Echinococcus Granulosus

International Journal for Parasitology 44 (2014) 865877
Contents lists available at ScienceDirect
International Journal for Parasitology

journal homepage: www.elsevier.com/locate/ijpara
Invited Review
Echinococcus as a model system: biology and epidemiology

R.C.A. Thompson a,, D.J. Jenkins b,
a
b
School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA 6150, Australia
Animal and Veterinary Sciences, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia
a r t i c l e
i n f o
Article history:
Received 11 June 2014
Received in revised form 19 July 2014
Accepted 21 July 2014
Available online 11 August 2014
Keywords:
Echinococcus
Development
Cytodifferentiation
Hostparasite interface
Taxonomy
Epidemiology
Wildlife
Domestic hosts
a b s t r a c t
The introduction of Echinococcus to Australia over 200 years ago and its establishment in sheep rearing
areas of the country inicted a serious medical and economic burden on the country. This resulted in
an investment in both basic and applied research aimed at learning more about the biology and life cycle
of Echinococcus. This research served to illustrate the uniqueness of the parasite in terms of developmental biology and ecology, and the value of Echinococcus as a model system in a broad range of research,
from fundamental biology to theoretical control systems. These studies formed the foundation for an
international, diverse and ongoing research effort on the hydatid organisms encompassing stem cell
biology, gene regulation, strain variation, wildlife diseases and models of transmission dynamics. We
describe the development, nature and diversity of this research, and how it was initiated in Australia
but subsequently has stimulated much international and collaborative research on Echinococcus.
2014 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
1. Introduction
Echinococcus remains a major cause of zoonotic diseases of
public health and economic signicance (Jenkins et al., 2005b;
Budke et al., 2006; Davidson et al., 2012; Hegglin and Deplazes,
2013). Despite advances in control strategies, clinical management
and vaccine development, the parasite continues to thrive in countries throughout the world.
Hydatid disease, cystic and alveolar, is a typical cyclozoonosis
that can be perpetuated in nature in wild animal cycles without impacting on public health but with human interference
(Thompson, 2013), directly or accidentally, with spillover to
domestic cycles can lead to severe clinical disease and death. It is
also an important cause of economic losses to livestock industries,
particularly Echinococcus granulosus in sheep and cattle (Table 1).
It is now well known that Echinococcus has a two-host life cycle
with a sexual stage in the intestine of a carnivore denitive host
and a unique, cystic larval stage in the tissues of non-carnivorous
mammals and omnivores (Thompson, 1995). It is interesting that
much of the research that revealed the unique features of the parasites way of life were undertaken in Australia. This is not a coincidence and relates to the impact Echinococcus had on a developing
Tel.: +61 8 9360 2466; fax: +61 8 9310 4144 (R.C.A. Thompson). Tel./fax: +61 02
6933 4179 (D.J. Jenkins).
E-mail addresses: [email protected] (R.C.A. Thompson), djjenkins@
csu.edu.au (D.J. Jenkins).
agricultural society following early European settlement of a continent with huge temperate areas perfect to exploit for raising
livestock.
It was the upsurge in sheep farming at the end of the 19th
century, with expanding exports to Europe, that contributed to
the serious and largely undocumented human health problem that
existed during the late 19th and early 20th centuries (Gemmell,
1990). During the rst half of the 20th century, there was a high
incidence of cystic hydatid disease in Australia, and to a lesser
extent alveolar hydatid disease, either contracted in Australia
(E. granulosus) or in migrants from endemic areas overseas
(E. granulosus and Echinococcus multilocularis) (Dew, 1935). There
was thus a need for regular surgical intervention. It was surgeons
such as Harold Dew who had an interest in the basic biology of
the parasite and who published in international journals such as
the British Journal of Surgery and British Medical Journal that
led to widespread recognition of the research being undertaken
on hydatid disease in Australia. This was enhanced by Dews contributions in the literature (Dew, 1953) and at conferences to the
debate raging at the time on whether cystic and alveolar hydatid
disease were caused by the same or different species of Echinococcus (dualists versus monists) as well as his collaboration with
researchers in Europe such as Flix Dv.
Dew recognised the developmental differences of the two
stages in the life cycle and studied the metacestode stage of
the cystic and alveolar forms (Fig. 1) in depth, both in human
cases and animals (Dew, 1922, 1925, 1928, 1935). He thus
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866
R.C.A. Thompson, D.J. Jenkins / International Journal for Parasitology 44 (2014) 865877
Table 1
Current taxonomy of Echinococcus spp.
Species
Strain/genotype
Known intermediate hosts
Known denitive hosts
Infectivity to
humans
Echinococcus granulosus
Echinococcus equinus
Echinococcus ortleppi
Echinococcus canadensis
Echinococcus intermedius
Echinococcus felidis
Sheep/G1
Tasmanian sheep/G2
Buffalo/G3
Horse/G4
Cattle/G5
Cervids/G8,G10
Camel/Pig/G6/G7
Lion/
Dog, fox, dingo, jackal and hyena

Dog, fox
Dog
Dog
Dog
Wolves, dog
Dog
Lion
Yes
Yes
Yes
Probably not
Yes
Yes
Yes
Uncertain
Echinococcus
multilocularis
Echinococcus shiquicus
Echinococcus vogeli
Echinococcus oligarthrus
Some isolate
variation
/
None reported
None reported
Sheep (cattle, pigs, camels, goats, macropods)

Sheep
Buffalo
Horses and other equines
Cattle
Cervids
Camels, pigs, sheep
Warthog (possibly zebra, wildebeest,
bushpig, buffalo, various antelope, giraffe,
hippopotamus)
Rodents, domestic and wild pig, dog, monkey
Fox, dog, cat, wolf, racoon-dog,

coyote
Tibetan fox
Bush dog
Wild felids
Yes
Pika
Rodents
Rodents
Uncertain
Yes
Yes
Data from: Thompson et al. (1995), Thompson and McManus (2002), Jenkins et al. (2005b), Thompson (2008), and Carmena and Cardona (2014).
complemented much of Dvs research undertaken in rodents

