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Committee Report:
Emerging pathogens
—
viruses, protozoa,
and algal toxins
Water utility managers will need to know important issues
about microbes of concern in drinking water.
AWWA Research Division
Microbiological Contaminants
Research Committee
A
coordinated effort is needed to
deal with emerging pathogens in drinking water so
that water utilities and regulators alike can develop
a response plan.1 This plan must assess what is known
as well as gaps in information about potential pathogens so that microbial and
chemical risks can be balThe American Water Works Association Research Division
anced.2,3 In 1995, a group
Microbial Contaminant Committee reviewed three viral and three
of experts was convened
protozoan microorganisms and one set of bacterial toxins of
by the International Life
greatest concern to the water industry: enterovirus, calicivirus
Sciences Institute, the US
and Norwalk virus, and hepatitis; Cyclospora cayetanensis,
Environmental Protection
microsporidia, and Toxoplasma gondii; and cyanobacterial toxins.
Agency, and the AWWA
To help the water quality specialist, this report describes the
Research Foundation to
virus, protozoan, or toxin; reviews its health effects; summarizes
develop a general frameinformation on its occurrence, waterborne outbreaks, and water
work for assessing the risk
treatment; discusses analytical procedures; and outlines needed
research.
For executive summary,
see page 191.
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JOURNAL AWWA
Water suppliers are
familiar with the protozoa
Giardia lamblia and
Cryptosporidium parvum
(left) but may want to
learn more about
Toxoplasma (below)—a
protozoan parasite that
can be waterborne and
that occurs worldwide.
of human disease following exposure to pathogens.4 eter; they replicate in the cytoplasm of host cells, and
In 1996, the AWWA Research Division Microbial
they resist both high and low pH.
Contaminant Committee polled its members and then
Health effects. Human enteroviruses cause a varifocused on four bacterial, three viral, and three pro- ety of clinical illnesses ranging from paralytic
tozoan microorganisms and one set of bacterial tox- poliomyelitis, myocarditis (heart infection), and diains of greatest concern to the water industry.
betes to the common cold. Poliomyelitis (“polio”) has
The first part of this report reviewed bacterial
been known since ancient times, but it was a major
pathogens in water and provided a model for assessconcern in the earlier part of the twentieth century
ing the risk of microbes in water.5 This article reviews
as epidemics (primarily afflicting young children)
other organic contaminants:
the caliciviruses and specifically Norwalk virus, enterovirus, and hepatitis virus; the
he 1990s can be characterized as the
protozoa Cyclospora cayetanensis, microsporidia, and Toxodecade of the microbe.
plasma gondii; and cyanobacteria toxins (Table 1). The
committee has provided an assessment of risk for became common during the summer and fall. The
these microorganisms and toxins by characterizing virus can cause permanent nerve damage that paratheir occurrence and concentration in water, their lyzes the arms, legs, or lungs. Most symptomatic infecsusceptibility to treatment, and their health effects. For tions result only in influenzalike or respiratory illeach contaminant investigated, the following report ness. Because of the development of poliovirus vaccine
contains a brief overview, a summary of outstandand large-scale vaccination programs, paralytic
ing issues, and access to the relevant literature. Al- poliomyelitis has been absent from the Western Hemithough some would debate whether the organisms sphere for the past five years. Coxsackievirus and
listed are emerging pathogens (as opposed to microbes echoviruses are now recognized as a leading cause
already recognized as pathogens), the committee’s of acute fevers among young children and infants
objective was to highlight organisms that might not and, in developed countries, as the most common
be well known to water utility personnel.
cause of aseptic meningitis.6 The mortality rate in
more severe illnesses (meningitis, myocarditis, paraViruses
lytic disease) ranges from 0.01 to 0.9 percent.
Enteroviruses. Description. The enteroviruses
Occurrence, survival, and outbreaks. Enteroviruses
form a genus of the Picornaviridae family that are may be transmitted by either the fecal–oral route or
among the smallest ribonucleic acid (RNA) viruses— the respiratory route. One route may predominate,
thus the name “pico (small) RNA virus.” Human depending on the serotype. All enteroviruses (except,
enteroviruses are divided into four groups: poliovirus possibly, enterovirus type 70) are believed to be capa(three types), coxsackievirus (30 types), echovirus ble of fecal–oral transmission. Enterovirus type 70,
(34 types), and enterovirus (68–71 types). They are which causes eye infections, may be transmitted only
all nonenveloped, icosahedral, and 25–30 nm in diam- by direct contact with contaminated hands or other
T
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© 1999 American Water Works Association, Journal AWWA September 1999
COMMITTEE REPORT
111
they may not all grow in the
same cell line. Enteroviruses
are usually isolated from
water or other environmental
samples by the production
AWWA Microbiological
US Environmental Protection
of CPE in the buffalo green
Category
Contaminants Research Committee
Agency (Contaminant Candidate) 5
monkey kidney cell line.
