452

Review

TRENDS in Parasitology Vol.18 No.10 October 2002

Towards a taxonomic revision of the

genus Echinococcus
R.C. Andrew Thompson and Donald P. McManus
Echinococcus remains a significant public health problem worldwide and, in
several regions, the aetiological agents of cystic hydatid disease/echinococcosis
are extending their range. The taxonomy of Echinococcus has been a
controversial issue for decades, but the outcome of recent molecular
epidemiological studies has served to reinforce proposals made ten years ago to
revise the taxonomy of Echinococcus. A formal nomenclature is essential for
effective communication, and provides the stability that underpins
epidemiological investigations. It will also serve to recognize the contribution of
early taxonomists.
Published online: 21 August 2002

The taxonomy of Echinococcus has been extensively

reviewed, as have the reasons for rationalizing the
numbers of species and subspecies described during
the first half of the 20th century (reviewed in Ref. [1]).
Inadequate descriptions and the sympatric
occurrence of described subspecies were the major
considerations in proposals to recognize only four
species of Echinococcus (Table 1). However, opposing
views on the breeding system and population genetics
of Echinococcus further complicated discussion on
taxonomy [2].
Phenotypic variation

R.C. Andrew Thompson*

WHO Collaborating
Centre for the Molecular
Epidemiology of Parasitic
Infections, Division of
Veterinary and
Biomedical Sciences,
Murdoch University,
Murdoch, Western
Australia 6150, Australia.
*e-mail: andrew_t@
central.murdoch.edu.au
Donald P. McManus
Molecular Parasitology
Laboratory, Australian
Centre for International
and Tropical Health and
Nutrition, The
Queensland Institute of
Medical Research and The
University of Queensland,
Brisbane, Queensland
4029, Australia.

During the past 40 years, observations in the

laboratory and the field have revealed considerable
phenotypic variability among isolates of
Echinococcus. This variation has largely been
observed in Echinococcus granulosus, and between
isolates of the parasite from different species of
intermediate host (Box 1). Of most significance
was the initial research by Desmond Smyth that
demonstrated fundamental differences in the
developmental biology of E. granulosus of horse
and sheep origin [3]. These seminal studies
provided a platform of understanding for both
earlier and subsequent observations on differences
in the development and infectivity between
isolates of the parasite from various host species in
different parts of the world. The realization that
variants of E. granulosus develop at different
rates in the definitive host has meant that the
timing of anthelmintic administration designed
to remove worm burdens before patency should
be reconsidered. The fact that some variants
appear to be poorly infective to humans has
resulted in a reappraisal of the public health
significance of Echinococcus in areas where such
variants are endemic.
http://parasites.trends.com

Concept of a strain

Given the epidemiological significance of such

intraspecific variation in E. granulosus and the
international efforts to establish control programs in
different endemic regions, an informal
nomenclature was needed to reflect the phenotypic
variability evident between host-derived isolates of
E. granulosus. Thus, the concept of a strain was
developed and defined as variants which differ
statistically from other groups of the same species
in gene frequencies, and in one or more characters
of actual or potential significance to the
epidemiology and control of echinococcosis [2].
This variability may be delineated on the basis of
differences in nucleic acid sequences, and reflected
in phenotypic characters that affect the life cycle
pattern, host specificity, development rate,
pathogenicity, antigenicity and sensitivity to
chemotherapeutic agents, transmission dynamics,
epidemiology and control of cystic hydatid
disease/echinococcosis (CE) [4].
From a practical point of view, the recognition of
strain variation is a major prerequisite for control
efforts aimed at limiting transmission in endemic
regions. CE caused by E. granulosus continues to
rank as one of the most important parasitic zoonoses
worldwide, especially where there is a close
association between humans and livestock.
Under such circumstances, human behaviour
reflected in inadequate husbandry practices is
largely responsible for sustaining cycles of
transmission. Education and surveillance underpin
control efforts to break these cycles, and it is
therefore essential to recognize which strains are
present and which hosts support the perpetuation
of the life cycle (Fig. 1).
The concept of a strain also grew from increasing
evidence of genetic differences between E. granulosus
from different species of intermediate host.
Increasingly, such genetic variation has been found to
correlate with phenotypic variability and, from this,
the concept of a series of host-adapted strains of
E. granulosus was developed (Table 1).
Genetic basis for phenotypic variation