(Dv, 1919, 1946) and built on this. Dew demonstrated that an
intact laminated layer was a fundamental and unique component
of the healthy hydatid cyst and considered this layer to be of host
origin, and demonstrated that elements of the cyst wall (germinal
layer) could regenerate (Dew, 1935). He realised that the cyst
enclosed a sterile environment and was under intracystic pressure,
and speculated on the reasons for this being indicative of viability
and a function of the germinal layer. In observations of what we
now know to be the metacestode of E. multilocularis, Dew
described naked prolongations of the nucleated germinal membrane (layer) in direct contact with host tissues (Dew, 1935), a fundamental feature of the inltrating metastatic metacestode of E.
multilocularis (Fig. 1) subsequently described using electron
microscopy 60 years later (Mehlhorn et al., 1983; and see Section 2.4). Thus it was Harold Dew that led to Australia being
referred to as the home of hydatids in terms of research. He paved
the way for other researchers and did much to establish Echinococcus as a model organism. In this country of Australia we all have
unrivalled opportunities to investigate this disease, both in man
and in animals, and it is our duty to contribute our share to future
advances in its study (Dew, 1935).
The economic impact and public health signicance of cystic
hydatid disease in Australia worsened over the next 30 years,
which provided an opportunity for obtaining research funds
from organisations supporting health and livestock research. J.D.
Smyth obtained funds from these sources and took a physiological
approach in his research aimed at increasing understanding of the
developmental biology of Echinococcus. Having forged an interest
in developing in vitro cultivation procedures for Schistocephalus
with success in establishing much of the life cycle of this cestode
in culture (Smyth, 1946, 1950), he turned his attention to Echinococcus (see Smyth, 1990) for which the ability to study and maintain the parasite in vitro would provide a great research tool for
investigating methods of control.
The practical and ethical difculties of undertaking in vivo
studies in the canid or felid denitive hosts of Echinococcus further
reinforced the need to develop in vitro systems. It was these pioneering studies of Smyth (Smyth et al., 1966 and reviewed in
Smyth and Davies, 1974a; Howell and Smyth, 1995) that demonstrated the potential of Echinococcus as a model for studying
principles of developmental biology, differentiation, hostparasite
relationships and evolutionary biology (Smyth, 1969; Smyth et al.,
1966), and which have inuenced research and theoretical understanding far beyond parasitology (Thompson and Lymbery, 2013).
Smyth saw the potential of exploiting Echinococcus as a novel
A
d
c
b
a
e
d
host tissue
adventitial layer
E. granulosus
laminated layer
germinal layer
vesicles
protrusions of
germinal layer
circulation
distant
metastatic
foci
E. multilocularis
Fig. 1. Diagrams illustrating the structural differences between the metacestodes of

(A) Echinococcus granulosus (ad, stages in development of protoscoleces and brood
capsule; e, daughter cyst) and (B) Echinococcus multilocularis (redrawn from
Thompson, 1995).
model system for studying parasitism as distinct from a model

for studies on evaluating anthelmintic or other anti-parasitic drugs
(Smyth, 1969). He thus expanded the denition of a model to
embrace studies on all the biological activities that supported the
867
parasite life style of Echinococcus, as well as the potential of this

model system for broader studies of a more fundamental nature
in biology, for example stem cells (Smyth, 1969, 1987). As such
the promotion of such a eukaryotic, metazoan model was at the
time somewhat of a rst.
Smyth worked closely with his Australasian colleague Michael
Gemmell, who also had an interest in Echinococcus but who was
keen to understand the epidemiology of hydatid disease, its economic impacts and impediments to control (Gemmell, 1990). As
such, he was the rst to apply mathematical models to Echinococcus and the concept of the basic reproductive rate (R0) in order to
dene the conditions under which transmission of Echinococcus
and other taeniids occur, and the regulatory role of immunity
(Gemmell, 1990; Gemmell and Roberts, 1995).
In this review, we describe the research, particularly that
undertaken in Australia, which has demonstrated the value of Echinococcus as a model system inuencing advances in biology and
epidemiology of parasites and parasitic infections.
studies of the importance of the host intestinal ecosystem in

providing the correct physical and physiochemical conditions
necessary to support fertilisation (Smyth, 1982; Smyth and
Davies, 1974a; Lymbery and Thompson, 1988, 2012; Lymbery
et al., 1989; Howell and Smyth, 1995).
The success with cultivating Echinococcus and the elucidation of
conditions that would support maturation stimulated studies on
other taeniids including Taenia pisiformis and Taenia crassiceps
(Esch and Smyth, 1976; Osuna-Carrillo and Mascar-Lazcano,
1982), as well as Mesocestoides corti (Barrett et al., 1982;
Thompson et al., 1982). These largely supported the observations
made with Echinococcus but also served to illustrate the uniqueness of the Echinococcus model system.
During the 25 years Smyth and his colleagues spent studying
and optimising strobilate development and maturation of Echinococcus in vitro, many valuable observations were made that have
served to establish Echinococcus as a model system not only in
terms of developmental biology, but also for cytodifferentiation
and the hostparasite interface.
2. Developmental biology
2.2. Developmental plasticity
2.1. Growth and maturation
Studies on the in vitro cultivation of Echinococcus from the

larval protoscolex to the adult worm demonstrated the inherent
plasticity of the parasite a phenomenon eloquently described
as heterogeneous morphogenesis (Smyth et al., 1967; Smyth,
1987), unique in most metazoan organisms apart from coelenterates such as Hydra, and making Echinococcus an unusual model
for differentiation studies. Depending upon the culture conditions,
protoscoleces can either develop in a cystic or adult direction. Cystic development itself may take a variety of paths, again inuenced
by environmental conditions. These alternative developmental
pathways have been described in detail by Howell and Smyth
(1995). Protoscoleces can also develop into an adult tapeworm
under different conditions to those supporting cystic development,
most importantly the need for a diphasic medium incorporating a
solid supporting substrate thought to provide nutrients and/or a
contact stimulus (see Section 2.1). However, observations on the
development of adult E. granulosus and E. multilocularis demonstrated that in addition to normal worms, cultures often contained worms that had matured but not segmented (monozoic)
and worms with more than one scolex and other malformations
(reviewed in Howell and Smyth, 1995). Interestingly, adult worms
that have developed from protoscoleces can de-differentiate in a
cystic direction under adverse conditions (see Sections 2.3 and
2.4; Smyth, 1969; Thompson and Lymbery, 1990; Thompson
et al., 1990). These observations raised two important and fundamental questions: how is this complex and plastic development
controlled and what cells have the potential to develop in such a
myriad of different routes?
Echinococcus has two developmental stages in its life cycle; the

adult tapeworm, which is the sexual stage, and the cystic or inltrative larval metacestode that reproduces asexually (Fig. 1). The
metacestode of E. granulosus, which was easily accessible from
infected livestock in the abattoir or from human surgical cases,
was the logical starting point for experimental manipulations. Initially, these were undertaken in rodents where the asexual proliferative nature of the parasite was rst observed, a phenomenon
that was subsequently exploited with the development of rodent
models of secondary hydatidosis (Dv, 1919). These provided a
means to maintain the parasite virtually indenitely in vivo by
serial passage (e.g., Thompson, 1976; Whiteld and Evans, 1983;
Kamiya et al., 1985).
Although a number of workers had reported vesicular/cystic
development and proliferation of protoscoleces in vitro, a major
goal was to provide appropriate conditions to stimulate and support development in an adult (strobilate) direction. It was not until
Smyth and his colleagues rened procedures with the aim to
reproduce the conditions that protoscoleces would be exposed to
in the gut of the denitive host that strobilate development was
obtained (Smyth et al., 1966). Smyth took a physiological approach
to this research, with the cyst as a starting point. Its sterile environment provided the perfect entry point if accessed aseptically to
carefully remove essentially dormant invaginated protoscoleces
and then expose them to appropriate physiochemical conditions
(Smyth and Davies, 1974a). Of particular signicance was the
provision, in addition to the liquid medium, of a solid proteinaceous base in the culture ask (diphasic medium) which was found
to be important in stimulating proglottisation and segmentation in
E. granulosus with maturation to the pre-fertilisation stage
(reviewed in Smyth and Davies, 1974a; Howell and Smyth,
1995). Similar results were obtained with E. multilocularis but
proglottisation without segmentation will take place without a
solid proteinaceous base (Smyth and Davies, 1975; Smyth, 1979;
Thompson et al., 1990). This and other developmental abnormalities observed in E. multilocularis were considered to reect a difference in gene expression between the two species (Howell and
Smyth, 1995 and see Section 2.3). Although the conditions developed supported reproducible strobilate development, fertilisation
and egg production eluded Smyth and other workers. However,
they served to emphasise the complexity of the process and to
support observations made from in vivo and population genetic
2.3. Developmental control