Viruses
Enteroviruses
Caliciviruses
Many of the enteroviruses
Norwalk virus/Calicivirus
Echoviruses
can also be isolated by the
Hepatitis viruses
Coxsackieviruses
Adenoviruses
plaque-forming unit method.
Protozoa
Cyclospora cayetanensis
Microsporidia
In addition, molecular techMicrosporidia
Toxoplasma gondii
niques such as polymerase
Toxins
Cyanobacteria toxins
Cyanobacteria toxins
chain reaction (PCR) have
Acanthamoeba
been used to detect enteroviruses in water samples.
Water treatment. Conventional water treatment
objects (fomites). Most transmission is believed to be
with disinfection removes essentially all (99.99 perperson-to-person. Common-source outbreaks of coxcent or more) enterovirus. Coxsackievirus appears
sackievirus and echoviruses that originated in water to be more resistant to ultraviolet light disinfection
or food have been documented.
than the other enteroviruses.
The concentration of enteroviruses in raw sewage
Research needs. The Information Collection Rule12
has been reported to vary from a few hundred to
will provide important information on the occur> 100,000/L. In 279 raw surface water samples and
rence of culturable enteroviruses in surface water
260 untreated groundwater samples assayed by cell
used for large (>100,000 population) water systems.
culture, 25 and 8.1 percent, respectively, were posi- Data are needed for other surface water and groundtive for enteroviruses.7 With the exception of polio- water systems. How viruses avoid treatment barrivirus, coxsackieviruses are the enteric viruses that
ers and contaminate distribution system water should
have been most commonly isolated from water, even be investigated. Additional disinfection data are
treated drinking water. Enteroviruses may not be needed under real-world conditions. Simple methods
completely removed by domestic sewage treatment, using PCR should be developed for use in water utilincluding disinfection as normally practiced, and they ity laboratories.
can usually be isolated. Enteroviruses have been isoCalicivirus and Norwalk virus. Description. The
lated in almost any environment that has been caliciviruses are members of the viral genus caliexposed to human fecal contamination—surface water
civirus, two of which are characteristically associated
and groundwater, marine water and sediments, shellwith humans. The first, human calicivirus, contains
fish, crabs, crops irrigated with sewage, domestic solid five recognized strains (Norwalk virus, and Hawaii,
waste, soil, aerosols, and fields spray-irrigated with Taunton, Snow Mountain, and Southampton strains)
sewage water.
and others whose common names are not yet officially
The survival of enteroviruses and other enteric recognized. The second is hepatitis E virus. Other
viruses depends on many factors, including tem- caliciviruses are associated with infections in mammals
perature, sewage pollution, microbial activity, and other than humans.
adsorption to solids (clays and sediments). Generally,
Health effects. The classic calicivirus illness typically
the lower the temperature, the longer the survival
affects infants aged 1–24 months. However, calicivirus
time. Below 5 oC, enteroviruses may survive for
infections and illnesses occur in all age groups. Geriyears in the environment. They are stable at pH 3–5
atric outbreaks are characterized by diarrhea averfor 1–3 hours and can tolerate pH 10–11 for sev- aging four days (range 1–11 days). The incubation
eral minutes.
period before diarrhea is 48–72 hours. Norwalk virus
Several reports have attributed poliovirus out- and Norwalk-like caliciviral strains typically act faster;
breaks to contaminated drinking water, although the
incubation takes 24–48 hours and symptoms last
studies were not conclusive.8 Coxsackieviruses have 12–60 hours. Norwalk or Norwalk-like illness typically
been associated with two recreational outbreaks,9,10 produces vomiting in children but diarrhea in adults.
and an epidemiological study of bathers in surface
It is estimated that 40 percent of the outbreaks of
water found a significant increased risk of enterovi- gastroenteritis in adults can be attributed to the Norral infection in children.11 Although enteroviruses
walk and Norwalk-like viruses.13 Other symptoms
have been isolated from water during waterborne
associated with human caliciviruses include abdomdisease outbreaks associated with drinking water, epiinal pain, cramping, low fever, headache, nausea,
demiological investigations are lacking.
tiredness (malaise), and muscle pain (myalgia). These
Analytical methods. All enteroviruses can be grown
diseases may be severe and prolonged in immunoin primate or human animal cell cultures with the logically debilitated and elderly patients, but death
production of cytopathogenic effects (CPE), although is unlikely if supportive care is available.
TABLE 1
112
Viral, protozoan, and other contaminants of concern proposed
by AWWA Microbiological Contaminants Research Committee and US
Environmental Protection Agency
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© 1999 American Water Works Association, Journal AWWA September 1999
JOURNAL AWWA
Norwalk virus (left), a member of the viral genus calicivirus (right), is believed to be the cause of 40 percent
of the outbreaks of gastroenteritis in adults.
