Appl Microbiol Biotechnol (2003) 61:424–428
DOI 10.1007/s00253-003-1302-y
MINI-REVIEW
S. Sharma · P. Sachdeva · J. S. Virdi
Emerging water-borne pathogens
Received: 1 October 2002 / Revised: 27 February 2003 / Accepted: 28 February 2003 / Published online: 9 April 2003
Springer-Verlag 2003
Abstract Emerging water-borne pathogens constitute a
major health hazard in both developed and developing
nations. A new dimension to the global epidemiology of
cholera—an ancient scourge—was provided by the
emergence of Vibrio cholerae O139. Also, water-borne
enterohaemorrhagic Escherichia coli (E. coli O157:H7),
although regarded as a problem of the industrialized west,
has recently caused outbreaks in Africa. Outbreaks of
chlorine-resistant Cryptosporidium have motivated water
authorities to reassess the adequacy of current waterquality regulations. Of late, a host of other organisms,
such as hepatitis viruses (including hepatitis E virus),
Campylobacter jejuni, microsporidia, cyclospora, Yersinia enterocolitica, calciviruses and environmental bacteria
like Mycobacterium spp, aeromonads, Legionella pneumophila and multidrug-resistant Pseudomonas aeruginosa have been associated with water-borne illnesses.
This review critically examines the potential of these as
emerging water-borne pathogens. It also examines the
possible reasons, such as an increase in the number of
immunocompromised individuals, urbanization and horizontal gene transfer, that may underlie their emergence.
Further, measures required to face the challenge posed by
these pathogens are also discussed.
Emerging water-borne pathogens
In 1992, the Institute of Medicine described an emerging
infection as any new, re-emerging, or drug-resistant
infection whose incidence in humans has increased within
the past two decades or whose incidence threatens to
increase in the near future (Lederberg et al. 1992). A
S. Sharma · P. Sachdeva · J. S. Virdi ())
Microbial Pathogenicity Laboratory, Department of Microbiology,
University of Delhi South Campus,
Benito Juarez Road, 110 021 New Delhi, India
e-mail: [email protected]
Tel.: +91-11-26879950
Fax: +91-11-26885270
number of reviews and other publications available on the
subject discuss emerging and re-emerging pathogens in
general, including water-borne, without addressing the
issues specifically pertinent to emerging water-borne
pathogens. This review critically examines which organisms really qualify as emerging water-borne pathogens,
the possible reasons underlying their emergence and
specific measures to face the challenge posed by them.
Due to the paucity of data, it may be difficult to decide
which of all water-borne pathogens are emerging. Nevertheless, there are some clear-cut candidates.
No organism other than Vibrio cholerae could serve as
a better example of an emerging water-borne pathogen.
Cholera is an ancient scourge and to date seven
pandemics have been recorded. Of the several recognized
serogroups, V. cholerae O1 has been responsible for these
pandemics. In 1992 however, a new strain called V.
cholerae O139 Bengal appeared in South India and
caused explosive outbreaks of cholera-like disease (Ramamurthy et al. 1993). In a matter of one year, the new
strain spread to several parts of India and to neighbouring
Bangladesh and Thailand (Nair et al. 1994). By the end of
1993, cholera outbreaks due to V. cholerae O139 were
reported from South Asia and other countries of the
world. Soon after its appearance, V. cholerae O139
outnumbered V. cholerae O1 and became the dominant
serogroup in India and other parts of the Indian subcontinent. It was thought that this was probably the
beginning of a new pandemic—the eighth pandemic of
cholera (Nair et al. 1996). But, by 1994, there was a
dramatic decrease in V. cholerae O139 and once again V.
cholerae O1 became the dominant species. It is thought
that, in the years to come, V. cholerae O139 is going to
play an important role in the global epidemiology of
cholera (Garg et al. 1998).
Following identification of the O139 serogroup and the
finding that environmental, non-toxigenic strains may
play an important role in the evolution of toxigenic V.
cholerae (Karaolis et al. 1995), there has been a lot of
interest in the study of non-O1, non-O139 serogroups. At
least three localized outbreaks of diarrhoea caused by
425
non-O1, non-O139 serogroups have been described in the
recent literature. These include an outbreak caused by V.
cholerae O10 and O12 in February 1994 in Lima, Peru
(Dalsgaard et al. 1995), another caused by O10 in Delhi,
India (Rudra et al. 1996) and an epidemic caused by
stable toxin producing non-O1 V. cholerae among
Khmers in a camp in Thailand (Bagchi et al. 1993). In
1996, an inexplicable upsurge in the incidence of non-O1,
non-O139 V. cholerae infections was observed among
hospitalized patients in Kolkata, India, which even
outnumbered the O1 and O139 serogroups (Sharma et
al. 1998). Although non-O1, non-O139 V. cholerae are
not regarded as important enteropathogens currently, their
increasing incidence suggests their potential as important
future water-borne pathogens.
