Bacterial Waterborne Pathogens — Current and Emerging Organisms of Concern

Bacterial Waterborne Pathogens — Current and Emerging Organisms of Concern
Health
Canada
Santé
Canada
Guidelines for Canadian Drinking Water Quality:
Guideline Technical Document
Bacterial Waterborne Pathogens —
Current and Emerging Organisms
of Concern
Prepared by the
Federal-Provincial-Territorial Committee on Drinking Water
of the
Federal-Provincial-Territorial Committee on Health and the Environment
Health Canada
Ottawa, Ontario
February 2006
This document is one of several that supersede the previous guideline technical document
(formerly known as a supporting document) on Bacteriological quality that was published in June
1988. It may be cited as follows:
Health Canada (2006) Guidelines for Canadian Drinking Water Quality: Guideline Technical
Document — Bacterial Waterborne Pathogens — Current and Emerging Organisms of Concern.
Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch, Health
Canada, Ottawa, Ontario.
The document was prepared by the Federal-Provincial-Territorial Committee on Drinking Water
of the Federal-Provincial-Territorial Committee on Health and the Environment.
Any questions or comments on this document may be directed to:
Water Quality and Health Bureau
Healthy Environments and Consumer Safety Branch
Health Canada
269 Laurier Ave West, Address Locator 4903D
Ottawa, Ontario
Canada K1A 0K9
Tel.: 613-948-2566
Fax: 613-952-2574
E-mail: [email protected]
Other Guideline Technical Documents for the Guidelines for Canadian Drinking Water Quality
can be found on the Water Quality and Health Bureau web page at
http://www.healthcanada.gc.ca/waterquality.
Table of Contents
1.0
Guideline
..........................................................1
2.0
Executive summary for microbiological quality of drinking water . . . . . . . . . . . . . . . . . . 1
2.1
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2.2
Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2.3
Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.4
Health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.5
Exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.6
Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3.0
Application of the guideline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
4.0
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
5.0
Current bacterial pathogens of concern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5.1
Escherichia coli O157:H7 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5.1.1 Description, sources, health effects, and exposure . . . . . . . . . . . . . . . . . . 5
5.1.2 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.1.3 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.2
Salmonella and Shigella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.2.1 Description, sources, health effects, and exposure . . . . . . . . . . . . . . . . . . 6
5.2.2 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.2.3 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.3
Campylobacter and Yersinia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5.3.1 Description, sources, health effects, and exposure . . . . . . . . . . . . . . . . . . 7
5.3.2 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5.3.3 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6.0
Emerging bacterial pathogens of concern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6.1
Legionella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6.1.1 Description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6.1.2 Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
6.1.3 Health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
6.1.4 Exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
6.1.5 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
6.1.6 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
6.2
Mycobacterium avium complex (Mac) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
6.2.1 Description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
6.2.2 Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
6.2.3 Health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
6.2.4 Exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
6.2.5 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
6.2.6 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
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6.3
6.4
Aeromonas hydrophila . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
6.3.1 Description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
6.3.2 Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
6.3.3 Health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
6.3.4 Exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
6.3.5 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
6.3.6 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
Helicobacter pylori . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
6.4.1 Description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
6.4.2 Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
6.4.3 Health effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
6.4.4 Exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
6.4.5 Treatment technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
6.4.6 Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
7.0
Conclusions and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
8.0
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Appendix A: List of acronyms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
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Bacterial Waterborne Pathogens — Current and Emerging
Organisms of Concern
1.0
Guideline
No maximum acceptable concentration (MAC) for current or emerging bacterial
waterborne pathogens has been established. Current bacterial waterborne pathogens include
those that have been previously linked to gastrointestinal illness in human populations.
Emerging bacterial waterborne pathogens include, but are not limited to, Legionella,
Mycobacterium avium complex, Aeromonas hydrophila, and Helicobacter pylori.
Note: Further information on the current and emerging bacterial waterborne pathogens is outlined
beginning in section 3.0, Application of the guideline.
2.0
Executive summary for microbiological quality of drinking water
2.1
Introduction
The information contained in this Executive summary applies to the microbiological
quality of drinking water as a whole. It contains background information on microorganisms,
their health effects, sources of exposure, and treatment. Information specific to bacteria is
included as a separate paragraph. It is recommended that this document be read in conjunction
with other documents on the microbiological quality of drinking water, including the guideline
technical document on turbidity.
2.2
Background
There are three main types of microorganisms that can be found in drinking water:
bacteria, viruses, and protozoa. These can exist naturally or can occur as a result of
contamination from human or animal waste. Some of these are capable of causing illness in
humans. Surface water sources, such as lakes, rivers, and reservoirs, are more likely to contain
microorganisms than groundwater sources, unless the groundwater sources are under the direct
influence of surface water.
The main goal of drinking water treatment is to remove or kill these organisms to reduce
the risk of illness. Although it is impossible to completely eliminate the risk of waterborne
disease, adopting a multi-barrier, source-to-tap approach to safe drinking water will reduce the
numbers of microorganisms in drinking water. This approach includes the protection of source
water (where possible), the use of appropriate and effective treatment methods, well-maintained
distribution systems, and routine verification of drinking water safety. All drinking water
supplies should be disinfected, unless specifically exempted by the responsible authority. In
addition, surface water sources and groundwater sources under the direct influence of surface
water should be filtered. Drinking water taken from pristine surface water sources may be
exempt from filtration requirements (Health Canada, 2003).
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The performance of the drinking water filtration system is usually assessed by monitoring
the levels of turbidity, a measure of the relative clarity of water. Turbidity is caused by matter
such as clay, silt, fine organic and inorganic matter, plankton, and other microscopic organisms,
which is suspended within the water. Suspended matter can protect pathogenic microorganisms
from chemical and ultraviolet (UV) light disinfection.
Currently available detection methods do not allow for the routine analysis of all
microorganisms that could be present in inadequately treated drinking water. Instead,
microbiological quality is determined by testing drinking water for Escherichia coli, a bacterium
that is always present in the intestines of humans and other animals and whose presence in
drinking water would indicate faecal contamination of the water. The maximum acceptable
concentration (MAC) of E. coli in drinking water is none detectable per 100 mL.
2.3
Bacteria
E. coli is a member of the total coliform group of bacteria and is the only member that is
found exclusively in the faeces of humans and other animals. Its presence in water indicates not
only recent faecal contamination of the water but also the possible presence of intestinal diseasecausing bacteria, viruses, and protozoa. The detection of E. coli should lead to the immediate
issue of a boil water advisory and to corrective actions being taken. Conversely, the absence of E.
coli in drinking water generally indicates that the water is free of intestinal disease-causing
bacteria. However, because E. coli is not as resistant to disinfection as intestinal viruses and
protozoa, its absence does not necessarily indicate that intestinal viruses and protozoa are also
absent. Although it is impossible to completely eliminate the risk of waterborne disease, adopting
a multi-barrier approach to safe drinking water will minimize the presence of disease-causing
microorganisms, reducing the levels in drinking water to none detectable or to levels that have
not been associated with disease.
While E. coli is the only member of the total coliform group that is found exclusively in
faeces, other members of the group are found naturally in water, soil, and vegetation, as well as
in faeces. Total coliform bacteria are easily destroyed during disinfection. Their presence in
water leaving a drinking water treatment plant indicates a serious treatment failure and should
lead to the immediate issue of a boil water advisory and to corrective actions being taken. The
presence of total coliform bacteria in water in the distribution system (but not in water leaving
the treatment plant) indicates that the distribution system may be vulnerable to contamination or
may simply be experiencing bacterial regrowth. The source of the problem should be determined
and corrective actions taken.
In semi-public and private drinking water systems, such as rural schools and homes, total
coliforms can provide clues to areas of system vulnerability, indicating source contamination as
well as bacterial regrowth and/or inadequate treatment (if used). If they are detected in drinking
water, the local authority responsible for drinking water may issue a boil water advisory and
recommend corrective actions. It is important to note that decisions concerning boil water
advisories should be made at the local level based upon site-specific knowledge and conditions.
The heterotrophic plate count (HPC) test is another method for monitoring the overall
bacteriological quality of drinking water. HPC results are not an indicator of water safety and,
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as such, should not be used as an indicator of adverse human health effects. Each system will
have a certain baseline HPC level and range, depending on site-specific characteristics; increases
in concentrations above baseline levels should be corrected.
There are naturally occurring waterborne bacteria, such as Legionella spp. and
Aeromonas hydrophila, with the potential to cause illnesses. The absence of E. coli does not
necessarily indicate the absence of these organisms, and for many of these pathogens, no suitable
microbiological indicators are currently known. However, the use of a multiple-barrier approach,
including adequate treatment and a well-maintained distribution system, can reduce these
bacterial pathogens to non-detectable levels or to levels that have never been associated with
human illness.
2.4
Health effects
The health effects of exposure to disease-causing bacteria, viruses, and protozoa in
drinking water are varied. The most common manifestation of waterborne illness is
gastrointestinal upset (nausea, vomiting, and diarrhoea), and this is usually of short duration.
However, in susceptible individuals such as infants, the elderly, and immunocompromised
individuals, the effects may be more severe, chronic (e.g., kidney damage), or even fatal. Bacteria
(such as Shigella and Campylobacter), viruses (such as norovirus and hepatitis A virus), and
protozoa (such as Giardia and Cryptosporidium) can be responsible for severe gastrointestinal
illness. Other pathogens may infect the lungs, skin, eyes, central nervous system, or liver.
If the safety of drinking water is in question to the extent that it may be a threat to public
health, authorities in charge of the affected water supply should have a protocol in place for
issuing, and cancelling, advice to the public about boiling their water. Surveillance for possible
waterborne diseases should also be carried out. If a disease outbreak is linked to a water supply,
the authorities should have a plan to quickly and effectively contain the illness.
2.5
Exposure
Drinking water contaminated with human or animal faecal wastes is just one route of
exposure to disease-causing microorganisms. Outbreaks caused by contaminated drinking water
have occurred, but they are relatively rare compared with outbreaks caused by contaminated
food. Other significant routes of exposure include contaminated recreational waters (e.g., bathing
beaches and swimming pools) and objects (e.g., doorknobs) or direct contact with infected
humans or domestic animals (pets or livestock). Although surface waters and groundwater under
the direct influence of surface water may contain quantities of microorganisms capable of
causing illness, effective drinking water treatment can produce water that is virtually free of
disease-causing microorganisms.
2.6
Treatment
The multi-barrier approach is an effective way to reduce the risk of illness from
pathogens in drinking water. If possible, water supply protection programs should be the first line
of defence. Microbiological water quality guidelines based on indicator organisms (e.g., E. coli)
and treatment technologies are also part of this approach. Treatment to remove or inactivate
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pathogens is the best way to reduce the number of microorganisms in drinking water and should
include effective filtration and disinfection and an adequate disinfection residual. Filtration
systems should be designed and operated to reduce turbidity levels as low as reasonably
achievable without major fluctuations.
It is important to note that all chemical disinfectants (e.g., chlorine, ozone) used in
drinking water can be expected to form disinfection by-products, which may affect human health.
Current scientific data show that the benefits of disinfecting drinking water (reduced rates of
infectious illness) are much greater than any health risks from disinfection by-products. While
every effort should be made to reduce concentrations of disinfection by-products to as low a level
as reasonably achievable, any method of control used must not compromise the effectiveness of
water disinfection.
3.0
Application of the guideline
Routine monitoring is not recommended for either current or emerging bacterial
waterborne pathogens. E. coli is used to indicate the presence of the current bacterial waterborne
pathogens, but it does not indicate the presence of the emerging bacterial waterborne pathogens.
The use of a multiple-barrier approach, including adequate treatment, a well-maintained
distribution system, and source protection (in the case of enteric bacteria), can reduce both
current and emerging bacterial pathogens to non-detectable levels or to levels that have not been
associated with human illness.
4.0
Introduction
Throughout history, consumption of drinking water supplies containing enteric
pathogenic bacteria has been linked to illnesses in human populations. These illnesses commonly
present as gastrointestinal-related symptoms, such as diarrhoea and nausea. Faecal indicators,
such as E. coli, are the best available surrogates for predicting the presence of such organisms. In
this document, these organisms have been identified as current bacterial pathogens of concern.
However, in recent decades, there has been an increasing amount of interest in naturally
occurring waterborne bacteria with the potential to cause gastrointestinal and non-gastrointestinal
illnesses, particularly respiratory illnesses. These organisms have been defined within this
document as emerging pathogens of concern. In most cases, although E. coli is able to indicate
the presence of enteric pathogenic bacteria, it does not correlate with the presence of these
emerging organisms. In addition, there are currently no suitable microbiological indicators for
many of these bacterial pathogens.
It is not necessary to establish MACs for current and emerging waterborne pathogens at
this time. The use of a multiple-barrier approach, including adequate treatment, a wellmaintained distribution system, and source protection, in the case of enteric bacteria, can reduce
these bacterial pathogens to non-detectable levels or to levels that have not been associated with
human illness.
The following bacteria, identified as either current or emerging concerns, are those
commonly recognized as the etiological agents in waterborne outbreaks or those being
recognized more often as causes of other serious illnesses that have the potential for waterborne
transmission. The information provided in this document focuses on emerging bacteria of
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concern, as there are more unknowns associated with these organisms, and their overall
significance, in many cases, still needs to be established. Additionally, the bacteria identified
should not be considered a complete list of bacterial pathogens that may be present and
potentially responsible for isolated cases of waterborne illness. However, they do encompass the
majority that have been responsible for waterborne outbreaks. Information on protozoan and viral
pathogens of concern can be found, respectively, in the protozoa and enteric viruses guideline
technical documents of the Guidelines for Canadian Drinking Water Quality (Health Canada,
2004a, 2004b).