Research needs. A quantitative cell culture techHepatitis E virus has an incubation period of 2–8
nique must be developed for assaying the infectivity
weeks. Children typically do not show symptoms
(their infection is subclinical), although in adults
of these viruses. Such a technique will enable the
jaundice can persist for many weeks. Mortality caused
gathering of better disinfection data and better analyby hepatitis E in the general population is 0.1–4 persis of other water treatment processes.
cent,14 but for pregnant women in the third trimester
Hepatitis A virus. Description. Hepatitis A virus
it can be > 20 percent.13,14 The virus appears to be
(HAV) is a small (27-nm diameter), nonenveloped
similar to one that causes illness in domesticated
picornavirus containing a single-stranded RNA molpigs. At present no antimicrobial therapies effececule. It is a cause of acute infectious hepatitis and was
tively treat human calithe first enteric virus to be
civiral diseases.
associated with a waterOccurrence, survival,
borne disease outbreak in
and outbreaks. Human
the United States.16 HAV
caliciviruses and hepatitis
is the predominant cause
E virus are transmitted
of infectious hepatitis in
even
viral,
protozoan,
by ingestion of contamithe United States; about
nated surface water or
25,000 cases are reported
and algal toxin
groundwater, ice, conannually. 17 The true
pathogens that cause
taminated shellfish, or by
annual incidence may be
swimming in sewagehigher by a factor of two
waterborne illness
contaminated water.14,15
to ten.
are profiled.
Outbreaks of human caliHealth effects. More
civiruses can occur year
than half of the United
round, and the incidence
States population older
increases somewhat during winter months. Illness
than 40 years has serum antibody to HAV.18 It is of
caused by hepatitis E virus tends to peak in the
concern as a cause of gastroenteritis because its sympautumn in temperate areas of the world; it peaks
toms are among the most serious of those caused by
during floods caused by the rainy season in tropical enteric viruses, and it has a mortality rate of about 0.1
or monsoon areas.13
percent. HAV infects liver cells, causing inflammaAnalytical methods. The human caliciviruses
tion, cell damage, and cell death. Symptoms begin
currently cannot be cultured in vitro using animal
four to six weeks after infection and include fever,
tissues or animal cell lines. Therefore, it is necessary
nausea, loss of appetite (anorexia), and tiredness,
often with mild diarrhea, followed shortly by jaundice
to use detection techniques that do not provide in(yellowness of skin). Asymptomatic infection is comformation regarding viral infectivity. These techmon in children. Symptoms usually last one to two
niques include visual detection by transmission
weeks but may persist for several months.
electron microscopy; enzyme-linked immunosorOccurrence, survival, and outbreaks. HAV is transbent assay, which detects viral proteins; and reverse
transcriptase–polymerase chain reaction, which mitted by the fecal–oral route, and transmission by
fecally contaminated water and food is documented,19
detects viral RNA.
Water treatment. Little is known about how effecbut person-to-person transmission is much more comtively water treatment physically removes or inacti- mon. Waterborne transmission of the virus has been
vates these viruses, although some work is in progress.
reported by a number of investigators. The virus sur-
S
SEPTEMBER 1999
© 1999 American Water Works Association, Journal AWWA September 1999
COMMITTEE REPORT
113
Cyclospora cayetanensis was proposed28 for the species infecting humans on the basis of
Attribute
Cryptosporidium parvum
Cyclospora cayetanensis
sporulation and excystation
studies conducted in vitro;
Oocyst
4–6-µm spheres are
Autofluorescent spheres, 8–10immediately infectious
µm diameter, require five- to
however, others have ques10-day sporulation to be
tioned this species name.27,29
infectious; sporulation is
Cyclospora spp. are obligate
temperature-dependent.
Animal hosts
Cross transmissible among most
Documented only in humans and
intracellular parasites characmammals
various nonhuman primates
terized with other coccidia,
Disease
Acute self-limiting diarrhea
More prolonged diarrhea with
such as Isospora and ToxoNo effective drug treatment
bouts of relapse
Treatable by co-trimaxazole
plasma, because they are inWaterborne
10 in North America, 1985–95
Chicago, 199094 and Nepal,
testinal spore- (oocyst-) formoutbreaks
1994102
ing protozoa. 28 Molecular
analysis of Cyclospora has suggested that it is closely related
vives more than four months at both 5 and 25oC in to Eimeria species.30 Similar oocysts have been found
water, wastewater, and sediments.16 However, at 25oC,
in nonhuman primates in East Africa,29,31 and the
HAV generally survived longer than poliovirus and
possibility of transmission from other animals to
echovirus, regardless of soil and water quality.20 Stud- humans has been raised.
ies suggest that HAV survives for relatively long periCyclospora completes its life cycle in an individual
ods in water and soils and that it is not completely
host, and the environmentally resistant spherical
adsorbed by soils. That HAV survives in the environoocyst (8–10 µm) is excreted in stools.27 The oocysts
ment and migrates through soil helps to explain why
appear under light microscopy as nonrefractile spheres
it has been found in contor ovoids containing a
aminated groundwater. Of
variable number of incluwaterborne disease outsions. The infectious stage
breaks in the United States
of the life cycle is the
from 1946 through 1980
sporulated oocyst. Sporufor which a causative
lation takes 5–14 days at
ater suppliers should
agent was identified, HAV
temperatures of 22–32oC
stay updated regarding
caused > 20 percent (68 of
in the laboratory. 28,32
21
322 outbreaks).
