasized. The rationale

indicated that the frequency of occurrence of Salmonella falls between 60 and 100% when

the fecal coliform density was greater than 200 per 100 ml. This recommended criterion is the

one most widely used in the United States today.
10

SECTION 4

 

FRESHWATER STUDIES

The establishment of a sound relationship between swimming-associated illness and

marine water quality still left unanswered the question of whether or not this criterion could

be used in fresh water environments. The USPHS studies on the Ohio River indicated that

there was an excess of gastrointestinal illnesses among swimmers when compared to control

populations, which could properly be characterized as barely detectable (4). Furthermore,

the USPHS studies could not find a swimming-associated gastrointestinal illness effect at

Chicago beaches or at marine beaches on Long Island Sound. Since the EPA studies did

show an effect at marine bathing beaches, the expectation was that, not only would a

swimming-associated effect be found, but that the freshwater swimming-associated illness

rates might be significantly higher than the marine rates.

This report examines the data collected during studies carried out by the University of

Oklahoma, Oklahoma City, Oklahoma and Gannon University, Erie, Pennsylvania under the

auspices of the EPA. The objectives of this report were to: (1) determine if the swimmingassociated health effect/water quality criterion model established in the marine studies could

be confirmed at freshwater bathing beaches, (2) determine which indicator of water quality

shows the strongest relationship to swimming-associated health effects, if such a relationship

exists and (3) determine if the marine water quality criterion is applicable to freshwater

bathing areas.

Experimental Design

The design of the freshwater studies followed, whenever possible, the plan used in all of

the marine studies (6). The highlights will be reviewed here for the convenience of the

reader. The beach surveys or trials were conducted only on weekends to take advantage of

the large populations using the bathing beaches and to permit more intensive monitoring of

water quality during the time of swimming activity.

Swimming activity was rigidly defined as having all upper body orifices exposed to the

water. Interviewers were instructed to observe the individuals they were interviewing for

signs of complete body immersion, such as wet hair. This was not always possible and

reliance was then placed in the responses to questions about swimming activity. The

nonswimming control group was selected from beachgoers who did not meet the definition

of a swimmer.

The beach interviews were conducted in two phases. In the first phase, trained

interviewers approached beachgoers who were about to leave the beach area and solicited

their cooperation in the study. Whenever possible, family units were sought because

information on multiple individuals could be obtained from one person, usually an adult

member of a family. During this initial contact, the following information was obtained on

each participant: sex, age, race and ethnicity, if the person swam and got their head and face

wet, length of time and time of day in the water, the illness symptoms they may have had

in the previous week, and for those who did not swim, the reason for not going into the

water. An address and telephone number was requested so that follow-up information could

be obtained. If an individual had gone swimming in the previous five days, they were not

asked to participate in the study. Telephone interviews were conducted 8 to 10 days after

the swimming experience. The eligibility of each participant was confirmed, i.e., they had

not swam in the week following the initial contact, before they were queried about the
11

onset of any symptoms of illness that might have occurred during the time interval

between the swimming experience and the follow-up telephone call.

The sites for the freshwater bathing beach studies were located at Keystone Lake,

which is about 15 miles from Tulsa, Oklahoma, and on Lake Erie at Erie, Pennsylvania.

Two sites were used on Keystone Lake, one set of beaches was less than three miles

from the point of discharge of a sewage treatment facility (Beach W), and the other was

located about five miles from the outfall (Beach E). In 1979 the sewage treatment

system was two “full retention” lagoons, which discharged an average of 120,000

gallons per day of unchlorinated sewage. The following year the practice of releasing

non-disinfected sewage into the lake was discontinued. After April of 1980,

approximately 60,000 gallons per day of sewage was passed through one of the lagoons,

then through an aeration basin after which it was adequately treated with chlorine

before being discharged. Two sites also were used in the Lake Erie studies. Both sites

were located at a State Park which is situated on a peninsula just north of the City of

Erie. One beach is approximately three-quarters of a mile northwest of the outfall which

discharges the treated sewage of a large urban population (Beach B). An activated

sludge process is used to treat an average of 45 million gallons per day of sewage. The

secondary treatment effluent was chlorinated before being discharged into the lake. The

second beach is located on the opposite side of the peninsula from the effluent outfall

(Beach A). This site does not receive pollutants from a point source and the quality of

the water is usually good.