5.0
Current bacterial pathogens of concern
5.1
Escherichia coli O157:H7
5.1.1
Description, sources, health effects, and exposure
Escherichia coli is a bacterium found exclusively in the digestive tract of warm-blooded
animals, including humans. As such, it is used in the drinking water industry as the definitive
indicator of recent faecal contamination of water. While most strains of E. coli are nonpathogenic, some can cause serious diarrhoeal infections in humans. The pathogenic E. coli are
divided into six groups based on serological and virulence characteristics: enterohaemorrhagic,
enterotoxigenic, enteroinvasive, enteropathogenic, enteroaggregative, and diffuse adherent
(APHA et al., 1998; Rice, 1999). One enterohaemorrhagic strain, E.coli O157:H7, has been
implicated in many foodborne and a few waterborne outbreaks. It was first recognized in 1982,
when it was associated with two foodborne outbreaks of bloody diarrhoea and abdominal cramps
(Gugnani, 1999). The primary reservoir of this bacterium has been found to be healthy cattle
(Jackson et al., 1998). In foodborne transmission, outbreaks are generally through the
consumption of undercooked minced beef and unpasteurized juices or milk that have been
contaminated with the bacteria (Gugnani, 1999). Although E. coli O157:H7 is not usually a
concern in treated drinking water, outbreaks involving consumption of drinking water
contaminated with human sewage or cattle faeces have been documented (Swerdlow et al., 1992;
Bruce-Grey-Owen Sound Health Unit, 2000).
E. coli serotype O157:H7 causes abdominal pain, bloody diarrhoea, and haemolytic
uraemic syndrome (HUS). This bacterium produces potent toxins (verotoxins) related to Shigella
toxins. The incubation period is 3–4 days, and the symptoms occur for 7–10 days (Moe, 1997;
Rice, 1999). It is estimated that 2–7% of E. coli O157:H7 infections result in HUS, in which the
destruction of erythrocytes leads to acute renal failure (Moe, 1997).
Studies have shown that the dose required to produce symptoms is lower than that for
most other enteric pathogenic bacteria. The probability of becoming ill depends on the number of
organisms ingested, the health status of the person, and the resistance of the person to the
organism or toxin (AWWA Committee Report, 1999). Children and the elderly are most
susceptible to HUS complications. Evidence suggests that the incidence of E. coli O157:H7
infections and HUS has increased since the serotype was first recognized.
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5.1.2
Treatment technology
Similar to the non-pathogenic strains of E. coli, E. coli O157:H7 is susceptible to
disinfection (Kaneko, 1998; Rice et al., 2000). Further information on treatment technology for
E.coli can be found in the Escherichia coli guideline technical document of the Guidelines for
Canadian Drinking Water Quality (Health Canada, 2006a). In addition, a multi-barrier approach
based upon source protection (where possible), effective treatment, and a well-maintained
distribution system will reduce the levels of E. coli O157:H7 in drinking water to none
detectable or to levels that have never been associated with human illness.
5.1.3
Assessment
Studies have shown that the survival rate of E. coli O157:H7 approximates that of typical
E. coli in the aquatic environment (AWWA Committee Report, 1999; Rice, 1999). Also,
although routine examination methods for generic E. coli will not detect E. coli O157:H7, the
former will always occur in greater concentration in faeces than the pathogenic strains, even
during outbreaks. E. coli O157:H7 will also never occur in the absence of generic E. coli. As a
result, the presence of E. coli can be used as an indicator of the presence of E. coli O157:H7.
5.2
Salmonella and Shigella
5.2.1
Description, sources, health effects, and exposure
Salmonella and Shigella are common etiological agents of gastrointestinal illnesses.
Consequently, they are present in the faeces of colonized individuals. These organisms are also
commonly present in the faeces of a variety of other animals. The presence of either of these
organisms in the environment is generally the result of recent faecal contamination. Numerous
outbreaks linked to contaminated drinking water have been reported (Boring et al., 1971; White
and Pedersen, 1976; Auger et al., 1981; CDC, 1996; Angulo et al., 1997; Alamanos et al., 2000;
R. Taylor et al., 2000; Chen et al., 2001). In most cases, the drinking water was not treated or
was improperly treated prior to consumption.
5.2.2
Treatment technology
Salmonella and Shigella survival characteristics in water and their susceptibility to
disinfection have been demonstrated to be similar to those of coliform bacteria (McFeters et al.,
1974; Mitchell and Starzyk, 1975). Further information on treatment technology for coliforms
can be found in the total coliforms guideline technical document of the Guidelines for Canadian
Drinking Water Quality (Health Canada, 2006b). In addition, a multi-barrier approach based
upon source protection, effective treatment, and a well-maintained distribution system will
reduce the levels of Salmonella and Shigella in drinking water to none detectable or to levels that
have never been associated with human illness.
5.2.3
Assessment
The absence of E. coli during routine verification should be an adequate indication of the
absence of Salmonella and Shigella. However, instances have been reported in which these
pathogens were isolated from drinking water in the absence of coliforms (Seligmann and Reitler,
1965; Boring et al., 1971). Coliform suppression by elevated HPCs and poor recovery of stressed
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coliforms seem to be the most plausible explanations for these discrepancies. Total coliform and
E. coli recoveries are not affected by elevated HPCs and environmental stress in the newer
defined-substrate methods.
5.3
Campylobacter and Yersinia
5.3.1
Description, sources, health effects, and exposure
Waterborne outbreaks of gastroenteritis involving Campylobacter jejuni and Yersinia
enterocolitica have been recorded on numerous occasions (Eden et al., 1977; McNeil et al.,
1981; Mentzing, 1981; Vogt et al., 1982; Taylor et al., 1983; Lafrance et al., 1986; Sacks et al.,
1986; Thompson and Gravel, 1986). The most notable Canadian waterborne outbreak involving
Campylobacter in recent history occurred in Walkerton, Ontario, in May 2000 (Clark et al.,
2003). This outbreak was linked to faecally contaminated well water that was not properly treated
before consumption. Other reports of Campylobacter and Yersinia isolation from surface and
well waters can be found in the literature (Caprioli et al., 1978; Schiemann, 1978; Blaser et al.,
1980; OME, 1980; Taylor et al., 1983; Weagant and Kaysner, 1983; El-Sherbeeny et al., 1985).
The survival characteristics of C. jejuni are similar to those of coliforms, but the frequency of
isolation of Y. enterocolitica is higher in winter months, indicating that it can survive for
extended periods and perhaps even multiply when water temperatures are low (Berger and
Argaman, 1983).
5.3.2
Treatment technology
The findings of Wang et al. (1982) indicated that conventional water treatment and
chlorination will probably destroy C. jejuni and Y. enterocolitica in drinking water. In addition, a
multi-barrier approach based upon source protection (where possible), effective treatment, and a
well-maintained distribution system will reduce the levels of Campylobacter and Yersinia in
drinking water to none detectable or to levels that have never been associated with human illness.
5.3.3
Assessment
The presence of Y. enterocolitica has been demonstrated to be poorly correlated with
levels of coliforms and HPC bacteria (Wetzler et al., 1979). In addition, studies have shown no
correlation between indicator organisms (e.g., E. coli, thermotolerant coliforms) and the presence
of Campylobacter in raw surface water supplies (Carter et al., 1987; Hörman et al., 2004). Thus,
coliforms may not be adequate indicators of the presence of both C. jejuni and Y. enterocolitica.
6.0
Emerging bacterial pathogens of concern
6.1
Legionella
6.1.1
Description
Legionellae were first recognized as human pathogens after a 1976 outbreak of
pneumonia among veterans attending a convention in Philadelphia. Since that time, at least 42
distinct Legionella species have been identified. Approximately half of these species have been
associated with disease in humans, with the majority of illnesses resulting from Legionella
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pneumophila infection. Other than L. pneumophila, human illnesses are generally the result of
infection with L. micdadei, L. bozemanii, L. longbeachae, and L. dumoffi, although many other
species have been implicated on occasion.
6.1.2
Sources
Unlike most other common waterborne pathogens, Legionella species are naturally
present in water environments, including surface water (Palmer et al., 1993) and groundwater
(Lieberman et al., 1994). Their ubiquitous nature reflects their ability to survive under varied
water conditions, including temperatures from 0 to 63°C and a pH range of 5.0–8.5 (Nguyen et
al., 1991). Their survival is, at least in part, attributed to their interactions with other members of
the heterotrophic flora. For example, their ability to develop symbiotic relationships with other
bacteria, such as Flavobacterium, Pseudomonas, Alcaligenes, and Acinetobacter, is thought to be
important for their survival and proliferation in water (Lin et al., 1998). In addition, some
protozoa that are naturally occurring in water, such as Hartmanella sp., Acanthamoeba
castellanii, and Echinamoeba, can harbour Legionella organisms, protecting them from
environmental stresses and providing a suitable environment for their amplification (Kilvington
and Price, 1990; Kramer and Ford, 1994; Fields, 1996). In general, the amount of legionellae in
source waters is low compared with the concentrations that can be reached in human-made
systems, as natural water conditions are not as conducive to growth.
In human-made systems, Legionella colonizes various locations within buildings (e.g.,
cooling towers, hot water tanks, shower heads, aerators) and contaminates potable water and air.
Generally, the areas of a human-made system contaminated with legionellae are those where
biofilm formation is most prevalent. This is because Legionella can thrive in biofilms.
Concentrations have been found to be as much as 10 times higher in biofilms from faucets than
from water collected from that faucet (Ta et al., 1995). There is some evidence that pipe material
can also affect colonization by legionellae. For example, studies have found that copper piping
may be inhibitory for Legionella growth (Tiefenbrunner et al., 1993; Rogers et al., 1994; van der
Kooij et al., 2002). Water temperature is an additional factor that influences colonization, with
temperatures between 20°C and 50°C being hospitable for colonization, although legionellae
generally only grow to high concentrations at temperatures below 42°C. Measurable inactivation
of legionellae begins at temperatures greater than 50°C (WHO, 2002). It is through human-made
systems that Legionella is most often disseminated, causing sporadic or outbreak cases of illness.
6.1.3
Health effects
There are two distinct illnesses caused by Legionella: Legionnaires’ disease and Pontiac
fever. Collectively, these illnesses are referred to as legionellosis.
Legionnaires’ disease is a severe pneumonia that can be accompanied by extrapulmonary
manifestations, such as renal failure, encephalopathy, and pericarditis (Oredugba et al., 1980;
Johnson et al., 1984; Nelson et al., 1985). Other common early features include confusion,
disorientation, lethargy, and possible gastrointestinal symptoms, such as nausea, vomiting, and
diarrhoea (U.S. EPA, 2001). The incubation period is generally 2–10 days. One problem in
diagnosing Legionnaires’ disease is a lack of any specific symptom that distinguishes it from
other bacterial pneumonias. Early diagnosis and consequently appropriate antibiotic therapy
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are important in successfully treating the disease. Overall, the mortality rate of Legionnaires’
disease is approximately 15% (Oredugba et al., 1980; Johnson et al., 1984; Nelson et al., 1985).
Pontiac fever, on the other hand, is a non-pneumonic, febrile illness with an incubation
period of 24–48 hours. Unlike Legionnaires’ disease, Pontiac fever has a high attack rate
(Mangione et al., 1985). However, this illness typically resolves without complications in 2–5
days (Glick et al., 1978; Fallon et al., 1993).
6.1.4
Exposure
Individuals considered to be at the highest risk of contracting Legionnaires’ disease are
those who are immunocompromised, especially transplant patients, and those with underlying
lung conditions. Outside of the high-risk category, other predisposing risk factors commonly
acknowledged include being male, smoking, alcoholism, being over 40 years of age, working
more than 40 hours a week, and spending nights away from home. It is therefore not surprising
that children and young people are rarely affected by the disease (WHO, 1990; Straus et al.,
1996). An additional determinant for human infection is the concentration of Legionella present,
as a minimum infectious dose is required to cause illness. It is not known precisely what this
dose is, as infection is dependent on other factors, including the virulence of the organism and, as
mentioned previously, the health status of the host. There is some evidence that replication
within amoebae may contribute to enhanced virulence of legionellae (Kramer and Ford, 1994). It
is speculated that infectivity may also be enhanced if amoebae containing Legionella cells are
inhaled or aspirated, as this provides a mechanism for introducing hundreds of Legionella cells
into the respiratory tract (Rowbotham, 1986; Berk et al., 1998).
Since Legionella is a respiratory pathogen, systems that generate aerosols, such as cooling
towers, whirlpool baths, and shower heads, are the more commonly implicated sources of
infection, with the hot water supply system generally being the origin of the contamination
(Spitalny et al., 1984; Mangione et al., 1985; Fallon and Rowbotham, 1990; Jernigan et al.,
1996; Hershey et al., 1997; Brown et al., 1999; Benin et al., 2002). However, the cold water
supply, when held within the range of Legionella multiplication (25°C), has also been implicated
(Hoebe et al., 1998). Legionella contamination is particularly troublesome in hospitals, where
susceptible human populations are present and can be exposed to aerosols containing hazardous
concentrations of Legionella spp., generally L. pneumophila (Dufour and Jakubowski, 1982).
Although more prominent in hospital settings (up to 50% of nosocomial pneumonias) (Breiman
and Butler, 1998), Legionella spp. have been estimated to cause 1–15% of community-acquired
pneumonias (Lieberman et al., 1996; Breiman and Butler, 1998). Within the community, large
buildings such as hotels, community centres, industrial buildings, and apartment buildings are
most often implicated as sources of infection (Yu, 2002). Single-family dwellings have rarely
been identified as the source of infection. However, studies have shown that contamination of
domestic hot water systems in single-family homes with Legionella does occur (Arnow et al.,
1985; Lee et al., 1988; Stout et al., 1992b; Borella et al., 2004). In a few instances, cases of
Legionnaires’ disease have been linked to these dwellings (Stout et al., 1992a).
The challenge to preventing Legionella-associated illnesses is controlling their growth in
these human-made environments. Once Legionella becomes established in a water system (i.e.,
in the biofilm), it is nearly impossible to eradicate it. However, it can be kept to a minimum by
implementing some control procedures. This is particularly important in health care settings.