The application of molecular tools for characterizing

isolates of Echinococcus has had a major impact on
our understanding of the population genetics,
epidemiology and taxonomy of the parasite. DNA
analysis has also provided some insights into the

1471-4922/02/$ see front matter 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(02)02358-9

Review

TRENDS in Parasitology Vol.18 No.10 October 2002

Table 1. Echinococcus species, strains, isolates and genotypes

Species strain/isolate
(genotype)

Known intermediate Infective to Known definitive

hosts
humans? hosts

Echinococcus granulosus
Sheep strain (G1)
Sheep, cattle, pigs,
camels, goats,
macropods
Tasmanian sheep strain Sheep, cattle?
(G2)
Buffalo strain (?)
Buffalo, cattle?
Horse strain (G4)
Horses and other
equines
Cattle strain (G5)
Cattle
Camel strain (G6)

Camels, goats,
cattle?
Pig strain (G7)
Pigs
Cervid strain (G8)
Cervids
Lion strain
Zebra, wildebeest,
warthog, bushpig,
buffalo, various
Antelope, giraffe?
hippopotamus?
Echinococcus multilocularis
European isolate
Rodents, domestic
and wild pig, dog,
monkey
Alaskan isolate
Rodents
North American isolate Rodents
Hokkaido isolate
Rodents, pig,
monkey, horse
Echinococcus vogeli
None reported
Rodents
Echinococcus oligarthrus
None reported
Rodents

Yes

453

Probable geographical distribution

Proposed
taxonomic
b
designation
Echinococcus
granulosus

Yes

Dog, fox, dingo, jackal Australian mainland, Europe, USA,

and hyena
New Zealand, Africa, China, Middle East,
South America and Russian Federation
Dog, fox
Tasmania, Argentina

?
No

Dog, fox?
Dog

Yes

Dog

Yes

Dog

Asia
Europe, Middle East, South Africa,
(New Zealand? USA?)
Europe, South Africa, India, Sri Lanka,
Russian Federation, South America?
Middle East, Africa, China, Argentina

E. granulosus
Echinococcus
equinus
Echinococcus
ortleppi
E. granulosus?

Yes
Yes
?

Dog
Wolf, dog
Lion

Europe, Russian Federation, South America E. granulosus?

North America, Eurasia
E. granulosus?
Africa
E. granulosus?

Yes

Fox, dog, cat, wolf,

raccoondog

Europe, China?

Echinococcus
multilocularis

Yes
Yes
Yes

Fox, dog, cat

Fox, dog, cat, coyote
Fox, dog, cat,
raccoon dog

Alaska
North America
Japan

E. multilocularis
E. multilocularis
E. multilocularis

Yes

Bush dog

Central and South America

Echinococcus vogeli

Yes

Wild felids

Central and South America

Echinococcus
oligarthrus

E. granulosus

Abbreviation: ?, uncertain, further data and/or research required.

Data obtained from Ref. [42].

genetic basis for the phenotypic variation that is

characteristic for E. granulosus. In early studies,
techniques used for Echinococcus strain and
species characterization employed morphological
(e.g. rostellar hook) traits [5], and biochemical
and isoenzyme markers [6]. As they became
available, more sensitive molecular approaches
were used, and these have been successful in
discriminating species and strains, and have
confirmed the complexity of genetic variation within
E. granulosus [4,6,7].
Molecular typing methods

Early molecular studies investigating genetic

variation in Echinococcus used restriction fragment
length polymorphism (RFLP) analysis involving a
Southern blot hybridization approach. Specifically,
plasmid-cloned DNA probes derived from ribosomal
RNA (rRNA) genes of Schistosoma mansoni, a 2.3 kb
DNA segment of E. granulosus and internal
transcribed spacer-1 (ITS-1) ribosomal DNA (rDNA)
were used to characterize isolates of E. granulosus
from different hosts and geographical areas
http://parasites.trends.com

(see Ref. [4]). Building on this work, a procedure

was developed that linked PCR with RFLP
analysis of the ITS-1 region of rDNA and this
method (PCR-RFLP analysis) was used successfully
to study variation in E. granulosus isolates from
several regions.
Mitochondrial (mt) sequences provide rich sources
of data for research in evolutionary biology,
population genetics and phylogenetics, and are
increasingly being used in studies of the genus
Echinococcus. To date, molecular studies, using
mainly mtDNA sequences [cytochrome c oxidase 1
(cox1) and NADH dehydrogenase 1 (nad1) genes],
have identified nine distinct genotypes (G1G9)
within E. granulosus [812] (Table 1). This
categorization follows very closely the pattern of
strain variation emerging based on biological
characters [4]. Other studies have analyzed
heterogeneity between Echinococcus strains and
species using the random amplified polymorphic
DNA-PCR (RAPD-PCR) [11], single-strand
conformation polymorphism (SSCP) [13,14] and
dideoxy fingerprinting [15].