The key bacterial indicators of water quality which showed the strongest relationship

to swimming-associated illness in the marine bathing beach studies were E. coli and

enterococci. These two indicators were monitored in all phases of the freshwater

studies. Fecal coliforms, the currently accepted bacterial indicator of water quality, were

monitored in both years of the Keystone Lake Study and in two years of the Lake Erie

Study. The enterococci, an indicator group which includes two species, Streptococcus

faecalis and Streptococcus faecium, were enumerated with the method of Levin et al.

(36). E. coli was enumerated by the method of Dufour et al. (37) and fecal coliforms

were quantified according to the procedures outlined in Standard Methods for the

Examination of Water and Wastewater (38).

The data from the freshwater bathing beach studies were analyzed with respect to the

objectives of the recreational water quality research program. One of the goals of the

program was to determine whether swimming in freshwater contaminated with sewage

effluents results in a higher rate of gastrointestinal illness in swimmers relative to the

rate observed in a beach-going, nonswimming reference group. This latter group had a

tendency to be quite small at one of the study sites. The small number of nonswimmers

is a phenomenon of freshwater beaches. Unlike marine beaches, where wading and

sunning are more popular than swimming, the beach goers at freshwater beaches have

a tendency to go into the water for extended periods and to immerse their bodies totally

in the water. This greater water activity results in a much smaller nonswimming

population from which a control group can be chosen. In order to overcome this

limitation of the freshwater studies, it was necessary to pool the nonswimming control

groups from each beach within a single swimming season to form a single control

population. The homogeneity of the nonswimming control groups at the beaches of each

study location with regard to age, sex, race, and socioeconomic status lent itself to this

adjustment. The pooling of nonswimming control groups for each year increased the

probability of detecting a difference in the incidence of illness between swimmers and

nonswimmers if it does exist. The variables used to examine this relationship were the

differences in symptomatic illness rates between swimmers and nonswimmers, and the

density of bacterial indicators in the water at the time of swimming activity. Age was shown

to be a confounding risk factor in the marine bathing beach studies (6) and, therefore, this

factor was controlled in the analysis of the data. The Mantel-Haensel Chi Square

test was used to determine if something other than random processes might account for
12

the observed differences in illness rates between swimmers and nonswimmers, i.e.,

exposure to contaminated bathing water (39). 

A second goal was to determine if there is a direct relationship between swimming

associated gastrointestinal illness and water quality as observed in the marine bathing

beach studies. Regression analysis was used to determine if a direct relationship exists

between these variables (40). 

Another goal of the study was to determine which bacterial indicator of water quality

showed the strongest relationship to swimming-associated illness. Correlation analysis

was used to measure the degree of association between gastroenteritis and the various

indicators examined. Three statistics, the correlation coefficient, the regression

coefficient and the standard error of the estimate, were used to characterize the strength

of the association. 

Finally, the relationship between health effects and water quality observed at

freshwater bathing beaches was compared to the results obtained at marine bathing

beaches. This latter comparison was used to determine if the criterion developed for

marine bathing beaches is applicable to freshwater environments.

Lake Erie Study

The Lake Erie studies were conducted in 1979, 1980 and 1982 at beaches in a State

Park near Erie, Pennsylvania. in 1979 and 1980 two beaches were used, one with good

water quality and the other of excellent water quality, while in 1982 only the good

quality beach was used. Both beaches met local and state standards for recreational

waters. 