Upon complete sporulathese pathogens.
Analytical methods.
tion, two sporocysts conHAV is difficult to isolate
taining two sporozoites
in cell culture, and it grows
each are formed within
inefficiently without producing CPE. The preferred
the oocyst. Laboratory exposure to an excystation
host cells are primary monkey kidney, a fetal rhesus
solution or ingestion and exposure to gastric condikidney-derived cell line (FRhk-4), and a liver carcitions will liberate the four sporozoites.28
noma cell line. Molecular techniques such as PCR and
Health effects. Cyclosporiasis is caused by ingesgene probe have been used to detect HAV in water tion of food or liquids that have been contaminated
samples.
by infectious (sporulated) oocysts. Unsporulated
Water treatment. HAV can be removed by conoocysts are not infectious to susceptible hosts. Illventional water treatment (coagulation, flocculation,
ness is characterized by watery diarrhea, abdominal
and filtration) and disinfection; however, it has been cramping, decreased appetite, and low-grade fever
detected in samples containing a free chlorine resid- that can persist several weeks with bouts of remitual of 0.2 mg/L.22
tance and relapse. Oocysts are shed in the feces durResearch needs. Data on HAV distribution in sur- ing illness. Oocysts have been described in the stools
face water and groundwater are needed, as well as
of residents of and travelers from developing nations
additional data about chlorine and other common
and in association with diarrheal illness in individudisinfectants. The mechanisms by which HAV may
als from North, Central, and South America; the
avoid physical and chemical treatment barriers and Caribbean; the Indian subcontinent; Southeast Asia;
enter finished drinking water supplies need to be
Australia; and Europe. In immunocompetent indiunderstood.
viduals the illness is normally self-limiting, whereas
in immunocompromised individuals the illness may
Protozoa
be prolonged. Although clinical disease can resolve
Cyclospora. Description. Cyclospora has emerged
without treatment, it can be treated with trimethoas a pathogen of concern to public health officials.23–27
prin-sulfamethoxazole (co-trimaxazole), and illness
This parasite was likely first observed in 1979,23 but
will subside within several days.33
the organism’s coccidian nature and particular genus
Occurrence, survival, and outbreaks. Evidence
identity were not confirmed until 1993.28 The name
strongly suggests that Cyclospora is transmitted by
TABLE 2
Attributes of Cryptosporidium and Cyclospora
W
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JOURNAL AWWA
Because little is known about microsporidia and
Cyclospora, water purveyors should keep
themselves updated regarding these
pathogens. It has been only during the past
decade that microsporidia (above left and right)
have been documented as human pathogens.
Its identity confirmed only recently in 1993,
Cyclospora (right) has emerged as a pathogen
of concern to health officials.
water. Two waterborne outbreaks have
been described. In an outbreak among
British soldiers and dependents stationed
in a small military detachment in Nepal, 12
of 14 people developed diarrhea. Cyclospora
oocysts were detected in stool samples from six of
eight patients. Water treatment by filtration and chlorination did not affect the integrity of the oocysts.
Chlorine residuals remained within acceptable limits (0.3–0.8 mg/L), and no coliform-indicator bacteria were detected. However, Cyclospora oocysts were
recovered from the drinking water supply by membrane filtration and detected by light microscopy.34
The only suspected waterborne outbreak of cyclosporiasis in the United States occurred in a hospital in
Chicago. Stool samples from 14 of the 21 people
reporting diarrheal illness after exposure to a common water source (a storage tank) were collected
and examined using a modified acid-fast stain. Samples from 11 of the patients were positive for
Cyclospora. Although no Cyclospora sp. oocysts were
found in the water supply, an epidemiological survey
strongly suggested correlation with the source. The
source of the contamination was never positively
identified.26
In 1996, 17 geographically unrelated outbreaks of
Cyclospora occurred in North America—in Texas,
Florida, New York, New Jersey, Massachusetts, Illinois, Pennsylvania, Ohio, South Carolina, Connecticut, Maryland, Vermont, New Hampshire, Virginia, and Washington, D.C., and in Toronto, Canada.
The suspected vehicle of transmission was Guatemalan raspberries. A 1995 outbreak of cyclosporiasis was also attributed to the consumption of contaminated raspberries.35
SEPTEMBER 1999
Little is known about
survival of the oocysts in
various conditions or what
treatment can effectively
inactivate the oocysts.