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In addition to being a waterborne illness, outbreaks of Legionnaires’ disease have been
associated with potting soils. In these cases, the causative agents were found to be L.
longbeachae, L. bozemanii, and L. dumoffi, as opposed to L. pneumophila.
6.1.5
Treatment technology
As with other bacteria, physical removal mechanisms used during drinking water
treatment, such as coagulation, flocculation, sedimentation, and filtration, will reduce the number
of Legionella present in finished water. Disinfection can further lower the number present. In
comparison with indicator organisms commonly used in the drinking water industry, such as E.
coli or total coliforms, a higher CT value (i.e., a longer contact time, a higher disinfectant
concentration, or a combination of both) is necessary to achieve a comparable level of reduction
in Legionella using chlorine, chlorine dioxide, and ozone. The one exception appears to be with
the use of chloramine. Laboratory tests have shown that legionellae seem to be more susceptible
to chloramination than E. coli (Cunliffe, 1990). As further support for this finding, it was found
that hospitals with a free chlorine residual were 10 times more likely to have reported cases of
Legionnaires’ disease than hospitals with monochloramine residuals (Kool et al., 1999). Kool et
al. (1999) also reported that when a few selected municipalities were investigated, it was found
that legionellae could be isolated from systems with a free chlorine residual, but those systems
with monochloramination were negative for the bacterium. UV light is also effective for
inactivating Legionella, at doses commonly used in drinking water treatment (WHO, 2002). In
the distribution system, current recommended disinfectant residuals are sufficient to keep the
concentration of Legionella at levels that have not been associated with disease (WHO, 2002).
6.1.6
Assessment
Unlike the case with gastrointestinal pathogens, where E. coli can be used to indicate
their potential presence, no suitable indicators have been identified to signal increasing
concentrations of Legionella spp. in a building’s plumbing system. There is some evidence that
increasing Legionella concentrations are accompanied by, or preceded by, an increase in other
bacteria, resulting in an elevated HPC measurement (i.e., >100 CFU/mL) (WHO, 2002). Hence,
elevated HPCs may indicate the presence of Legionella. However, the correlation between HPC
and Legionella is not consistent. This may partially result from the accompanying chlorination of
the water, since HPC bacteria are more readily killed than legionellae (Zacheus and Martikainen,
1996).
The ubiquitous nature of legionellae in water ensures that water supplies, regardless of
their source, may contain Legionella spp. in low quantities. On a daily basis, the population at
large is exposed to these low levels with no reaction or with asymptomatic production of
antibodies. In Canada, Legionella pneumophila and other Legionella species have been recovered
in low concentrations from the drinking water (Dutka et al., 1984; Tobin et al., 1986). However,
no illnesses have ever been linked to these low concentrations. For these reasons, the presence of
the organism is not sufficient evidence to warrant remedial action in the absence of disease cases
(Dufour and Jakubowski, 1982; Tobin et al., 1986).
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6.2
Mycobacterium avium complex (Mac)
6.2.1
Description
The Mycobacterium avium complex (Mac) consists of 28 serovars of two distinct species:
Mycobacterium avium and Mycobacterium intracellulare. Based on phenotypic and genetic
characteristics, three subspecies of M. avium, including M. avium subsp. avium, M. avium subsp.
paratuberculosis, and M. avium subsp. silvaticum, have been identified (Nichols et al., 2004). .
Mac organisms, along with many other environmental mycobacteria species, comprise the nontuberculous mycobacterium (NTM) group. These organisms are designated as NTM to
distinguish them from Mycobacterium tuberculosis and Mycobacterium leprae, the infectious
agents of tuberculosis and leprosy. Unlike their NTM counterparts, neither of the latter organisms
is present in the environment, and, consequently, they are not a concern in drinking water.
6.2.2
Sources
Mac organisms have been identified in a broad range of environmental sources, including
marine waters, rivers, lakes, streams, ponds, springs, soil, piped water supplies, plants, and house
dust (Ichiyama et al., 1988; Covert et al., 1999; Falkinham et al., 2001). Falkinham et al. (2001)
did note, however, that both M. avium and M. intracellulare were seldom recovered from well
water. In addition to these sources, Wendt et al. (1980) reported the isolation of NTM (mostly M.
intracellulare) from aerosol samples taken near a river. It should be noted that although water is
the focus of this document, M. avium levels can be hundreds or thousands of times higher in soils
than in treated drinking water (LeChevallier, 1999).
The ubiquitous nature of Mac organisms results from their ability to survive and grow
under varied conditions. For example, Mac organisms can proliferate in water at temperatures up
to 51°C (Sniadack et al., 1992). In one instance, it was found that temperatures between 52°C
and 57°C encouraged proliferation of M. avium in hospital water supplies (du Moulin et al.,
1988). Mac organisms have also been shown to grow in natural waters over a wide pH range
(Kirschner et al., 1999). As with most organisms, some conditions will favour their growth. For
example, humic and fulvic acids stimulate the growth of M. avium (Kirschner et al., 1999). As
well, natural water with zinc concentrations greater than 0.75 mg/L (Kirschner et al., 1992) and
waters with a low pH and a high organic content (Iivanainen et al., 1993) are more likely to
contain Mac organisms. The survival of Mac organisms can also be enhanced by their ability to
invade and survive in some species of amoeba (Plum and Clark-Curtiss, 1994; Bermudez et al.,
1997; Cirillo et al., 1997), such as Acanthamoeba polyphaga or A. castellanii, as well as to grow
as free-living saprophytes on products secreted by these organisms (Steinert et al., 1998).
Similar to Legionella, Mac organisms survive and persist in biofilms. In one study of 50
biofilm samples from water treatment plants, domestic water supply systems, and aquaria, 90%
were positive for mycobacteria species, with concentrations up to 5.6 × 106 CFU/cm2 (SchulzeRöbbecke et al., 1992). Although this study did not identify the percentage of Mac organisms
within the mycobacteria species isolated, a separate study found that 131 of 267 biofilm
mycobacteria isolates were M. intracellulare (average 600 CFU/cm2), and 4 were M. avium (<0.5
CFU/cm2). This confirms that Mac organisms are present in biofilm matrices. An additional
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study into several types of commonly used plumbing materials concluded that the frequency of
recovery of Mac organisms from biofilm was not dependent on the material type (Falkinham et
al., 2001).
6.2.3
Health effects
The clinical presentation of Mac infections can include a productive cough, fatigue, fever,
weight loss, and night sweats. It is also a leading cause of mycobacterial lymphadenitis in
children less than 12 years of age. Current research suggests a possible role for Mac organisms in
the development of Crohn’s disease, an inflammatory bowel disease similar to Johne’s disease in
sheep, cattle, and goats. Johne’s disease is caused by M. avium subsp. paratuberculosis. Strains
of M. avium subsp. paratuberculosis have been isolated from some Crohn’s patients. Although
the evidence is still inconclusive, due mainly to difficulties in reliably detecting the pathogen,
improvements in detection methodologies are providing better evidence linking the pathogen to
Crohn’s disease (Reynolds, 2001; Hermon-Taylor and El-Zaatari, 2004). Diagnosis of Mac
infections is difficult and time-consuming. Therefore, treatment is usually initiated before
confirmation is made as to the cause of the infection. The treatment regimen for Mac infections
may include high doses of antimicrobials. These drugs can have a variety of side effects,
including nausea, vomiting, diarrhoea, rashes, abdominal pain, hearing loss, eye inflammation,
and damage to blood vessels or the liver (Reynolds, 2001).
The symptoms encountered with Mac infections result from colonization of either the
respiratory or the gastrointestinal tract, with possible dissemination to other locations in the body.
Unlike Mycobacterium tuberculosis (the infectious agent of tuberculosis), Mac organisms have
low pathogenicity, so individuals can become colonized with the organisms without any adverse
health effects. Individuals who are immunocompetent without underlying disease conditions
have a very low risk of becoming symptomatic with a Mac infection. Recently, reports have
shown an increasing recognition of Mac in individuals, especially women, with apparently no
predisposing disorders of the lungs or immune system. Although recognition of this disease in
immunocompetent individuals is increasing, the risks of becoming ill are still very low. Whereas
the majority of healthy individuals who contract Mac infections have localized infection,
disseminated Mac infections occur in a large proportion of AIDS patients (80% of those patient
that are colonized), as well as in other immunosuppressed populations, such as those with severe
combined immunodeficiency syndrome, transplant recipients, and patients treated with
corticosteroids or cytotoxic drugs (von Reyn et al., 1993a,b). The true prevalence of Mac
infections is not known, as it is not a reportable illness in Canada or the United States. It has been
suggested, based on studies in Houston and Atlanta, that the rate of illness is 1 in 100 000
persons per year (Reynolds, 2001).
6.2.4
Exposure
Exposure to Mac organisms may occur through the consumption of contaminated food,
the inhalation of air with contaminated soil particles, or contact with or ingestion, aspiration, or
aerosolization of potable water containing the organisms. Person-to-person contact is thought to
be possible but has not yet been observed (Reynolds, 2001; Le Dantec et al., 2002).
With respect to water supplies, infection with M. avium and M. intracellulare has been
well documented (Wendt et al., 1980; Grange, 1991; von Reyn et al., 1993a, 1994; Glover et al.,
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1994; Montecalvo et al., 1994; Kahana et al., 1997; Aronson et al., 1999; Mangione et al., 2001)
with M. avium being the leading cause of NTM infections. The route of exposure, in most cases,
is inhalation of contaminated aerosols, particularly through contaminated hot tubs. Some research
has shown that one M. avium strain in particular (Mav-B sequevar) is responsible for the majority
of cases. This may be the result of a higher virulence of this strain or an increased prevalence of
this strain in the environment (Hazra et al., 2000). The proportion of infections caused by M.
avium and M. intracellulare has been shown to vary between populations. In one study, AIDS
patients were more often infected with M. avium (98% of 45 patients) than with M. intracelluare
when compared with non-AIDS patients, in whom 60% of the infections were shown to be
caused by M. avium and the remaining 40% were the result of M. intracellulare (Guthertz et al.,
1989). The infectious dose appears to range from 104 to 107 organisms, but this number depends
on numerous factors, including, but not limited to, the virulence of the organism and the immune
status of the host.
6.2.5
Treatment technology
Water treatment technologies commonly used, including chemical disinfection and
physical removal methods, have been tested for their ability to inactivate or remove mycobacteria
from water supplies. Of these technologies, the most effective has been physical removal using
sand filtration and coagulation–sedimentation techniques . For example, it was shown, using a
surface water source, that mycobacterial numbers were reduced by almost 2 log, with the
majority of the 2 log removal attributed to removal by filtration (Falkinham et al., 2001). The
disinfection employed contributed only slightly to the overall log removal. In comparison with
conventional indicators, Mac organisms are more resistant to the commonly used disinfectants .
For example, the CT values necessary for inactivation using free chlorine (pH 7, 23°C) are 2–3
orders of magnitude higher for M. avium than for E. coli. Therefore, in a typical drinking water
system, the chlorine dose added will unlikely be effective in controlling the Mac organisms
(AWWA Committee Report, 1999). Similar results have been found with other commonly used
disinfectants in the drinking water industry (Yu-Sen et al., 1998; R.H. Taylor et al., 2000). Nonchemical treatment methods should be effective for Mac removal and/or inactivation. Even with
good removal of organisms from the source water, the number of Mac organisms may increase in
the distribution system (Falkinham et al., 2001). Conditions identified to encourage growth in the
distribution system include old pipes, long storage times, and high assimilable organic carbon
levels (Falkinham et al., 2001).
6.2.6
Assessment
Unlike gastrointestinal pathogens, where E. coli can be used to indicate their potential
presence, no suitable indicators have been identified to signal increasing concentrations of Mac
organisms in water systems. For example, studies have found no relationship between the
numbers of NTM recovered from reservoir water and coliform counts, HPCs, and total and free
chlorine levels (Glover et al., 1994; Aronson et al., 1999). There is some evidence that M. avium
presence is associated with turbidity in raw waters (Falkinham et al., 2001), but further
exploration of this issue is needed.
Currently, the presence of mycobacteria in water is not regulated by any countries or
international organizations, including Canada. The U.S. Environmental Protection Agency (EPA)
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has identified M. avium and M. intracellulare as waterborne health-related microbes that need
additional research on their health effects, their occurrence in water, and their susceptibility to
treatment methods (Reynolds, 2001). These organisms have also been included in a list of
candidate contaminants for possible regulation by the U.S. EPA (LeChevallier, 1999). At the
present time, there is not sufficient information to warrant actions based on the presence of the
organisms in the absence of disease.
6.3
Aeromonas hydrophila
6.3.1
Description
Aeromonas hydrophila are Gram-negative, non-spore-forming, rod-shaped, facultative
anaerobic bacilli belonging to the family Aeromonadaceae. Although A. hydrophila is the focus
of this section, other aeromonads, such as A. caviae and A. sobria, have also been isolated from
human faeces and from water sources (Havelaar et al., 1992; Janda and Abbott, 1998; Villari et
al., 2003). Morphologically, aeromonads are indistinguishable from members of the
Enterobacteriaceae family, such as E. coli. They also share many biochemical characteristics,
with the differentiation being that aeromonads are oxidase positive and Enterobacteriaceae are
oxidase negative.
6.3.2
Sources
Previous work has firmly established that Aeromonas species, including A. hydrophila,
are ubiquitous in the environment. These organisms have been found in lakes, rivers, marine
waters, sewage effluents, and drinking waters, among other places (Allen et al., 1983; Nakano et
al., 1990; Poffe and Op de Beeck, 1991; Payment et al., 1993; Ashbolt et al., 1995; Bernagozzi
et al., 1995; Chauret et al., 2001; El-Taweel and Shaban, 2001). The concentration of Aeromonas
species varies with the environment being investigated. In clean rivers, lakes, and storage
reservoirs, concentrations of Aeromonas spp. have been found to typically be around 102
CFU/mL. Groundwaters generally contain less, with fewer than 1 CFU/mL. Additionally,
drinking water immediately leaving the treatment plant has been found to contain between 0 and
102 CFU/mL, with potentially higher concentrations in drinking water distribution systems,
attributed to growth in biofilms (Payment et al., 1988; U.S. EPA, 2000; Chauret et al., 2001).