Pathogenic Escherichia coli, such as enteroinvasive E.
coli, enteropathogenic E. coli, enteroaggregative E. coli
and shiga toxin-producing E. coli (STEC), constitute a
very large and important group of water-borne pathogens.
STEC and particularly E. coli O157:H7 (also called as
enterohaemorrhagic E. coli or EHEC) have been associated clinically with presentations ranging from asymptomatic infection to severe bloody diarrhoea, which may
lead to life-threatening sequelae, such as haemolytic
uraemia syndrome. This organism, although primarily
associated with food-borne outbreaks, has also become an
important public health concern as a water-borne pathogen. Water-borne E. coli O157:H7 outbreaks due to
drinking water (Dev et al. 1991; Swerdlow et al. 1992)
and recreational water exposure have been reported
(Brewster et al. 1994; Keene et al. 1994). A large
epidemic of haemorrhagic colitis in Africa was also
reported to be a water-borne outbreak of E. coli O157:H7
(Isaacson et al. 1993). Although generally considered to
be a problem in the developed nations, STEC have
recently been isolated from developing countries (Dutta et
al. 2000; Khan et al. 2002a, 2002b). These isolates have
been obtained from either cattle or diarrhoeic human
subjects, both of which can act as sources for water-borne
E. coli O157:H7. The non-O157 verotoxin-producing
strains are also transmitted by water (Chalmers et al.
2000) and need to be studied more intensively (Goldwater
and Bettelheim 1998). Efficient methods to detect STEC,
including E. coli O157:H7, in water have been reported
recently (De Boer and Heuvelink 2000), which would be
extremely useful in studying the prevalence of this
organism in water.
Cryptosporidium, a coccidian parasite, causes persistent diarrhoea (cryptosporidiosis) in immunocompromised individuals, particularly patients suffering from
acquired immunodeficiency syndrome (AIDS). Such
patients suffer from life-threatening infections due to this
pathogen. The organism is transmitted by ingestion of
water contaminated with the oocysts of Cryptosporidium
and also by direct contact with the infected persons or
animals. In the past, it has caused large water-borne
outbreaks (Krammer et al. 1996). The largest water-borne
outbreak due to Cryptosporidium was reported in 1993, in
Milwaukee, involving an estimated 400,000 cases (Mack-
enzie et al. 1994). The oocysts of Cryptosporidium are
resistant to the microbiocidal concentrations of chlorine
normally used for the disinfection of drinking water. Like
E. coli O157:H7, Cryptosporidium has also been regarded
as a problem in the developed countries. Nevertheless, the
organism has been isolated from the stools of diarrhoeic
patients in developing countries (Nath et al. 1999).
However, nothing is known about the prevalence of this
pathogen in the environmental waters of developing
nations, which needs to be studied. Other enteric protozoa, like microsporidia and cyclospora, have been
detected in surface, ground and treated wastewaters,
indicating their potential as water-borne pathogens. They
have been recognized as gastrointestinal pathogens with
increasing frequency since the AIDS epidemic. However,
microsporidia have also been implicated as pathogens in
otherwise healthy individuals (Goodgame 1996). Further
research is required to understand the distribution and
survival of microsporidia and cyclospora in aquatic
environments, so that their true potential as emerging
water-borne pathogens may be evaluated.
Campylobacters are becoming increasingly important
as the cause of acute gastroenteritis in both industrialized
and developing nations. During recent years, an increasing incidence of campylobacteriosis has been reported in
many developed countries (Shane 2000). Although
mainly food-borne, water is also regarded as an important
route for the transmission of campylobacters. Most of the
cases are sporadic, although large water-borne outbreaks
have also been reported. Between 1992–1996, six
outbreaks of campylobacteriosis occurred in Sweden
(Furtado et al. 1998). Two water-borne outbreaks of this
organism were reported in Central Norway in 1994 and
1995. Recently, a water-borne Campylobacter jejuni
outbreak was reported from a Danish town due to
contamination of the water supply with ground water
(Engberg 1998).
Yersinia enterocolitica, an important food- and waterborne bacterium is known to cause a variety of gastrointestinal problems. Most commonly, it causes acute
diarrhoea, terminal ileitis and mesenteric lymphadenitis.
Post-infectious sequelae are manifested in the form of
reactive arthritis. World-wide surveillance data on Y.
enterocolitica show great changes over the past two
decades and bring forth its emerging nature (Ostroff
1995). The strains present in the aquatic environment are
extremely heterogeneous, belonging to biotype 1A. It has
been shown that biotype 1A strains of Y. enterocolitica
may be pathogenic by some novel mechanisms. Thus, the
importance of Y. enterocolitica as an emerging waterborne pathogen needs to be assessed further.
