Veterinary Parasitology 182 (2011) 70–78
Contents lists available at ScienceDirect
Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar
Zoonotic enteric protozoa
R.C.A. Thompson ∗ , A. Smith
WHO Collaborating Centre for the Molecular Epidemiology of Parasitic Infections, School of Veterinary and Biomedical Sciences, Murdoch University, South
Street, Murdoch, Western Australia 6150, Australia
a r t i c l e
Keywords:
Enteric protozoa
Zoonoses
Transmission
Foodborne
Polyparasitism
Clinical significance
Giardia
Cryptosporidium
Entamoeba
Blastocystis
Balantidium
i n f o
a b s t r a c t
A growing number of enteric protozoan species are considered to have zoonotic potential.
Their clinical impact varies and in many cases is poorly defined. Similarly, the epidemiology
of infections, particularly the role of non-human hosts, requires further study. In this review,
new information on the life cycles and transmission of Giardia, Cryptosporidium, Entamoeba,
Blastocystis and Balantidium are examined in the context of zoonotic potential, as well as
polyparasitism and clinical significance.
© 2011 Elsevier B.V. All rights reserved.
1. Introduction
Humans are susceptible to infection with numerous
species of protozoa that colonise the intestinal tract. An
increasing number of these protozoa are being shown to
have zoonotic potential although their clinical significance
varies. Apart from Entamoeba histolytica and Balantidium
coli, they do not invade the mucosal tissues or other organs.
Cryptosporidium has an epicellular association with the
host cell, principally in the mucosal epithelium, but cannot
be considered to be invasive. In most cases, the pathogenesis of most enteric protozoa is poorly understood and with
some species, such as Entamoeba coli, opinions vary as to
whether they should be considered as parasites.
In this review, we update the latest information on
individual species of enteric protozoa, and then examine
∗ Corresponding author at: WHO Collaborating Centre for the Molecular Epidemiology of Parasitic Infections and the State Agricultural
Biotechnology Centre, School of Veterinary and Biomedical Sciences, Murdoch University, South Street, Western Australia 6150, Australia.
Tel.: +61 08 9360 2466.
E-mail address: [email protected] (R.C.A. Thompson).
0304-4017/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.vetpar.2011.07.016
transmission, polyparasitism and clinical significance on a
broad scale.
2. The parasites
2.1. Giardia
The molecular characterisation of Giardia isolates from
different species of mammalian hosts throughout the
world has confirmed the existence of host specific species
and two species with broad host ranges and which are
zoonotic (Table 1). A revised taxonomy has consequently
been proposed which largely reflects the species nomenclature reported by early workers in the field (Monis et al.,
2009; Thompson and Monis, 2011).
The application of multilocus genotyping to Giardia
from human and other mammalian hosts in different parts
of the world has clearly demonstrated the occurrence of
zoonotic species in human and non-human hosts (dogs,
cats, livestock and wildlife) in the same geographical areas
supporting the potential for zoonotic transmission (rev. in
Thompson, in press; Leonhard et al., 2007). Although such
studies do not provide evidence of actual zoonotic transmission, a number of studies in defined endemic foci have
R.C.A. Thompson, A. Smith / Veterinary Parasitology 182 (2011) 70–78
Table 1
Proposed and existing species in the genus Giardia.
Species
Hosts
G. duodenalis (=Assemblage A)
Wide range of domestic and
wild mammals including
humans
Humans and other primates,
dogs, some species of wild
mammals
Amphibians
Rodents
Birds
Birds
Rodents
Dogs, other canids
Cats
Cattle and other hoofed
livestock
Rats
G. enterica (=Assemblage B)
G. agilis
G. muris
G. ardeae
G. psittaci
G. microti
G. canis (=Assemblage C/D)
G. cati (=Assemblage F)
G. bovis (=Assemblage E)
G. simondi (=Assemblage G)
provided convincing evidence involving dogs and humans
(Traub et al., 2004; Inpankaew et al., 2007; Salb et al.,
2008). Although the focus of these studies has been on
the dog as a reservoir of human infection, several reports
demonstrate that ‘reverse zoonotic transmission’ (zooanthroponotic) is an important factor that must be considered
in understanding the epidemiology of Giardia infections.
