Acta Tropica 128 (2013) 441–460

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Review

Canine echinococcosis: Global epidemiology and genotypic diversity

David Carmena a,∗ , Guillermo A. Cardona b
a
Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Ctra. Majadahonda-Pozuelo Km 2,
28220 Majadahonda, Madrid, Spain
b
Livestock Laboratory, Regional Government of Álava, Ctra. de Azua 4, 01520 Vitoria-Gasteiz, Spain

a r t i c l e i n f o a b s t r a c t

Article history: Canine echinococcosis is a potential zoonotic infection caused by the adult form of several cestode species
Received 26 May 2013 belonging to the genus Echinococcus, of which E. granulosus sensu lato and E. multilocularis are the most
Received in revised form 29 July 2013 epidemiologically relevant. Dogs infected with E. granulosus and E. multilocularis are widely regarded as
Accepted 2 August 2013
the main source of infection for human cystic and alveolar echinococcosis, diseases that cause substan-
Available online 13 August 2013
tial morbidity and socio-economic burden in several regions of the world. Following our previous review
on the global situation of cystic echinococcosis in livestock species (Cardona and Carmena. Vet. Para-
Keywords:
sitol. 2013;192:10–32), we summarize here current knowledge on the global epidemiology, geographical
Echinococcus
Dogs
distribution and molecular diversity of Echinococcus spp. infection in dogs. We address relevant topics
Epidemiology including the implications of the increasing urbanization of wildlife species such as foxes, coyotes, and
Molecular characterization dingoes in the establishment of urban cycles of Echinococcus spp., or the rising concerns regarding the
Zoonoses role of unsupervised translocation of infected dogs in spreading the infection to Echinococcus-free areas.
The involvement of wildlife species as natural reservoirs of disease to domestic animals and humans
and the epidemiological significance of the sympatric occurrence of different Echinococcus species in the
same geographical region are also debated. Data presented are expected to be useful for policy makers,
educational and health authorities responsible for designing and implementing effective measures for
disease control and prevention.
© 2013 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 442
2. Estimating the prevalence of Echinococcus infection in dogs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 442
3. Canine echinococcosis in Africa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 443
4. Canine echinococcosis in Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 444
4.1. Current situation of canine echinococcosis in North Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 444
4.2. Current situation of canine echinococcosis in Central Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445
4.3. Current situation of canine echinococcosis in Western Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445
4.4. Current situation of canine echinococcosis in South Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 448
4.5. Current situation of canine echinococcosis in East Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 448
4.6. Current situation of canine echinococcosis in Southeast Asia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449
5. Canine echinococcosis in Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449
5.1. Current situation of canine echinococcosis in Northern Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 449
5.2. Current situation of canine echinococcosis in Western Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 451
5.3. Current situation of canine echinococcosis in Eastern Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 451
5.4. Current situation of canine echinococcosis in Southern Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 452
6. Canine echinococcosis in the Americas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 452
6.1. Current situation of canine echinococcosis in Northern America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 452
6.2. Current situation of canine echinococcosis in Central America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 453
6.3. Current situation of canine echinococcosis in South America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 453

∗ Corresponding author. Tel.: +34 918223775; fax: +34 915097919.

E-mail addresses: dacarmena@isciii.es, d.carmena71@gmail.com (D. Carmena).

0001-706X/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.actatropica.2013.08.002
442 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

7. Canine echinococcosis in Oceania . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 455

8. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 455
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 456