Several other microbial agents which may not unequivocally qualify as emerging water-borne pathogens
nevertheless are potential candidates. These include
several enteric viruses, environmental mycobacteria,
aeromonads, Legionella pneumophila, Pseudomonas
aeruginosa and calciviruses. Of the large number of
enteric viruses known, infections due to the hepatitis E
virus have definitely increased in the past few years.
426
However, it is difficult to decide whether this is a true
increase in its incidence, or whether our ability to detect
the virus more frequently now than previously is being
perceived as emergence. The epidemic hepatitis E affects
mostly young adults between 20–40 years of age.
However, children and old people are not immune to this
disease. Calciviruses cause acute gastroenteritis. Although mainly food-borne, the importance of human
calciviruses as water-borne pathogens needs further
investigation. The so-called environmental mycobacteria—the Mycobacterium avium–intracellularae complex,
M. kansasi and M. fortuitum—are present in soil and
water. They can cause infections of the skin, the lymph
nodes and the respiratory and gastrointestinal tracts.
Disseminated infections are seen only in immunocompromised individuals. Although infections due to environmental mycobacteria have increased in the past
(Falkinham 1996), there is no evidence of the acquisition
of infection by water. Aeromonads (Aeromonas sobria, A.
caviae, A. hydrophila) are widespread in surface waters
and have been isolated regularly from drinking-water
distribution systems. Like environmental mycobacteria
and aeromonads, L. pneumophila and P. aeruginosa can
also get into water distribution systems from source
waters. All these organisms have the ability to regrow in
such distribution systems. The ability of L. pneumophila
to grow inside fresh-water amoebae is noteworthy,
especially in hot- and cold-water distribution systems.
The use of such contaminated waters for heating or
cooling towers results in the production of an aerosol of L.
pneumophila which may be inhaled, leading to Legionnaire’s disease—a form of severe pneumonia (States et al.
1990). In contrast, P. aeruginosa is an opportunist par
excellence (Lyczak et al. 2000). The importance of these
organisms as water-borne pathogens is based primarily on
their ability to live in biofilms in water distribution
systems, where they can act as a continuous source of
contamination (Szewzyk et al. 2000). This is because
organisms in biofilms differ considerably from their
planktonic counterparts in terms of gene expression,
metabolic activity and virulence characteristics
(Morschhauser et al. 2000).
Emergence—possible causes
The reasons underlying the emergence of water-borne
pathogens can, at best, be discussed in terms of possibilities only. Unequivocal answers must await further
research. For a better understanding of the causes of
emergence, it may be advisable to divide emerging waterborne pathogens as newly recognized and newly originated. The majority of the emerging water-borne pathogens belong to the former category, which means that,
although the etiologic agent was known for a long time, it
was recognized only recently as the cause of water-borne
illness. This includes parasitic protozoa like Cryptosporidium and Microsporidia, Campylobacter jejuni, several
viruses including calciviruses and hepatitis E virus and a
host of environmental bacteria, namely Mycobacterium
spp, aeromonads, L. pneumophila and P. aeruginosa. The
newly originated category represents the truly new
pathogens exemplified by V. cholerae O139 and EHEC.
A variety of reasons may underlie the emergence of
newly recognized pathogens. An important reason, which
is probably relevant to all, is the development of efficient
detection methods, including molecular, immunological
and immunomagnetic techniques (Hurst and Toranzus
1997). Another reason, which is more relevant to the
emergence of Cryptosporidium, is the increase in the
number of immunocompromised persons, which is best
exemplified by patients receiving therapy for cancer or
organ transplantation, elderly individuals and patients
with AIDS. This also seems to be true for the emergence
of microsporidia. The emergence of these pathogens in
the industrialized west is probably related to the relatively
higher number of immunocompromised individuals in
this region.
Increasing urbanization, necessitating the use of vast
drinking-water distribution systems and the attendant
problems, has mainly been responsible for the emergence
of water-borne Mycobacterium spp, aeromonads, L.
pneumophila and P. aeruginosa.
Of late, the ever-increasing movement of human
beings from one part of the world to another may
introduce exotic pathogens into geographical areas where
the native population may have little immunity to them.
Akin to this reasoning is the introduction of pathogens
into newer geographical areas via the increasing international trade in food and foodstuffs. In fact, several foodborne pathogens are also transmitted by water. This may
account for the introduction of European strains of Y.
enterocolitica into the American continent and vice versa
witnessed in the past decade or so (Ostroff 1995).
Multidrug resistance has been responsible for the
emergence or re-emergence of several pathogens, like M.
tuberculosis, methicillin-resistant staphylococci, Neisseria meningitides and enterococci. Among the emerging
water-borne pathogens however, multidrug-resistant P.
aeruginosa is probably the only organism which qualifies
for this category (Bert et al. 1998).