Depending on the study, A. hydrophila comprised 20–60% of the aeromonads isolated
(Millership et al., 1986; Notermans et al., 1986; Kühn et al., 1997). Aeromonas spp. have been
found to grow between 5°C and 45°C (U.S. EPA, 2000). Water temperature is a significant factor
for Aeromonas growth (Sautour et al., 2003). Coinciding with the optimal growth range of
Aeromonas, seasonal variation has been reported for public water systems, with Aeromonas more
often recovered during the warmer months (Gavriel et al., 1998). The same trend has been
observed with stool samples (Burke et al., 1984; Moyer, 1987).
6.3.3
Health effects
In recent years, A. hydrophila has gained public health recognition as an opportunistic
pathogen. It has been implicated as a potential agent of gastroenteritis, septicaemia, cellulitis,
colitis, and meningitis, and is frequently isolated from wound infections sustained in aquatic
environments (Krovacek et al., 1992; Gavriel et al., 1998). It has also recently been implicated
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in respiratory infections (Janda and Abbott, 1998). Treatment for infection with Aeromonas is
generally not necessary for gastrointestinal illness. However, for other presentations of infection,
antibiotic therapy is usually implemented. Individuals at the greatest risk of infection are
children, the elderly, and the immunocompromised (Merino et al., 1995).
6.3.4 Exposure
The common routes of infection suggested for Aeromonas are the ingestion of
contaminated water or food or contact of the organism with a break in the skin (Schubert, 1991).
No person-to-person transmission has been reported. It should be noted that although A.
hydrophila is water based, waterborne outbreaks have not been reported, and waterborne
transmission has not been well established. For example, various studies have been unsuccessful
in linking patient isolates of A. hydrophila with isolates recovered from the water supply
(Havelaar et al., 1992; Moyer et al., 1992; Hänninen and Siitonen, 1995; WHO, 2002; Borchardt
et al., 2003). As mentioned above, the growth of A. hydrophila is temperature dependent.
Therefore, the risk of infection is highest in the summer months, when these microorganisms are
multiplying more rapidly (Holmes and Nicolls, 1995).
The dose necessary to cause infections in humans has not been established. In the limited
number of studies done, the dose was quite high, and only a limited number of participants were
infected (Morgan et al., 1985; Janda and Abbott, 1998; WHO, 2002). The virulence of the strain
is one factor that can influence the infectious dose needed. For A. hydrophila, the virulence of the
organism is, at least in part, thought to result from the production of specific enterotoxins
(Schubert, 1991). The primary toxins are haemolysins(Janda, 1991). In addition, some
aeromonads produce a range of cell surface and secreted proteases that may enhance their
virulence (Janda, 1991; Gosling, 1996). It has been demonstrated that a significant proportion of
the A. hydrophila isolated from water (chlorinated and unchlorinated supplies) contained genes
responsible for enterotoxigenic or cytotoxic activity (Ormen and Ostensvik, 2001). Expression of
virulence factors has been shown to be influenced by environmental temperature. A. hydrophila
isolated from the environment produced significantly less enterotoxins when grown at 37°C
compared with 28°C, whereas the clinical isolates tested produced more enterotoxins at 37°C
than at 28°C (Mateos et al., 1993). The temperature of the human body is approximately 37°C;
therefore, strains that produce virulence factors at this temperature are likely to be more
important as pathogens.
6.3.5
Treatment technology
As mentioned previously, aeromonads are ubiquitous in many water environments.
Consequently, they will be present in most source waters used for drinking water production. The
methods currently used for treatment and disinfection are effective in minimizing the level of
aeromonads in the finished drinking water. For example, it has been shown that A. hydrophila is
generally more susceptible to chlorine and monochloramine than coliforms (Knøchel, 1991; Sisti
et al., 1998). Chlorine dioxide has also been shown to be an effective disinfectant (Medema et
al., 1991). In the distribution system, there is the potential for Aeromonas to regrow. Maintaining
chlorine at or above 0.2 mg/L should provide adequate control of A. hydrophila in the water
(Holmes and Nicolls, 1995). However, it is difficult to control its growth in biofilms (Gavriel et
al., 1998; Chauret et al., 2001; WHO, 2002). The most effective approach for controlling
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Aeromonas growth is to limit the Aeromonas spp. entering the distribution system through
effective treatment and maintenance, to maintain temperatures below 14°C, to provide free
chlorine residuals above 0.1–0.2 mg/L, and to limit the levels of organic carbon compounds
(WHO, 2002). If there are significant increases in Aeromonas concentrations in a drinking water
supply, this indicates a general deterioration of bacteriological quality.
6.3.6
Assessment
Some studies have been undertaken to determine if the indicators currently used in the
drinking water industry, including E. coli, total coliforms, and HPC, can be used as surrogates for
the presence of Aeromonas. Several studies, including a large study in England, showed no
relationship between Aeromonas incidence and coliforms, E. coli, or HPCs (Holmes et al., 1996;
Gavriel et al., 1998; Fernandez et al., 2000). Although all the studies had similar findings, not all
could draw definite conclusions, because of limited sample sizes, minimal occurrences of
coliforms, and/or the absence of E. coli in the water.
When looking at the overall public health significance of A. hydrophila in drinking water,
further epidemiological studies are needed to ascertain the relationship between Aeromonas
illness and the presence of these organisms in drinking water (WHO, 2002). The European
Community has established a drinking water standard for A. hydrophila of no more than 20
CFU/100 mL in water leaving the treatment plant and 200 CFU/100 mL in distribution system
water (van der Kooj, 1993; Moyer, 1999). These values are based on an assessment of
achievability, motivated by a precautionary approach, and not on the public health significance of
their occurrence in drinking-water (WHO, 2002). Based on what is currently known, treated
drinking water probably represents a very low risk. However, it is advisable to minimize the
concentration of A. hydrophila, as well as other aeromonads, in drinking water supplies until
their public health significance has been fully investigated.
6.4
Helicobacter pylori
6.4.1
Description
Helicobacter pylori, formerly known as Campylobacter pylori, was first recognized as a
human pathogen in 1983 (Postius, 2001) and was subsequently identified as a human carcinogen
by the International Agency for Research on Cancer (IARC, 1994).
Two morphologically distinct forms of H. pylori, a spiral shape and a coccoid form, have
been identified (van Duynhoven and de Jonge, 2001). The spiral shape is cultured routinely from
clinical samples. To date, the coccoid form has been found to be non-culturable. Transformation
from the spiral-shaped bacterium grown in culture to the non-culturable coccoid form is thought
to result from variations in the environment, such as oxygen stress, temperature changes, the
presence of antibiotics, and other stress-inducing conditions (Engstrand, 2001). At present, it is
still unclear whether the coccoid form is viable but non-culturable (VBNC), similar to VBNC
states found with Salmonella, Campylobacter, and Vibrio spp. (Byrd et al., 1991), and therefore
able to infect humans, or if it is simply non-viable (van Duynhoven and de Jonge, 2001).
Attempts to revert the coccoid form to the spiral form using nutrient supplementation (Sörberg et
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al., 1996) have been unsuccessful. Reversion has been successful in only one report, using mice
(Wang et al., 1995). Attempts to use the same procedure in pigs resulted in contradictory results
(Eaton et al., 1995).
6.4.2
Sources
H. pylori has not yet been isolated from environmental sources, including water.
However, other methods have been able to detect H. pylori. For example, it has been found
microscopically, using a fluorescent antibody, in surface waters and shallow groundwaters
(Hegarty et al., 1999). Molecular methods, such as polymerase chain reaction, have also been
used to detect the presence of H. pylori DNA in water (Enroth and Engstrand, 1995). Under
laboratory conditions, H. pylori has been shown to survive for days, up to weeks, in sterile river
water, saline solution, and distilled water at a wide variety of pH levels and in temperatures
ranging from 4°C to 15°C (West et al., 1992; Shahamat et al., 1993). These results indicate that
water may be a potential source of transmission for H. pylori. Currently, the only substantial
reservoir of H. pylori has been found to be the human stomach (Dunn et al., 1997). Domestic
cats have been found to harbour the organisms, but studies conducted have been unsuccessful at
linking pet ownership with H. pylori seropositivity (Webb et al., 1996b; Bode et al., 1998). The
bacterium has also been isolated from primates, but, due to rare contact, primates are unlikely to
be important reservoirs.
6.4.3
Health effects
Human infection with H. pylori has been linked to gastritis, duodenal ulcers, and an
increased risk of gastric adenocarcinoma (Jekel, 1993; Hunter, 1997; Engstrand, 2001). These
health effects reflect the ability of H. pylori to colonize the human stomach and establish a
chronic infection associated with an inflammatory response. In addition to gastrointestinal
disorders, some studies have shown an association between H. pylori infection and anaemia (i.e.,
decreased serum ferritin levels) (Milman et al., 1998; Peach et al., 1998; CDC, 1999), although
there are also studies to the contrary (Haruma et al., 1995; Perez-Perez, 1997). The prevalence of
H. pylori infection in the world is assumed to be 50%, with higher prevalence in developing
countries (90%). Both immunocompromised and immunocompetent individuals can become
infected with H. pylori, and both groups can develop associated illnesses (Battan et al., 1990;
Edwards et al., 1991; Vaira et al., 1995). In children, H. pylori can cause antral gastritis and
duodenal ulcer disease, although most infections in children are asymptomatic (Rowland and
Drumm, 1998). It has been well established that infections with H. pylori are generally acquired
during childhood, with a lower frequency of infection in adults (Feldman et al., 1998; Allaker et
al., 2002). The infectious dose necessary for colonization of humans is not known. It is assumed
to be low because of the high percentage of infected individuals; in human testing, however, it
was shown that the minimum required dose was 3 × 105 CFU when given in combination with an
acid suppressant (Morris and Nicholson, 1987). Incidences of accidental infection, such as
ingestion resulting from laboratory work (Matysiak-Budnik et al., 1995) and use of improperly
maintained endoscopes, suggest that the dose could be much lower. Of those individuals who
become infected, only a subpopulation (6–20%) will develop gastroduodenal disease (Go, 1997;
Parsonnet, 1998; Patchett, 1998; Engstrand, 2001), with approximately 1% of all infections
progressing ultimately to gastric cancer. Gastric cancer is the second most common cause of
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Bacterial Waterborne Pathogens (February 2006)
cancer, and 40–50% of these cases are related to H. pylori (Parsonnet, 1998; Parkin et al., 1999).
Infection with H. pylori is treatable using a combination of bismuth and antibiotics or a
combination of a proton-pump inhibitor and antibiotics (Scott et al., 1998). This translates into a
significant number of cases of disease due to H. pylori that are preventable.
6.4.4
Exposure
How the organism is transmitted is still not fully understood; however, the fact that it has
been recovered from saliva, dental plaques, the stomach, and faecal samples strongly indicates
oral–oral or faecal–oral transmission (Ferguson et al., 1993; Jekel, 1993; Nguyen et al., 1993;
Goodman et al., 1996; Dunn et al., 1997; Feldman et al., 1998). Associations between the
seroprevalence of hepatitis A, which is known to be transmitted by the faecal–oral route, and H.
pylori shows the potential for faecal–oral transmission (Hazell et al., 1994; Rudi et al., 1997). As
well, consumption of uncooked vegetables irrigated with untreated sewage has been suggested as
a risk factor for H. pylori (Hopkins et al., 1993). On the other hand, there have been studies using
hepatitis A showing no association with H. pylori infection and consequently no link to
faecal–oral transmission (Webb et al., 1996a; Furuta et al., 1997). Additional studies examining
H. pylori seropositivity in sewage workers (Friis et al., 1996) and in travellers recently returned
from areas of the world with a high prevalence of H. pylori (Lindkvist et al., 1995) also found no
connection to faecal–oral transmission. It has been suggested that the link to faecal samples is
better when looking at transmission routes for children than for adults (Thomas et al., 1992;
Mapstone et al., 1993). Studies in some developing countries found that transmission of H.
pylori was due to environmental conditions, such as poor hygiene or the consumption of
contaminated water (Klein et al., 1991; Hopkins et al., 1993) . Evidence that waterborne
transmission may be important in areas of the world with less than adequate water quality comes
from studies conducted worldwide, including in Inuit communities in Canada (Klein et al., 1991;
Goodman et al., 1996; Hulten et al., 1996; McKeown et al., 1999). Epidemiological studies
conducted in developed countries have found no association between environment and infection
(Hultén et al., 1998). In the latter studies, clustering of infections within families was prevalent,
supporting the oral–oral route (Brenner et al., 1999; Allaker et al., 2002), with infected mothers
playing a key role in transmission (Rothenbacher et al., 1999). In contrast, it was found that
oral–oral transmission between spouses was unlikely to be an important mode of transmission
(Luman et al., 2002).
Overall, the predominant transmission route for H. pylori seems to be situation
dependent, with person-to-person transmission playing a key role in many circumstances. Water
and food appear to be of lesser direct importance, but they can still play a significant role in
situations with improper sanitation and lax hygiene. Further investigation into the role of water is
needed.