1. Introduction definitive host populations is pivotal not only for measuring the
progress of CE and AE control programmes already in place, but also
Since their domestication during the Upper Palaeolithic period for assessing the distribution, host specificity, transmission dynam-
near 33,000 BP (Ovodov et al., 2011), dogs have developed a ics, and risk of infection for humans in a specific area (Barnes et al.,
unique relationship with man, resulting in the strongest of any 2012; Craig and Larrieu, 2006; Craig et al., 2003). With this aim
human–animal bond. In addition to their traditional value as work- in mind, we have summarized here relevant epidemiological and
ing animals, it is currently well accepted that companion dogs molecular data published on canine echinococcosis globally. The
exert also positive effects on the quality of life of their owners, search was conducted in PubMed covering the period from 2000 to
not only by promoting physical, psychological, and social health, date. Publications with an English abstract were primarily consid-
but also by improving recovery rates from a number of serious ered, although a number of non-English sources were also included
health conditions (Beck and Meyers, 1996; Paul et al., 2010; Wells, after careful examination to ensure data relevance and consistency.
2007). In spite of these unquestionable benefits, dog ownership Geographical sub-regions used here followed the classification
may also be associated to potential health hazards related to the proposed by the Statistics Division of the United Nations (avail-
transmission of zoonoses such as echinococcosis, leishmaniasis, able at http://unstats.un.org/unsd/methods/m49/m49regin.htm).
toxocariasis, rabies, Chagas disease, plague, and other bacterial The interested reader is invited to read this paper in conjunction
infections (Chomel and Sun, 2011; Deplazes et al., 2011). with our previous review on the global prevalence of CE in livestock
Canine echinococcosis is chiefly caused by adult stages of species (Cardona and Carmena, 2013) for additional complemen-
taeniid cestodes belonging to the species Echinococcus granulosus tary information.
sensu lato (E. granulosus s.l.) and E. multilocularis. Other Echinococ-
cus species including E. vogeli, E. oligarthrus, and E. shiquicus can 2. Estimating the prevalence of Echinococcus infection in
sporadically induce canine intestinal infections. E. granulosus s.l. dogs
has a world-wide distribution and its transmission is primarily
maintained in a synanthropic cycle through dogs as definitive Estimation of canine echinococcosis prevalence may be
hosts and livestock species as intermediate hosts (McManus et al., attempted using ante- and post-mortem diagnostic techniques, each
2003). E. multilocularis is restricted to the Northern hemisphere one with its own set of advantages and limitations. The gold
and its life cycle is predominantly sylvatic, with carnivorous standard method for the detection of Echinococcus spp. infection
species such as foxes, wolves, and coyotes (and, to a lesser extent, in definitive hosts comprises post-mortem examination of the
dogs) acting as definitive hosts, and a variety of small rodent intestine using the scraping (estimated sensitivity ∼78%) or the
species such as voles, pikas, and lemmings serving as intermediate sedimentation and counting (estimated sensitivity: 96–100%) tech-
hosts (Vuitton et al., 2003). Dogs infected by E. granulosus s.l. and niques (Barnes et al., 2012; Duscher et al., 2005; Eckert, 2003).
E. multilocularis are the main source of infection for human cystic While highly specific and sensitive, these procedures present
(CE) and alveolar (AE) echinococcosis, respectively. Both CE and AE some drawbacks, including intensive labour, requirement of special
are important zoonotic diseases that represent major public health safety precautions, ethically questionable principles, and unsuit-
problems in several regions of the world, causing a considerable ability for mass screening surveys or investigations involving work-
socio-economic burden (Benner et al., 2010; Budke et al., 2006; ing or companion dogs. Additionally, studies based on necropsy
Torgerson et al., 2010). may be biased if a particular dog class (e.g. unwanted, older or
Recent molecular genetic studies based on mitochondrial sick) is more likely to be sampled. Thus, a number of ante-mortem
genome analysis have revealed that E. granulosus s.l. is a cryptic methods have been developed for diagnostic purposes. Arecoline
species complex including E. granulosus sensu stricto (E. granulosus hydrobromide purging followed by examination of faecal mate-
s.s., genotypes G1–G3), E. equinus (genotype G4), E. ortleppi (geno- rial discharged has been used for mass surveillance in Echinococcus
type G5), and E. canadensis (genotypes G6–G10) (Nakao et al., 2007; spp. control programmes worldwide. This technique is near 100%
Thompson, 2008; Thompson and McManus, 2002). E. granulosus specific in endemic regions, although discrimination among differ-
s.s., particularly the genotype G1, is responsible for most cases of ent Echinococcus species may be problematic in co-endemic areas
human infections. E. canadensis and E. ortleppi are also infective to of Canada, Central Asia, China, and Russia (see below). Necropsy
humans, but to a much lesser extent than E. granulosus s.s. Although and arecoline treatment allow the estimation of worm burdens and
the genetic diversity of E. multilocularis is more limited in com- purge worm counts, respectively, which are critical parameters for
parison with E. granulosus s.l., recent taxonomic studies at global assessing infection pressure and modelling the transmission of the
scale have demonstrated intra-specific variations within E. multilo- parasite. Both techniques are also a source of parasitic material for
cularis, allowing the identification of four geographically-restricted downstream molecular studies. However, arecoline purging has a
genetic groups, European, North American, Asian, and Mongolian highly variable sensitivity, is time-consuming, costly, and biohaz-
(Davidson et al., 2012; Ito et al., 2010; Knapp et al., 2009; Nakao ardous. Some dogs may also suffer serious side-effects, so replacing
et al., 2009). this drug by a less traumatic purgative would be highly desirable
Intestinal infection with Echinococcus spp. adult worms in dogs (Barnes et al., 2012). Likewise, faecal egg detection is hampered
does not cause significant pathology and is typically asymptomatic, by low sensitivity associated to erratic egg production and the
even in animals with high parasite burdens. Besides, E. multilocu- fact that eggs of Echinococcus and Taenia species cannot be differ-
laris metacestode infection in domestic dogs has also been sporad- entiated by light microscopy. However, conventional microscopy
ically reported in the literature (Heier et al., 2007; Jenkins et al., followed by taeniid egg enrichment and further characterization of
2012; Peregrine et al., 2012). However, estimating the prevalence, Echinococcus species by PCR (see below) are widely used in geno-
mean abundance, and genotype frequencies of these parasites in typing studies. Regarding immunodiagnostic assays, detection of
 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
serum antibodies has shown highly variable sensitivities and cross-
reactivity with other parasite species, although may be useful as a
validation test in population studies (Benito et al., 2006). Current
diagnosis of canine echinococcosis is mainly based on the detection
of Echinococcus copro-antigens using ELISA (CpAg-ELISA) assays.
This simply, safe, and relatively high sensitive technique allows the
detection of the parasite in both necropsied and living definitive
hosts and, because of the stability of copro-antigens, also in fae-
cal samples collected in the field. However, obtained results in the