The demographic characteristics of the study participants have been given elsewhere

(41). In general, the sex ratio among swimmers was about 1:1 and among nonswimmers

there was approximately twice as many females as males. These ratios were rather

constant over the three-year study period. The age distribution at the beaches also was

rather constant during the course of the studies. Among swimmers, the age group

between 1 and 19 years old made up between 43 and 55% of the population, whereas

in the nonswimmers that age group comprised approximately 23% of the population.

The racial distribution of swimmers and nonswimmers, and the socioeconomic status

of these two groups, as measured by a crowding index, was remarkably similar. 

The high success rate for follow-up contacts was the result of repeated telephone calls

until the participant was reached (Table 2). The average overall success rate was 92%

during the three-year course of the study.
13

A detailed analysis of the individual symptom rates is presented elsewhere (41). The rate

of symptoms grouped by category is given in Table 3. Gastrointestinal (GI) symptoms

include a positive response for any of the following individual symptoms vomiting, diarrhea

stomachache or nausea. The individual symptoms in the respiratory category were sore

throat, bad cough or a chest cold, and in the “other” category they were fever (greater than

100oF), headache for more than three hours, and backache, Disabling gastrointestinal

symptoms (DGI) were defined as any one gastrointestinal symptoms plus any one of the

following characteristics: stayed home due to symptoms, stayed in bed due to symptoms or

sought medical help due to symptoms. The highly credible gastrointestinal (HCGI)

symptoms are a combination of unmistakably recognized individual symptoms used to

establish the credibility of the gastrointestinal illness. HCGI symptoms are defined as any

one of the following: (1) vomiting, (2) diarrhea with a fever or disabling condition

(remained home, remained in bed or sought medical advice due to symptoms) and (3)

stomachache or nausea accompanied by a fever.

In general, the symptom rates for swimmers were higher than those for nonswimmers, in

all the categories. However, most of the symptom rates, especially those unrelated to enteric

illness, were not statistically significant (p<0.05). This finding was similar to that observed

in the early USPHS studies (4) conducted in the 1950's and in the marine recreational water

studies conducted by the USEPA in the 1970's (6). Most of the statistically significant

differences between swimmer and nonswimmer illness rates, with one exception, occurred

in those symptomatic illness categories associated with enteric disease. Differences which

occurred in the “other” category were usually due to a fever with a temperature greater than

1000 F. The significant swimming related illness rates also had a tendency to occur at the

beach with poorer quality water, Beach B. These data clearly show that there is a

swimming- associated health effect and that the effect appears to be related to the

microbiological quality of the bathing water. The illness rates by age showed a pattern

similar to that observed in the marine bathing beach studies (6), wherein the highest rates

for gastrointestinal illness occurred in children under 10 years old.

The geometric mean density and range of each of the indicators for each of the years is

given in Table 4. The indicator densities were unexpectedly low at both beaches in 1979.

In 1980, on the other hand, the indicator densities were high and on one or two occasions,

extremely high as indicated by the range. The levels in 1982 were only moderately high

relative to those observed in 1979. The bacterial indicator densities maintained their

relative position at both beaches during the course of the study. The E. coli density was

always highest and enterococci densities were always lowest. Similarly, Beach B indicator

densities were always greater than those observed at Beach A reflecting on the nearness of

the sewage treatment plant outfall.

Keystone Lake

 The Keystone Lake studies were conducted in the summers of 1979 and 1980. The

beaches were selected in a 1978 pilot study which showed the water quality of these two

sites was different based on bacterial indicator densities. 

 The demographic characteristics of the study participants are given elsewhere

(42, 43). The ratio of females to males was about equal in the swimmer category,

but among nonswimmers about three-fifths of the participants were females.

Similar ratios were observed in both 1979 and 1980. The socioeconomic status of

swimmers and nonswimmers in each year of the study also was very similar. As in

the Lake Erie study population, the age distribution of swimmers and nonswimmers

was nearly constant from one year to the next. Individuals under the age of 20 years

only comprised 45 to 50% of the swimmer population, whereas this age group made up 18
14
15

to 20% of the nonswimmer population. In the nonswimmers, the largest age group was

the 20 to 39 year old portion which ranged from 60 to 70%. The racial characteristics of

the study populations in 1979 and 1980 were similar to each other and to that observed

in the Lake Erie studies. About 96% of all swimmers and nonswimmers over the two

years of the study were Caucasian. 