However, the behavior of
Cyclospora may be similar
to that of Cryptosporidium,
a related pathogen.
Analytical methods.
Under fluorescent illumination (excitation 375
nm, emission > 420 nm),
the oocyst walls autofluoresce and the bluish
spherical oocysts can easily be seen at 200X magnification.36 Clinically, Cyclospora sp. oocysts in stools are
identified by staining with an acid-fast stain. Some
oocysts commonly fail to take up the dye, which may
complicate identification.28,37 A modified safranin
technique with microwave heating is reported to uniformly stain the oocysts a brilliant orange.38
An epidemiological study in the United Kingdom
reported that the coccidian Cryptosporidium and Cyclospora are often confused in the laboratory.27 Although
these parasites look similar, differences do exist (Table
2). Cyclospora is twice as large as Cryptosporidium and
autofluoresces under ultraviolet illumination using
a 330–380-nm filter.
Research needs. Fundamental research is needed
to develop both species-specific monoclonal antibodies and molecular techniques to determine oocyst
viability, taxonomy, species identification, infectivity
and virulence; to determine water treatment
processes that remove and inactivate Cyclospora
oocysts; and to better understand the epidemiology
of cyclosporiasis in humans, such as the significance
of waterborne transmission and the public health
importance of exposure to low concentrations of
Cyclospora oocysts.
Microsporidia. Description. The word microsporidia
(a nontaxonomic term) describes organisms in the
order Microsporidia of the phylum Microspora. Only
in the past decade have these parasites been documented as human pathogens. Since the first case was
© 1999 American Water Works Association, Journal AWWA September 1999
COMMITTEE REPORT
115
documented in 1985, seven genera of microsporidia
Occurrence, survival, and outbreaks. In the
have been implicated in human disease (EnterocytoUnited States no data suggest widespread occurzoon, Encephalitozoon, Nosema, Pleistophora, Vittaforma,
rence of human strains of microsporidia in surface
Trachipleistophora, and a catchall genus, “micro- water, although the lack of appropriate analytical
sporidium”).39–46 Host specificity may be only modmethods makes this conclusion uncertain. Because
erately selective because human infection by nonmicrosporidia spores are excreted, they likely occur
mammalian genera has been documented, and in sewage-contaminated water. Also, because the
experimental in vitro infection of cells from various
apparent reservoir of various types of animal hosts
animals does not appear to be particularly restrictive.47 is large, infected hosts might maintain or even
Microsporidia are obligate intracellular parasites that
amplify the environmental presence of human
form environmentally resistant spores. Different species
infectious microsporidia. The spores of microsporidia
differ in size, location in host cells, and processes of appear able to survive for weeks or months, espespore production. Human
cially in cold water.49–51
species are typically ovoid
Their small size may
or pyriform and 1–5 µm
make waterborne microlong. Human infection is
sporidia difficult to rethought to follow ingesmove by filtration, and
tion or inhalation of spores
they could have an inethods
for
detecting
from a contaminated envicreased ability to reach
ronmental source or by
groundwater under the
all of these pathogens
direct contact with infected
influence of contamineed to be improved.
individuals or animals. Innated surface water.
fection begins by environAnalytical methods.
mental stimulation (e.g.,
Standard methods for the
pH shift or changing ionic
sampling, identification,
concentration or osmotic pressure) of the spore to
and enumeration of microsporidia in water or other
extrude its coiled polar filament. That filament becomes
environmental media are not yet available. Howa polar tubule through which the spore injects its infecever, sampling and analysis methods currently used
tious constituents (sporoplasm) into the host cell. Inside
for other protozoa, such as for Giardia and Crypthe cell, the parasite undergoes its replicative life cycle.
tosporidium, may allow limited recovery and enumeration of microsporidia. Detection and identifiMature spores have a layer of chitin that protects the
cation of microsporidia may be best served by direct
transmissible spores. After a period of infection, damaged infected host cells rupture and release large num- or indirect immunofluorescent staining using either
bers of infective spores into the original host or into monoclonal or polyclonal antibodies against various
components of the spore walls or other structures.