latter case should be interpreted with caution as faeces cannot be
traced back to the animal of origin and multiple samples may have
originated from a single dog. An important factor to bear in mind
is that the sensitivity of copro-antigen detection is generally good
in dogs with moderate to high parasite burdens (>100 worms), but
significantly lower in dogs carrying few parasites (<100 worms)
(Deplazes et al., 1992). Taking together, these features make CpAg-
ELISA the method of choice for routine mass-screening. There have
been a number of excellent reviews on the immunodiagnosis of
Echinococcus infection in dogs in the last few years (Allan and Craig,
2006; Carmena et al., 2007, 2006; Zhang and McManus, 2006), and
the interested reader is referred to these for more detailed informa-
tion. Finally, a number of species-specific PCR-based assays have
been developed for use directly on faeces or on taeniid eggs iso-
lated from faeces to confirm the presence of Echinococcus infection
(Barnes et al., 2012; Deplazes et al., 2011; Dinkel et al., 2004). How-
ever, PCR is a laborious and relatively expensive method, features
that hamper considerably its use for routine diagnostic or in field
surveys. Therefore, PCR is more rationally used for confirmatory
purposes of copro-antigen results, particularly in dog populations
where low parasite prevalences are suspected (Abbasi et al., 2003;
Deplazes et al., 2003).
In addition, it should be noted that physical environmental (e.g.
climate, seasonal variations), biological (e.g. worm burden, dog’s
age and immune status, parasite’s strain), and human behavioural
(e.g. slaughtering practices, dog management, religious belief,
migratory patterns) factors determine the dispersal and survival of
Echinococcus eggs in a given region, influencing the infection pres-
sure to intermediate hosts. Burden rates may also greatly affect
the diagnostic performance of the method used to detect the infec-
tion in a specific definitive host population (Romig et al., 2011).
These factors may help explaining, at least partially, the aggregated
distribution of canine echinococcosis frequently reported in the lit-
erature (Al-Qaoud et al., 2003; Dalimi et al., 2002; Himsworth et al.,
2010b; Jenkins et al., 2008; Lahmar et al., 2001), and should be taken
into consideration when designing field epidemiological studies or
analyzing and evaluating infection prevalence and burden data.
3. Canine echinococcosis in Africa
E. granulosus s.l. is widespread in all North African states includ-
ing Algeria, Egypt, Libya, Morocco, and Tunisia (Dakkak, 2010;
Sadjjadi, 2006), and also in most of the sub-Saharan countries
stretching from Sudan to South Africa (Magambo et al., 2006; Romig
et al., 2011; Wahlers et al., 2012). Very limited information is cur-
rently available from Western, Central, and Southern Africa, where
updated, reliable epidemiological data is greatly needed. The infec-
tion affects primarily rural pastoralist communities with close con-
tact with dogs, poor hygiene, and limited access to health services.
E. granulosus s.l. is mainly transmitted between dogs as defini-
tive host and sheep, goats, cattle, camels, pigs, and equines as
intermediate hosts (see Cardona and Carmena, 2013). A wildlife
cycle is also known to occur through jackals, hyenas, wild dogs/cats,
foxes, and lions acting as definitive hosts and a large number of
ungulates as intermediate hosts (Huttner and Romig, 2009; Lahmar
et al., 2009; Romig et al., 2011). E. multilocularis seems to be
extremely rare in Africa, with only two autochthonous cases of
443
human AE reported in Tunisia (Robbana et al., 1981; Zitouna et al.,
1985) and an additional one in Morocco (Maliki et al., 2004). No
E. multilocularis infection cases have been documented in African
wildlife or domestic dogs to date. Factors recurrently mentioned in
the literature as associated with higher risk of canine echinococ-
cosis in African dogs include unsupervised home slaughtering,
feeding raw offal to dogs, improper disposal of carcasses, dogs
scavenging on infected carcasses, elevated number of stray, free-
roaming or unrestrained dogs, and poor public awareness about
the disease (e.g. Azlaf et al., 2007; Buishi et al., 2006; Inangolet
et al., 2010; Jones et al., 2011; Kebede et al., 2009;).
Available molecular data reveal that E. granulosus s.s., E. ortleppi,
E. canadensis, and probably E. equinus are circulating in African
livestock species (reviewed in Cardona and Carmena, 2013), con-
firming the existence of sheep–dog, cattle–dog, camel–dog, and
pig–dog transmission cycles. Unfortunately, the lack of published
data on the molecular characterization of Echinococcus isolates
from African dogs does not allow elucidating the full extent of the
relative importance of each genotype in the transmission dynamic
of Echinococcus in this continent. A fifth Echinococcus species (E.
felidis) has been recently found in wild carnivores (lions and hye-
nas), although the infectivity of this genotype to farm animals or
dogs is still unclear (Huttner and Romig, 2009; Huttner et al., 2008).
Canine echinococcosis prevalence data documented in African
countries from 2000 to date are presented in Table 1. Very high
infection rates have been consistently reported in dogs from Egypt
(5–16%), Ethiopia (17–62%), Kenya (26–33%), Libya (20–26%), Mau-
ritania (14%), Morocco (55–58%), Tunisia (3–21%), Uganda (66%),
and Zambia (8%). Furthermore, high prevalences were typically
associated to elevated infection intensities (see Table 1), with
dogs harbouring heavy infections accounting for up to 32–40%
of the infected population (Buishi et al., 2005b; Inangolet et al.,
2010). It has been previously estimated that a single infected
dog sheds, in average, more than 8000 Echinococcus eggs per day
(Gemmell, 1990), resulting in considerable environmental contam-
ination. Therefore, elevated canine echinococcosis prevalence rates
combined with high parasite burdens will inevitably increase the
risk of Echinococcus dispersal by raising the infection pressure to
production animals in a given region. Not surprisingly, elevated
CE infection rates have been commonly reported in most live-
stock species from the above mentioned countries (reviewed in
Cardona and Carmena, 2013). However, it is important to bear in
mind that high numbers of infections in livestock and dogs do not
necessarily translate into elevated human CE prevalence rates, as
parasite’s genotype and socio-behavioural factors greatly deter-
mine the extent of human disease (Wahlers et al., 2012).
Epidemiological studies carried out in Kenya (Buishi et al., 2006),
Libya (Buishi et al., 2005b), and Uganda (Inangolet et al., 2010)
based on necropsy and/or CpAg-ELISA have evidenced a pattern
of age related infection, with young dogs bearing higher preva-
lence and abundance rates compared to older dogs. High canine
echinococcosis prevalence (range: 26–66%) and mean intensity of
infection (range: 540–1064 worms) rates were reported in those
surveys. It has been suggested that the age pattern observed may
be due to the development of a host protective immune response
caused by successive re-infections or by ingestion of a large num-
ber of protoscoleces. Indeed, a mathematical model assuming the
presence of acquired immunity was the best fit for the Echinococcus
infection in dogs in Morocco (Azlaf et al., 2007). Canine echinococ-
cosis prevalence and intensity of infection rates considered in this
model were 55–58% and 75–547 worms, respectively, well in the
range for the data reported in Kenya, Libya, and Uganda (see above).
On the contrary, a field survey conducted in urban stray dogs in
Nouakchott, Mauritania, has found a much lower global preva-
lence of 14% and a mean intensity of infection of 1277 worms, with
older dogs having higher infection and burden rates than younger
444 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