The success rate for follow-up contacts are shown in Table 5. The overall success rate

was about 85% with a range of 83 to 88%. Table 5 also shows the distribution of

swimmers and nonswimmers in the total participating study population for the years 1979

and 1980. The percentage of nonswimmers in the total study population for each of the

two beaches was 15% and 13% at the W beach and l5%and 11% at the E beach for the

respective 1979 and 1980 swimming seasons. The pooling of nonswimming control

groups within years increased the average percentage of nonswimmers in the total study

population from an average of 13.7% to 24.2%. 

The detailed health effects data for the Keystone Lake study trials are presented

elsewhere (42,43). The symptom rates grouped by category are shown in Table 6.

The symptoms which make up each category are the same as those defined previously

for the Lake Erie studies. The trend toward higher symptomatic illness rates in
16
17

swimmers, relative to nonswimmers, observed in the Lake Erie studies also was evident

in the Keystone Lake studies. The only exception to the trend occurred at Beach E in

1979 where the respiratory symptom rate in nonswimmers apparently was greater than

that for swimmers although the difference was not statistically significant. In 1979

there was only one symptom category where the difference in illness rates between

swimmers and nonswimmers was shown to be statistically different, and that occurred

in the “other” category. Conversely, in 1980 statistically significant differences in

illness rates between swimmers and nonswimmers were observed in three categories:

GI, respiratory and “other” at Beach W, and in the GI and “other” categories at Beach

E. The failure to find swimmer-nonswimmer differences in the highly credible GI

category, in spite of the fact that statistically significant differences were found in the

GI and “other”' categories, was not unexpected since this was observed on a number of

occasions in the marine studies (6). 

The bacterial indicator densities observed during the 1979 swimming season were

consistent between indicators (Table 7). Indicator densities at the beach nearest the

source of the pollution were always higher than those at the more distant beach. The

1980 data, however. do not reflect such constancy. The enterococci and fecal coliform

densities are not different between beaches as would be expected and the E. coli

densities appear to be higher at the beach more distant from the pollution source. These

inconsistent results may have been caused by heavy rains which occurred in the four

days before the start of the beach study trials. In that short four-day period, 8.15 inches

of rain was measured. This, in turn, caused the lake elevation to rise approximately

nine feet above its normal level. The lake elevation did not return to its normal level

until July 18, about a month after the heavy rains. The turbidity of the water also was

increased during this time period. The effect these unusual events might have had on

the swimmer illness rates is unknown.
18

SECTION 5

 

DEVELOPMENT OF A CRITERION

The development of a criterion which relates swimming-associated health effects to

some measure of water quality requires that certain basic information must be available

before a valid model can be established. One of the critical elements in such a model is

to show that there is a significant excess of illness in bathers who swim in surface waters

contaminated with domestic wastewater. The USPHS studies on the Ohio River and at

other locations were an attempt to reach this objective (4).

Those studies did show that there was a barely detectable health effect when the

bathing water contained about 2,300 coliforms per 100 ml, an indication that the water

was contaminated with fecal material from humans or warm-blooded animals. The effect

was shown only for symptomatic gastrointestinal illness and not for the respiratory or

“other” categories of symptoms.

The more recent EPA marine bathing beach studies also showed, in unquestionable

terms, that one of the main health effects related to swimming in sewage-polluted water

was gastrointestinal illness (6). Although increased rates of respiratory and

“other”symptomatic illness were related to swimming activity alone, only the rate of

gastrointestinal illness increased significantly as the quality of the bathing water

decreased. The EPA marine studies also accomplished what the early USPHS studies

could not accomplish, that is, show that there is a risk of enteric illness due to swimming

in polluted marine waters.