454

Review

TRENDS in Parasitology Vol.18 No.10 October 2002

Box 1. Variability between isolates of Echinococcus

Phenotypic variation has largely been observed in Echinococcus granulosus and
between isolates of the parasite from different species of intermediate host.
Morphology
Hook number and dimensions (e.g. 1986 in number, and 1944 m in total length
for protoscoleces)
Strobilar dimensions (e.g. reports of total adult worm length from 2 mm to 11 mm)
Reproductive anatomy (e.g. 2580 testes)
Development
Metacestode (e.g. cyst growth and protoscolex formation) and adult (e.g. growth
and maturation), in vitro and in vivo
Host infectivity and specificity
Experimental infections and epidemiological observations
Chemical composition
Protein, RNA and lipids in metacestodes
Proteins
Electrophoretic separation
Metabolism
Carbohydrate metabolism of metacestodes and adults
Hostparasite relationship
Immunoreactivity and/or antigenicity

Molecular epidemiology

The value of DNA analysis in molecular epidemiological

studies of CE, as well as in clarifying the complex
issue of strain variation in E. granulosus, is well
recognized. Some molecular epidemiological surveys
are summarized below.
In China, CE is a major public health problem
having been recorded in 22 provinces, including
autonomous and municipality regions. Examination
by a combination of DNA techniques has indicated
that the common sheep strain is the most
predominant in the northwest region of China and,
from the public health perspective, the majority of
infected livestock there could act as reservoirs of
human infection [16,17].
In Kenya, there is a very high prevalence of CE,
which is hyperendemic between two pastoral
communities, the Turkana in the northwest and the
Massai in the southwest [18]. Molecular analysis
showed the presence of two strains (sheep and camel)
in Kenya and that the camel strain appeared
restricted to the Turkana region, where camels are
kept as livestock. The range of intermediate hosts for
both strains appeared to be similar (sheep, cattle and
camel), except that the camel strain was not isolated
from any human cases examined [18]. However, this
strain has now been isolated from humans in
Argentina, Nepal and Iran [19,20,21].
CE is also a major public health problem in
Argentina, being endemic in many areas of the
country, and numerous human cases have been
reported [22]. Molecular analysis demonstrated the
presence of several distinct genotypes there including
the common sheep (G1) and Tasmanian (G2) strains
in sheep and humans, the pig strain (G7) in pigs, and
http://parasites.trends.com

the camel strain (G6) in humans [19]. The finding

that pigs harbored the pig strain and the occurrence
of the Tasmanian sheep strain has considerable
implications for the implementation of hydatid
control programs that include regular drug treatment
of dogs, due to the shorter maturation time of both
strains in dogs compared with the common sheep
strain [1,4]. Furthermore, this was the first report
of the presence of the Tasmanian sheep (G2) and
camel (G6) strains in humans, which may also have
important consequences for human health. Similarly
in Nepal, where CE is recognized as a significant
public health and environmental problem in all urban
areas, three strains of E. granulosus [sheep (G1),
cattle (G5) and camel (G6)] have been identified in
buffalo, sheep, goat and human hosts [20], of which
two human isolates were identified as the camel
strain (G6). There are no reports of camels being
infected with E. granulosus in Nepal or Argentina;
hence, the reservoir of the G6 genotype there remains
undetermined although, as is the case in Argentina,
goats are a likely source of infection. Following a
survey in 1998 [23], a recent comprehensive
molecular epidemiological study in Iran of
200 isolates found that the sheep strain was the most
common genotype of E. granulosus affecting sheep,
cattle, goats and occasionally camels [21]. The
majority of camels were infected with the camel
strain (G6), as were three of 33 human cases; the first
time that CE cases in humans have been identified in
an area where a transmission cycle exists for the
camel strain. In addition, the camel strain was found
to cause infection in sheep and in cattle.
It is well recognized that E. granulosus is
maintained in two cycles of transmission on mainland
Australia. One cycle principally involves domestic
sheep as the major intermediate host, with cattle and
pigs as potential accidental intermediate hosts, which
appear to play a small role in transmission because
the cysts are usually sterile. The other cycle involves
numerous species of macropod marsupials (kangaroos
and wallabies). There is interaction between these
cycles through a range of carnivores (domestic dogs,
feral dogs, dingoes and red foxes) that act as definitive
hosts. Early evidence of morphological, biochemical
and developmental differences between isolates of
E. granulosus of domestic and sylvatic origin led to
their proposed designation as distinct strains.
However, additional morphological studies, isoenzyme
analysis and DNA analysis indicated that only the
common sheep strain was present [2426].
Pairwise genetic comparisons and phylogenetic
analyses