Smyth developed a hypothetical yet logical model to explain
how genes regulate differentiation and developmental shifts in
Echinococcus (Smyth, 1969). This was based on the JacobMonod
model of genetic expression and showed the complex interactions
and regulatory switches that may be involved in controlling development and differentiation in Echinococcus. Since then a number of
studies have isolated and characterised regulatory genes from Echinococcus (reviewed in Thompson, 1995 and Parkinson et al., 2012)
but how they t together in a control network has yet to be determined. Recently, Parkinson et al. (2012) identied long non-coding
(nc)RNAs that may be involved in the regulation of gene expression
in response to environmental cues in the host. They also identied
a number of genes reecting specicities of particular stages,
868
including those whose expression is up-regulated by pepsin-acid

activation. It is to be hoped that Smyths models will help to provide functionality to the genomic data that is now available for
both E. granulosus and E. multilocularis (Tsai et al., 2013; Zheng
et al., 2013). However, differences in development between E.
granulosus and E. multilocularis highlighted by studies in vitro are
considered to reect differences in the control of gene expression
(Howell and Smyth, 1995).
2.4. Cytodifferentiation
Slais (1973) demonstrated that the post-oncospheral development of Echinococcus was initiated by the growth and division of
primary germinal cells, and Swiderski (1983) described ve pairs
of these cells in the posterior pole of the oncosphere. Observations
on the development of Echinococcus in vitro demonstrated that the
fundamental processes of germinal and somatic differentiation,
comprising cystic development, proglottisation, maturation,
growth and segmentation (strobilisation), can take place independently. This not only illustrated the complexity of cytodifferentiation but also the possible existence of several primitive cell lines.
However, to date all the evidence suggests that only one primitive
morphological cell type exists as a pool of uncommitted, undifferentiated multipotent germinal, or stem, cells in both the adult and
metacestode (Smyth, 1969; Gustafsson, 1976; Thompson et al.,
1990; Thompson, 1995; Koziol et al., 2014). The undifferentiated
germinal cells are a component of the syncytial germinal layer of
the metacestode and neck region of the adult cestode. Ultrastructural studies reveal unremarkable rounded cells of variable size
of approximately 4 lm diameter (Gustafsson, 1976; Mehlhorn
et al., 1983; Albani et al., 2010). Cell proliferation derives from
the continuous replicative activity of these dividing stem cells
located in the germinal layer or neck region of the adult tapeworm
(Gustafsson, 1976; Galindo et al., 2003). They have considerable
proliferative potential (Eckert et al., 1983; Mehlhorn et al., 1983;
Galindo et al., 2003; Martnez et al., 2005), and are the only proliferating cells in Echinococcus (Koziol et al., 2014). This is particularly
well illustrated by the capacity of the parasite for indenite perpetuation in the larval stage by passage of protoscoleces or germinal
layer material in rodents (secondary hydatidosis; Howell and
Smyth, 1995). In alveolar hydatid disease caused by the metacestode of E. multilocularis, the proliferating larval parasite has an
inltrative capacity to establish distant foci of infection due to
the distribution via blood or lymph of detached germinal cells
(Ali-Khan et al., 1983; Eckert et al., 1983; Mehlhorn et al., 1983;
Fig. 1).
Problems with host cell contamination dogged early attempts
to establish germinal cell lines of E. granulosus and E. multilocularis
(reviewed in Howell and Smyth, 1995). In addition, their isolation
from the germinal layer, and their in vitro propagation, could have
been hampered by the fact that the germinal layer is a syncytium.
However, the establishment and long-term perpetuation of Echinococcus germinal cells has now been achieved for both species
(Yamashita et al., 1997; Spiliotis and Brehm, 2009; Spiliotis et al.,
2008; Albani et al., 2010). The germinal cells behave similarly to
classical stem cells with the formation of cell aggregates and clusters with cavity formation, and there is cytological evidence of
transformation (Spiliotis et al., 2008; Albani et al., 2013).
Galindo et al. (2003) found evidence of the regionalisation of
DNA and protein synthesis in developing stages of Echinococcus,
although no morphological evidence has been found of different
primitive or germinal cell lines to explain the concept of heterogeneous morphogenesis (Smyth, 1969). However, such heterogeneity
has now been conrmed at the molecular level. Germinal cells are
in fact heterogeneous, with the existence of subpopulations with
different gene expression patterns (Koziol et al., 2014), thus conrming Smyths predictions.
2.5. Hostparasite interface
2.5.1. Denitive host
Observations that contact of the scolex with a proteinaceous
base stimulated strobilate development in E. granulosus led to
studies on the nature of the interface both in vitro and in vivo,
and the discovery of the rostellar gland which comprises a modied group of tegumental cells situated in the apical rostellum
(Smyth, 1964; Smyth et al., 1969; Thompson et al., 1979;
Thompson and Eckert, 1983; Fig. 2). The rostellar gland releases
secretory material by a holocrine process into the interface
between parasite and host (Thompson et al., 1979). The origin
and site of synthesis of the secretion has still to be determined,
although large amounts occur in both the perinuclear and distal
cytoplasm of the tegument as well as in the tegumental nuclei
(Thompson et al., 1979; Herbaut et al., 1988). The secretion is proteinaceous, containing cystine and lipid. It is not known if there are
one or more proteins secreted but Siles-Lucas et al. (2000) demonstrated that the secretion contains a regulatory protein (14-3-3)
that is released into the hostparasite interface.
The rostellar gland of Echinococcus is seemingly unique to
Echinococcus. Although rostellar secretions have been described
in larval T. crassiceps (Krasnoshchekov and Pluzhnnikov, 1981),
no gland has been described. Rostellar glands have been described
in other adult cestodes, particularly proteocephalids, but their
function is also unclear and structurally they are different to the
rostellar gland in Echinococcus (McCullough and Fairweather,
1989; Zdrsk and Nebesrov, 2003). There is clearly a need for
more studies on the interface of attached adult cyclophyllidean
cestodes (Pospekhova and Bondarenko, 2014).
This intimate association of the rostellar gland and its
secretions suggests a role(s) that enhances the hostparasite
relationship in favour of the parasite, which may be regulatory,
nutritional and/or protective. The relationship between rostellar
gland activity and localised humoral and cellular reactions
(Deplazes et al., 1993) is not known but such localised reactions
demonstrate stimulation of host immune effector mechanisms.
The secretory molecules would seem to be obvious candidates
for exploitation in vaccine studies since a focus on prophylaxis of
the denitive host may be more attractive than the intermediate
host, particularly for the control of E. multilocularis, from both commercial and practical perspectives. As pointed out by Heath (1995)
the scolex is in intimate contact with the systemic circulation even
in the Peyers patches and would appear to maintain its privileged
integrity by suppression of cytotoxic and effector cell activity in
the region of the scolex.
The few studies on denitive host vaccines do not seem to have
targeted rostellar gland secretions and have produced results
which are controversial and open to contrasting interpretation
(Zhang et al., 2006; Petavy et al., 2008; Torgerson, 2009;
Kouguchi et al., 2013). The studies by Petavy et al. (2008) demonstrated a strong inammatory response in the intestine of vaccinated compared with infected controls but did not show if this
was localised to where worms were situated. More recently,
Kouguchi et al. (2013) used a surface glycoprotein from E. multilocularis as a vaccine in dogs which induced signicant protection
when administered via a mucosal route and demonstrated antibodies raised by their vaccine on the surface of the suckers, rostella
and hooks. These results emphasise the importance of characterising the secretions produced by the rostellar gland of Echinococcus
which will contribute to the further development of vaccines
against the adult parasite. Unfortunately in vivo studies require
research on the denitive host, usually dogs, which is ethically
869
Fig. 2. Diagram illustrating adult Echinococcus in situ in the intestine, with suckers on the scolex grasping the epithelium at the base of the villi. Rostellum is deeply inserted
into a crypt of Lieberkhn (A, B) and extensibility of the apical rostellar region is shown in B. Rostellar gland with secretory material is anterior to the rostellar pad (r).
challenging and hazardous if patent infections are maintained.