The studies described in this report clearly confirm that the risk of contracting

gastrointestinal illness greatly increases if a person swims in water contaminated with

human domestic wastes. The Lake Erie bathing beach trials showed that almost all of the

statistically significant differences in swimming-associated illness rates occurred only

in those symptom categories related to gastroenteric illness and that there was a greater

preponderance of significant differences at those beaches having the highest degree of

fecal contamination. The results of the Keystone Lake study were not as clear-cut as

those at the Lake Erie beaches, but the observed statistically significant swimmingassociated illness rates were related mainly to gastrointestinal symptomatology and

“other” symptoms such as fever greater than 100oF. Two single exceptions to these

findings were the swimmer-nonswimmer rate differences in the respiratory category

which occurred at Lake Erie and Keystone Lake beaches in 1980.

The second objective of this report was to determine which indicator of fecal

contamination, enterococci, E. coli or fecal coliforms showed the strongest relationship

to swimming-associated illness. Enterococci and E. coli were considered because they

showed the “best” relationship to swimming-associated illness in the marine recreational

water quality studies. Enterococci were judged to be superior to E. coli for use in marine

waters (44). Fecal coliforms also were examined in the freshwater studies because they

are the currently recommended indicator group for monitoring recreational water quality.

Three statistics related to regression and correlation analysis were used to

determine which bacterial indicator had the strongest relationship to swimmingassociated illness in freshwater environments. They are the slope of the regression

equation, the standard error of the estimate and the correlation coefficient. In the

marine bathing beach studies, only the correlation coefficient was used to compare

the “strength of association” of various indicator bacteria to swimming-associated

illness. Since the number of paired data points available in the freshwater studies is

small, it seemed appropriate to use ancillary descriptive information to arrive at a
19

judgment as to which indicator should be used to establish the relationship between

water quality and swimming-associated health effects. The slope was chosen because

it indicates how large a change in a health effect will be associated with a change in

water quality. It also has the advantage of being amenable to statistical testing to

determine if it is different from zero or some other slope. The standard error of the

estimate is useful because it is an average measure of the vertical distances of the

observed points from the regression line. It is defined as the square root of the sum of

the squared vertical distances from the regression line divided by the number of points.

Thus, the smaller this value, the closer the points are to the regression line. The

correlation coefficient is included so that the results of the freshwater data can be

directly compared to the marine data. Since the correlation coefficient can be affected

by the magnitude of the slope and the standard error of the estimate, but gives no

indication of the relative influence of these two components, less weight will be

attached to this statistic relative to the other two. 

Table 9 is a summary of the statistics used to describe the relationship of

gastrointestinal illness to enterococci, E. coli and fecal coliforms. The statistics were

generated using the summary data given in Table 8. The first conclusion that can be

drawn from the data in this table is that fecal coliform densities in freshwater are

unrelated to swimming-associated gastroenteritis. The slope of the regression lines of

highly credible and total GI symptomatic illness on fecal coliform densities were not

significantly different from zero. This finding was very similar to that reported for the

relationship of HCGI and total GI symptoms to fecal coliform densities in studies at

marine bathing beaches (6). In those studies, correlation-coefficients for HCGI and

total GI symptoms on fecal coliform densities for data analyzed by summer and by

beach were respectively -0.01 and 0.01. The implication of these results is quite clear.

Bacteria from sources other than the gastrointestinal tract of man and other warmblooded animals, which fit the definition of fecal coliform given in Standard Methods

for the Examination of Water and Wastewater (38), are present at densities high

enough to sufficiently eliminate the usefulness of fecal coliforms as an indicator
20

of fecal contamination of surface waters. This hypothesis is supported by the

numerous reports that at least one genus within the fecal coliform group can readily

grow to high densities in the presence of industrial wastewaters. Klebsiella

pneumonia and other Klebsiella species grow to extremely high densities in pulp

mill wastes (45,46), textile processing plant wastes (47) and cotton mill wastes

(48). Industrial wastes are not the only source of thermotolerant Klebsiella. The