Humans are considered to be the source of infection in
non-human primates and painted dogs in Africa, marsupials in Australia, beavers and coyotes in North America,
muskoxen in the Canadian arctic, house mice on remote
islands and marine mammals in various parts of the world
(Graczyk et al., 2002; Sulaiman et al., 2003; Moro et al.,
2003; Appelbee et al., 2005, 2010; Kutz et al., 2008; Dixon
et al., 2008; Teichroeb et al., 2009; Thompson et al., 2009,
2010a,b; Ash et al., 2010; Johnston et al., 2010). These
reports raise important issues for conservation. This is
because we do not understand the impact Giardia may
have on what are possibly naïve hosts that may have been
exposed to the parasite relatively recently as a consequence of habitat disturbance and human encroachment
(Thompson et al., 2010a; Johnston et al., 2010). In contrast,
in Aboriginal communities in isolated regions of northern Australia, reverse zoonotic transmission undoubtedly
occurs between humans and dogs but the fact that the
dogs are frequently infected with their own host-adapted
species of Giardia, Giardia canis, demonstrates that competitive interactions likely limit opportunities for zoonotic
species to establish in dogs (Hopkins et al., 1997, 1999;
Thompson and Monis, 2004). However, the fact that dogs
have contact with young children passing Giardia cysts,
as well as discarded nappies/diapers, means that dogs are
likely to act as mechanical transmitters of zoonotic Giardia
since their coats are likely to be contaminated with cysts.
Although competitive interactions between different
species/assemblages of Giardia has been proposed to
explain the predominance of single assemblage infections
in both dogs and cattle, this may reflect the consequences
of mixed infections in endemic foci where the frequency of
transmission is very high. In other situations where transmission is sporadic mixed infections may co-exist and have
been increasingly reported from multilocus studies in several countries in humans, dogs and cattle (e.g. Hussein et al.,
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2009; Sprong et al., 2009; Dixon et al., 2011; Covacin et al.,
2011).
The two zoonotic species/assemblages of Giardia are
geographically widespread and as more isolates are genotyped some patterns are emerging on host occurrence.
Recent studies in dogs have shown that it is not possible
to extrapolate from one geographical region to another
in terms of the prevalence or species/assemblage composition of Giardia infections in dogs (Ballweber et al.,
2010; Covacin et al., 2011). Until recently, comprehensive data on the assemblage distribution of Giardia in
dogs in the USA was not available, and studies in Europe
had suggested that assemblage B has a predominantly
human distribution (Sprong et al., 2009). However, a
recent study of dogs infected with Giardia in the USA
found a higher frequency of infections with assemblage
B than assemblage A, which has not been reported elsewhere (Covacin et al., 2011). This suggests that in North
America at least, we cannot assume that assemblage A
is the most common of the zoonotic assemblages found
in non-human hosts. Indeed in wildlife, assemblage B
often predominates (e.g. Johnston et al., 2010) whereas
in cattle, assemblage A is most often reported (Sprong
et al., 2009). However, there is extensive genetic substructuring within assemblage B, and it is possible that
some subgroups are more commonly associated with
zoonotic infections than others. As regards Giardia infections in humans, there is some evidence of geographic
sub-structuring (Wielinga et al., 2011) and assemblage
B may be more common in isolated and/or community settings where the frequency of transmission is high
(Thompson, 2000). Under such circumstances, the parasite is likely to be exposed to greater selection pressure
in terms of exposure to antigiardial drugs and competitive interactions which might explain why evidence of
recombination in Giardia is mostly confined to assemblage
B isolates (Lasek-Nesselquist et al., 2009; Thompson and
Monis, 2011).
It is still not yet clear whether the different
species/assemblages of Giardia are associated with
differences in pathogenesis. Although differences have
been reported in human populations infected with assemblage A vs B, no clear picture has emerged (Thompson and
Monis, 2011). This may be particularly relevant to the two
main disease syndromes of diarrheoa and failure to thrive.
Similarly, it is not known whether there is any difference
in the clinical outcome in dogs infected with the zoonotic
assemblages or G. canis.