Pairwise differences among genes can give a measure

of relative levels of divergence among taxa. Complete
mt genomes for the sheepdog and horsedog strains
were recently obtained and compared with those of
Echinococcus multilocularis, Taenia crassiceps and
Hymenolepis diminuta [27]. A comparison of the

Review

TRENDS in Parasitology Vol.18 No.10 October 2002

455

Case for a revised taxonomy

Echinococcus granulosus
Sheep
Cattle, goats
and camel

Echinococcus equinus
Horse

Human

Dog, dingo,
wolf and fox

Echinococcus granulosus?
Pig

Dog

Echinococcus granulosus?
Camel
Sheep, cattle
and goat

Human?

Human

Dog

Dog
Possibly other canids?

Echinococcus granulosus?

Echinococcus ortleppi

Cervid

Cattle

Human

Human

Wolf
Dog

Dog

Molecular characterization has thus revealed that the

genetic differences between what were perceived to be
host-adapted strains of E. granulosus are conserved and
occur consistently in isolates derived from different
species of intermediate hosts throughout the world. This
has been well demonstrated for the sheep, horse, cattle,
pig and camel strains in molecular epidemiological
studies undertaken in Europe, Iran, Africa and South
America [1,4,28]. In many cases, these investigations
have also used morphology to characterize isolates [1].
The fact that certain morphological characteristics have
a genetic basis provides a useful practical means for
strain typing in situations where molecular
characterization is not possible.
We would argue that the morphological, biological
and genetic differences that separate strains and/or
genotypes of Echinococcus are sufficient to justify
species rank in, at present, at least two forms; the horse
and cattle strains. This would increase the number of
recognized species of Echinococcus from four to six.
Formalizing the nomenclature taxonomically is
important for effective communication at all levels.
A species name will receive broad recognition
internationally, particularly by those involved in
control programs and clinical management, much
more so than genotype and to a lesser extent strain,
terms that are subject to misinterpretation and
misleading manipulation. A sound classification is
not simply a tool for identification, but provides
stability and predictive value about the properties of
the named species.

TRENDS in Parasitology

The case for Echinococcus equinus

Fig. 1. Cycles supporting
the major species and/or
strains of Echinococcus
granulosus, showing
major definitive and
intermediate hosts
(green) and other hosts
(red) that might be
involved. Question marks
(?) indicate that the hosts
susceptibility to infection
is uncertain.

complete mt nucleotide sequences of the proteinencoding genes and of the two subunits of rRNA
(small; rrnS and large; rrnL) indicated that the sheep
and horse strains differed by 12.4% in their nucleotide
(nt), and 11.6% in their amino acid level (aa)
sequences, a level similar to differences between these
two genotypes and E. multilocularis (1315% nt; and
11.513.5% aa). As expected, divergence was
considerably higher when any member of the genus
Echinococcus was compared with T. crassiceps
(2630% differences in both nt and aa), suggesting that
saturation has not been reached within Echinococcus.
Sequences for the variable genes atp6 and nad3 were
obtained from additional genotypes of E. granulosus,
from Echinococcus vogeli and Echinococcus
oligarthrus. Again, pairwise comparisons showed the
distinctiveness of the G1 and G4 genotypes. Another
approach to investigating levels of divergence is by
means of phylogenetic trees (Box 2). Phylogenetic
analyses of concatenated atp6, nad1 (partial) and cox1
(partial) genes from E. multilocularis, E. vogeli,
E. oligarthrus, five genotypes of E. granulosus, and
using T. crassiceps as an outgroup, yielded the same
results. Overall, the comparisons reported suggested
that the horse and sheep strains are as distinct from
each other as either is from E. multilocularis.
http://parasites.trends.com