proportion of Klebsiella in fecal coliform populations observed in secondary

effluent samples from seven sewage treatment plants has been found to range from

13 to 42% (unpublished data). Furthermore, this genus was shown by Kinney,

Drummond and Hanes (49) to be much more resistant to chlorine than other genera

of the fecal coliform group. This latter observation might account for the finding

that more than one-half of 24 water samples collected over a 15-day period from

Beach B on Lake Erie had fecal coliform populations that were more than 30%

thermotolerant Klebsiella. The percentage of Klebsiella ranged from 17 to 73% of

the fecal coliforms. This ubiquitous organism, many strains of which fit the fecal

coliform definition, may very well be a partial reason why fecal coliform densities

do not show a direct relationship to swimming-associated GI illness. 

Eschericia coli densities on the other hand show an excellent relationship to

swimming-associated GI illness. Since E. coli is by definition a fecal coliform, this

strong association to GI illness can only be attributed to the use of a highly

selective differential enumeration method which effectively eliminates potential

interfering organisms. The slopes of regression lines calculated using illness rates

from the HCGI and total GI categories against E. coli densities both showed a

statistically significant change in illness rates with changes in indicator densities.

The standard error of the estimate associated with HCGI symptom rates was the

smallest of all the estimates, indicating that this indicator had the closest fit of

points to the regression equation. The correlation coefficient for the association

between HCGI symptoms and E. coli densities was 0.804, the largest of all the

correlation coefficients and indicating that E. coli shows the “best” relationship to

swimming-associated GI illness. This rationale, which was used in the marine

recreational water quality studies to choose the “best” indicator, may not he

applicable to the freshwater studies. This is suggested because of the equally

excellent relationship between GI illness rates and enterococci densities. The

slopes for the two symptom categories generated using enterococci as the

independent variable are very similar to those obtained using E. coli. 

If a statistical significance test is performed to test the hypothesis that the slope of

the regression line of HCGI illness rates on enterococci densities equals the slope of the

regression line of HCGI illness rates on E. coli densities, it can be shown that the
21

slopes are not significantly different (p >0.05). Furthermore, it cannot be shown

that the y-intercepts or the correlation coefficients associated with these two

indicators are significantly different (p >0.05). Since the two indicators show

equally strong associations to swimming-associated gastrointestinal illness, it

seems that an appropriate approach would be to present two criteria and

recommend one of the two based on factors unrelated to the statistics of regression

and correlation analysis.

Criteria for Freshwater Bathing Areas

Cabelli (6) has defined a water quality criterion developed for use with indicator

systems as “a quantifiable relationship between the density of the indicator in the

water and the potential human health risks involved in the water's use.” The health

effects-water quality criterion that will be developed in this section fits the above

definition, and its purpose will be to provide a quantifiable relationship which can

be used to set water quality guidelines or standards for fresh bathing waters. The

regression lines which characterize the relationship between highly credible and

total gastrointestinal symptom rates, and bacterial indicator densities were

developed from the regression coefficients given in Table 9. It was assumed that

the logarithm of the bacterial density would graph linearly against the incidence of

disease since this model had previously been shown to be applicable to similar data

in the marine bathing beach studies (6). The validity of the linear relationship was

examined using the run test (50), a crude but simple method for determining

departures from linearity. None of the estimated lines showed statistically

significant departures from linearity (p >0.05). The regression lines for highly

credible and total gastrointestinal symptom rates on indicator densities are shown

for E. coli, enterococci and fecal coliforms in Figures 1, 2 and 3. Each point

represents a pair of variables, the geometric mean indicator density obtained from

water samples collected at a beach over a single bathing season and the

corresponding swimming-associated illness rate. The gastrointestinal illness rate

and fecal coliform density data displayed in Figure 3 serve to emphasize the lack

of association between these two variables. This lack of association was indicated

in Table 9 by the low value of the correlation coefficient and the flatness of the