the environment. Environmental contamination by
Special care must be taken because both monoclonal
spores has been attributed to feces, urine, respiratory
secretions, or other body fluids of infected individuals and polyclonal antibodies have shown cross-reactivity among species.52–54 Because microsporidia are
or animals.39,40,42,44,46
Health effects. Because microsporidia are now
in a size range similar to that of bacteria and algae,
recognized as capable of infecting humans, reports other organisms may interfere with or mask them
of human infection are increasing. The role of micro- during analysis of environmental samples. Research
sporidia in waterborne disease in the United States indicates that PCR may be able to detect and deteris yet to be determined. They may pose problems mine species and that tissue culture may be able to
for the elderly or immunocompromised. Microdetermine viability.48,55,56
sporidia are isolated from 7 to 50 percent of stool
Research needs. The lack of adequate data on the
specimens and intestinal biopsies from acquired
concentrations or infectivity of the various genera
immunodeficiency syndrome (AIDS) patients with and species of microsporidia makes it impractical to
otherwise unexplained chronic diarrhea, and they assess potential health risks in the United States. Neihave been detected in coinfections with Crypto- ther is it prudent to determine removal requirements
sporidium.39,42,46,48,49 Infections are self-limiting in needed in drinking water treatment to meet US Enviimmunocompetent individuals.42
ronmental Protection Agency goals for health proIn immunocompromised individuals typical symptection. Reliable methods are needed to detect mitoms of microsporidial infection are chronic diarrhea, crosporidia in water so that its prevalence in raw and
finished water can be determined. Additional data
dehydration, and significant weight loss (> 10 percent
of body weight). Microsporidial infection, which may on disinfection and removal by conventional water
treatment processes need to be developed.
appear like cryptosporidiosis, may contribute to higher
Toxoplasma. Description.Toxoplasma is a memmortality rates. Microsporidia may infect the eyes,
liver, kidney, heart, and the central nervous system. ber of the same phylum (Apicomplexa) of protozoan
The pathology of microsporidia infection varies parasites as Cryptosporidium and Cyclospora. Unlike
these parasites, Toxoplasma requires two hosts to comdepending on the organs that are infected. Drug treatplete its life cycle: an intermediate host and a final
ment is available.34,35,37,39,41
M
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JOURNAL AWWA
TABLE 3
Waterborne viruses, protozoa, and algal toxins of concern to the water industry*
Agent
Viruses
Norwalk virus
and
caliciviruses
Enteroviruses
Hepatitis virus
Protozoa
Cyclospora
Microsporidia
Toxoplasma
gondii
Toxins
Algal toxins
Priority
for Water
Industry
Drinking
Water†
Treatment
Moderate
Occurrence
In Water
Unknown
jaundice,
death
Removed by
conventional
treatment
Removed by
conventional
treatment
Diarrhea, vomiting
Unknown
Unknown
Yes
0.035–0.04
Varied, from
diarrhea to
paralysis
Liver infection
and damage
Common
Long; years
Yes
0.025–0.03
Common
Long; >4 months
Yes
0.027
Moderate
Unknown
Diarrhea
Unknown
Unknown
8–10§
Moderate
Unknown
Unknown
Unknown
Low
Unknown
Diarrhea,
weight loss
Birth defects,
brain infection
Suspected,
mainly
foodborne
No
Unknown
Long; up to
18 months
Yes, but rare
Moderate
Not readily
removed by
conventional
treatment
Neurotoxins,
liver disease
Associated
with
blooms
Not
applicable
No
Low
Low
Environmental
Persistence
Documented
Waterborne
Outbreaks‡
Health
Effects
Size
µm
1–5§
10–12§
Not applicable
*See text for complete review.
†Priorities reflect research needs and treatment capabilities.
‡In North America
§Size of cyst
(definitive) host. The species name “gondii” is derived
from the name of the north African rodent (the
gondii, Ctenodactylus gundi) in which the parasite was
first described. Toxoplasma occurs worldwide. A variety of warm-blooded animals, including humans,
livestock, feral animals, and birds serve as intermediate
hosts, and in these Toxoplasma multiplies asexually.
Only felines act as definitive hosts; in them sexual
reproduction, resulting in the formation and excretion
of oocysts, occurs in the cells lining the intestinal
tract. Felines acquire the infection from eating infected
tissues of mammals and birds or, more rarely, from
ingesting sporulated oocysts. Oocyst excretion occurs
for 7–20 days. As with Cyclospora, immature oocysts
are excreted in the feces of felines, and an external
maturation period of one to five days is required
before they become infective. Sporulated oocysts contain two sporocysts, and each sporocyst contains four
sporozoites. Following ingestion, sporocysts excyst
in the small intestine and release tachyzoites that can
spread through the blood and lymphatic systems.
Tachyzoites are rapidly dividing forms that multiply
within invaded cells, causing their rupture, and that
can penetrate other adjacent cells. Tissue cysts, which
can contain several thousand bradyzoites (the quiescent or slowly multiplying asexual stage) encased
in a cyst wall, develop in various tissues and can
transmit infection to both intermediate and definitive
hosts that eat the uncooked meat.
Health effects. Toxoplasmosis can be acquired in
four ways. Sporulated oocysts in soil, inadequately
washed vegetables or fruit, and water may be ingested,
SEPTEMBER 1999
as may tissue cysts in raw or undercooked meat.