Table 1
Prevalence and molecular epidemiology of Echinococcus granulosus s.l. infection in dogs in Africa (2000 onwards).

Country Period Dog population No. samplesa Prevalence (%) Worm burden (n) Diagnostic procedure Reference

Egypt NS Stray 540 5.0 421b Necropsy El Shazly et al. (2007)

NS Stray 50 16.0 NS Necropsy Mazyad et al. (2007)

Ethiopia NS Stray 18 16.7 NS Necropsy Kebede et al. (2009)

NS Stray 13 61.5 NS Necropsy Jones et al. (2011)

Kenya NS Stray 42 33.3 540b Necropsy Buishi et al. (2006)

NS Farm 161 26.1e – CpAg-ELISA Buishi et al. (2006)

Libya 2001–02 Stray 58 25.8 1064b Necropsy Buishi et al. (2005b)

2001–02 Farm 334 20.1d , e – CpAg-ELISA Buishi et al. (2005b)

Mauritania NS Stray 121 14.0 1227b /172c Necropsy Salem et al. (2011)
Morocco NS Stray 151 55.0–58.0 75–547 Necropsy Azlaf et al. (2007)

Tunisia NS Stray NS 21.0 2534b Necropsy Lahmar et al. (2001)

NS Semi-stray 375 3.5 NS Purgation Lahmar et al. (2008)
2007 Stray 60 18.4 848b Necropsy Lahmar et al. (2009)

Uganda 2007–08 Mixed 327 66.3 845b Necropsy Inangolet et al. (2010)
Zambia 2005–06 Farm 540 8.0e – Coproscopy/CpAg-ELISA Nonaka et al. (2011)
a
Number of dogs analyzed by necropsy or number of faecal supernatants analyzed by CpAg-ELISA (ELISA for the detection of copro-antigens).
b
Mean intensity of infection (mean number of parasites per infected dog).
c
Mean abundance of infection (mean number of parasites per dog examined).
d
Prevalence adjusted for the sensitivity and specificity of the diagnostic technique used.
e
Estimated prevalence for Echinococcus spp.