6.4.5
Treatment technology
Some work has been carried out on the relative sensitivities of H. pylori and E. coli to
currently used drinking water treatment methods. Further information on the role of E. coli in
drinking water can be found in The Guideline for Canadian Drinking Water Quality: Guideline
Technical Document — E. coli (Health Canada, 2006a). Similar to other bacteria, a proportion of
the H. pylori present in the source water will be removed using physical methods, such as
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Bacterial Waterborne Pathogens (February 2006)
coagulation, sedimentation, and filtration. This organism is also susceptible to disinfectants
commonly used in drinking water treatment. In laboratory disinfectant testing, E.coli proved to
be more sensitive to chlorine and ozone than H. pylori (Johnson et al., 1997; Baker et al., 2002);
however, there was little difference between the effectiveness when monochloramine was used
(Baker et al., 2002). Although E. coli is easier to inactivate than H. pylori with some
disinfectants, the CT provided by a typical water treatment plant is sufficient to inactivate H.
pylori in the finished water (Peeters et al., 1989; Johnson et al., 1997). However, if H. pylori
does enter the distribution system, potentially through a break in treatment or infiltration into the
system, the disinfectant residuals found in the distribution system are probably not sufficient for
inactivation (Baker et al., 2002).
6.4.6
Assessment
Currently, there are no regulations governing the presence of H. pylori in drinking water,
either nationally or internationally. The U.S. EPA has included it on their list of candidate
contaminants for possible regulation in drinking water. Further studies are needed to confirm
that H. pylori are present in drinking water in a viable state and that they can be transmitted by
this medium.
7.0
Conclusions and recommendations
The organisms identified as current bacterial waterborne pathogens of concern within this
document are those that have a well-established history of being responsible for bacterial
waterborne outbreaks, presenting as gastrointestinal illnesses. Drinking water is not tested for
these organisms directly; instead, E. coli is used as an indicator of their presence. The guideline
value of no E. coli in 100 mL of drinking water is set to protect human health from these
organisms.
The emerging pathogenic bacteria of concern outlined here also have the potential to be
spread through drinking water, but they do not correlate with the presence of E. coli or with other
commonly used drinking water quality indicators, such as total coliforms and HPC bacteria. In
most cases, there are no satisfactory microbiological indicators of their presence. Although
surrogate organisms are not known, it is not practical to routinely monitor the drinking water for
the pathogens themselves. The use of a multiple-barrier approach, including source water
protection (where possible), adequate treatment, and a well-maintained distribution system, can
reduce these pathogens to non-detectable levels or to levels that have never been associated with
human illness.
8.0
References
Alamanos, Y., Maipa, V., Levidiotou, S., and Gessouli, E. (2000) A community waterborne outbreak of
gastro-enteritis attributed to Shigella sonnei. Epidemiol. Infect., 125: 499–503.
Allaker, R.P., Young, K.A., Hardie, J.M., Domizio, P., and Meadows, N.J. (2002) Prevalence of Helicobacter pylori
at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission. J. Med. Microbiol., 51:
312–317.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
19
Bacterial Waterborne Pathogens (February 2006)
Allen, D.A., Austin, B., and Colwell, R.R. (1983) Aeromonas media, a new species isolated from river water. Int. J.
Syst. Bacteriol., 33: 599–604.
Angulo, F.J., Tippen, S., Sharp, D.J., Payne, B.J., Collier, C., Hill, J.E., Barrett, T.J., Clark, R.M., Geldreich, E.E.,
Donnell, H.D., Jr., and Swerdlow, D.L. (1997) A community waterborne outbreak of salmonellosis and the
effectiveness of a boil water order. Am. J. Public Health, 87: 580–584.
APHA (American Public Health Association) / AWWA (American Water Works Association / WEF (Water
Environment Federation) (1998) Standard methods for the examination of water and wastewater. 20th edition.
Washington, DC.
Arnow, P.M., Weil, D., and Para, M.F. (1985) Prevalence and significance of Legionella pneumophila
contamination of residential hot-tap water systems. J. Infect. Dis., 152(1): 145–151.
Aronson, T., Holtzman, A., Glover, N., Boian, M., Froman, S., Berlin, O.G.W., Hill, H., and Stelma, G., Jr. (1999)
Comparison of large restriction fragments of Mycobacterium avium isolates recovered from AIDS and non-AIDS
patients with those of isolates from potable water. J. Clin. Microbiol., 37(4): 1008–1012.
Ashbolt, N.J., Ball, A., Dorsch, M., Turner, C., Cox, P., Chapman, A., and Kirov, S.M. (1995) The identification of
human health significance of environmental aeromonads. Water Sci. Technol., 31: 263–269.
Auger, P., Pouliot, B., De Grace, M., Milot, C., Lafortune, M., and Bergeron, Z. (1981) Epidemic of bacillary
dysentery. Can. Med. Assoc. J., 125: 733–736.
AWWA Committee Report (1999) Emerging pathogens — bacteria. J. Am. Water Works Assoc., 91(9): 101–109.
Baker, K.H., Hegarty, J.P., Redmond, B., Reed, N.A., and Herson, D.S. (2002) Effect of oxidizing disinfectants
(chlorine, monochloramine, and ozone) on Helicobacter pylori. Appl. Environ. Microbiol., 68: 981–984.
Batton, R., Raviglione, M.C., Palagiano, A., Boyle, J.F., Sabatini, M.T., Sayad, K., and Ottaviano, L.J. (1990)
Helicobacter pylori infection in patients with acquired immune deficiency syndrome. Am. J. Gastroenterol., 85:
1576–1579.
Benin, A.L., Benson, R.F., Arnold, K.E., Fiore, A.E., Cook, P.G., Williams, L.K., Fields, B., and Besser, R.E.
(2002) An outbreak of travel-associated Legionnaires’ disease and Pontiac fever: the need for enhanced surveillance
of travel-associated legionellosis in the United States. J. Infect. Dis., 185: 237–243.
Berger, P.S. and Argaman, Y. (eds.). (1983) Assessment of microbiology and turbidity standards for drinking water.
U.S. Environmental Protection Agency, Washington, DC (EPA 570-9-83-001).
Berk, S.G., Ting, R.S., Turner, G.W., and Ashburn, R.J. (1998) Production of respirable vesicles containing live
Legionella pneumophila cells by two Acanthamoeba spp. Appl. Environ. Microbiol., 64: 279–286.
Bermudez, L.E., Parker, A., and Goodman, J.R. (1997) Growth within macrophages increases the efficiency of
Mycobacterium avium in invading other macrophages by a complement receptor-independent pathway. Infect.
Immun., 65: 1916–1925.
Bernagozzi, M., Bianucci, F., and Sacchetti, R. (1995) Prevalence of Aeromonas spp. in surface waters.
Water Environ. Res., 67(7): 1060–1064.
Blaser, M.J., Wells, J.H., Powers, B., and Wang, W.L. (1980) Survival of Campylobacter fetus subsp. jejuni
in biological milieus. J. Clin. Microbiol., 11: 309–313.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
20
Bacterial Waterborne Pathogens (February 2006)
Bode, G., Rothenbacher, D., Brenner, H., and Adler, G. (1998) Pets are not a risk factor for Helicobacter pylori
infection in young children: results of a population-based study in southern Germany. Pediatr. Infect. Dis. J., 17:
909–912.
Borchardt, M.A., Stemper, M.E., and Standridge, J.H. (2003) Aeromonas isolates from human diarrheic stool and
groundwater compared by pulse-field gel electrophoresis. Emerg. Infect. Dis., 9: 224–228.
Borella, P., Montagna, M.T., Romano-Spica, V., Stampi, S., Stancanelli, G., Triassi, M., Neglia, R., Marchesi, I.,
Fantuzzi, G., Tatò, D., Napoli, C., Quaranta, G., Laurenti, P., Leoni, E., De Luca, G., Ossi, C., Moro, M., and Ribera
D’Alcalà, G. (2004) Legionella infection risk from domestic hot water. Emerg. Infect. Dis., 10(3): 457–464.
Boring, J.R., III, Martin, W.T., and Elliott, L.M. (1971) Isolation of Salmonella typhimurium from municipal water,
Riverside, California, 1965. Am. J. Epidemiol., 93: 49–54.
Breiman, R.F. and Butler, J.C. (1998) Legionnaires’ disease: clinical, epidemiological, and public health
perspectives. Semin. Respir. Infect., 13: 84–89.
Brenner, H., Rothenbacher, D., Bode, G., Dieudonné, P., and Adler, G. (1999) Active infection with Helicobacter
pylori in healthy couples. Epidemiol. Infect., 122: 91–95.
Brown, C.M., Nuorti, P.J., Breiman, R.F., Hathcock, A.L., Fields, B.A., Lipman, H.B., Llewellyn, G.C., Hofmann,
J., and Cetron, M. (1999) A community outbreak of Legionnaires’ disease linked to hospital cooling towers: an
epidemiological method to calculate dose of exposure. Int. J. Epidemiol., 28: 353–359.
Bruce-Grey-Owen Sound Health Unit (2000) The investigative report on the Walkerton outbreak of waterborne
gastroenteritis. May–June, Owen Sound (http://www.publichealthgreybruce.on.ca/_private/Report/SPReport.htm).
Burke, V., Robinson, J., Gracey, M., Peterson, D., and Partridge, K. (1984) Isolation of Aeromonas hydrophila from
a metropolitan water supply: seasonal correlation with clinical isolation. Appl. Environ. Microbiol., 48(2): 361–366.
Byrd, J.J., Xu, H.S., and Colwell, R.R. (1991) Viable but nonculturable bacteria in drinking water. Appl. Environ.
Microbiol., 57: 875–878.
Caprioli, T., Drapeau, A.J., and Kasatiya, S. (1978) Yersinia enterocolitica: serotypes and biotypes isolated from
humans and the environment in Quebec, Canada. Appl. Environ. Microbiol., 8: 7–11.
Carter, A.M., Pacha, R.E., Clark, G.W., and Williams, E.A. (1987) Seasonal occurrence of Campylobacter spp.
in surface waters and their correlation with standard indicator bacteria. Appl. Environ. Microbiol., 53: 523–526.
CDC (Centers for Disease Control and Prevention) (1996) Shigella sonnei outbreak associated with contaminated
drinking water — Island Park, Idaho, August 1995. J. Am. Med. Assoc., 275: 1071.
CDC (Centers for Disease Control and Prevention) (1999) Iron deficiency anemia in Alaska native children —
Hooper Bay, Alaska, 1999. Morb. Mortal. Wkly. Rep., 48: 714–716.
Chauret, C., Volk, C., Creason, R., Jarosh, J., Robinson, J., and Warnes, C. (2001) Detection of Aeromonas
hydrophila in a drinking-water distribution system: a field and pilot study. Can. J. Microbiol., 47: 782–786.
Chen, K.T., Chen, C.J., and Chiu, J.P. (2001) A school waterborne outbreak involving both Shigella sonnei and
Entamoeba histolytica. J. Environ. Health, 64: 9–13.
Cirillo, J.D., Falkow, S., Tompkins, L.S., and Bermudez, L.E. (1997) Interaction of Mycobacterium avium with
environmental amoebae enhances virulence. Infect. Immun., 65(9): 3759–3767.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
21
Bacterial Waterborne Pathogens (February 2006)
Clark, C.G., Price, L., Ahmed, R., Woodward, D.L., Melito, P.L., Rodgers, F.G., Jamieson, F., Ciebin, B., Li, A.,
and Ellis, A. (2003) Characterization of waterborne outbreak-associated Campylobacter jejuni, Walkerton, Ontario.
Emerg. Infect. Dis., 9: 1232–1241.
Covert, T.C., Rodgers, M.R., Reyes, A.L., and Stelma, G.N., Jr. (1999) Occurrence of nontuberculous mycobacteria
in environmental samples. Appl. Environ. Microbiol., 65(6): 2492–2496.
Cunliffe, D.A. (1990) Inactivation of Legionella pneumophila by monochloramine. J. Appl. Bacteriol., 68: 453–459.
Dufour, A.P. and Jakubowski, W. (1982) Drinking water and Legionnaires’ disease. J. Am. Water Works Assoc., 74:
631–637.
du Moulin, G.C., Stottmeier, K.D., Pelletier, P.A., Tsang, A.Y., and Hedley-White, J. (1988) Concentration of
Mycobacterium avium by hospital hot water systems. J. Am. Med. Assoc., 260: 1599–1601.
Dunn, B.E., Cohen, H., and Blaser, M.J. (1997) Helicobacter pylori. Clin. Microbiol. Rev., 10: 720–741.
Dutka, B.J., Walsh, K., Ewan, P., El-Shaarawi, A., and Tobin, R.S. (1984) Incidence of Legionella organisms
in selected Ontario (Canada) cities. Sci. Total Environ., 39: 237–249.
Eaton, K.A., Catrenich, C.E., Makin, K.M., and Krakowka, S. (1995) Virulence of coccoid and bacillary forms
of Helicobacter pylori in gnotobiotic piglets. J. Infect. Dis., 171: 459–462.
Eden, K.V., Rosenburg, M.L., Stoopler, M., Wood, B.T., Highsmith, A.K., Skaliy, P., Wells, J.G., and Feeley, J.C.
(1977) Waterborne gastrointestinal illness at a ski resort. Public Health Rep., 92: 245–250.
Edwards, P.D., Carrick, J., Turner, J., Lee, A., Mitchell, H., and Cooper, D.A. (1991) Helicobacter pylori-associated
gastritis is rare in AIDS: antibiotic effect or a consequence of immunodeficiency? Am. J. Gastroenterol,. 86:
1761–1764.
El-Sherbeeny, M.R., Bopp, C., Wells, J.G., and Morris, G.K. (1985) Comparison of gauze swabs and membrane
filters for isolation of Campylobacter spp. from surface water. Appl. Environ. Microbiol., 50: 611–614.
El-Taweel, G.E. and Shaban, A.M. (2001) Microbiological quality of drinking water at eight water treatment plants.
Int. J. Environ. Health Res., 11: 285–290.
Engstrand, L. (2001) Helicobacter in water and waterborne routes of transmission. J. Appl. Microbiol., 90: 80S–84S.
Enroth, H. and Engstrand, L. (1995) Immunomagnetic separation and PCR for detection of Helicobacter pylori
in water and stool specimens. J. Clin. Microbiol., 33: 2162–2165.