2.2. Cryptosporidium
Current evidence indicates that the main reservoirs
of zoonotic Cryptosporidium remain livestock, with the
potential transmission of Cryptosporidium parvum (=Cryptosporidium pestis; see Slapeta, 2011), including the
so-called cervine genotype, to humans via contaminated
water or through direct contact with livestock (Robertson
et al., 2010; Gormley et al., 2011). Sub-genotyping continues to reveal genetic sub-structuring within C. parvum
but whether this is reflected in variation in host specificity and zoonotic potential remains unclear. The recent
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demonstration of zoonotic transmission to humans in the
U.K. of a newly described genotype of Cryptosporidium from
rabbits (Chalmers et al., 2009) has raised concerns that
humans may be at risk of Cryptosporidium infection from
rabbits in other geographical areas, as recently proposed
in Australia where the rabbit genotype has been identified (Nolan et al., 2010). Although given a new species
name, Cryptosporidium cuniculi, by Robinson et al. (2010),
it is genetically very close to C. parvum and Cryptosporidium hominis and thus it may be prudent to reconsider the
taxonomic status of all three ‘species’ in the future, particularly given the intra-specific genetic variability that
has been described. In contrast, available evidence suggests that the evolving nomenclature for what appear
to be host specific forms in different species of domestic and wild animals, is likely to be stable and largely
reflective of the early taxonomy (see O’Donoghue, 1995)
proposed before the advent of molecular characterisation.
Phylogenetically, Cryptosporidium has been shown to
have closer affinities to gregarine protozoa than the coccidians (Barta and Thompson, 2006; Borowski et al., 2010).
This is reflected in the life cycle, developmental biology,
metabolism and host parasite relationship of Cryptosporidium and will require a reappraisal of its biotic potential, in
terms of survival, particularly in aquatic environments.
2.3. Entamoeba
Of the zoonotic amoebae, E. histolytica is undoubtedly of most clinical significance and is considered by
some authorities as the only amoeba parasitic in the
human intestine (Schuster and Visvesvara, 2004). However, the public health risk from zoonotic transmission of
E. histolytica would appear to be minimal. Dogs can be a
potential source of human infections following coprophagy
of human faeces, although this reverse zoonosis is unlikely
to result in significant environmental contamination since
E. histolytica rarely encysts in dogs (Eyles et al., 1954; Barr,
1998). Similarly, E. histolytica is found in non-human primates (Schuster and Visvesvara, 2004) but the risk to public
health would appear to be minimal as such infections
appear to again reflect reverse zoonosis.
A number of other potentially zoonotic species of Entamoeba have been reported in humans including E. coli, E.
polecki and E. hartmanni (Meloni et al., 1993; Stensvold
et al., 2011). They have generally been considered to
be ‘non-pathogenic’ and ‘commensals’ but increasing
evidence of their widespread and common occurrence, particularly as co-infections with other enteric protozoa and
helminths, warrants a re-evaluation of their potential clinical significance. Of the three species, E. coli is one of the
most commonly reported enteric protozoa in human surveys (Chunge et al., 1991; Ouattara et al., 2008; Youn, 2009;
Boeke et al., 2010), and apart from non-human primates
(e.g. Howells et al., 2011) has been recovered from dogs
and marsupials (Campos Filho et al., 2008; Youn, 2009).
It also exhibits extensive genetic diversity with at least
two major subtypes. Although previous reports have considered E. polecki to be zoonotic (Barnish and Ashford,
1989), recent molecular studies suggest this species is
restricted to humans whereas E. hartmanni is potentially
zoonotic with infections reported in non-human primates
(Stensvold et al., 2011).
2.4. Blastocystis
Blastocystis is an emerging pathogen in terms of its association with disease and zoonotic potential (Vassalos et al.,
2008; Boorom et al., 2008; Parkar et al., 2010). Now that
robust molecular tools are available to detect and characterise Blastocystis, it has been shown to be both more
common and genetically diverse than previously envisaged
(Parkar et al., 2010). Blastocystis is a ubiquitous parasite of humans usually associated with chronic infections,
the prevalence of which increases with age. In addition
to humans, Blastocystis is common in numerous species
of wild and domestic animals (Parkar et al., 2007, 2010;
Yoshikawa et al., 2008).
As has been shown with Giardia and Cryptosporidium,
Blastocystis comprises a genetically variable complex of
interspecific and intraspecific variants and a stable taxonomy has yet to be established. Humans are susceptible
to infection with a variety of genetically distinct subtypes
some of which have also been reported in domestic and
wild animals (Parkar et al., 2007, 2010; Yoshikawa et al.,
2008). Studies in defined endemic foci, such as zoos, have
provided convincing evidence of zoonotic transmission
(Parkar et al., 2010). However, the frequency of zoonotic
transmission and risk factors have still to be clearly defined.