The form of Echinococcus that uses horses as its

intermediate host was formally recognized
taxonomically by Williams and Sweatman in 1963 [29]
as a subspecies Echinococcus granulosus equinus.
They proposed that this form of the parasite was
adapted to horses as the intermediate host and
provided a comprehensive description of both
E. g. equinus and the form in sheep, E. g. granulosus.
A subsequent review of Echinococcus taxonomy by
Rausch [30] in 1967 proposed that E. g. equinus should
be invalidated because it occurred sympatrically with
the other subspecies, E. g. granulosus. There was no
evidence of any segregating mechanism that could
retain the genetic identity of the two subspecies
because they both use the dog as a definitive host and
thus could potentially interbreed in areas where the
sheepdog and horsedog cycles interact. Although
the two may be sympatric, their epidemiological
patterns and host ranges vary and the form adapted to
horses, unlike the sheep form, appears poorly infective
or non-infective to humans [31]. However, we now
know that, biologically, the two parasites are distinct
and, genetically, the two forms are more distantly
related as either is from well-established species such
as E. multilocularis. Careful phylogenetic analysis of
the mt sequence data, in combination with additional

456

Review

TRENDS in Parasitology Vol.18 No.10 October 2002

Box 2. Phylogeny of Echinococcus

An invaluable approach for investigating levels of divergence between taxa is by
means of phylogenetic trees. Accordingly, complete atp6, partial nad1 [a] and
partial cox1 [b] DNA sequences for genotypes 1, 4, 6, 7, 8 (EgrG1, EgrG4, EgrG6,
EgrG7 and EgrG8) of Echinococcus granulosus, Echinococcus multilocularis,
Echinococcus vogeli, Echinococcus oligarthrus and Taenia crassiceps were used [c,d].
The alignment was 1353 nucleotides (nt) [451 amino acids (aa)] long with
543 variable sites (168 for aa) and 262 parsimony-informative sites (67 for aa).
It is clear that EgrG4, EgrG1, E. vogeli and E. oligarthrus are almost equidistant
from each other in terms of mitochondrial sequences [c,d]. Furthermore, the
E. granulosus G1 and G4 genotypes are also almost equidistant from the G6G8
genotype cluster, although there is some structure in G6G8 group. Echinococcus
multilocularis appears as basal within the genus, but again the branch placing
it there is rather poorly supported. Given this, recognition of the sheepdog
(G1 genotype) and the horsedog (G4 genotype) strains (and possibly also the
G6G8 genotypes) as separate species is appropriate. The discrete nature of the
two forms is clear, and the molecular and phylogenetic evidence from this and
previous studies suggests the case for reinstatement of their formal taxonomic
status as species is now overwhelming.
References
a Bowles, J. and McManus, D.P. (1993) NADH dehydrogenase 1 gene sequences compared
for species and strains of the genus Echinococcus. Int. J. Parasitol. 23, 969972
b Bowles, J. et al. (1992) Genetic variants within the genus Echinococcus identified by
mitochondrial DNA sequencing. Mol. Biochem. Parasitol. 54, 165174
c Le, T.H. et al. (2002) Complete mitochondrial genomes confirm the distinctiveness of the
horsedog and sheepdog strains of Echinococcus granulosus. Parasitology 124, 97112
d Le, T.H. et al. (2002) Mitochondrial genomes of parasitic flatworms. Trends Parasitol. 18,
206213

Acknowledgements
R.C.A.T. acknowledges the
support provided by the
Australian Research
Council, WHO and
Murdoch University, and
the collaboration of Russ
Hobbs, Alan Lymbery,
John Eckert, Clare
Constantine, Majid Fasihi
Harandi and Lakshmi
Kumaratilake. D.P.M.
acknowledges the
National Health and
Medical Research Council
of Australia, the
Australian Research
Council, The Wellcome
Trust and the UNDP/World
Bank/WHO Special
Programme for Research
and Training in Tropical
Diseases for financial
support of his research.
D.P.M. also thanks
numerous collaborators,
especially Josephine
Bowles, Thanh Hoa Le,
David Blair, Mark Pearson
and Li Hua Zhang, for
their contribution to the
DNA analysis.