Falkinham, J.O., III, Norton, C.D., and LeChevallier, M.W. (2001) Factors influencing numbers of Mycobacterium
avium, Mycobacterium intracellulare, and other mycobacteria in drinking water distribution systems. Appl. Environ.
Microbiol., 67(3): 1225–1231.
Fallon, R.J. and Rowbotham, T.J. (1990) Microbiological investigations into an outbreak of Pontiac fever due to
Legionella micdadei associated with use of a whirlpool. J. Clin. Pathol., 43: 479–483.
Fallon, R.J., Goldberg, D.J., Wrench, J.G., Green, S.T., and Emslie, J.A.M. (1993) Pontiac fever in children. In:
Legionella: Current status and emerging perspectives. J.M. Barbaree, R.F. Breiman, and A.P. Dufour (eds.).
American Society for Microbiology, Washington, DC. pp. 50–51.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
22
Bacterial Waterborne Pathogens (February 2006)
Feldman, R.A., Eccersley, A.J.P., and Hardie, J.M. (1998) Epidemiology of Helicobacter pylori: acquisition,
transmission, population prevalence and disease-to-infection ratio. Br. Med. Bull., 54: 39–53.
Ferguson, D.A., Jr., Li, C., Patel, N.R., Mayberry, W.R., Chi, D.S., and Thomas, E. (1993) Isolation of Helicobacter
pylori from saliva. J. Clin. Microbiol., 31: 2802–2804.
Fernandez, M.C., Giampaolo, B.N., Ibanez, S.B., Guagliardo, M.V., Esnaola, M.M., Conca, L., Valdivia, P.,
Stagnaro, S.M., Chiale, C., and Frade, H. (2000) Aeromonas hydrophila and its relation with drinking water
indicators of microbiological quality in Argentine. Genetica, 108: 35–40.
Fields, B.S. (1996) The molecular ecology of Legionellae. Trends Microbiol., 4: 286–290.
Friis, L., Engstrand, L., and Edling, C. (1996) Prevalence of Helicobacter pylori infection among sewage workers.
Scand. J. Work Environ. Health, 22: 364–368.
Furuta, T., Kamata, T., Takashima, M., Futami, H., Arai, H., Hanai, H., and Kaneko, E. (1997) Study of
transmission routes of Helicobacter pylori in relation to seroprevalence of hepatitis A virus. J. Clin. Microbiol., 35:
1891–1893.
Gavriel, A.A., Landre, J.P.B., and Lamb, A.J. (1998) Incidence of mesophilic Aeromonas within a public drinking
water supply in north-east Scotland. J. Appl. Microbiol., 84: 383–392.
Glick, T.H., Gregg, M.B., Berman, B., Mallison, G., Rhodes, W.W., Jr., and Kassanoff, I. (1978) Pontiac fever: an
epidemic of unknown etiology in a health department. I: Clinical and epidemiologic aspects. Am. J. Epidemiol., 107:
149–160.
Glover, N., Holtzman, A., Aronson, T., Froman, S., Berlin, O.G.W., Dominguez, P., Kunkel, K.A., Overturf, G.,
Steima, G., Jr., Smith, C., and Yakrus, M. (1994) The isolation and identification of Mycobacterium avium complex
(MAC) recovered from Los Angeles potable water, a possible source of infection in AIDS patients. Int. J. Environ.
Health Res., 4: 63–72.
Go, M.F. (1997) What are the host factors that place an individual at risk for Helicobacter pylori-associated disease?
Gastroenterology, 113(6): S15–20.
Goodman, K.J., Correa, P., Tengana, A.J., Ramírez, H., DeLany, J.P., Pepinosa, O.G., Quiñones, M.L., and Parra,
T.C. (1996) Helicobacter pylori infection in the Colombian Andes: a population-based study of transmission
pathways. Am. J. Epidemiol., 144: 290–299.
Gosling, P.J. (1996) Pathogenic mechanisms. In: The genus Aeromonas. B. Austin, M. Altwegg, P. Gosling, and
S. Joseph (eds.). John Wiley and Sons, London.
Grange, J.M.. (1991) Environmental mycobacteria and human disease. Lepr. Rev., 62: 353–361.
Gugnani, H.C. (1999) Some emerging food and water borne pathogens. J. Commun. Dis., 31(2): 65–72.
Guthertz, L.S., Damsker, B., Bottone, E.J., Ford, E.G., Midura, T.D., and Janda, J.M. (1989) Mycobacterium avium
and Mycobacterium intracellulare infections in patients with and without AIDS. J. Infect. Dis., 160: 1037–1041.
Hänninen, M.L. and Siitonen, A. (1995) Distribution of Aeromonas phenospecies and genospecies among strains
isolated from water, foods or from human clinical samples. Epidemiol. Infect., 115: 39–50.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
23
Bacterial Waterborne Pathogens (February 2006)
Haruma, K., Komoto, K., Kawaguchi, H., Okamoto, S., Yoshihara, M., Summii, K., and Kajiyama, G. (1995)
Pernicious anemia and Helicobacter pylori infection in Japan: evaluation in a country with a high prevalence of
infection. Am. J. Gastroenterol., 90: 1107–1110.
Havelaar, A.J., Schets, F.M., van Silfhout, A., Jansen, W.H., Wieten, G., and van der Kooij, D. (1992) Typing of
Aeromonas strains from patients with diarrhoea and from drinking water. J. Appl. Bacteriol., 72: 435–444.
Hazell, S.L., Mitchell, H.M., Hedges, M., Shi, X., Hu, P.J., Li, Y.Y., Lee, A., and Reiss-Levy, E. (1994) Hepatitis A
and evidence against the community dissemination of Helicobacter pylori in feces. J. Infect. Dis., 170: 686–689.
Hazra, R., Lee, S.H., Maslow, J.N., and Husson, R.N. (2000) Related strains of Mycobacterium avium cause disease
in children with AIDS and in children with lymphadenitis. J. Infect. Dis., 181: 1298–1303.
Health Canada (2003) Guidelines for Canadian drinking water quality: Supporting documentation — Turbidity:
Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch, Health Canada,
Ottawa, Ontario.
Health Canada (2004a) Guidelines for Canadian drinking water quality: Supporting documentation — Protozoa:
Giardia and Cryptosporidium. Water Quality and Health Bureau, Healthy Environments and Consumer Safety
Branch, Health Canada, Ottawa, Ontario.
Health Canada (2004b) Guidelines for Canadian drinking water quality: Supporting documentation — Enteric
viruses. Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch, Health Canada,
Ottawa, Ontario.
Health Canada (2006a) Guidelines for Canadian drinking water quality: Technical Guideline Document—
Escherichia coli. Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch,
Health Canada, Ottawa, Ontario.
Health Canada (2006b) Guidelines for Canadian drinking water quality: Technical Guideline Document — Total
coliforms. Water Quality and Health Bureau, Healthy Environments and Consumer Safety Branch, Health Canada,
Ottawa, Ontario.
Hegarty, J.P., Dowd, M., and Baker, K.H. (1999) Occurrence of Helicobacter pylori in surface water in the
United States. J. Appl. Microbiol., 87: 697–701.
Hermon-Taylor, J. and El-Zaatari, F.A.K. (2004) The Mycobacterium avium subspecies paratuberculosis problem
and its relation to the causation of Crohn disease. In: Pathogenic mycobacteria in water, a guide to public health
consequences, monitoring and management. S. Pedley, J. Bartram, G. Rees, A. Dufour, and J.A. Cotruvo (eds.).
Published by IWA Publishing, London, on behalf of the World Health Organization, Geneva. pp. 74–94.
Hershey, J., Burrus, B., Marcussen, V., Notter, J., Watson, K., Wolford, R., Shaffner, R.E., III, Barrett, E., Woolard,
D., Branch, L., Hackler, R., Rouse, B., Gibson, L., Jenkins, S., Rullan, J., Miller, G., Jr., and Curran, S. (1997)
Legionnaires disease associated with a whirlpool spa display — Virginia, September–October, 1996. Morb. Mortal.
Wkly. Rep., 46: 83–86.
Hoebe, C.J.P., Cluitmans, J.J.M., and Wagenvoort, J.H.T. (1998) Two fatal cases of nosocomial Legionella
pneumophila pneumonia associated with a contaminated cold water supply. Eur. J. Clin. Micriobiol. Infect. Dis., 17:
740–749.
Holmes, P., and Nicolls, L.M. (1995) Aeromonads in drinking water supplies — their occurrence and significance.
J. Chartered Inst. Water Environ. Manage., 5: 464–469.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
24
Bacterial Waterborne Pathogens (February 2006)
Holmes, P., Nicolls, L.M., and Sartory, D.P. (1996) The ecology of mesophilic Aeromonas in the aquatic
environment. In: The genus Aeromonas. B. Austin, M. Altwegg, P. Gosling, and S.W. Joseph (eds.). John Wiley &
Sons, New York, NY. p. 127.
Hopkins, R.J., Vial, P.A., Ferreccio, C., Ovalle, J., Prado, P., Soromayor, V., Russell, R.G., Wassermann, S.S., and
Morris, J.G., Jr. (1993) Seroprevalence of Helicobacter pylori in Chile: vegetables may serve as one route of
transmission. J. Infect. Dis., 168: 222–226.
Hörman, A., Rimhanen-Finne, R., Maunula, L., von Bonsdorff, C., Torvela, N., Heikinheimo, A., and Hänninen,
M. (2004) Campylobacter spp., Giardia spp., Cryptosporidium spp., Noroviruses, and indicator organisms in surface
water in southwestern Finland, 2000–2001. Appl. Environ. Microbiol., 70(1): 87–95.
Hultén, K., Han, S.W., Enroth, H., Klein, P.D., Opekun, A.R., Gilman, R.H., Evans, D.G., Engstrand, L., Graham,
D.Y., and El-Zaatari, F. (1996) Helicobacter pylori in the drinking water in Peru. Gastroenterology, 110:
1031–1035.
Hultén, K., Enroth, H., Nyström, T., and Engstrand, L. (1998) Presence of Helicobacter species DNA in Swedish
water. J. Appl. Microbiol., 85: 282–286.
Hunter, P.J. (1997) Mycobacterial disease. In: Waterborne disease epidemiology and ecology. John Wiley and Sons,
Chichester, England. pp. 189–198.
IARC (International Agency for Research on Cancer) (1994) Schistosomes, liver flukes and Helicobacter pylori.
IARC Monogr. Eval. Carcinog. Risks Hum., 61: 1–241.
Ichiyama, S., Shimokata, K., and Tsukamura, M. (1988) The isolation of Mycobacterium avium complex from soil,
water, and dusts. Microbiol. Immunol., 32(7): 733–739.
Iivanainen, E.K., Martikainen, P.J., Vaananen, P.K., and Katila, M.L. (1993) Environmental factors affecting the
occurrence of mycobacteria in brook waters. Appl. Environ. Microbiol., 59: 398–404.
Jackson, S.G., Goodbrand, R.B., Johnson, R.P., Odorico, V.G., Alves, D., Rahn, K., Wilson, J.B., Welch, M.K., and
Khakhria, R. (1998) Escherichia coli O157:H7 diarrhoea associated with well water and infected cattle on an
Ontario farm. Epidemiol. Infect., 120: 17–20.
Janda, J.M. (1991) Recent advances in the study of taxonomy, pathogenicity, and infectious syndromes associated
with the genus Aeromonas. Clin. Microbiol. Rev., 4(4): 397–410.
Janda, J.M. and Abbott, S.L. (1998) Evolving concepts regarding the genus Aeromonas: an expanding panorama
of species, disease presentations, and unanswered questions. Clin. Infect. Dis., 27: 332–344.
Jekel, P. (1993) Mode of transmission of Helicobacter pylori. J. Can. Inst. Public Health Inspect., 37(1): 22, 27.
Jernigan, D.B., Hofmann, J., Cetron, M.S., Genese, C.A., Nuorti, J.P., Fields, B.S., Benson, R.F., Carter, R.J.,
Edelstein, P.H., Guerrero, I.C., Paul, S.M., Lipman, H.B., and Breiman, R.F. (1996) Outbreak of Legionnaires’
disease among cruise ship passengers exposed to a contaminated whirlpool spa. Lancet, 347: 494–499.
Johnson, C., Rice, E., and Reasoner, D. (1997) Inactivation of Helicobacter pylori by chlorination. Appl. Environ.
Microbiol., 63: 4969–4970.
Johnson, J.D., Raff, M.J., and Van-Arsdall, J.A. (1984) Neurological manifestations of Legionnaires’ disease.
Medicine, 63: 303–310.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
25
Bacterial Waterborne Pathogens (February 2006)
Kahana, L.M., Kay, J.M., Yakrus, M.A., and Waserman, S. (1997) Mycobacterium avium complex infection in an
immunocompetent young adult related to hot tub exposure. Chest, 111: 242–245.
Kaneko, M. (1998) Chlorination of pathogenic E. coli O157. Water Sci. Technol., 38(12): 141–144.
Kilvington, S. and Price, J. (1990) Survival of Legionella pneumophila within cysts of Acanthamoeba polyphaga
following chlorine exposure. J. Appl. Bacteriol., 68: 519–525.
Kirschner, R.A., Parker, B.C., and Falkinham, J.O., III (1992) Epidemiology of infection by nontuberculous
mycobacteria: Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum in acid,
brown-water swamps of the southeastern United States and their association with environmental variables. Am. Rev.
Respir. Dis., 145: 271–275.
Kirschner, R.A., Jr., Parker, B.C., and Falkinham, J.O., III (1999) Humic and fulvic acids stimulate the growth of
Mycobacterium avium. FEMS Microbiol. Ecol., 30: 327–332.
Klein, P.D., Graham, D.Y., Gaillour, A., Opckun, A.R., and Smith, E.O. (1991) Water source as risk factor for
Helicobacter pylori infection in Peruvian children. Lancet, 337: 1503–1506.
Knøchel, S. (1991) Chlorine resistance of motile Aeromonas spp. Water Sci. Technol., 24: 327–330.