Thus reports of successful patent infections in experimentally
infected immunosuppressed rodents (Kamiya and Sato, 1990a,b)
were regarded as an important breakthrough (Howell and Smyth,
1995; Thompson, 1995). Unfortunately, these results have not
been further exploited and should perhaps form the basis for
future research.
2.5.2. Intermediate host
A unique interface is also found in the intermediate host where
the laminated layer presents a physiochemical barrier with apparent multifunctionality and a structure whose biosynthesis has
become a model system for carbohydrate chemistry (Diaz et al.,
2011a,b; Parkinson et al., 2012). The laminated layer is a specialised extracellular matrix unique to Echinococcus (Fig. 1), whose
synthesis is a major metabolic activity of the much thinner germinal layer (Diaz et al., 2011a; Lin et al., 2012; Parkinson et al., 2012).
The origin of the laminated layer was controversial for some time,
i.e. whether it is entirely of parasite origin or if there is a host contribution. Holcman and Heath (1997) demonstrated that it is
entirely of parasite (germinal layer) origin by studying the early
stages of cyst development from oncospheres in vitro.
Considerable metabolic activity in the germinal layer is
required to synthesise and maintain the interfacial barrier of the
laminated layer (Parkinson et al., 2012). The role of the laminated
layer would appear to be one of protection since cyst survival is
dependent upon its integrity (Gottstein et al., 2002). Whether this
is purely physical or if there is selective permeability is not known.
Monteiro et al. (2010) identied several molecules in hydatid cyst
uid that could play a role in host evasion. Smyth commented on
the signicance of the presence of a human blood group P-like substance in the laminated layer of Echinococcus and its signicance as
a model system in better understanding the immunological basis
of the host-parasite relationship. This P1 blood-antigen motif has
since attracted much attention and has been further characterised
as a protein-carbohydrate, trisaccharide/mucin complex containing galactosamine, yet no biological function has been described
to date (Lin et al., 2012). There is also increasing evidence of the

immune-regulatory role of the laminated layer, probably in association with the immuno-modulatory activities of the glycoproteins
known as Antigen 5 and Antigen B (Diaz et al., 2011b).
2.6. Taxonomy and speciation
One of the most important observations made as a result of
studies on the in vitro cultivation of Echinococcus was the failure
of protoscoleces collected from hydatid cysts in horses to develop
in the same way as those of sheep origin. Protoscoleces from horses
evaginated and increased in length but failed to undergo proglottisation or segmentation, even though they were grown in exactly
the same diphasic medium (Smyth and Davies, 1974b). This fairly
simple observation resulted in radical shifts in our understanding
of the epidemiology of hydatid disease and transmission of the
aetiological agents as well as their taxonomy and phylogenetic
relationships. The results demonstrated that there were fundamental physiological differences between E. granulosus of sheep
and horse origin and the coining of the term physiological strain
differences (Smyth and Davies, 1974b; Smyth, 1982). This had a
broad inuence beyond Echinococcus, and in particular the importance of combining phenotypic and genetic differences in the characterisation and description of parasites at the intraspecic level
(Thompson and Lymbery, 1990, 1996; Lymbery and Thompson,
2012).
In terms of Echinococcus, the observation of physiological
differences between the two parasites of sheep and horse origin
complemented earlier epidemiological and taxonomic studies on
Echinococcus of horse origin (Williams and Sweatman, 1963). These
demonstrated morphological differences between the two forms
which were considered to be taxonomically signicant, and to
reect differences in host specicity and the life cycles which
maintained the two parasites. This was subsequently shown to
be correct with the sympatric occurrence of distinct sheep- and
horse-dog cycles in several European countries (Thompson and
Smyth, 1975; Thompson, 2001; Gonzalez et al., 2002). In addition,
870
epidemiological evidence has not only demonstrated distinct differences in intermediate host specicity but also that, unlike the
sheep strain (E. granulosus), the horse strain (Echinococcus equinus)
(Table 1) does not appear to be infective to humans (Thompson
and Lymbery, 1988, 1991).
The concept of host-adapted strains of E. granulosus led to studies on other forms of the parasite in other species of intermediate
hosts such as cattle, pigs, camels and cervids. These studies not
only conrmed the existence of a number of host-adapted life
cycles in different parts of the world but also provided additional
data on developmental differences between strains which may
impact on control (reviewed in Thompson and Lymbery, 1988;
Thompson et al., 1995; Thompson, 2008).
Subsequent molecular characterisation of host-adapted strains
of Echinococcus, coupled with molecular epidemiological studies in
endemic areas, has conrmed their genetic and morphological distinctness and revealed phylogenetic relationships which support a
robust, meaningful taxonomy based on a previously suggested
nomenclature (Table 1; Bowles et al., 1994; Thompson et al., 1995,
2006; Cruz-Reyes et al., 2007; Harandi et al., 2002; Thompson and
McManus, 2002; Lavikainen et al., 2003; Jenkins et al., 2005a;
Romig et al., 2006; Moks et al., 2008; Thompson, 2008; Huttner
et al., 2009; Saarma et al., 2009; Nakao et al., 2013). Interestingly,
the nomenclature used for these species conforms to that proposed
by observational parasitologists in the 1920s1960s, before molecular tools were available to conrm their morphological descriptions and epidemiological observations (Thompson et al., 1995;
Thompson and McManus, 2002; Thompson, 2008).
(Gemmell, 1990). Domestically, the parasite spread rapidly