nuclear sequence data [32], formally demonstrated

the evolutionary distinctiveness of the sheep and
horse strains of E. granulosus and confirmed their
species identity. The recent study by Le et al. [27] has
reinforced this view. In addition, data have
accumulated from throughout the world
demonstrating the conserved nature of the horse and
sheep strains and/or genotypes of E. granulosus.
Furthermore, the fact that their genetic
characteristics are maintained in sympatry in
endemic areas where the life cycles overlap (e.g. UK,
Spain and Jordan [33,34]) reinforces the argument
that the two forms represent separate species.
Rausch correctly identified the problem of
recognizing the form in horses as a subspecies
because Williams and Sweatman [26] provided no
evidence of a segregating mechanism and, subspecies,
by definition can interbreed. Consequently, if
Williams and Sweatman had proposed species status
for the form in horses, its taxonomic status is unlikely
to have been questioned as rigorously. Considering
the additional evidence that has accumulated in the
intervening 40 years, we propose that E. equinus be
recognized as a distinct species, following the
description given by Williams and Sweatman [29].

molecular data are not as extensive as those available

for comparing the horse and sheep strains, there is no
question of its genetic distinctiveness, as clearly
shown by pairwise distance matrix and phylogenetic
analysis, using nuclear and mt genes [32]. The cattleadapted form has a widespread geographical
distribution that includes parts of central Europe,
South Africa, India, Sri Lanka, Nepal and possibly
South America [1,4,28]. Although cattle are commonly
found to harbor hydatid cysts throughout the world,
the aetiological agent is usually the sheep strain of
E. granulosus, and infected cattle are an accidental
host with resultant cysts rarely fertile. The cysts of
the cattle strain are invariably fertile and well
developed [35]. As with Echinococcus of horse origin,
the cattle form of Echinococcus was given taxonomic
status by Lopez-Neyra and Soler Planas in 1943 [36]
based on their re-evaluation of a description by Ortlepp
in 1934 [37] of Echinococcus in South Africa, where we
now know the cattle strain occurs. The taxonomic status
of E. ortleppi was not accepted by Rausch and Nelson
in 1963 [38], but subsequent studies by Verster [39]
revealed that previous taxonomic considerations were
based on only a limited appraisal of the morphological
features that characterize this form of Echinococcus.
We therefore propose that E. ortleppi should be
reinstated and recognized as the cattle-adapted form
of Echinococcus, a comprehensive morphological
description of which is provided by Verster [39].
(a)

(b)

The case for Echinococcus ortleppi

The form of Echinococcus that is adapted to cattle as

its intermediate host also warrants taxonomic
recognition. This form is characterized by the nature
of its pulmonary metacestode development with the
production of predominantly fertile cysts, the unusual
strobilar morphology and rapid rate of development of
the adult worm (Fig. 2). In addition, although the
http://parasites.trends.com

TRENDS in Parasitology

Fig. 2. Adult worms (35 days old) of Echinococcus granulosus of

(a) sheep origin (2.2 mm long), and (b) cattle origin (3.6 mm long)
representing sheep and cattle strains, respectively. (Reproduced,
with permission, from Ref. [35]).