2.5. Balantidium
This is the only ciliate known to cause infections in
humans and is considered to be zoonotic with pigs as the
asymptomatic natural reservoir, although other domestic
livestock such as cattle may be infected in some areas (Bilal
et al., 2009). Non-human primates are also susceptible to
infection (see Howells et al., 2011) but their role in zoonotic
transmission is likely to be minimal.
Balantidium is most common in tropical and subtropical regions (Zaman, 1998; Farthing et al., 2003; Owen,
2005) and the risk of infection in humans is in communities that have a close association with pigs (Schuster
and Ramirez-Avila, 2008). However, infection in humans
is rarely reported (Farthing et al., 2003; Schuster and
Visvesvara, 2004; Conlan et al., in press). The parasite
is invasive in humans and can cause serious disease but
cases are reported sporadically (Schuster and Visvesvara,
2004; Conlan et al., in press). The low reported prevalences, even in pig rearing communities (Owen, 2005;
Kirkoyun Uysal et al., 2009) would suggest that even if
cysts are ingested from the environment, the parasite rarely
establishes ‘patent’ infections. However, the only reported
waterborne outbreak originating from contaminated pig
faeces, resulted in 110 people infected (Walzer et al., 1973
[in Farthing]). This would suggest that sporadic and/or isolated infections usually go unnoticed or that sojourn in
water may enhance infectivity to humans in some way.
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3. Transmission
3.1. Pathways of transmission
Specific transmission pathways for enteric protozoan
parasites can be difficult to determine though some routes
are more common than others. Direct transmission via the
faecal/oral route is likely to be the most common form of
transmission, whether zonotic (see above) or direct person
to person. However, indirect transmission, where infection
results through the mechanical transmission of oo/cysts on,
for example, flies (Szostakowska et al., 2004) or other animals such as dogs or livestock, or by the contamination of
food or water sources (Smith et al., 2007; Karanis et al.,
2007; Nyarango et al., 2008), poses a significant threat particularly in the developing world. Quantifying the level of
protozoan parasite infection using commonly applied metrics such as the DALY (e.g. Pruss et al., 2002) is impractical
unless gross non-specific estimates are required as distinguishing between all possible sources of infection and
the confounding impact of polyparasitism is rarely if ever
possible (Payne et al., 2009; King, 2010). Epidemiological
analysis of focal point contaminations such as water or
specific food contamination events can provide good estimates of the spread and impact of parasite infection, but on
a global scale, due to the uncertainty caused by the scarcity
of data (Payne et al., 2009) the impact of these occurrences
remains poorly understood.
3.2. Enhancing transmission
Children are a particularly high risk group for infection with enteric protozoan parasites although the relative
risk for infection with different parasites varies between
different geographic regions of the world (Fig. 1). Interestingly, based on a major review of the number of reports in
the scientific literature (Smith and Thompson, unpublished
report, Food Safety, Zoonoses and Foodborne Diseases,
World Health Organization, Geneva) the risk of infection
appears greater within rural environments than within
urban areas; presumably because of the increased opportunity for both direct and indirect transmission to occur in
areas with poor sanitation and higher contact rates with
wildlife and domestic animal reservoirs of infection.
Poor hygiene has been shown to be a crucial factor in
enhancing the transmission of enteric protozoa (Ang, 2000;
Alvarado and Vásquez, 2006; Diaz et al., 2006; Balcioglu
et al., 2007; Azian et al., 2007). However, the term ‘poor
hygiene’ is broad and does not fully describe the range of
risk factors involved.
Blastocystis, Cryptosporidium, Giardia, Entamoeba spp.,
and Balantidium can all be transmitted in water, including drinking water sources, recreational water, as well as
lakes and streams. The impact of infection obtained from
lakes and streams varies greatly depending on geographic
location as there exists significant variation in the use of
such water bodies throughout the world as well as within
regions depending on socioeconomic status. For example the predominant use of lakes and streams in Europe
is recreational whereas in Africa or Asia there is a much
greater reliance on these water sources for drinking and
73
in the preparation of food and personal hygiene. Waterborne transmission of parasites in the developed world is
therefore more likely to be the result of contamination, or a
process failure within water utilities, industry or in public
places such as swimming pools (Welch, 2000; Stuart et al.,
2003; Dawson, 2005; Shields et al., 2008). In the developing world in particular, areas which are prone to flooding
face an increased risk of waterborne infection particularly
where basic sewerage systems such as long-drop latrines
are common. The risk is further increased in those communities and societies where the keeping of animals (pets and
livestock) within or near the home is common and the risk
of infection with specific parasites including concurrent
infections will vary culturally depending on the species of
zoonotic reservoir involved (Hunter and Thompson, 2005).