Tachyzoites from an infected mother may pass into the
developing fetus. Such congenital toxoplasmosis may
be clinically unobservable or may present as hydrocephalus, mental retardation, cerebral calcification
and retinochoroiditis, or death. Less commonly toxoplasmosis may be acquired from infected organs that
are transplanted.
Although many infected individuals show no clinical signs or symptoms, others experience a flulike illness or swollen glands in the neck, armpits, or groin.
Most people with toxoplasmosis recover without drug
treatment. The incubation period is one to three
weeks: 10–23 days after consumption of undercooked
meat and 5–20 days in an outbreak associated with
cats. Immunity is long-lasting, and the degree of immunity depends on age, exposure, and immunological status. Toxoplasmosis can be severe and widely
disseminated in immunocompromised individuals,
and it is the most common cause of focal brain lesions
in AIDS patients. Toxoplasma is a frequent opportunistic infection in AIDS patients.
Occurrence, survival, and outbreaks. Sporulation,
which produces eight sporozoites within two sporocysts, depends on both temperature and aeration and
takes one to five days. Unsporulated oocysts are more
sensitive than sporulated oocysts to harsh environmental conditions. For example, unsporulated oocysts
fail to sporulate following exposure to 60–70oC for 10
seconds, 4oC for 90 days, –5oC for 14 days, or –20oC
for one day, whereas sporulated oocysts remain infectious following exposure to –5oC for 120 days.57 Ex-
© 1999 American Water Works Association, Journal AWWA September 1999
COMMITTEE REPORT
117
posure of sporulated oocysts to a relative humidity of
third is a colonial blue-green alga that is related to
82 percent for 30 days or 21 percent for 3 days ren- the unicellular blue-green algae. Toxins are proders them noninfective. Oocysts can remain infecduced by many but not all representatives of these
tious in moist soils up to 18 months.
species. The toxins produced by Anabaena and AphTwo outbreaks of toxoplasmosis associated with
anizomenon are generally neurotoxins (affecting the
the consumption of contaminated water have been
nervous system), although those from Microcystis
documented. In 1979, 32 US Army soldiers showed
are hepatotoxins (affecting the liver). Other toxic
evidence of infection with Toxoplasma after their return cyanobacteria are less common. Toxic cyanobactefrom maneuvers in Panama. The most likely source of
ria have been reported from localities in the United
infection was creek water contaminated with oocysts States, Canada, Australia, New Zealand, Japan,
excreted by jungle cats,58 even though most affected
China, South Africa, and Europe.
individuals claimed to
The toxins themselves
have treated their drinkare fairly complex organic
ing water with iodine
compounds. The chemitablets. The second outcal structures of some
break occurred in British
have been known for
Columbia, Canada, in
many years, and new
orwalk virus and
1995. Acute Toxoplasma
ones have been identified
calicivirus, Cyclospora,
infections were identified
and their structures deterin 110 people, of whom
mined only recently.
microsporidia, and algal
42 were pregnant. Eleven
Health effects. Most
infants became infected.
reports of poisonings by
toxins were ranked
Epidemiological evidence
cyanobacterial toxins
of moderate concern.
was consistent with a waworldwide have involved
terborne source and imcattle, horses, sheep, dogs,
plicated the municipal
and waterfowl. Of the
drinking water.59 Domesfew well-documented
tic and feral cats and cougars were likely sources of
cases describing humans, most involved single indioocysts that contaminated the reservoir or its feeder
viduals or small groups—likely because few people
streams. Water was treated by chloramine disinfec- would drink water covered by a thick algal bloom.
tion without filtration. Primary chlorination was
The symptoms of the various algal toxins depend
thought to be unlikely to either prevent Toxoplasma on which type of toxin is involved, the amount of
oocysts from sporulating or to kill sporulated oocysts.
material ingested, and the body weight of the aniLittle is known about disinfection regimes that inacmal or human. Generally, the neurotoxins cause
tivate oocysts.
convulsions, difficulty breathing, and eventual death
Analytical methods. Analytical methods to detect
in susceptible animals. Humans can experience tinthe organism in water are not readily available. In
gling of the fingers and toes, numbness, and hay
one study,60 conventional Cryptosporidium methods
fever-like symptoms. The hepatotoxins (called
were used to concentrate and clarify water samples,
microcystins) lead to abdominal pain, diarrhea,
and after an aeration step to trigger sporulation, the vomiting, injury to the liver, and death. The effects
water concentrates were fed to mice. Tissue from
of the neurotoxins are more rapid than those of
mice that died following inoculation were examined
the hepatotoxins.
microscopically for evidence of Toxoplasma infections.