The acquisition of virulence traits by horizontal gene
transfer is responsible for the appearance of the truly new
pathogens. Evidence indicates this may be the cause for
the emergence of V. cholerae O139 and E. coli O157:H7.
Natural ecosystems like aquatic habitats contain diverse
microbial communities. These are characterized by the
presence of both resident (environmental/non-pathogenic)
microflora and faecally shed pathogenic forms from
animal reservoirs or human patients. The environmental
or non-pathogenic forms may serve as a storehouse of
genetic determinants which, if transferred to other strains,
may confer novel virulence capabilities. Such inter- or
intra-specific movement of genetic determinants may be
mediated by bacteriophages, which are also an integral
part of the aquatic ecosystems. Besides phages, transposon-like elements, conjugative plasmids and integrans can
also mediate similar transfer of genetic determinants.
427
Nucleotide analysis of the asd genes of 45 strains of V.
cholerae has yielded evidence which indicates that the
classic and El Tor biotypes and the United States Gulf
Coast strains of V. cholerae O1 evolved independently
from environmental non-toxigenic, non-O1 strains
(Karaolis et al. 1995). Therefore, it has become increasingly clear that the non-O1, non-O139 serogroups are
involved in the emergence of newer variants of V.
cholerae, a fact supported by the genesis of V. cholerae
O139. This serogroup is believed to have evolved as a
result of horizontal gene transfer between the O1 and the
non-O1 serogroups (Bik et al.1995). However, genetic
evidence in respect of the emergence of E. coli O157:H7
is more nebulous. The genotyping of E. coli O157:H7 has
shown that strains collected from geographically diverse
areas are identical or nearly identical, indicating their
recent descent from an ancestral cell. These are related
only distantly to other verotoxin-producing strains of E.
coli (Whittam et al.1998). Indirect evidence however
indicates that genetic exchange among these is possible
(Bilge et al.1996)
Finally, the influence of sustained climatic changes on
the emergence of water-borne pathogens also needs to be
considered. Both Cryptosporidium and E. coli O157:H7
were known to be present in cattle reservoirs before these
were recognized as water-borne human pathogens. Is it
possible that these pathogens, under certain environmental conditions, made their way into surface waters and
survived there, to emerge as water-borne pathogens later?
Could there be a link between the degree of precipitation
and their entry into water bodies? Although these are
provocative suggestions, they nevertheless provide a
framework to explore the reasons underlying the emergence of such water-borne pathogens. It was reported that
heavy rainfall appeared to increase the concentration of
Cryptosporidium in river water (Atherholt et al. 1998).
Surveillance, resource protection
and disinfection—the mainstays of control
As a matter of fact, we do not have much control over the
emergence of new pathogens. Surveillance, resource
protection and adequate disinfection seem to be the major
mainstays in safeguarding ourselves against emerging
water-borne pathogens. Rigorous surveillance would
serve to identify the new pathogens. Following identification, the problem may be tackled on several fronts, e.g.
documenting the spread of the pathogen through drinkingwater and other routes, developing accurate monitoring
systems, establishing effective disinfection or filtration
methods and assessing relative health risks (Gostin et al.
2000). It has been well established that improvement in
the quality of resource waters has a major impact on the
control of water-borne pathogens. Developing efficient
and rigorous disinfection methodologies, for example the
use of ultraviolet radiation and ozone in addition to
chlorination can go a long way in controlling chlorineresistant pathogens like Cryptosporidium. Although the
measures suggested above pose a formidable task, a
beginning has already been made. This is evident from the
fact that much more is known about these pathogens
today than five years ago. Studies on the molecular
epidemiology of V. cholerae O139 has opened new vistas
on the aquatic ecology of water-borne pathogens, e.g. the
role of autochthonous, non-pathogenic microbes in the
emergence of new pathogens and the role of zooplanktons
and environment (especially temperature) in the spread of
water-borne pathogens. Cryptosporidium and E. coli
O157:H7 have brought to the fore how extremely low
levels of certain pathogens in water may pose a serious
threat to human health. The emergence of water-borne
Cryptosporidium has motivated water authorities to
reassess the adequacy of current water quality regulations
(Gostin et al. 2000). Areas where further research is
warranted include: the development of simple, quick and
foolproof methods for the detection of these pathogens in
water, their survival in aquatic habitats, their ability to
form biofilms in drinking-water distribution systems and
their resistance to disinfection. This is an enormous task
and requires dedicated inputs from researchers, public
health officials and water authorities.
Acknowledgements This work is supported by grants from the
Department of Science and Technology, the Ministry of Environment and Forests and the Indian Council of Medical Research.
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