dogs (Salem et al., 2011). It is tempting to speculate that, in this
particular epidemiological scenario, a lower infection pressure to
dogs may not be sufficient to trigger a parasite-induced host pro-
tective immunity in a significant number of dogs re-infected with
Echinococcus s.l.
A seasonal variation in canine echinococcosis occurrence has
been reported in Uganda, with a higher prevalence being recorded
during the rainy season compared to that in the dry season
(Inangolet et al., 2010). Torrential rains and floods causing the death
of large numbers of livestock (and consequently facilitating the
access of dogs to infected carcasses) were proposed by the authors
as the most likely explanation to this phenomenon. Differences in
Echinococcus infection rates have also been documented between
rural and urban dogs (El Shazly et al., 2007), and between stray and
domesticated dogs (Inangolet et al., 2010). Sex was not identified
as a significant risk factor for canine echinococcosis in some stud-
ies (Buishi et al., 2005b; El Shazly et al., 2007; Salem et al., 2011),
although male dogs have been found carrying higher worm burdens
than female dogs in an Ugandan study (Inangolet et al., 2010).
4. Canine echinococcosis in Asia
E. granulosus s.l. is endemic or re-emerging in large parts of Asia
including East Asian countries (Sadjjadi, 2006), the former Soviet
republics of Central Asia (Torgerson et al., 2006), North and West-
ern China (McManus, 2010; Wang et al., 2008), and Northeastern
Siberia and Western Arctic (Rausch, 2003). The infection is his-
torically known to be present in many of the East Mediterranean
regions (Abdel-Hafez and Kamhawi, 1997), the Arab states bor-
dering the Persian Gulf (Dar and Alkarmi, 1997) and a number of
Southeast Asian countries (Schantz et al., 1995), although no recent,
or very limited, epidemiological information is currently available
from these areas. E. multilocularis is present in Armenia, Azerbaijan,
Russia, the Central Asian Republics, Mongolia, Northeastern, Cen-
tral and Northwestern China, and North of Japan (Davidson et al.,
2012; Vuitton et al., 2003; Wang et al., 2008).
Transmission of E. granulosus s.l. in Asia is typically through
a domestic cycle with dogs acting as definitive host and sheep,
goats, cattle, buffaloes, camels, yaks or pigs serving as intermedi-
ate hosts (Cardona and Carmena, 2013). Wild carnivores including
foxes, jackals and wolves have been reported to harbour E. gra-
nulosus adult worms in China (reviewed in Wang et al., 2008),
Iran (Beiromvand et al., 2011; Dalimi et al., 2002) and Kazakhstan
(Abdybekova and Torgerson, 2012), providing evidence of the co-
existence and overlapping of domestic and sylvatic cycles of the
parasite in certain geographical areas. In contrast, E. multilocularis is
predominantly transmitted in the wild between carnivores (foxes,
jackals, wolves and raccoon dogs) and a number of small mam-
mal species, mainly voles and pikas (Vuitton et al., 2003; Wang
et al., 2008). Importantly, an E. multilocularis peri-domestic cycle
is also known to exist through dogs preying on infected rodents
in close proximity to human settlements in endemic areas from
China and Japan (Kamiya et al., 2006; Vaniscotte et al., 2011).
Indigenous peoples engaged in livestock herding and/or hunt-
ing activities involving dogs are at higher risk of being infected
with Echinoccocus spp. Major contributing factors to the mainte-
nance of canine echinococcosis in endemic regions include poor
awareness of the disease, inadequate sanitation and hygiene prac-
tices, religious beliefs promoting large dog populations (Yang
et al., 2009; Yu et al., 2008) improper control of condemned offal
at abattoirs, unsupervised domestic slaughtering (Huang et al.,
2007), feeding infected viscera to dogs, and allowing dogs to roam
freely feeding on animal carcasses, or preying on small mam-
mals (Nonaka et al., 2009; Vaniscotte et al., 2011; Xiao et al.,
2006).
Regarding the genotypic diversity of Echinococcus in Asia, E. gra-
nulosus s.s., E. ortleppi, and E. canadensis, but not E. equinus, have
been documented infecting livestock intermediate host species in
recent years (reviewed in Cardona and Carmena, 2013). In addi-
tion, E. shiquicus, a newly Echinococcus species identified in China,
is also known to be transmitted in the wild between red foxes
and pikas (Xiao et al., 2005) and to infect domestic dogs (Boufana
et al., 2013). Recent molecular and phylogenetic evidence seems
to indicate that E. multilocularis isolates from different intermedi-
ate and definitive Asian hosts cluster together into a well-defined,
geographical-specific clade that differs significantly from European
and North American isolates (Nakao et al., 2009).
4.1. Current situation of canine echinococcosis in North Asia
Echinococcus spp. occurs sympatrically through the boreal
forests and tundra areas of Northern Russia, including much of
Siberia. E. granulosus s.l. is transmitted in a sylvatic cycle involving
wolves as definitive hosts and reindeers and elks as intermediate
 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
Fig. 1. Global molecular epidemiology of Echinococcus granulosus s.l. (font in blue), E. multilocularis (font in red), and E. shiquicus (font in green) intestinal infections in dogs
based on published literature from 2000 to date. Grey areas indicate countries were canine echinococcosis has been reported during the same period, but no molecular data
are currently available.
hosts. A domestic cycle is also known to exist among domestic dogs
and domesticated reindeers. Similarly, E. multilocularis is main-
tained in the wild by wolves feeding on small rodents such voles and
lemmings (reviewed in Rausch, 2003). In endemic areas, domestic
dogs preying on wild rodents may be expected to become infected
by E. multilocularis, although such possibility has not been con-
firmed to date.
4.2. Current situation of canine echinococcosis in Central Asia
Canine echinococcosis is highly endemic or co-endemic in
the former Soviet Republics of Central Asia as consequence of the
increase in home slaughtering practices and the withdrawal of peri-
odic compulsory anthelmintic treatment for rural dogs after the fall
of the Soviet Union (Torgerson et al., 2003). Epidemiological and,
to a lesser extent, molecular data on Echinococcus infection in dogs
are currently available from Kazakhstan, Kyrgyzstan, Tajikistan,
and Uzbekistan (Fig. 1 and Table 2), but not from Turkmenistan.
In these areas rural dogs associated to livestock husbandry are
thought to play the most important role in the transmission of
E. granulosus s.l. This hypothesis is supported by mathematical
modelling analyses demonstrating that farm dogs at a prevalence
of 23% and a mean abundance of 631 worms per dog evidenced
a marked age-related distribution of infection, consistent with
high infection pressures and the development of a host protective
immune response against re-infection. On the contrary, domestic
dogs at a much lower prevalence of 5.8% and a mean abundance of
27 worms per dog could not be demonstrated to develop a signifi-
cant protection against re-infection (Torgerson et al., 2003). On the
other hand, the spatial distribution of E. multilocularis in Central
Asia seems to be based on small foci of infection determined by
local environmental conditions, with the presence of stable, high-
density population of rodents and humidity playing a critical role
in the survival and dispersal of the parasite (Shaikenov, 2006). A
445
similar patchy distribution has been reported in other field surveys
carried out in different European countries (see Section 5.2).
Dog infections caused by E. granulosus s.l. has been estimated
to be in the range of 6–28% in Kazakhstan, 11–19% in Kyrgyz-
stan, 15% in Tajikistan, and 8–20% in Uzbekistan. Regarding canine
echinococcosis caused by E. multilocularis, epidemiological data are
only available from Kazakhstan and Kyrgyzstan, where reported
prevalence rates were 5% and 18%, respectively (Table 2). In most
instances, Echinococcus spp. infection was associated to elevated
worm burdens, indicative of high environmental contamination
with eggs of this cestode.
Echinococcus genotyping analyses have been only performed
in dogs from Kazakhstan and Kyrgyzstan (Fig. 1 and Table 2).
These studies have revealed the presence of co-endemic regions
in these countries, where E. granulosus s.s. is the most commonly
reported species (genotype frequency: 33–57%), followed by E. mul-
tilocularis (genotype frequency: 38–45%), E. canadensis (genotype
frequency: 5–22%) and E. equinus (genotype frequency: 1%). Tak-
ing together, this information provides evidence of the presence of
well-established sheep–dog, pig–dog, camel–dog and horse–dog
transmission cycles of E. granulosus s.l., though more research is
necessary to determine the frequency of the parasite genotypes in
livestock intermediate host species and humans in Central Asia.
4.3. Current situation of canine echinococcosis in Western Asia
Echinococcus granulosus s.l. has been mainly reported infecting
stray dogs from Irak (17–50%), Iran (13–48%) and Jordan (14–30%),
whereas E. multilocularis infection has been found only in Iranian
dogs at a prevalence of 7% (see Table 2). Heavy worm burdens
(>1000 worms) have been documented in 37% of infected dogs in
Irak (Saeed et al., 2000), 4.5% in Iran (Razmi et al., 2006) and 15–24%
in Jordan (Al-Qaoud et al., 2003; el-Shehabi et al., 2000), suggesting
an epidemiological scenario where high infection pressures for
ruminant (and humans) intermediate hosts are commonplace.
 446
Table 2
Prevalence and/or molecular epidemiology of Echinococcus granulosus s.l. (font in black), E. multilocularis (font in red), and E. shiquicus (font in green) infections in dogs in Asia (2000 onwards).