3.3. Foodborne transmission
Cases of foodborne transmission have until recently
been difficult to determine, and linking infection to a
contaminated food source remains so for the majority of
scenarios. Small scale outbreaks, where the point of initial contamination may be the result of poor hygiene by
an individual resulting in localised foodborne transmission to family members or the immediate community, are
extremely common particularly in the developing world.
Transmission resulting from contamination of food or drink
that leads on to larger scale infections, such as an outbreak of cryptosporidiosis in the USA in 1993 arising from
the consumption of infected fresh-pressed apple cider is a
relatively much rarer event (Millard et al., 1994). Again,
according to reports published in the primary scientific
literature, the risk of becoming infected with Blastocystis
from contaminated food appears low, although infection
arising through poor hygiene practices of food handlers
has a potentially much higher infection rate. For example, a survey of 150 apparently healthy food handlers
in Bolivar State, Venezuela, showed that 25.8% (n = 107)
were in fact positive for Blastocystis (Requena et al., 2003),
whereas a review of 103 published reports concerning Blastocystis infection between 1990 and 2008 showed that
none were able to conclusively ascribe infection to conventional foodborne transmission (Smith and Thompson,
unpublished report, Food Safety, Zoonoses and Foodborne
Diseases, World Health Organization, Geneva). However,
other enteric parasites are readily transmitted on food
and in some regions of the world farming and agricultural
practices such as the use of human waste for fertilisation
and inefficient or absent pasteurisation techniques positively enhance transmission. None the less, the majority
of indirect transmission from contaminated food arises
from more proximate sources of infection such as infected
food handlers and poor hygiene, often resulting from overcrowded living conditions where clean running water is
scarce, and also from children and adults with little or no
health education.
Foodborne transmission, whether arising as a result
of agricultural practices or poor hygiene within households, or by food handlers, is undoubtedly responsible
for a significant number of infections every year. Preliminary estimates derived from a literature review of
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Fig. 1. Estimated prevalence of Blastocystis, Cryptosporidium, Giardia and Entamoeba within children from rural and urban regions for each or the World
Health Organisation (WHO) defined regions of the world: European Region (EUR), South-East Asian Region (SEAR), Western Pacific Region (WPR), African
Region (AFR), Region of the Americas (AMR) and Eastern Mediterranean Region (EMR).
published reports and case notes for Cryptosporidium and
Giardia occurrence, suggest that the number of cases of
foodborne transmission resulting in infection by Giardia range from 13 million in the WHO derived Eastern
Mediterranean region (EMR) to 76 million in the Western
Pacific Rim (WPR) region (Fig. 1). Similarly, preliminary
estimates for Cryptosporidium suggest there may be as
many as 6 million cases of foodborne transmission annually in the EMR region and up to 27 million in the
African region. However, these estimates must be interpreted with extreme caution as the majority of publications
upon which most estimates are based simply do not, or
cannot, ascribe infection to a particular source or event
such as contact with contaminated food. Transmission
between humans, either involving intermediate vessels
such as contaminated food or water, or via direct contact, is ultimately responsible for most reported cases,
with zoonotic parasites and parasite strains as well as
zoonotic sources of human strains also a major source of
infection in many parts of the world (Thompson, 2000;
Feltus et al., 2006; Ng et al., 2008; Thompson et al.,
2008).
4. Polyparasitism
The clinical impact of zoonotic enteric protozoan infections is greatest in the developing world where inadequate
sanitation, poor hygiene and proximity to zoonotic reser-
voirs, particularly companion animals and livestock are
greatest. In such circumstances, it is not surprising that
infections with more than one species of enteric protozoan is common, and in fact single infections are rare
(see above). Unfortunately, the impact on health of such
concurrent/co-infections has not been adequately taken
into account. Awareness of the significance of polyparasitism (concurrent/concomitant infections) in terms of
malaria, schistosome infections and more recently gastrointestinal (GI) helminths, is now well established (Cox,
2001; Pullan and Brooker, 2008; Midzi et al., 2008;
Koukounari et al., 2010; Supali et al., 2010). However, the
impact of polyparasitism in the context of enteric protozoan infections has not been considered (Ouattara et al.,
2008).