through sheep and dog populations (Gemmell, 1990), due mainly
to a complete lack of understanding of the association between
taeniid tapeworms in dogs and cysts in sheep. It was not until
1851, (63 years after the rst European settlers and their animals
arrived in Australia) that infection experiments were undertaken,
demonstrating the relationship between cysts and tapeworms.
Kchenmeister, working in Germany, fed metacestodes of T. pisiformis to foxes and obtained tapeworms (Kchenmeister, 1851)
and in 1853 fed tapeworm eggs to sheep and obtained metacestodes. In the next few years von Siebold and Kchenmeister, working independently, fed protoscoleces of Echinococcus to dogs and
obtained tapeworms (von Siebold, 1853; Kchenmeister, 1855).
An additional important infection experiment, also undertaken in
Germany, was that of Naunyn in 1863 who fed protoscoleces from
a human cyst to dogs and obtained adult E. granulosus, reporting
his results the same year. This experiment demonstrated for the
rst time the association between hydatid cysts of sheep and
humans and the role of dogs in the life cycle of human hydatidosis.
However it was not until 1876 that Leuckart demonstrated eggs of
Echinococcus when fed to intermediate hosts (pigs) led to the
development of hydatid cysts (Leuckart, 1876). A detailed review
of the elucidation of the Taenia and Echinococcus life cycles can
be found in Grove (1990). Word of these discoveries took time to
reach Australia but it was not long before experimental studies
were undertaken in Australia that conrmed Naunyns data
(Thomas, 1884).
Hydatid disease soon became a major public health problem in
the growing population of new Australians (Gemmell, 1990) causing serious illness and leading to the deaths of many colonists.
3. Epidemiology of E. granulosus in Australia

3.2. Wildlife hosts of E. granulosus in Australia
3.1. Introduction
Much of the basic knowledge regarding the epidemiology and
control of E. granulosus in Australia was generated by Michael
Gemmell. His contribution to the eld has been immense; the
breadth of his studies were wide, covering the impact of climate
on egg longevity, immune responses against the parasite in denitive and intermediate hosts, prevalence in domestic dogs and livestock, studies on infection in wildlife and mathematical modelling
of transmission as an aid to more effective control (Gemmell and
Lawson, 1986). Gemmells work has provided a solid platform for
many of the current studies reviewed below. However, probably
his greatest legacy was his contribution to the development of
strategies for the control of E. granulosus transmission. Nevertheless, in the Australian situation, although control of E. granulosus,
domestically, has largely been achieved (Jenkins et al., 2014), the
presence of an extensive wildlife reservoir on mainland Australia
ensures the compete eradication of E. granulosus is unlikely to ever
become a reality. Further, unlike the situation with E. multilocularis
and Echinococcus canadensis which are maintained in natural wildlife cycles, the wildlife cycle in Australia is an articial one established as a result of anthropogenic activities and spillover from
domestic cycles (Thompson, 2013).
The work of Gemmell had broad ramications internationally in
terms of the epidemiological principles of hydatid control. Many
subsequent hydatid control programmes world-wide looked at
Gemmells critical analysis of the epidemiology in Australia and
New Zealand and based their programmes on his data. These
served as a foundation for the development of control programmes
in many countries, and the epidemiological principles he developed similarly have been used as a model (Eckert et al., 2001).
Echinococcus granulosus is the only member of the genus to
occur in Australia, having been introduced with domestic dogs
and livestock, mainly sheep, during European settlement
Data generated in studies on wildlife in Australia have worldwide relevance, an example being the work of Barnes (Barnes
et al., 2007a,b, 2008, 2011) investigating the health impacts and
growth rate of hydatid cysts in macropodids. Barnes showed that
hydatid cysts have a major impact on respiration capacity in macropods, indicating infected animals to be more susceptible to predation by wild dogs. This work complements and validates the
studies of Mech (1966) and Jolly and Messier (2004) in the USA
with respect to the impact of hydatid disease on moose (Alces
alces), rendering infected animals more susceptible to predation
by wolves (Canis lupus). Another good example is the study on
the encroachment of E. granulosus-infected foxes (Vulpes vulpes)
and wild dogs into urban areas in Australia and associated public
health implications (Jenkins and Craig, 1992; Jenkins et al.,
2008). These studies complement and support work undertaken
in Europe with the encroachment into urban centres of foxes
infected with E. multilocularis (Deplazes et al., 2004) and studies
in Alberta, Canada on E. multilocularis in urban coyotes (Canis
latrans) (Catalano et al., 2012).
Australian native wildlife species evolved in isolation from
E. granulosus; consequently, they were highly susceptible to infection with this new parasite and wildlife species were soon acting as
a major sylvatic reservoir for the perpetuation of E. granulosus in
Australia (Durie and Riek, 1952), a situation that prevails today
(Jenkins and Morris, 2003).
Initially, transmission of E. granulosus to macropodids occurred
through accidental consumption of eggs spread in the environment
by the dogs of colonists. Infection in dingoes eventuated through
predation of sheep on the recently established sheep farms. However, it would not have been long before the dingoes themselves
began to spread eggs throughout their territories, exposing an ever
increasing population of macropodids to infection with hydatid
disease. Transmission of E. granulosus to wildlife from domestic
animals in the more remote areas of Australia was likely to have

been enhanced through transhumance grazing (King, 1959). Transhumance grazing was undertaken for over 100 years in the states
of New South Wales and Victoria, with the last Snow Lease in
New South Wales being revoked in 1972. In this process hundreds
of thousands of sheep (and tens of thousands of cattle), accompanied by drovers and their dogs, were moved to the higher altitudes
of the Great Dividing Range each summer to graze the alpine pastures. This was a highly organised process where families leased
dened areas of pasture for their animals to graze for 3 - 4 months
each year. Therefore, annually these pastures would have become
contaminated with eggs from infected sheep dogs acting as a
source of infection of both sheep and macropodids. Dingoes would
have been infected through predating on sheep and opportunist
scavenging of dead sheep and offal discarded by the drovers when
they killed a sheep to eat whilst staying on the lease.
3.2.1. Dingoes
The Australian wildlife top-order predator coincidentally was a
placental canid, the dingo (Canis lupus dingo), introduced from
south-eastern Asia by visiting seafarers (Corbett, 1995). Dingoes
were medium sized wild dogs (1117 kg) capable of killing sheep.
Settlers moving to Australia also brought their domestic dogs
and it soon became evident that dingoes were able to breed with
domestic dogs and produce fertile hybrid offspring. The result
has been that currently in most areas of remaining suitable habitat
in south-eastern and eastern Australia the resident top order predator populations no longer consist of pure-bred dingoes but mainly
dingo/domestic dog hybrids with occasional pure-bred dingoes
(Claridge et al., in press). Animals in these populations are referred
to as wild dogs. Pure-bred dingoes are mostly restricted to remote
areas, especially in northern parts of Western Australia. Nevertheless, there is no indication that hybrid dingoes are any more or less
susceptible to infection with E. granulosus than pure-bred animals
since no difference in the range of worm burdens has been noted
between hybrid and pure-bred dingoes (Jenkins and Morris,
2003; Jenkins et al., 2008). The hunting and pack behaviours of
dingo hybrids compared with dingoes also appear to be similar
(Claridge et al., in press). The one important physiological difference between dogs and dingoes is breeding capacity; female
domestic dogs come into oestrus twice each year whilst for dingoes it is only once. Data collected on the breeding behaviour of
dingo hybrids does not indicate they are having more litters per
year than pure-bred dingoes, but there have been reports that litter
sizes in hybrids are larger than those of pure-bred dingoes and the
size of wild dogs has increased approximately 20% during the last
40 years (Claridge et al., in press).
Anecdotally, in many areas wild dog population numbers
appear to be increasing, a likely combination of increased litter size
and increased food resources due to environment modication.
Provision of more pasture and watering points for livestock has
led to major increases in macropodid populations in many areas,
providing increased food supply for wild dogs. With increased wild
dog populations it is reasonable to assume that the biomass and
rate of transmission of E. granulosus in wildlife is also increasing.
3.3. Echinococcus granulosus-infected wild dog encroachment into
urban areas
With increasing wild dog numbers and the spread of urbanisation into areas of hitherto wild dog habitat has displaced young
and old animals seeking new uncontested habitat. These animals
are encroaching into outer urban areas and bringing E. granulosus
with them (Brown and Copeman, 2003; Jenkins et al., 2008).
Reports of E. granulosus-infected wild dog encroachment into
outer suburban areas have begun to appear; Townsville (Brown
871
and Copeman, 2003), Maroochy Shire (Jenkins et al., 2008), the