Country Period Dog No. samplesa Prevalence (%) Worm burden Diagnostic Molecular characterization Reference
population (n) procedure

No. Gene markers Genotype

isolatesb frequency (%)

China NS NS 53 13.2; 17.0 NS Necropsy – – – He et al. (2000)

2003–03 Farm 371 8.0–19.0c ; 80e ; 131e Purgation – – – Budke et al. (2005a)
13.0–33.0c
NS Domestic 139 36.0f – CpAg-ELISA – – – Wang et al. (2005)
2004–05 Stray – – NS Necropsy/PCR 13 (45 AW) cox1 G1 (93.3%); G6 Bart et al. (2006)
(6.7%)
NS Farm – – 10,000 Necropsy/PCR 1 (NS AW) 12S rRNA G1 (NS); E.m. (NS) Wen et al. (2006)
NS Domestic – – NS Purgation/PCR 1 (65 AW) rrnL E.g. (27.7%); E.m. Xiao et al. (2006)
(72.3%)

D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

2004–05 Stray 30 56.7; 3.3 NS Necropsy/PCR 17 (NS AW) 12S rRNA G1 (NS); E.m. (NS) Zhang et al. (2006)
2000 Stray 23 27.0; 32.0 NS Necropsy – – – Huang et al. (2007)
NS Stray – – – Necropsy 4 (AW) atp6, coxI, nadI G1 (100%) Ma et al. (2008)
NS Stray 12 66.7; 8.3 NS Necropsy – – – Yu et al. (2008)
NS Stray 149 38.9f – Coproscopy/CpAg- 14 (E) 12S rRNA E.g. (100%) Yu et al. (2008)
ELISA/PCR
2007 Stray 9 55.5 NS Necropsy – – – Han et al. (2009)
2000 Stray 22 27.0; 36.0 10–50; Necropsy – – – Yang et al. (2009)
500–100,000
2000 Mixed 580 50.0f – CpAg-ELISA – – – Yang et al. (2009)
1987–90 Farm 291 17.0 <100–35,000 Purgation – – – Zhang et al. (2009)
2004–07 Mixed 74 23.0; 5.4 NS Purgation – – – Zhao et al. (2009)
2002 Domestic 228 14.8 39.6e Purgation/Copro- – 12S rRNA – Wang et al. (2010)
PCR
2006–07 Domestic 142 22.5 – Copro-PCR – 12S rRNA – Vaniscotte et al. (2011)
2006–10 NS – – NS Necropsy/PCR 1 (2 AW) cox1 E.g. (50.0%); E.m. Ma et al. (2012)
(50.0%)
2003–03 Farm 371 – – Purgation/PCR 8 (AW, E) nad1 E.m. (75.0%); E.s. Boufana et al. (2013)
(62.5%)
NS Stray 35 11.4; 2.8 NS/1 Necropsy – – – Huang et al. (in press)
NS Stray 35 8.6–11.4f – CpAg-ELISA – – – Huang et al. (in press)

Irak 1991–98 Stray 97 49.5 200–1000 Necropsy – – – Saeed et al. (2000)

1997–99 Stray 120 16.7 1026d Necropsy – – – Abdullah and Jarjees
(2005)

Iran NS Stray 60 48.3 NS Necropsy – – – Maleky and

Moradkhan (2000)
1997–00 Stray 115 19.1 421d Necropsy – – – Dalimi et al. (2002)
NS Stray 83 13.2 NS Necropsy – – – Dalimi et al. (2006)
2002–03 Stray 100 22.0 636d Necropsy – – – Razmi et al. (2006)
NS Domestic 59 27.1f – CpAg-ELISA – – – Zare-Bidaki et al.
(2009)
2009–10 Mixed 77 16.9; 6.5 – Copro-PCR – nad1, 12S rRNA – Beiromvand et al.
(2011)
2011 Stray 71 28.2 NS Necropsy/PCR 20 (20 AW) cox1, nad1 G1 (75.0%); G2 Parsa et al. (2012)
(10.0%); G3 (15.0%)
 Japan 1966–99 Mixed 9849 1.0 NS Necropsy – – – Takahashi and Mori
(2001)
2003–04 Domestic 183 1.1 – CpAg-ELISA/PCR 1 (E) 12S rRNA E.m. (100%) Morishima et al. (2006)
1999–05 Shelter 550 0.2 – Coproscopy/PCR 1 (E) 12S rRNA E.m. (100%) Yamamoto et al. (2006)
2004–05 Domestic 1460 0.3 – Copro-PCR – 12S rRNA – Kamiya et al. (2007)
2004–05 Domestic 1460 0.4 – CpAg-ELISA – – – Kamiya et al. (2007)
1997–07 Domestic 4768 0.9 – Coproscopy/ 18 (E) cox1, 12S rRNA, E.m. (100%) Nonaka et al. (2009)
CpAg-ELISA/ U1 snRNA
PCR

Jordan 1994–95 Stray 94 13.8 3 to >10,000 Necropsy – – – el-Shehabi et al. (2000)

1994–95 Stray 94 17.0f – CpAg-ELISA – – – el-Shehabi et al. (2000)
1998–99 Stray 112 29.5 1306d Necropsy/PCR 23 (115 ITS2 G1 (92.8%); G4-like Al-Qaoud et al. (2003)
AW) (7.2%)

D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

India NS Stray 268 4.1f – CpAg-ELISA – – – Prathiush et al. (2008)

Kazakhstan NS Farm 606 23.0 631e Purgation – – – Torgerson et al. (2003)

NS Domestic 1463 5.8 27e Purgation – – – Torgerson et al. (2003)
2002 Farm 131 13.7f NS Purgation/ 31 (E) 12S rRNA G1 (57.1%); E.m. Stefanic et al. (2004)
Coproscopy/ (42.9%)
PCR
2002 Farm 131 28.2f – CpAg-ELISA – – – Stefanic et al. (2004)
2002 Farm – – – Coproscopy/PCR 9 (E) nad1, 12S rRNA G1 (33.3%); G6–G7 Trachsel et al. (2007)
(22.2%); E.m.
(44.5%)
2003–05 Domestic 632 13.4; 4.6 812d ; 72d Purgation – – – Torgerson et al. (2009)
d
Kyrgyzstan 2001 Mixed 1214 11.2 496 Necropsy – – – Torgerson et al. (2006)
2005 Domestic 466 19.0c ; 18.0c 50e ; 65e Purgation/ 139 (E, AW) nad1, 12S rRNA G1–G3 (56.2%); G4 Ziadinov et al. (2008)
Coproscopy/ (0.7%); G6–7
PCR (5.0%); E.m. (38.1%)