Kool, J.L., Carpenter, J.C., and Fields, B.S. (1999) Effect of monochloramine disinfection of municipal drinking
water on risk of nosocomial Legionnaires’ disease. Lancet, 353: 272–276.
Kramer, M.H.J. and Ford, T.E. (1994) Legionellosis: Ecological factors of an environmentally “new” disease.
Zentralbl. Hyg., 195: 470–482.
Krovacek, K., Faris, A., Baloda, S.J., Lindberg, T., Peterz, M., and Mansson, I. (1992) Isolation and virulence
profiles of Aeromonas spp. from different municipal drinking water supplies in Sweden. J. Food Microbiol., 9(3):
215–222.
Kühn, I., Allestam, G., Huys, G., Janssen, P., Kersters, K., Krovacek, K., and Stenstrom, T. (1997) Diversity,
persistence, and virulence of Aeromonas strains isolated from drinking water distribution systems in Sweden. Appl.
Environ. Microbiol., 63: 2708–2715.
Lafrance, G., Lafrance, R., Roy, G.L., Ouellete, D., and Bourdeau, R. (1986) Outbreak of enteric infection following
a field trip — Ontario. Can. Dis. Wkly. Rep., 12: 171–172.
LeChevallier, M.W. (1999) Mycobacterium avium complex. In: Manual of water supply practices, waterborne
pathogens. American Water Works Association, Denver, CO. pp. 99–102.
Le Dantec, C., Duguet, J., Montiel, A., Dumoutier, N., Dubrou, S., and Vincent, V. (2002) Chlorine disinfection of
atypical mycobacteria isolated from a water distribution system. Appl. Environ. Microbiol., 68(3): 1025–1032.
Lee, T.C., Stout, J.E., and Yu, V.L. (1988) Factors predisposing to Legionella pneumophila colonization in
residential water systems. Arch. Environ. Health, 43(1): 59–62.
Lieberman, R.J., Shadix, L.C., Newport, B.S., Crout, S.R., Buescher, S.E., Safferman, R.S., Stetler, R.E., Lye, D.,
Shay Fout, D., and Dahling, D.R. (1994) Source water microbial quality of some vulnerable public ground water
supplies. In: Proceedings of the 1994 Water Quality Technology Conference, Part II. pp. 1425–1436. American
Water Works Association, Denver, CO.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
26
Bacterial Waterborne Pathogens (February 2006)
Lieberman, D., Porath, A., Schlaeffer, F., Lieberman, D., and Boldur, I. (1996) Legionella species communityacquired pneumonia. A review of 56 hospitalized adult patients. Chest, 109: 1243–1249.
Lin, Y.E., Stout, J.E., Yu, Y.L., and Vidic, R.D. (1998) Disinfection of water distribution systems for Legionella.
Semin. Respir. Infect., 13: 147–159.
Lindkvist, P., Wadström, T., and Giesecke, J. (1995) Helicobacter pylori and foreign travel. J. Infect. Dis., 172:
1135–1136.
Luman, W., Zhao, Y., Ng, H.S., and Ling, K.L. (2002) Helicobacter pylori infection is unlikely to be transmitted
between partners: evidence from genotypic study in partners of infected patients. Eur. J. Gastroenterol. Hepatol., 14:
521–528.
Mangione, E.J., Remis, R.S., Tait, K.A., McGee, H.B., Gorman, G.W., Wentworth, B.B., Baron, P.A., Hightower,
A.W., Barbaree, J.M., and Broome, C.V. (1985) An outbreak of Pontiac fever related to whirlpool use, Michigan
1982. J. Am. Med. Assoc., 253: 535–539.
Mangione, E.J., Huitt, G., Lenaway, D., Beebe, D., Bailey, A., Figoski, M., Rau, M.P., Albrecht, K.D., and Yakrus,
M.A. (2001) Nontuberculous mycobacterial disease following hot tub exposure. Emerg. Infect. Dis., 7(6):
1039–1042.
Mapstone, N.P., Lynch, D.A., Lewis, F.A., Axon, A.T., Tompkins, D.S., Dixon, M.F., and Quirke, P. (1993) PCR
identification of Helicobacter pylori in faeces from gastritis patients [Letter]. Lancet, 341: 447.
Mateos, D., Anguita, J., Naharro, G., and Paniagua, C. (1993) Influence of growth temperature on the production of
extracellular virulence factors and pathogenicity of environmental and human strains of Aeromonas hydrophila. J.
Appl. Bacteriol., 74: 111–118.
Matysiak-Budnik, T., Briet, F., Heyman, M., and Megraud, F. (1995) Laboratory-acquired Helicobacter pylori
infection [letter]. Lancet, 346: 1489–1490.
McFeters, G.A., Bissonnette, G.K., Jezeski, J.J., Thomson, C.A., and Stuart, D.G. (1974) Comparative survival of
indicator bacteria and enteric pathogens in well water. Appl. Microbiol., 27: 823–829.
McKeown, I., Orr, P., MacDonald, S., Kabani, A., Brown, R., Coghlan, G., Dawood, M., Embil, J., Sargent, M.,
Smart, G., and Bernstein, C.N. (1999) Helicobacter pylori in the Canadian Arctic: seroprevalence and detection in
community water samples. Am. J. Gastroenterol., 94: 1823–1829.
McNeil, C.A., Out, K., Pagan, R.T., McMyre, P., Black, W.A., and Mathias, R.G. (1981) Possible waterborne
Campylobacter outbreak — British Columbia. Can. Dis. Wkly. Rep., 7: 223–227.
Medema, G.J., Wondergem, E., van Dijk-Looyaard, A.M., and Havelaar, A.H. (1991) Effectivity of chlorine dioxide
to control Aeromonas in drinking water distribution systems. Water Sci. Technol., 24: 325–326.
Mentzing, L.O. (1981) Waterborne outbreaks of Campylobacter enteritis in central Sweden. Lancet, ii: 352–354.
Merino, S., Rubires, X., Knochel, S., and Tomas, J.M. (1995) Emerging pathogens: Aeromonas spp. Int. J. Food
Microbiol., 28: 157–168.
Millership, S.E., Barer, M.R., and Tabaqchali, S. (1986) Toxin production by Aeromonas spp. from different
sources. J. Med. Microbiol., 22: 311–314.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
27
Bacterial Waterborne Pathogens (February 2006)
Milman, N., Rosenstock, S., Anderson, L., Jorgensen T., and Bonnevie, O. (1998) Serum ferritin, hemoglobin, and
Helicobacter pylori infection: a seroepidemiologic survey comprising 2794 Danish adults. Gastroenterology, 115:
268–274.
Mitchell, D.O. and Starzyk, M.J. (1975) Survival of Salmonella and other indicator microorganisms. Can. J.
Microbiol., 21: 1420–1421.
Moe, C.L. (1997) Waterborne transmission of infectious agents. In: Manual of environmental microbiology. C.J.
Hurst, G.R. Knudsen, M.J. McInerney, L.D. Stetzenbach, and M.V. Walter (eds.). ASM Press, Washington, DC.
Montecalvo, M.A., Forester, G., Tsang, A.Y., du Moulin, G., and Wormser, G.P. (1994) Colonisation of potable
water with Mycobacterium avium complex in homes of HIV-infected patients [letter]. Lancet, 343: 1639.
Morgan, D.R., Johnson, P.C., DuPont, H.L., Satterwhite, T.K., and Wood, L.V. (1985) Lack of correlation between
known virulence properties of Aeromonas hydrophila and enteropathogenicity for humans. Infect. Immun., 50:
62–65.
Morris, A., and Nicholson, G. (1987) Ingestion of Campylobacter pyloris causes gastritis and raised fasting gastric
pH. Am. J. Gastroenterol., 82: 192–199.
Moyer, N.P. (1987) Clinical significance of Aeromonas species isolated from patients with diarrhea. J. Clin.
Microbiol,, 25: 2044–2048.
Moyer, N.P. (1999) Aeromonas. In: AWWA manual M48: Waterborne pathogens. American Water Works
Association, Denver, CO. pp. 63–66.
Moyer, N.P., Luccini, G.M., Holcomb, L.A., Hall, N.H., and Altwegg, M. (1992) Application of ribotyping for
differentiating aeromonads isolated from clinical environmental sources. Appl. Environ. Microbiol., 58: 1940–1944.
Nakano, J., Kameyama, T., Venkateswaran, K., Kawakami, J., and Hashimoto, J. (1990) Distribution and
characterisation of hemolytic, and enteropathogenic motile Aeromonas in aquatic environment. Microbial Immunol.,
34: 447–458.
Nelson, D.P., Rensimer, E.R., and Raffin, T.A. (1985) Legionella pneumophila pericarditis without pneumonia.
Arch. Intern. Med., 145: 926.
Nguyen, M.H., Stout, J.E., and Yu, V.L. (1991) Legionellosis. Infect. Dis. Clin. North Am., 5: 561–584.
Nguyen, A.M.H., Engstrand, L., Genta, R.M., Graham, D.Y., and El-Zaatari, F.A.K. (1993) Detection of
Helicobacter pylori in dental plaque by reverse transcription–polymerase chain reaction. J. Clin. Microbiol., 31:
783–787.
Nichols, G., Ford, T., Bartram, J., Dufour, A., and Portaels, F. (2004) Introduction. In: Pathogenic mycobacteria
in water, a guide to public health consequences, monitoring and management. S. Pedley, J. Bartram, G. Rees, A.
Dufour, and J.A. Cotruvo. Published by IWA Publishing, London, on behalf of the World Health Organization,
Geneva. pp 1–14.
Notermans, S., Havelaar, A., Jansen, W., Kozaki, S., and Guinee, P. (1986) Production of “Asao toxin” by
Aeromonas strains isolated from feces and drinking water. J. Clin. Microbiol., 23: 1140–1142.
OME (Ontario Ministry of the Environment) (1980) Yersinia enterocolitica in recreational lakes and sewage
systems. Lakeshore Capacity Study, Laboratory Services Branch, Ontario Ministry of the Environment,
Toronto, Ontario.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
28
Bacterial Waterborne Pathogens (February 2006)
Oredugba, O., Mazumdar, D.C., Smoller, M.B., Meyer, J., and Lubowitz, H. (1980) Acute renal failure in
Legionnaires’ disease. Clin. Nephrol., 13: 142–145.
Ormen, O. and Ostensvik, O. (2001) The occurrence of aerolysin-positive Aeromonas spp. and their cytotoxicity
in Norwegian water sources. J. Appl. Microbiol., 90: 797–802.
Palmer, C.J., Tsai, Y-L., Paszko-Kolva, C., Mayer, C., and Sangermano, L.R. (1993) Detection of Legionella species
in sewage and ocean water by polymerase chain reaction, direct fluorescent-antibody, and plate culture methods.
Appl. Environ. Microbiol., 59: 3618–3624.
Parkin, D.M., Pisani, P., and Ferlay, J. (1999) Global cancer statistics. CA Cancer J. Clin., 49(1): 33–64.
Parsonnet, J. (1998) Helicobacter pylori. Infect. Dis. Clin. North Am., 12: 185–197.
Patchett, S.E. (1998) Helicobacter pylori eradication cost–benefit: the case against. Br. Med. Bull., 54: 251–257.
Payment, P., Gamache, F., and Paquette, G. (1988) Microbiological and virological analysis of water from two
water filtration plants and their distribution systems. Can. J. Microbiol., 34: 1304–1309.
Payment, P., Franco, E., and Siemiatycki, J. (1993) Absence of relationship between health effects due to tap water
consumption and drinking water quality parameters. Water Sci. Technol., 27: 137–143.
Peach, H.G., Bath, N.E., and Farish, S.J. (1998) Helicobacter pylori infection: an added stressor on iron status of
women in the community. Med. J. Aust., 169: 188–190.
Peeters, J.E., Mazas, E.A., Masschelein, W.J., Martinez de Maturana, I.V., and Debacker, E. (1989) Effect of
disinfection of drinking water with ozone or chlorine dioxide on survival of Cryptosporidium parvum oocysts. Appl.
Environ. Microbiol., 55: 1519–1522.
Perez-Perez, G.I. (1997) Role of Helicobacter pylori infection in the development of pernicious anemia. Clin. Infect.
Dis., 25: 1020–1022.
Plum, G. and Clark-Curtiss, J.E. (1994) Induction of Mycobacterium avium gene expression following phagocytosis
by human macrophages. Infect. Immun., 62: 476–483.
Poffe, R. and Op de Beeck, E. (1991) Enumeration of Aeromonas hydrophila from domestic wastewater treatment
plants and surface waters. J. Appl. Bacteriol., 71: 366–370.
Postius, S. (2001) Helicobacter pylori. Contrib. Microbiol., 8: 35–50.
Reynolds, K.A. (2001) Return of the MAC: Risks of waterborne Mycobacterium avium. Water Conditioning and
Purification Magazine, WC&P International, June. pp. 90–93.
Rice, E.W. (1999) Escherichia coli. In: AWWA manual M48: Waterborne pathogens. American Water Works
Association, Denver, CO. pp. 75–78.
Rice, E.W., Clark, R.M., and Johnson, C.H. (2000) Chlorine inactivation of Escherichia coli O157:H7. Emerg.
Infect. Dis., 5(3): 461–463.
Rogers, J., Dowsett, A.B., Dennis, P.J., Lee, J.V., and Keevil, C.W. (1994) Influence of temperature and plumbing
material selection on biofilm formation and growth of Legionella pneumophila in a model potable water system
containing complex microbial flora. Appl. Environ. Microbiol., 60(5): 1585–1592.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
29
Bacterial Waterborne Pathogens (February 2006)
Rothenbacher, D., Bode, G., Berg, G., Knayer, U., Gonser, T., Adler, G., and Brenner, H. (1999) Helicobacter
pylori among preschool children and their parents: evidence of parent–child transmission. J. Infect. Dis., 179:
398–402.