north-western suburbs of Brisbane in the Pine River Shire, Queensland and the outer suburbs of Katoomba in New South Wales (D.J.
Jenkins, unpublished data). In a number of urban areas, wild dogs
have become numerous and a public nuisance raiding garbage
bins, killing domestic pets and menacing residents. They have
become such a problem in a number of places that local authorities
have employed professional wild dog controllers to remove them
using lethal methods. Examination of the intestines of some of
these euthanised wild dogs from several locations has revealed
high prevalences and heavy worm burdens of E. granulosus
(Brown and Copeman, 2003; Jenkins et al., 2008). The establishment of peri-urban transmission cycles are unlikely, but regular
encroachment of E. granulosus-infected wildlife denitive hosts
into outer suburbs of urban centres has been demonstrated
(Brown and Copeman, 2003; Jenkins et al., 2008), which is difcult
to control and likely to be an ongoing issue for local councils to
manage.
Hitherto, it was supposed urban human populations in Australia
were insulated from exposure to E. granulosus, and clearly, with the
encroachment of E. granulosus-infected wild dogs (and foxes, see
Section 3.7.1) into urban areas this is no longer the case.
3.4. Australian native carnivores as denitive hosts for E. granulosus
Infection with adult E. granulosus has never been reported from
Australian native marsupial carnivores. In 2005, Jenkins et al.
undertook a small study investigating the faeces from wild-caught
spotted-tailed quolls (Dasyurus maculatus) for coproantigens of E.
granulosus and reviewed the literature regarding experimental
infection of dasyurids with E. granulosus. None of the quoll faeces
tested were found to be positive for coproantigens of E. granulosus
(Jenkins et al., 2005a) and in none of the attempted experimental
infections of several species of dasyurid have E. granulosus been
recovered. From these data, Jenkins et al. (2005a) concluded that
dasyurids are refractory to infection with E. granulosus.
3.5. Wildlife intermediate hosts
Macropodid marsupials are highly susceptible to infection with
the intermediate stage of E. granulosus (Jenkins and Morris, 2003;
Banks, 2006), often carrying multiple large metacestodes (hydatid
cysts). This is especially the case in a number of wallaby species,
namely swamp wallabies (Wallabia bicolor) in south-eastern Australia (Jenkins and Morris, 2003). Swamp wallabies are commonly
infected with E. granulosus (Jenkins and Morris, 2003) and are also
a favourite dietary item for wild dogs (Claridge et al., in press),
making them pivotal in the transmission of E. granulosus in wildlife
in south-eastern Australia. Other wallaby species appear to be of
similar importance in other parts of Australia (Banks et al., 2006a).
Curiously, on the island state of Tasmania macropodid marsupials never become infected with E. granulosus (Howkins, 1966),
despite there having been high levels of transmission in domestic
animals. This may have been associated with the absence of
dingoes and the presence of a dasyurid top order predator, the
thylacine (Thylacine cynocephalus), refractory to infection with
E. granulosus (see Section 3.4). Nevertheless, human hydatidosis
became such a major public health problem in Tasmania that a
program of intense control was introduced that continued for
30 years (Beard et al., 2001).
Other species of native wildlife susceptible to infection with E.
granulosus are wombats (Wombatus ursinus). However, hydatid
infection in wombats has only been reported once (Grainger and
Jenkins, 1996). Wombats are consumed periodically by wild dogs
but appear to only be an occasional host for E. granulosus, therefore
872
they cannot be regarded as an important component of the E. granulosus life cycle in Australia.
3.6. Factors contributing to the transmission success of E. granulosus in
Australian wildlife
Hydatid disease of macropodids is almost exclusively conned
to the lungs, causing major respiratory impairment (Jenkins and
Morris, 2003; Barnes et al., 2007a,b, 2008, 2011) that may lead to
the death of the host (Johnson et al., 1998; Barnes et al., 2008).
Why hydatid infection in macropods should be mainly conned
to the lungs is unclear, however, this is also seen with hydatid
infection in cervids (Schantz et al., 1995). Hydatid-infected macropodids are rendered highly susceptible to predation by dingoes, a
similar situation to that with the interaction of wolves and hydatid-infected moose (A. alces) in the USA (Mech, 1966; Jolly and
Messier, 2004). In addition, cysts in macropodids develop quickly,
becoming fertile (containing protoscoleces) in 89 months (Barnes
et al., 2007a), compared with sheep where the earliest time to fertility is approximately 2 years (Slias, 1980). The increased susceptibility of hydatid-infected macropodids to predation by wild dogs
means that wild dogs are catching and consuming a disproportionately large number of infected animals which is likely to be a major
contribution to the high worm burdens seen in many wild dogs.
Within all wild dog populations surveyed, a proportion of the
sample has been wild dogs with worm burdens in excess of
100,000 E. granulosus (Jenkins and Morris, 1991, 2003; Jenkins
et al., 2008). These animals are the super spreaders of the population (Gemmell and Lawson, 1986), ensuring large numbers of
eggs being released into the environment. The home range of wild
dogs varies depending on the sex of the animal and availability of
food and water; in eastern Australia home ranges average approximately 100 km2 (Claridge et al., in press). Therefore large areas can
become contaminated with eggs from a single animal, but since
packs of wild dogs consisting of several animals usually occupy
these spaces (Claridge et al., in press), contamination of the environment with faeces can become heavy in areas used commonly
by a resident pack.
The longevity of eggs of E. granulosus in the environment is
thought to be several months to perhaps approximately 1 year,
so long as the environment is not too hot and dry (Eckert and
Deplazes, 2004). However, in a study in Argentina (Thevenet
et al., 2005), E. granulosus egg-laden dog faeces were left in the
environment for 41 months. After this time eggs were separated
from the faeces and fed to each of four sheep. Hydatid cysts developed in each of the sheep, suggesting that the longevity of eggs of
E. granulosus in Australia under optimal conditions may be longer
than 12 months. Studies reported in Gemmell (1958) revealed
the most important environmental conditions required for transmission for E. granulosus in Australia to be at least 25 mm of rain
for 6 months of the year with temperatures up to 30 C. Consequently, E. granulosus has become more prevalent in eastern Australia, in areas associated with the Great Dividing Range, and in
an elevated area of Western Australia (Thompson et al., 1988;
Jenkins and Macpherson, 2003) (Fig. 3).
3.7. Echinococcus granulosus in introduced wildlife species
3.7.1. Foxes
The rst creditable report of E. granulosus infection in foxes in
Australia was by Gemmell (1959a) where a single terminal
segment was recovered from the intestine of one of 41 animals
collected in New South Wales. Nevertheless, based on the available
experimental infection and survey data, Gemmell (1959a) felt that
Australian foxes were not acting as a denitive host for E. granulosus. More recently, E. granulosus have been recovered from a
number of naturally infected foxes in various studies (Thompson