Review

TRENDS in Parasitology Vol.18 No.10 October 2002

Concluding comments

Although the strongest arguments can be made for

recognition of species status for E. equinus and
E. ortleppi, the camel, pig and cervid forms also
warrant taxonomic status. However, more isolates
of these forms require molecular characterization
from different geographical areas. Unlike the horse
and cattle forms, which have a high degree of
intermediate host specificity, the camel strain and/or
genotype is not host specific for camels, and pigs
harbor more than one closely related genotype.
References
1 Thompson, R.C.A. (2001) Echinococcosis. In
Principles and Practice of Clinical Parasitology,
(Gillespie, S.H. and Pearson, R.D., eds),
pp 595612, Wiley
2 Thompson, R.C.A. and Lymbery, A.J. (1988) The
nature, extent and significance of variation within
the genus Echinococcus. Adv. Parasitol. 27, 209258
3 Smyth, J.D. and Davies, Z. (1974) Occurrence of
physiological strains of Echinococcus granulosus
demonstrated by in vitro culture of protoscoleces
from sheep and horse hydatid cysts. Int. J.
Parasitol. 4, 443445
4 Thompson, R.C.A. and McManus, D.P. (2001)
Aetiology: parasites and life cycles. In Manual on
Echinococcosis in Humans and Animals a Public
Health Problem of Global Concern (Eckert, J.
et al., eds), pp 119, World Organisation for
Animal Health (OIE)
5 Lymbery, A.J. (1998) Combining data from
morphological traits and genetic markers to
determine transmission cycles in the tapeworm,
Echinococcus granulosus. Parasitology 117,
185192
6 McManus, D.P. and Bryant, C.A. (1995)
Biochemistry, physiology and molecular biology of
Echinococcus. In The Biology of Echinococcus and
Hydatid Disease (Thompson, R.C.A. and Lymbery,
A.J., eds), pp. 135181, CAB International
7 McManus, D.P. (2002) The molecular
epidemiology of Echinococcus granulosus and
cystic hydatid disease. Trans. R. Soc. Trop. Med.
Hyg. 96, 151157
8 Bowles, J. et al. (1992) Genetic variants within the
genus Echinococcus identified by mitochondrial
DNA sequencing. Mol. Biochem. Parasitol. 54,
165174
9 Bowles, J. et al. (1994) Molecular genetic
characterisation of the cervid strain (northern
form) of Echinococcus granulosus. Parasitology
109, 215221
10 Bowles, J. and McManus, D.P. (1993) NADH
dehydrogenase 1 gene sequences compared for
species and strains of the genus Echinococcus. Int.
J. Parasitol. 23, 969972
11 Scott, J.C. and McManus, D.P. (1994) The random
amplification of polymorphic DNA can
discriminate species and strains of Echinococcus.
Trop. Med. Parasitol. 45, 14
12 Scott, J.C. et al. (1997) Molecular genetic analysis
of human cystic hydatid cases from Poland:
identification of a new genotypic group (G9) of
Echinococcus granulosus. Parasitology 114, 3743
13 Gasser, R.B. et al. (1998a) Direct display of
sequence variation in PCR-amplified mtDNA
regions of Echinococcus by single-strand
conformation polymorphism, and its implications.
Acta Trop. 71, 107115

http://parasites.trends.com

457

Although, epidemiologically, there is much evidence

to support the proposal for species designation of the
form in cervids, only a limited number of isolates
have yet been characterized morphologically or
genetically [9]. Nevertheless, based on some unique
DNA sequence differences, the cervid form does
appear to represent a distinct genotype (G8) of
E. granulosus. Recent genetic analysis has also
confirmed earlier clinical and epidemiological
observations [40] that this genotype is infective to
humans [41].

14 Zhang, L.H. et al. (1999) Screening for different

genotypes of Echinococcus granulosus within
China and Argentina by single-strand
conformation polymorphism (SSCP) analysis.
Trans. R. Soc. Trop. Med. Hyg. 93, 329334
15 Gasser, R.B. et al. (1998b) Dideoxy fingerprinting
(ddF): application to the genotyping of
Echinococcus. Int. J. Parasitol. 28, 17751779
16 McManus, D.P. et al. (1994) A molecular genetic
survey indicates the presence of a single,
homogeneous strain of Echinococcus granulosus
in north-western China. Acta Trop. 56, 714
17 Zhang, L.H. et al. (1998a) Mitochondrial genomic
markers confirm the presence of the camel strain
(G6 genotype) of Echinococcus granulosus in
north-western China. Parasitology 116, 2933
18 Wachira, T.M. et al. (1993) Molecular examination
of the sympatric existence and distribution of sheep
and camel strains of Echinococcus granulosus in
Kenya. Am. J. Trop. Med. Hyg. 48, 473479
19 Rosenzvit, M.C. et al. (1999) Genetic variation
and epidemiology of Echinococcus granulosus in
Argentina. Parasitology 118, 523530
20 Zhang, L.H. et al. (2000) Three genotypes of
Echinococcus granulosus identified in Nepal
using mitochondrial DNA markers. Trans. R. Soc.
Trop. Med. Hyg. 94, 258260
21 Fasihi Harandi, M. et al. Molecular and
morphological characterisation of Echinococcus
granulosus of human and animal origin in Iran.
Parasitology (in press)
22 Schantz, P.M. et al. (1995) Epidemiology and
control of hydatid disease. In The Biology of
Echinococcus and Hydatid Disease (Thompson,
R.C.A and Lymbery, A.J., eds), pp. 233354, CAB
International
23 Zhang, L.H. et al. (1998b) Mitochondrial DNA
markers compared for human and animal isolates
indicate the presence of two distinct strains of
Echinococcus granulosus in Iran. Am. J. Trop.
Med. Hyg. 59, 171174
24 Hobbs, R.P. et al. (1990) Rostellar hook
morphology of Echinococcus granulosus (Batsch,
1786) from natural and experimental Australian
hosts and its implications for strain recognition.
Parasitology 101, 273281
25 Lymbery, A.J. et al. (1990) Genetic diversity and
genetic differentiation in Echinococcus
granulosus (Batsch, 1786) from domestic and
sylvatic hosts on the mainland of Australia.
Parasitology 101, 283289
26 Hope, M. et al. (1992) A genetic comparison of
human and wildlife Echinococcus granulosus in
Queensland. Med. J. Aust. 156, 2730
27 Le, T.H. et al. (2002) Complete mitochondrial
genomes confirm the distinctiveness of the
horse-dog and sheep-dog strains of Echinococcus
granulosus. Parasitology 124, 97112