Enteric protozoan infections are components of a complex ecological system, shared with helminths and bacteria.
As such, we should not study the components of such
an ecological system in isolation (e.g. see Rohani et al.,
2003) especially when considering their impact on disease
dynamics (Jolles et al., 2008). Polyparsitism will lead to
the stimulation of different components of the immune
system that may act synergistically, lead to competitive
interactions and/or alter pathogenic behaviour of one or
more species (Thompson and Lymbery, 1996; Cox, 2001;
Mideo, 2009; Koukounari et al., 2010; Supali et al., 2010).
These may have an additive and/or multiplicative impact
on nutrition and pathogenicity (Pullan and Brooker, 2008)
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leading to an increase or decrease in clinical severity,
and/or interfere with normal gut microflora.
Current measures of determining the impact on health
of parasitic disease (DALY) do not take into consideration the “co-morbidities of polyparasitism” (Payne et al.,
2009). Payne and colleagues suggest a new approach
where co-infections with more than one infectious agent
are defined as a specific disease, for example malaria,
hookworm, malaria + hookworm, etc. This would appear a
logical approach and should be readily achievable with diseases such as malaria and hookworm where the pathogenic
mechanisms of the individual aetiological agents are reasonably well understood. This would be much more of a
challenge with most of the enteric protozoa since their
pathogenesis is still poorly understood, particularly in
chronic infections. However, it is an area of future epidemiological research that should be given priority.
Available survey data, mostly from rural areas of developing countries, that provide data on the prevalence of
mixed infections with enteric protozoa show that they are
the rule rather than the exception and that children are
at most risk with the majority of the populations studied
infected with at least two species of protozoan (Chunge
et al., 1991; Ouattara et al., 2008; Nematian et al., 2008;
Nguhiu et al., 2009; Aly and Mostata, 2010). The most commonly represented protozoa in concurrent infections are
Giardia, Blastocystis, and Entamoeba coli, which are usually also found with the cestode Hymenolepis nana (Chunge
et al., 1991; Meloni et al., 1993; Ouattara et al., 2008;
Nematian et al., 2008). Chronic helminth infections could
have a significant influence over the immune response and
hence susceptibility to other pathogens (Rodriguez et al.,
1999). This was concluded in the context of GI nematode
infections but consideration should also be given to H. nana
which is rarely found on its own in developing areas of
the world and usually co-infects with one or more enteric
protozoan species. Depending on the endemic area, E. histolytica and Entamoeba dispar may also occur in mixed
infections. In addition, other potentially zoonotic protozoa, such as Chilomastix mesnili and Endolimax nana that
may have been dismissed as having no clinical consequence
and not reported, are also probably common (e.g. Chunge
et al., 1991) and in the context of polyparasitism should be
considered.
5. Clinical significance
The clinical impact of E. histolytica and Cryptosporidium
in humans are well understood. They have clearly defined
individual effects on the host and the resulting morbidity
will be worsened in an additive way when other enteric
protozoa are present. The severity of Cryptosporidium infections is greatest in individuals with an impaired or deficient
immune system. Much less is known about the clinical
impact of other enteric prototozoa particularly in chronic
and mixed infections.
The symptoms associated with Giardia infections vary
greatly but have mostly been documented on the basis of
individual infections with the expression of short-lasting
diarrhoea the most common manifestation (Eckmann,
2003). However, there is increasing realisation that the
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clinical impact of Giardia is greatest in children, particularly
in developing countries or disadvantaged communities
where poor hygiene and the proximity of animal reservoirs
favour a high frequency of transmission and the establishment of chronic infections (Thompson, 2009). In such
situations, nutrition may be suboptimal and Giardia infections contribute to poor growth and development (‘failure
to thrive’), zinc and iron deficiency, as well as predispose
to the development of allergic diseases (Muniz-Junqueira
and Queiroz, 2002; Muniz et al., 2002; Nematian et al.,
2008; Hesham et al., 2005; Savioli et al., 2006; Thompson,
2008; Boeke et al., 2010; Duran et al., 2010; Quihui et al.,
2010). Importantly, diarrheoa is not necessarily a symptom in such chronic infections (Nash et al., 1987; Chunge
et al., 1991; Flanagan, 1992; Rodriguez-Hernandez et al.,
1996; Troeger et al., 2007), which are often shared with
enteric parasites that contribute to the syndrome of failure to thrive, such as E. coli, Blastocystis and H. nana (see
above). Reports from around the world suggest there are
differences in the clinical outcome in humans of infections
with assemblage A (Giardia duodenalis) and assemblage B
(Giardia enterica) (Thompson and Monis, 2011). However,
it is difficult to directly compare between reported studies
because of differences in design and populations sampled.