Mongolia NS NS 67 25.4f – CpAg-ELISA – – – Zoljargal et al. (2001)

NS Stray 14 35.7 330 Necropsy – – – Wang et al. (2005)

Tajikistan NS Stray 120 15.2 NS Necropsy – – – Torgerson et al. (2006)

Turkey 2005–06 1 – – Purgation/PCR 1 (AW) cox1 G1 (100%) Utuk et al. (2008)

Uzbekistan NS Farm 279 20.1 NS Purgation – – – Torgerson et al. (2006)

NS Domestic 240 7.9 NS Purgation – – – Torgerson et al. (2006)

atp6: mitochondrial ATP synthase subunit 6; cox1: mitochondrial cytochrome c oxidase subunit 1; E.g.: Echinococcus granulosus sensu lato; E.m.: Echinococcus multilocularis; ITS2: ribosomal internal transcribed spacer 2; nad1:
mitochondrial NADH dehidrogenase subunit 1; NS: not specified; rrnL: large subunit of ribosomal RNA; U1 snRNA: U1 small nuclear RNA; 12S rRNA: 12S small subunit ribosomal RNA.
a
Number of dogs analyzed by necropsy/purgation or number of faecal supernatants analyzed by CpAg-ELISA (ELISA for the detection of copro-antigens).
b
An isolate is defined here as parasite DNA extracted from Echinococcus adult worms (AW) or taeniid eggs (E) from an individual, infected dog.
c
Prevalence adjusted for the sensitivity and specificity of the diagnostic technique used.
d
Mean intensity of infection (mean number of parasites per infected dog).
e
Mean abundance of infection (mean number of parasites per dog examined).
f
Estimated prevalence for Echinococcus spp.