Rowbotham, T.J. (1986) Current views on the relationships between amoebae, legionellae and man. Isr. J. Med. Sci.,
22: 678–689.
Rowland, M. and Drumm, B. (1998) Climical significance of Helicobacter infection in children. Br. Med. Bull., 54:
95–103.
Rudi, J., Toppe, H., Marx, N., Zuna, I., Theilmann, L., Stremmel, W., and Raedsch, R. (1997) Risk of infection with
Helicobacter pylori and hepatitis A virus in different groups of hospital workers. Am. J. Gastroenterol., 92:
293–295.
Sacks, J.J., Spencer, L., Baldy, L., Berta, S., Patton, C.M., White, M.C., Bigler, W.J., and Witte, J.J. (1986)
Epidemic campylobacteriosis associated with a community water supply. Am. J. Public Health, 76: 424–428.
Sautour, M., Mary, P., Chihib, N.E., and Hornez, J.P. (2003) The effects of temperature, water activity and pH on
the growth of Aeromonas hydrophila and on its subsequent survival in microcosm water. J. Appl. Microbiol., 95:
807–813.
Schiemann, D.A. (1978) Isolation of Yersinia enterocolitica from surface and well waters in Ontario. Can. J.
Microbiol., 24: 1048–1052.
Schubert, R.H.W. (1991) Aeromonads and their significance as potential pathogens in water. J. Appl. Bacteriol.
Symp. Suppl., 70: 131S–135S.
Schulze-Röbbecke, R., Janning, B., and Fischeder, R. (1992) Occurrence of mycobacteria in biofilm samples. Tuber.
Lung Dis., 73: 141–144.
Scott, D., Weeks, D., Melchers, K., and Sachs, G. (1998) The life and death of Helicobacter pylori. Gut, 43(Suppl.
1): S56–S60.
Seligmann, R. and Reitler, R. (1965) Enteropathogens in water with low Esch. coli titer. J. Am. Water Works Assoc.,
57: 1572–1574.
Shahamat, M., Mai, U., Paszko-Kolva, C., Kessel, M., and Colwell, R.R. (1993) Use of autoradiography to assess
viability of Helicobacter pylori in water. Appl. Environ. Microbiol., 59: 1231–1235.
Sisti, M., Albano, A., and Brandi, G. (1998) Bactericidal effect of chlorine on motile Aeromonas spp. in drinking
water supplies and influence of temperature on disinfection efficacy. Lett. Appl. Micriobiol., 26: 347–351.
Sniadack, D.E., Ostroff, S.D., Karlix, M.A., Smithwick, R.W., Schwartz, B., Spaucer, M.A., Silcox, V.A., and Good,
R.C. (1992) A nosocomial pseudo-outbreak of Mycobacterium xenopi due to a contaminated potable water supply:
lessons in prevention. Infect. Control Hosp. Epidemiol., 14: 636–641.
Sörberg, M., Nilsson, M., Iianberger, H., and Nilsson, L.E. (1996) Morphologic conversion of Helicobacter pylori
from bacillary to coccoid form. Eur. J. Clin. Microbiol. Infect. Dis., 15: 216–219.
Spitalny, K.C., Vogt, R.L., Orciari, L.A., Witherell, L.E., Etkind, P., and Novick, L.F. (1984) Pontiac fever
associated with a whirlpool spa. Am. J. Epidemiol., 120: 809–817.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
30
Bacterial Waterborne Pathogens (February 2006)
Steinert, M., Birkness, K., White, E., Fields, B., and Quinn, F. (1998) Mycobacterium avium bacilli grow
saprozoically in coculture with Acanthamoeba polyphaga and survive within cyst walls. Appl. Environ. Microbiol.,
64(6): 2256–2261.
Stout, J.E., Yu, V.L., Muraca, P., Joly, J., Troup, N., and Tompkins, L. (1992a) Potable water as a cause of sporadic
cases of community-acquired Legionnaires’ disease. N. Engl. J. Med., 326: 151–155.
Stout, J.E., Yu, V.L., Yee, Y.C., Vaccarello, S., Diven, W., and Lee, T.C. (1992b) Legionella pneumophila in
residential water supplies: environmental surveillance with clinical assessment for Legionnaires’ disease. Epidemiol.
Infect., 109: 49–57.
Straus, W.L., Plouffe, J.F., File, T.M., Lipman, H.B., Hackman, B.H., Salstrom, S., Benson, R.F., and Breiman, R.F.
(1996) Risk factors for domestic acquisition of Legionnaires disease. Arch. Intern. Med., 156: 1685–1692.
Swerdlow, D.L., Woodruff, B.A., Brady, R.C., Griffin, P.M., Tippen, S., Donnell, H.D., Jr., Geldreich, E., Payne,
B.J., Meyer, A., Jr., Wells, J.G., Greene, K.D., Bright, M., Bean, N.H., and Blake, P.A. (1992) A waterborne
outbreak in Missouri of Escherichia coli O157:H7 associated with bloody diarrhea and death. Ann. Intern. Med.,
17(10): 812–819.
Ta, A.C., Stout, J.E., Yu, V.L., and Wagener, M.M. (1995) Comparison of culture methods for monitoring
Legionella species in hospital potable water systems and recommendations for standardization of such methods.
J. Clin. Microbiol., 33: 2118–2123.
Taylor, D.N., McDermott, K.T., Little, J.R., Wells, J.G., and Blaser, M.J. (1983) Campylobacter enteritis from
untreated water in the Rocky Mountains. Ann. Intern. Med., 99: 38–40.
Taylor, R., Sloan, D., Cooper, T., Morton, B., and Hunter, I. (2000) A waterborne outbreak of Salmonella saintpaul.
Commun. Dis. Intell., 24: 336–340.
Taylor, R.H., Falkinham, J.O., III, Norton, C.D., and LeChevallier, M.W. (2000) Chlorine, chloramine, chlorine
dioxide, and ozone susceptibility of Mycobacterium avium. Appl. Environ. Microbiol., 66(4): 1702–1705.
Thomas, J.E., Gibson, G.R., Darboe, M.K., Dale, A., and Weaver, L.T. (1992) Isolation of Helicobacter pylori from
human faeces. Lancet, 340: 1194–1195.
Thompson, J.S. and Gravel, M.J. (1986) Family outbreak of gastroenteritis due to Yersinia enterocolitica serotype
0:3 from well water. Can. J. Microbiol., 32: 700–701.
Tiefenbrunner, F., Arnold, A., Dierich, M.P., and Emde, K. (1993) Occurrence and distribution of Legionella
pneumophila in water systems of central European private homes. In: Legionella: Current status and emerging
perspectives. J.M. Barbaree, R.F. Breiman, and A.P. Dufour (eds.). American Society for Microbiology,
Washington, DC. pp. 235–238.
Tobin, R.S., Ewan, P., Walsh, K., and Dutka, B. (1986) A survey of Legionella pneumophila in water in
12 Canadian cities. Water Res., 20: 495–501.
U.S. EPA (United States Environmental Protection Agency) (2000) Aeromonas criteria document. Prepared by A.
Highsmith and C. Bouma, GRAM Inc., Albuquerque, NM, for the Office of Science and Technology, Washington,
DC.
U.S. EPA (United States Environmental Protection Agency) (2001) Legionella: Drinking water health advisory.
Office of Water, Washington, DC (EPA-822-B-01-005).
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
31
Bacterial Waterborne Pathogens (February 2006)
Vaira, D., Miglioli, M., Menegatti, M., Holton, J., Boschini, A., Verguar, A., Ricci, C., Azzarone, P., Mule, P., and
Barbara, L. (1995) Helicobacter pylori status, endoscopic findings and serology in HIV-1-positive patients. Dig. Dis.
Sci., 40: 1622–1626.
van der Kooij, D. (1993) Importance and assessment of the biological stability of drinking water in the Netherlands.
In: Safety of water disinfection: Balancing the chemical and microbial risks. C. Craun (ed.). ILSI Press, Washington,
DC. pp. 165–179.
van der Kooij, D., Veenendaal, H.R., Slaats, N.P.G., and Vonk, D. (2002) Biofilm formation and multiplication
of Legionella on synthetic pipe materials in contact with treated water under static and dynamic conditions. In:
Legionella. R. Marre, Y.A. Kwaik, C. Bartlett, N.P. Cianciotto, B.S. Fields, M. Frosch, J. Hacker, and P.C. Luck
(eds.). ASM Press, Washington, DC. pp. 176–180.
van Duynhoven, Y.T.H.P. and de Jonge, R. (2001) Transmission of Helicobacter pylori: a role for food? Bull.
World Health Organ., 79(5): 455–460.
Villari, P., Crispino, M., Montuori, P., and Boccia, S. (2003) Molecular typing of Aeromonas isolates in natural
mineral waters. Appl. Environ. Microbiol., 69: 697–701.
Vogt, R.L., Sours, H.E., Barrett, T., Feldman, R.A., Dickson, R.J., and Witherell, L. (1982) Campylobacter enteritis
associated with contaminated water. Ann. Intern. Med., 96: 292–296.
von Reyn, C.F., Barber, T.W., Arbeit, R.D., Sox, C.H., O’Connor, G.T., Brindle, R.J., Gilks, C.F., Hakkarainen,
I.C., Ranki, A., Bartholomew, C., Edward, J., Tosteson, A.N.A., and Magnusson, M. (1993a) Evidence of previous
infection with Mycobacterium avium – Mycobacterium intracellulare complex among healthy subjects: an
international study of dominant mycobacterial skin test reactions. J. Infect. Dis., 168: 1553–1558.
von Reyn, C.F., Waddell, R.D., Eaton, T., Arbeit, R.D., Maslow, J.N., Barber, T.W., Brindle, R.J., Gilks, C.F.,
Lumio, J., Lahdevirta, J., Ranki, A., Dawson, D., and Falkinham, J.O., III (1993b) Isolation of Mycobacterium
avium complex from water in the United States, Finland, Zaire, and Kenya. J. Clin. Microbiol., 31: 3227–3230.
von Reyn, C.F., Maslow, J.N., Barber, T.W., Falkinham, J.O., III, and Arbeit, R.D. (1994) Persistent colonisation of
potable water as source of Mycobacterium avium infection in AIDS. Lancet, 343: 1137–1141.
Wang, W.L.L., Powers, B.W., Blaser, M.J., and Leuchtefeld, N.W. (1982) Laboratory studies of disinfectants
against Campylobacter jejuni. In: Proceedings of the Annual Meeting of the American Society of Microbiology.
American Society of Microbiology, Washington, DC.
Wang, X., Sturegard, E., Rupar, R., Nilsson, H.O., Alelijung, P.A., Carlén, B., Willen, R., and Wadstrom, T. (1995)
Infection of BALB/cA mice by spiral and coccoid forms of Helicobacter pylori. J. Med. Microbiol., 46: 657–663.
Weagant, S.D. and Kaysner, C.A. (1983) Modified enrichment broth for isolation of Yersinia enterocolitica from
non food sources. Appl. Environ. Microbiol., 45: 468–471.
Webb, P.M., Knight, T., Elder, J.B., Newell, D.G., and Forman, D. (1996a) Helicobacter pylori transmission:
evidence from a comparison with hepatitis A virus. Eur. J. Gastroenterol. Hepatol., 8: 439–441.
Webb, P.M., Knight, T., Elder, J.B., Newell, D.G., and Forman, D. (1996b) Is Helicobacter pylori transmitted from
cats to humans? Helicobacter, 1: 79–81.
Wendt, S.L., George, K.L., Parker, B.C., Gruft, H., and Falkinham, J.O., III (1980) Epidemiology of infection by
nontuberculous mycobacteria: isolation of potentially pathogenic mycobacteria from aerosols. Am. Rev. Respir. Dis.,
122: 259–263.
Guidelines for Canadian Drinking Water Quality: Guideline Technical Document
32
Bacterial Waterborne Pathogens (February 2006)
West, A.P., Millar, M.R., and Tomkins, D.S. (1992) Effect of physical environment on survival of Helicobacter
pylori. J. Clin. Pathol., 45: 228–231.
Wetzler, T.F., Rea, J.R., Ma, G.J., and Glass, M. (1979) Non-association of Yersinia with traditional coliform
indicators. In: Proceedings of the Annual Meeting of the American Water Works Association. American Water
Works Association, Denver, CO.
White, F.M. and Pedersen, A.T. (1976) Epidemic shigellosis on a worktrain in Labrador. Can. Med. Assoc. J., 115:
647–649.
WHO (World Health Organization) (1990) Epidemiology, prevention and control of legionellosis: memorandum
from a WHO meeting. Bull. World Health Organ., 68: 155–164.
WHO (World Health Organization) (2002) Guidelines for drinking-water quality. 2nd edition. Addendum:
Microbiological agents in drinking water. World Health Organization, Geneva.
Yu, V. (2002) Legionella surveillance: political and social implications — a little knowledge is a dangerous thing.
J. Infect. Dis., 185: 259–261.
Yu-Sen, E., Lin, R.D.V., Stout, J.E., McCartney, C.A., and Yu, V.L. (1998) Inactivation of Mycobacterium avium
by copper and silver ions. Water Res., 32: 1997–2000.
Zacheus, O.M. and Martikainen, P.J. (1996) Effect of heat flushing on the concentrations of Legionella pneumophila
and other heterotrophic microbes in hot water systems of apartment buildings. Can. J. Microbiol., 42: 811–818.
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Bacterial Waterborne Pathogens (February 2006)
Appendix A: List of acronyms
AIDS
CFU
CT
DNA
HPC
HUS
Mac
MAC
NTM
U.S. EPA
UV
VBNC
acquired immunodeficiency syndrome
colony-forming unit
product of disinfectant concentration and contact time
deoxyribonucleic acid
heterotrophic plate count
haemolytic uraemic syndrome
Mycobacterium avium complex
maximum acceptable concentration
non-tuberculous mycobacteria
United States Environmental Protection Agency
ultraviolet
viable but non-culturable
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