It has been suggested that infections with assemblage A
are usually short lasting, acute infections often associated
with diarrhoea whereas infections with assemblage B are
more common in community settings or localised endemic
foci where the frequency of transmission is high resulting
in chronic infections that may contribute to poor growth
(Thompson and Monis, 2011).
There is now increasing recognition that Blastocystis
is pathogenic, at least in humans, although the circumstances and mechanisms associated with disease are not
understood (Boorom et al., 2008). Similarly, the spectrum of disease manifestations associated with Blastocystis
infections have yet to be clearly defined. Many of the documented symptoms are non-specific and may be overlooked
but the realisation that Blastocystis is most often associated
with chronic infections and that prevalence increases with
age, demonstrates that such symptoms may be indicative
of a range of disorders, often sporadic, not necessarily associated with an enteric pathogen, for example inflammatory
bowel disorders (Boorom et al., 2008). As with Giardia,
it is possible that some ‘strains’ of Blastocystis are more
often associated with overt disease than others (Boorom
et al., 2008). The developmental cycle of Blastocystis is not
completely understood. It comprises a range of morphologically pleiomorphic stages and it is not clear whether
all are always represented and whether some are more
pathogenic than others.
Most attention on the clinical effects of zoonotic enteric
protozoa has focussed on infections in humans. Comparatively little is known about the clinical consequences of
infections in domestic animals and livestock.
Although infections with Giardia, and to a lesser extent
Cryptosporidium, are common in dogs and cats, infections
are usually asymptomatic (Thompson et al., 2008). Giardia infection in ruminants is also often asymptomatic, but
may also be associated with the occurrence of diarrhoea
and ill-thrift in calves (O’Handley et al., 1999; Geurden et
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al., 2006), as well as production losses (Olson et al., 1995).
In this respect, the effects of polyparasitism, with Giardia
as one member of an often diverse parasite community
in livestock (O’Handley and Olson, 2006), requires further
study. Infections with Cryptosporidium in calves can be clinically significant with profuse diarrhoea, depression and
anorexia, and is often life threatening in housed animals
where stress associated with overcrowding may predispose to disease (Thompson et al., 2008).
The impact of enteric protozoa on wildlife is not known,
but there is evidence of an association with clinical disease of infections with Giardia and Balantidium in primates
(Graczyk et al., 2002). The stress associated with captivity
may further predispose to disease, particularly in the case
of infections of Cryptosporidium in wildlife. This incredible
diversity of species and ‘strains’ of Cryptosporidium, Giardia and Balantidium in wildlife clearly warrants further
study in terms of their potential impact on wildlife health.
Habitat loss as a result of human encroachment can lead to
a variety of stressors (e.g. increased competition for food,
mates and refuge, as well as greater exposure to predators)
that may exacerbate the clinical consequences of infection
with enteric protozoa in wildlife (Thompson et al., 2010a;
Johnston et al., 2010; Howells et al., 2011).
6. Conclusions
Although tremendous advances have been made in
the development of molecular epidemiological tools, their
practical potential in terms of controlling enteric protozoan infections has yet to be realised. In both developed
and developing countries there has been little progress in
identifying risk factors for infection and understanding the
outcomes of infection. This is particularly so for the developing world where these infections are most common and
the frequency of infection very high. In such environments,
the epidemiology of diseases caused by enteric protozoa
is poorly understood in terms of transmission dynamics
and sources of infection. Importantly, we must not consider
enteric protozoan parasites in isolation in terms of impact
on their hosts. A child or dog, on good planes of nutrition,
harbouring a single infection with Giardia in a developed
country represents a very different host parasite relationship to that in a developing country where Giardia rarely
occurs as a single infection but is accompanied by several
other protozoa, nematodes and cestodes in an environment
usually deficient in some way, in terms of nutrients available to the host. Unravelling the interactions and impact on
their hosts in such circumstances is an important challenge
for the future.
Conflict of interest
The authors declare that there is no conflict of interest.
Acknowledgements
The Australian Research Council and Western Australian Department of Environment and Conservation have
supported some of the work reported here.
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