slope. The regression lines for E. coli and enterococci, on the other hand, show

significant changes in the symptomatic illness rates with changes in indicator

densities. Furthermore, all of the observed data points are in close proximity to the

estimated regression lines, especially those for the highly credible symptoms. The

regression lines for E. coli and enterococci are remarkably similar with respect to

slope, standard error of the estimate and correlation coefficient. The only

differences of any significance are the higher densities of E. coli relative to

enterococci as manifested by the greater y-intercepts associated with the E. coli

regression lines, especially in the case of the HCGI symptoms. The average highly

credible GI symptom rates were about 43% of the average rates observed for total

GI symptoms. The overall mean enterococci density for the nine trials was 18.9 per

100 ml, while that for E. coli was 71.9 per 100 ml. These results were not

unexpected, since enterococci are typically found at densities lower than E. coli,

both in human feces (51) and in sewage effluents (52).

The strength of the relationship between health effects and the various water

quality indicators examined in the marine recreational water quality study showed

clear-cut differences and, therefore, the choice of the “best” indicator was obvious.

The selection of the “best” indicator with respect to the strength of the relationship

between water quality indicator and swimming-associated illness is not obvious in

the results of the freshwater studies. The similarity of the data describing the

relationship of swimming-associated illness to E. coli and enterococci densities is

so great that a criterion will be presented for each bacterial indicator. The health

effects-water quality criteria for E. coli and enterococci are shown in Figures 4 and

5. Each figure shows the estimated lines of best fit and the 95% confidence limits

of the lines.
22
23
24

Although data for both highly credible and total GI symptomatic illness have been

shown, only the former will be used to develop criteria for fresh recreational bathing

waters. The reason for not considering a criterion using total GI symptomatology is twofold. First, the regression and correlation analyses indicate that the strength of the

relationship between the indicators and highly credible symptom rates is much greater

than that with total GI symptom rates, and second, as pointed out by Cabelli (6), highly

credible symptoms should be used “because of the greater credibility of its data base

and because it is more conducive to economic analysis.” 

The two figures shown are useful for approximately determining the number of

swimming-associated gastrointestinal illnesses that might be expected at a bathing

beach where the density of E. coli or enterococci falls within the range of the criterion.

However, a relationship of this type most likely will be used to determine. not what the

risk is but what the water quality should be after an acceptable risk level has been

agreed upon by a local or state authority. Since the two characteristics (indicator density

and Illness rate) used to develop the criterion both show variability and only the

variability of the dependent characteristic is accounted for in the regression equation

and its 95% confidence limits. it is necessary to show a second relationship where the

indicator densities play the role of the dependent characteristic. The regression line for

E. coli on swimming-associated illness. The equation of the line and the 95%

confidence limits of the line are shown in Figure 6. A similar equation. line and limits

for enterococci are shown in Figure 7. Either one of the relationships shown in Figures

6 and 7 can be used to establish guidelines or standards based on acceptable risk.
25
26
27

SECTION 6

 

MARINE VERSUS FRESHWATER CRITERIA

The recreational water quality studies carried out by the USPHS in the early 1950's (4)

could not detect a swimming-associated illness effect at two marine bathing beaches on Long

Island, New York. Since swimming-associated gastrointestinal health effects were observed

at a freshwater bathing site in the same study series, it was assumed that the results of the

EPA fresh recreational water quality studies would reveal higher swimming-associated

gastrointestinal illness rates than were found in the EPA marine bathing beach studies. This

assumption posed a further question as to whether or not a single criterion could be used for

both fresh and marine bathing beach waters. When the results of the freshwater studies were

compared to those of the marine studies (Figure 8), it was clear that the illness rates in

bathers swimming at marine bathing beaches were significantly higher (p <0.05) than those

in freshwater swimmers when the data were analyzed using the Wilcoxon rank sum test

(53). The mean of the marine highly credible GI illness rate data (15.2 per 1000), grouped

by beach and year, was 2.67 times greater than the mean for the highly credible GI illness

rates in freshwater swimmers (5.7 per 1000). The Wilcoxon rank sum test (53) also was

used to show that the means for the E.coli and enterococci indicator densities in marine

waters were not significantly different from the means of those two indicators in fresh waters

(Figure 8). The similarity in indicator densities in freshwater and seawater can be explained

on the basis of the limitations placed on the selection of study sites and the difference in

gastrointestinal illness rates between marine and freshwater swimmers can possibly be

accounted for by the die-off rates of indicator bacteria and pathogens in marine and

freshwaters.