et al., 1985; Obendorf et al., 1989; Jenkins and Craig, 1992;
Reichel et al., 1994; Jenkins and Morris, 2003). Almost exclusively,
worm burdens have been small, usually less than 50 tapeworms/
fox. However, in one study (Reichel et al., 1994) several thousand
E. granulosus in each of two foxes from Victoria were reported.
These data are so at odds with all other existing fox E. granulosus
worm burden data that they should be regarded cautiously. However, if corroborated then the role of foxes in the transmission of E.
granulosus may have to be re-evaluated. The current consensus is
that foxes act as denitive hosts for E. granulosus but are of minor
importance in the transmission of the parasite in rural areas of
Australia. However, foxes infected with E. granulosus are of potential public health importance when infected animals encroach into
urban areas (Jenkins and Craig, 1992).
3.7.2. Feral cats
Infection of Australian feral cats with adult E. granulosus has
never been reported. Jenkins and Morris (2003) examined the
intestines of 23 feral cats collected in an area of high E. granulosus
transmission in the local wildlife and none was found infected. Jenkins also fed protoscoleces recovered from a wallaby to two cats
and two fox cubs, and small numbers of E. granulosus were recovered from both foxes but nothing was found in the cats (D.J. Jenkins, unpublished data). It is generally considered that feral cats
in Australia are not denitive hosts for E. granulosus.
3.7.3. Feral pigs, goats, deer, horses and rabbits
Hydatid disease occurs in Australian feral pigs (Jenkins and
Morris, 2003; Lidetu and Hutchinson, 2007). The study of Jenkins
and Morris (2003) was conducted in south-eastern New South
Wales; 204 pigs were examined, 22.5% contained hydatid cysts
and depending on the survey area between 15 and 22% of the cysts
were fertile. In contrast, the study of Lidetu and Hutchinson (2007)
was conducted in tropical northern Queensland; 74 pigs were
examined and 31.1% contained hydatid cysts, but the rate of fertility
was almost three times that of the pigs collected in New South
Wales. The reason for this difference in cyst fertility is unclear. There
is no doubt feral pigs could contribute to transmission of E. granulosus in wildlife but the degree to which they contribute is debatable.
Adult feral pigs (the animals most likely to harbour fertile cysts) are
big and strong and difcult for wild dogs to catch and kill; consequently, wild dogs mainly predate on piglets, animals least likely
to contain fertile cysts. Inevitably, adult pigs eventually die and
their carcasses become available for scavenging by wild dogs and
foxes. However, particularly in summer, scavengers would need to
nd the carcass soon after death before fertile cysts became noninfective due to putrefaction. Therefore, the role of pigs in the transmission of E. granulosus in Australian is likely to be minor.
Hydatid infection in goats has never been reported except for an
anecdotal report from Western Australia (R.C.A. Thompson, unpublished data). Periodically, one of the current authors (D.J. Jenkins)
has examined small numbers of feral goats, collected from various
areas of south-eastern New South Wales, and has never found any
infected with hydatid cysts (D.J. Jenkins, unpublished data). The
absence of hydatid infection in Australian feral goats is curious
because in many countries goats are important intermediate hosts
(Schantz et al., 1993).
Hydatid cysts have never been reported from feral horses or
deer in Australia. Therefore, until data to the contrary are available,
feral goats, deer and horses appear not to be part of the lifecycle of
E. granulosus in Australia.
Rabbits naturally infected with hydatid disease have rarely
been reported. The two reports, (cited in Gemmell, 1959b) are
thought to be a mis-identication of metacestodes of Taenia
serialis. Wild Australian rabbits have been shown to be susceptible
873
Fig. 3. Map depicting areas of high, low, rare and no transmission of Echinococcus granulosus in Australia (red, high transmission; orange, low transmission; beige, rare
transmission; grey, no transmission). (Modied version of the map published by Jenkins and Macpherson (2003)).
to experimental infection with hydatid disease (Jenkins and

Thompson, 1995). The cysts established in the lungs and appeared
to be developing normally. However, the rabbits were given a large
dose of eggs, far higher than anything they would normally be
exposed to in the wild, which may have been the reason they
became infected.
3.8. Current prevalence of E. granulosus in Australian domestic dogs,
sheep and cattle on mainland Australia and the island state of
Tasmania
3.8.1. Dogs
The most recently published study on intestinal helminths in
Australian mainland dogs is that of Palmer et al. (2008) where
1400 faecal samples collected in vet clinics were sent to the authors
for testing. These samples were from urban dog owners with a close
interest in the health of their pets; unsurprisingly, no taeniid
cestodes were identied in any of the samples collected. The most
recent study of intestinal helminths in rural dogs (Jenkins et al.,
2014) screened faeces from 1425 rural dogs living in eastern Australia (1119 mainland; 306 Tasmania) with faecal otation, molecular methods and the E. granulosus coproantigen test (Jenkins et al.,
2000). Surprisingly, taeniid eggs in faeces were also uncommon,
being recovered from the faeces of only 11 dogs. This is likely to
be because more than 98% of owners reported feeding dry commercial dog food exclusively or as a major component of their dogs diet
and approximately 50% of owners either de-wormed their dog(s)
2 monthly or 4 monthly with a de-wormer containing praziquantel.
Nevertheless, an additional 45 dogs were positive in the E. granulosus coproantigen test (1.9% of mainland samples and 7.8% of
Tasmanian samples). Some coproantigen-positive faecal samples
were also positive in an E. granulosus coproPCR (Jenkins et al., 2014).
3.8.2. Sheep
Hydatid disease prevalence data are not collected in Australian
abattoirs, but in Tasmania occurrence of infection in livestock is
monitored and traced back to the property of origin. Hydatid
disease still occurs periodically in Australian sheep, however
the prevalence has declined steadily during the last 30 years (D.J.
Jenkins, personal observations), no doubt a reection of the decline
of E. granulosus infection in rural domestic dogs (Jenkins et al.,
2014). Sheep populations now most at risk of contracting hydatid
disease are those grazed on pasture abutting national and state
parks and forests containing populations of wild dogs (Grainger
and Jenkins, 1996). These wild dogs periodically enter pastures to
predate on the sheep but whilst there also defecate, contaminating
the pasture with eggs of E. granulosus. Nothing recent has been
published regarding the prevalence of hydatid disease in mainland
sheep. The most up-to-date data have been collected by the
National Sheep Health Monitoring Program (Animal Health Australia, 2011, http://www.animalhealthaustralia.com.au/programs/disease-surveillance/the-national-sheep-health-monitoring-project/).
Routine monitoring of slaughtered sheep for hydatid infection is
still undertaken in Tasmania. Since the declaration of provisional
eradication in 1996, there have been two reports of infection in
sheep; one in 2011 in sheep sent to a mainland abattoir for
slaughter (Jenkins et al., 2014) the other, more recently in 2013
(D.J. Jenkins, unpublished data) in a single animal, resident on a
property in the midlands area of Tasmania. Investigations have
shown this sheep was imported from South Australia so could have
become infected before arrival in Tasmania.
3.8.3. Cattle
High levels of hydatid disease in slaughtered cattle have been
reported, anecdotally, from abattoirs in south-eastern Queensland,
874
north-eastern New South Wales and eastern Victoria. No recent