28 Haag, K. et al. (1999) Breeding systems in

Echinococcus granulosus (Cestoda: Taeniidae):
selfing or outcrossing? Parasitology 118, 6371
29 Williams, R.J. and Sweatman, G.K. (1963) On the
transmission, biology and morphology of
Echinococcus granulosus equinus, a new
subspecies of hydatid tapeworm in horses in
Great Britain. Parasitology 53, 391407
30 Rausch, R.L. (1967) A consideration of
intraspecific categories in the genus Echinococcus
Rudolphi, 1801 (Cestoda: Taeniidae). J. Parasitol.
53, 484491
31 Thompson, R.C.A. and Smyth, J.D. (1975) Equine
hydatidosis: a review of the current status in
Great Britain and the results of an
epidemiological survey. Vet. Parasitol. 1, 107127
32 Bowles, J. et al. (1995) A molecular phylogeny of
the genus Echinococcus. Parasitology 110,
317328
33 Kamhawi, S. and Hijjawi, N. (1992) Current
studies on the epidemiology of unilocular
hydatidosis in Jordan and its social implications.
Report on Parasitic Diseases of the Middle East,
p. 8, National Institutes of Health
34 Siles Lucas, M. et al. (1994) Comparative genetic
analysis of Swiss and Spanish isolates of
Echinococcus granulosus by Southern
hybridization and random amplified
polymorphic DNA technique. Appl. Parasitol.
35, 107117
35 Thompson, R.C.A. et al. (1984) Observations on
Echinococcus granulosus of cattle origin in
Switzerland. Int. J. Parasitol. 14, 283291
36 Lopez-Neyra, C.R. and Soler Planas, M.A. (1943)
Revision del genero Echinococcus Rud y
description de una especie nuva Parasita
intestinal del porro en Almeria. Rev. Ibrica
Parasitologia 3, 169194
37 Ortlepp, R.J. (1934) Echinococcus in dogs from
Pretoria and vicinity. Onderstepoort J. Vet. Sci.
3, 97108
38 Rausch, R.L. and Nelson, G.S. (1963) A review of
the genus Echinococcus Rudolphi, 1801. Ann.
Trop. Med. Hyg. 57, 127135
39 Verster, A.J.M. (1965) Review of Echinococcus
species in South Africa. Onderstepoort J. Vet. Res.
32, 7118
40 Wilson, J.F. et al. (1968) Cystic hydatid disease in
Alaska. A review of 101 autochthonous cases of
Echinococcus granulosus infection. Am. Rev.
Respir. Dis. 98, 115
41 Castrodale, L.J. et al. (2002) Two atypical cases
of cystic echinococcosis (Echinococcus
granulosus) in Alaska, 1999. Am. J. Trop. Med.
Hyg. 66, 325327
42 Thompson, R.C.A. et al. (1995) Variation in
Echinococcus: towards a taxonomic revision of the
genus. Adv. Parasitol. 35, 145176