The constraints of the site selection process stipulated that the water quality at each

location had to meet local standards. All of the sites where studies were conducted used the

200 fecal coliform per 100 ml standard and since the bathing waters were usually in

compliance with the standard, it is not surprising that there is some uniformity of indicator

densities in the marine and fresh beach waters.

The survival of coliforms in seawater and freshwater was examined by Chamberlin and

Mitchell (54). They analyzed 87 seawater studies and 28 freshwater studies on indicator

bacteria die-off. The results of their analysis indicated that the median T90 value, i.e., the

time it takes for 90% of the indicator bacteria to die-off, from the seawater studies was 2.2

hours, whereas the mean T90 value from the freshwater studies was 57.6 hours. Hanes and

Fragala (55) have shown that under laboratory conditions enterococci and E. coli behave

much like coliforms do under field conditions. E. coli had a T90 of 18 hours in seawater and

110 hours in freshwater, while enterococci had a T90 of 47 hours in seawater and 71 hours

in freshwater. The differential die-off of indicators by itself, however, is not sufficient to

explain the difference in gastrointestinal illness rates between marine and freshwater

swimmers. The linear relationships between gastroenteritis and E. coli or enterococci

in marine and fresh recreational waters shown in Figures 9 and 10 provide additional

information which might be useful for answering the question. The coefficients used to

generate the regression lines in Figures 9 and 10 are given in Table 10. It is

noteworthy, that with the exception of the regression line showing the relationship

between swimming-associated illness in marine waters and E. coli densities, all of the

estimated lines in Figures 9 and 10 intersect the indicator density axis at mean

indicator densities greater than 1 per 100 ml. This suggests that the infectious dose

level of the etiologic agent disappears before the mean indicator densities become
28

unmeasurable in both marine and freshwater environments. The implication of this observation

is that the etiologic agent, which is assumed to be a virus (56), probably dies off at the same rate,

whether in seawater or freshwater, since the swimming-associated effect of the pathogen

infectious dose approaches zero as the indicator density approaches a value of 1 per 100 ml. This

would not be an unreasonable assumption, since Cioglio and Loddo (57) have shown that strains

of Polio, ECHO and Coxsackie virus had similar die-off rates in river and seawater held at 25oC.

Although it is unlikely that these viruses are the cause of swimming-associated gastroenteritis, it

is possible that the unidentified etiologic agent behaves in a similar fashion. The assumed similar

die-off rate of the pathogen in freshwater and seawater, coupled with the greater die-off of

indicator bacteria in seawater than in freshwater, could account for the difference in gastroenteritis

rates between marine and freshwater swimmers, especially when both types of recreational waters

are required to meet the same microbial standard. Thus, an indicator would decay rapidly in
29
30

seawater while the pathogen does not, leaving an excess of pathogen once the standard

is reached. In freshwater. the indicator decays at the same rate or slower than the

pathogen, which results in a low density of pathogen by the time the standard is

attained. At equivalent indicator densities, there will be an excess of pathogen in

marine waters relative to what would be found in freshwaters. and therefore a higher

illness rate will be observed in marine waters. Thus, the difference in marine and

freshwater swimmer illness rates is not only statistically significant. but also is

apparently compatible with many of the known characteristics of indicators and

pathogens associated with the observed phenomenon. The significance of these findings

is that a single water quality criterion for seawater and freshwater has been effectively

eliminated from consideration. and therefore a separate criterion should be used for

each type of bathing water.
31

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