Occurrence and outbreaks. A few reports
The blood of surviving mice was examined for anti- describe swimmers whose symptoms probably were
bodies to T. gondii.
caused by cyanobacterial toxins.61,62 Generally, these
Research needs. Fundamental research should
symptoms were brief (one to seven days) and were
develop both species-specific monoclonal antibodies correlated with exposure to water that contained a
and molecular techniques to identify oocysts and
cyanobacterial bloom. More cases likely have
determine oocyst viability, infectivity, and virulence;
occurred, as most physicians probably do not recogdevelop water treatment processes that remove and nize the symptoms of algal toxins.
inactivate Toxoplasma oocysts; and investigate the sigSeveral outbreaks of gastrointestinal disease
nificance of waterborne transmission and the public were attributed to the ingestion of water containhealth importance of exposure to low concentrations ing toxic cyanobacteria. One in Palm Island (off the
Queensland coast of Australia) in 1979,63 and one
of waterborne Toxoplasma oocysts.
in Salisbury, Rhodesia (now Harare, Zimbabwe),64
Toxins
occurred in the absence of any other identifiable
Description. Many cyanobacteria (blue-green
microbial agent. Each involved the ingestion of
algae) can produce toxins. The three most com- water in which a toxic cyanobacterial bloom was in
mon species in North America are Anabaena flos- progress or had just been killed with copper sulaquae, Aphanizomenon flos-aquae, and Microcystis aerugfate. In Armidale, Australia, people who received
inosa. The first two are filamentous species, and the
water from a particular reservoir that had a bloom
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118
VOLUME 91, ISSUE 9
© 1999 American Water Works Association, Journal AWWA September 1999
JOURNAL AWWA
of Microcystis developed elevated concentrations of
a certain liver enzyme, although those receiving
water from other sources did not. 65 One of the
hepatotoxins may strongly promote liver tumors.66
A study in China suggests a correlation between
exposure to water containing microcystins and the
incidence of liver cancer.67
Analytical methods. An older method is a bioassay, in which an extract is prepared from algal material and injected into laboratory animals, usually mice.
Early work on algal toxins incorporated this method,
which determines the effects of the various toxins
on animals. A newer method involves extraction and
analysis by high-performance liquid chromatography.68,69 This method obviates the need for laboratory
animals and identifies the particular toxins present,
which the bioassay does not.
Water treatment. Although conventional water
treatment methods do not readily remove or inactivate cyanobacterial toxins, 70,71 activated carbon
does.72,73 Ozone is also effective.70,71 Ozone oxidizes
microcystin-LR extremely fast—99 percent of the
toxin is removed in 15 seconds.70 The cells themselves can be removed by filtration, but it is best not
to allow their entry into a treatment plant, as they
may release toxins into the water upon lysis by chlorine or other disinfectants.
Controlling cyanobacterial blooms with copper
sulfate can cause its own problems. Cyanobacteria
killed by copper sulfate may release the toxin into
the water.74 However, treatment with lime has been
found to counteract cyanobacteria without the release
of the toxin, partly by precipitating phosphorus and
by causing sedimentation of the cells.74,75
Research needs. Further research is needed on
the relationship of toxic cyanobacteria to short-term
and long-term human health effects such as gastroenteritis and liver cancer. Treatment strategies that
use algicides such as copper sulfate and lime need
further study. Studies of how to protect watersheds to
prevent algal growth in reservoirs may ultimately
prove the most useful.
Summary—viruses, protozoa,
and algal toxins
Table 3 summarizes and prioritizes emerging
viruses, protozoa, and toxins on the basis of information reviewed in this report. The setting of priorities involves many subjective factors and can change
as new information becomes available.
No members of these categories were ranked of
high concern for the water treatment industry. Norwalk virus and calicivirus, Cyclospora, microsporidia,
and algal toxins were ranked of moderate concern
because so little is known about these agents. Water
suppliers should stay updated regarding these
pathogens and determine, for their utility, the likelihood of these pathogens causing waterborne disease
outbreaks. Ranked of low concern were enteroviruses
and hepatitis virus primarily because they can be
controlled by conventional treatment and disinfection.
SEPTEMBER 1999
Toxoplasma gondii was ranked low because of its
rarity as a waterborne pathogen and the likelihood
that it is controlled by measures that control Giardia
and Cryptosporidium.
However, methods for detecting all of these
pathogens need to be improved, and with a better
understanding of the occurrence and control of these
agents, the concern about their health risks in water
may change. Knowledge is the first line of defense for
those who provide safe drinking water.
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About the authors: This article is the work of the Microbiological Contaminants Research Committee of the AWWA
Research Division. It was prepared by Mark W. LeChevallier (chair) with contributions from committee members
Morteza Abbaszadegan, Anne K. Camper, Christon J. Hurst,
George Izaguirre, Marilyn M. Marshall, Donna Naumovitz,
Pierre Payment, Eugene W. Rice, Joan Rose, Steve Schaub,
Theresa R. Slifko, Darrell B. Smith, Huw V. Smith, Charles
R. Sterling, and Mic Stewart.
© 1999 American Water Works Association, Journal AWWA September 1999
COMMITTEE REPORT
121