data have been published regarding hydatid disease prevalence
in Australian cattle, but according to abattoir management prevalence is high enough to be causing substantial nancial losses to
the abattoirs through condemnation of offal. An estimated loss to
the northern Queensland beef industry of $6 million per year due
to hydatid-infected offal was reported for 2004, with prevalence
levels ranging between 2051% in cattle from coastal areas and
3% in those from inland areas (Banks et al., 2006b). The source of
infection in these cattle is likely from wildlife since cattle are commonly grazed in areas inhabited by wild dogs because predation
impacts are less severe than if sheep were grazed in the same
areas.
As with sheep, hydatid disease is monitored in slaughtered cattle in Tasmania. Since declaration of provisional eradication in
1996, over 200 hydatid-infected cattle have been identied. Most
of these animals proved to be imports from the mainland, mainly
Gippsland in Victoria, an area where hydatid infection in cattle is
common. However, 31 were animals less than 3 years old and
had never left Tasmania (Jenkins et al., 2014). DNA was extracted
and sequenced from cysts removed from four of the infected cattle;
their infections proved to be the G1 sheep strain of E. granulosus
(Jenkins et al., unpublished data). The G1 sheep strain not only
infects sheep but can also infect cattle, pigs, goats and macropodid
marsupials. Less than 5% of G1 hydatid cysts in Australian cattle
are fertile (Kumaratilake and Thompson, 1982), therefore cysts
from infected cattle, if consumed by dogs, dingoes or their hybrids,
commonly do not contribute to transmission of E. granulosus.
The 24 Tasmanian domestic dogs that tested positive in the E.
granulosus coproantigen ELISA and the hydatid-infection data from
sheep and cattle found since declaration of provisional freedom in
1996 indicate that hydatid disease has not been completely eradicated from the island as was previously thought but continues to
be transmitted at low levels (Jenkins et al., 2014).
3.9. Human prevalence
The prevalence of human hydatidosis on mainland Australia is
unknown, because in most jurisdictions human hydatid disease
has ceased to be notiable. The last published data on human
hydatid disease on mainland Australia was that of Jenkins and
Power (1996) but these data were only collected in New South
Wales and the Australian Capital Territory and are now out of date.
Nevertheless, new cases continue to be identied annually on
mainland Australia. A proportion of these new cases are in recently
arrived immigrants from a range of countries who were infected in
their country of origin. In the study of Jenkins and Power (1996),
60% of cases diagnosed in residents living in major urban centres
were recent immigrants. There has been a recent publication on
human hydatid disease in Tasmania (OHern and Cooley, 2013).
The authors described human hydatid disease in Tasmania since
the declaration of provisional freedom in 1996. Transmission of
hydatid disease to humans in Tasmania has now ceased, although
one or two new cases are diagnosed annually. However, all of these
new cases are in elderly people who were thought to have been
infected pre-1996.
4. Conclusions
Australia has a long history of research on hydatid disease and
the causative agent Echinococcus. Much of this was borne from
necessity, given the impact the parasite had on public health and
the agricultural economy in the late 19th and early 20th centuries
in Australia. However, the research that has been conducted in
Australia has contributed much to the international research effort
on Echinococcus and hydatid disease, in particular the value of the

organism as a model in studies on developmental biology and
epidemiology, not just concerned with Echinococcus but more
broad-ranging in terms of basic biology and theoretical models of
transmission dynamics. We hope that Australia will continue to
contribute to research on Echinococcus and that this will have an
impact internationally and sustain the collaborations that have
developed with research groups and centres world-wide.
Acknowledgements
We are very grateful to Mark Preston (Graphic Designer, Murdoch University, Australia) for producing the graphical images
and to Craig Poynter (Spacial Analysis Unit, Charles Sturt University, Australia) for preparing the map. Image of dingo and kangaroo
included on the front cover of this Special Issue is courtesy of the
Invasive Animals Cooperative Research Centre, Australia.
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International Journal for Parasitology 44 (2014) 865877

Contents lists available at ScienceDirect

International Journal for Parasitology

Echinococcus as a model system: biology and epidemiology

Known intermediate hosts

Known denitive hosts

Dog, fox, dingo, jackal and hyena

Sheep (cattle, pigs, camels, goats, macropods)

Fox, dog, cat, wolf, racoon-dog,

complemented much of Dvs research undertaken in rodents

Fig. 1. Diagrams illustrating the structural differences between the metacestodes of

model system for studying parasitism as distinct from a model

parasite life style of Echinococcus, as well as the potential of this

studies of the importance of the host intestinal ecosystem in

2.2. Developmental plasticity

2.1. Growth and maturation

Studies on the in vitro cultivation of Echinococcus from the

Echinococcus has two developmental stages in its life cycle; the

2.3. Developmental control

including those whose expression is up-regulated by pepsin-acid

challenging and hazardous if patent infections are maintained.

to date (Lin et al., 2012). There is also increasing evidence of the

(Gemmell, 1990). Domestically, the parasite spread rapidly

3. Epidemiology of E. granulosus in Australia

animals in the more remote areas of Australia was likely to have

and Copeman, 2003), Maroochy Shire (Jenkins et al., 2008), the

number of naturally infected foxes in various studies (Thompson

to experimental infection with hydatid disease (Jenkins and

north-eastern New South Wales and eastern Victoria. No recent

on Echinococcus and hydatid disease, in particular the value of the

Jenkins, D.J., Macpherson, C.N.L., 2003. Transmission ecology of Echinococcus

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