447
448 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
Neither dog sex nor dog age seemed to be significantly associated
with canine echinococcosis prevalence rates in Iran (Maleky and
Moradkhan, 2000; Razmi et al., 2006), although this information
should be interpreted with caution due to the comparatively low
number of dogs surveyed in this country.
Echinococcus genotyping data in infected dogs are currently only
available from Iran, Jordan and Turkey (Fig. 1 and Table 2). In all
these countries E. granulosus s.s. is the causative agent of the vast
majority of canine infections, with the G1 genotype accounting
for 75–100% of the isolates identified. Although limited in num-
ber, these somehow expected results corroborate our previous
knowledge of the parasite’s genotype frequency in livestock species
(reviewed in Cardona and Carmena, 2013) and humans (Pezeshki
et al., in press; Snábel et al., 2009) from these countries. E. granu-
losus s.s. G1 is the only genotype reported in Turkish dogs to date.
However, the recent identification of E. canadensis genotype G7 in
a single human CE case from Turkey (Snábel et al., 2009) suggests
that this strain may be also present in dogs. This finding would have
important consequences in the design of effective CE control cam-
paigns, as the G7 genotype has a shorter maturation rate in dogs
compared with E. granulosus s.s. (McManus et al., 2003). Of partic-
ular interest is the identification of a G4-like genotype infecting a
single dog in Jordan (Al-Qaoud et al., 2003). If confirmed, this would
constitute the first evidence of the presence of E. equinus in Western
Asia in recent years. Finally, although E. canadensis still has not been
reported infecting dogs in this geographical region, this strain is
also known to be circulating among sheep, cattle and camels in Iran
(and probably in other neighbouring states), providing evidence of
the presence of pig–dog and camel–dog transmission cycles of the
parasite.
4.4. Current situation of canine echinococcosis in South Asia
Echinococcosis is a serious animal health concern in India and
Pakistan. The infection has been also documented in Nepal (Baronet
et al., 1994; Joshi et al., 1997), although updated epidemiologi-
cal data from this country is lacking. In addition, the molecular
characterization of isolates from different livestock species has
demonstrated the presence of E. granulosus s.s., E. ortleppi, and E.
canadensis circulating in India and Pakistan (reviewed in Cardona
and Carmena, 2013). E. granulosus s.s. G1 is the only genotype
identified in human cases in Pakistan (Latif et al., 2010), but no
information about the genotypes of Echinococcus spp. infecting
human populations exists in India (Singh et al., 2012). Despite the
relative abundance of information available in production animals,
epidemiological data on Echinococcus infection in dogs are much
scarcer. An Echinococcus copro-antigen-positive rate of 4% has been
reported in Indian stray dogs (Prathiush et al., 2008). No reports on
the occurrence of E. multilocularis in dogs from India or Pakistan
have been found in the literature published since 2000. More
research should be conducted to improve our current knowledge on
canine echinococcosis prevalence rates and genotype frequencies
in South Asia.
4.5. Current situation of canine echinococcosis in East Asia
Canine echinococcosis is relatively well documented in China,
where a wealth of information has become available in recent years
(see Table 2). Reported prevalence rates were in the range of 8–67%
for infections caused by E. granulosus s.l. and 3–36% for infections
caused by E. multilocularis, depending on the dog population and
region of study and the diagnostic test used. High infection rates
were also typically paralleled with high infection intensities. Over-
all, prevalence figures based on purgation tended to be lower than
those obtained by necropsy or CpAg-ELISA. This is in line with pre-
vious investigations (see e.g. Ziadinov et al., 2008) highlighting the
fact that the intrinsic low diagnostic sensitivity of purging leads
to underestimate the true prevalence of canine echinococcosis. A
striking feature is the elevated number of surveys in which both
E. granulosus s.l. and E. multilocularis were found causing single
or even mixed infections in the same dog population (He et al.,
2000; Ma et al., 2012; Wen et al., 2006; Xiao et al., 2006; Yang
et al., 2009; Zhang et al., 2006). Furthermore, the finding that pikas
can also harbour concurrent infections with both E. multilocularis
and E. shiquicus strongly suggests that dual infections by these two
Echinococcus species may also occur in definitive hosts, including
domestic dogs (Xiao et al., 2006). Indeed, this seems to be the actual
case, as demonstrated in a recent molecular reappraisal survey
where canine coproDNA isolates from an earlier canine purgation
study (Budke et al., 2005a) and previously believed to belong to
E. granulosus or E. multilocularis has been now characterized as E.
shiquicus (Boufana et al., 2013). In addition, the fact that mature E.
multilocularis and E. shiquicus are morphologically very similar may
have led to misidentification of adult worms of both Echinococcus
species in definitive hosts in the past (Xiao et al., 2006). Clearly,
more research is needed to confirm the host range of E. shiquicus
and its potential to cause human infections. Taking together, all the
above findings demonstrate that E. granulosus s.l., E. multilocularis
and E. shiquicus occur sympatrically in large areas of China.
A transmission dynamics study carried out in the Sichuan
province has demonstrated the induction of protective immunity
in dogs infected with E. granulosus s.l. at a prevalence of 8–19% and a
mean abundance of 80 worms per dog, but not in dogs infected with
E. multilocularis at a prevalence of 13–33% and a mean abundance
of 131 worms per dog (Budke et al., 2005b). Seasonality, insuffi-
cient infection pressure and differences in the host immunological
response to E. granulosus s.l. versus E. multilocularis were proposed
by the authors as potential explanations for the failure of E. multilo-
cularis in stimulating host protective immunity. Moreover, Budke
et al. suggested that the degree of acquired immunity may be linked
to the marked differential distribution of mature E. granulosus s.l.
and E. multilocularis in the small intestine of infected dogs, with
E. granulosus s.l. occupying preferentially the anterior region and E.
multilocularis the posterior region. This pattern has been previously
observed in dogs harbouring natural mixed infections (Xiao et al.,
2006; Zhang et al., 2006) or experimentally co-infected (Thompson
and Eckert, 1983) with E. granulosus s.l. and E. multilocularis. It might
be also speculated that this preferential tropism is the result of a
co-evolutionary process where E. granulosus s.l. and E. multilocu-
laris avoid direct competition by exploiting nutrient resources in
different intestinal settings.
Significantly higher canine echinococcosis prevalence rates
were found in male dogs in a study conducted in Western China
(Budke et al., 2005a). Territorial behaviour and increased hunting
habits in male dogs were thought to be the most likely cause of
this finding. Notably, periodical anthelmintic treatment of dogs
and culling of unwanted and stray dogs have been proven effi-
cient, highly cost-effective measures to control the infection in the
Xinjiang Uyghur Autonomous Region (Zhang et al., 2009).
Available molecular diversity data shows that E. granulosus s.s.
G1 genotype is responsible not only for the vast majority of the
canine infections reported in China (see Table 2), but also for most of
the livestock (reviewed in Cardona and Carmena, 2013) and human
(Bart et al., 2006; Li et al., 2008) isolates characterized to date. Inter-
estingly, a mixed infection of E. granulosus G1 and E. canadensis
G6 has been detected in a single dog from the Xinjiang Uyghur
Autonomous Region (Bart et al., 2006). The G6 genotype has been
also identified in two human CE cases from the same region (Bart
et al., 2006) and more recently in two goat isolates from the Yushu
Tibetan Autonomous Prefecture (Liu et al., 2013).
E. multilocularis is the only native species of the genus Echinococ-
cus present in Japan. The infection is restricted to Hokkaido, the
 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
northernmost island of the country, where wild foxes are the pri-
marily source of infective eggs. However, the increase in urban
foxes overlapping with the habitat of susceptible intermediate
hosts in peri-urban areas is leading to an increased risk of infection
to domestic animals (Tsukada et al., 2000). Indeed, E. multilocula-
ris infection rates ranging from 0.2% to 1.1% have been reported in
domestic dogs from Hokkaido (Table 2). A rising concern in recent
years is the role of travelling dogs in spreading the infection. It
has been estimated that 10,000–12,000 dogs travel annually from
Hokkaido to other Japanese prefectures, with up to 30 of them
carrying mature worms of the parasite (Doi et al., 2003). Not sur-
prisingly, E. multilocularis infected dogs known (or suspected) to
have been originally raised in Hokkaido have been later identified
in the Saitama prefecture of the island of Honshu (Yamamoto et al.,
2006) and in the island of Kyushu (Nonaka et al., 2009). A third dog
has been also found infected with the parasite after a 5-day visit to
Hokkaido, a fact that suggests a high infection pressure of E. mul-
tilocularis to domestic dogs in that endemic area (Morishima et al.,
2006).
In an attempt to assess the extent of dogs’ involvement in the
transmission of E. multilocularis in Japan, a mandatory national
surveillance system for canine echinococcosis has been in force
since 2004 (Kamiya et al., 2006). By law veterinarians who diag-
nose the infection in dogs are required to report the case to the
health authorities. However, this initiative has not been supported
by the implementation of practical control measures (e.g. compul-
sory quarantine or anthelmintic treatment) to minimize the risk of
disease dispersal by dogs travelling to non-endemic areas (Kamiya
et al., 2006).
Finally, high E. multilocularis and E. granulosus infection rates
have been reported in dogs and foxes from Mongolia (Table 2),
strongly suggesting that this region is also co-endemic for canine
echinococcosis (Wang et al., 2005). In contrast, epidemiological
and/or molecular data on Echinococcus spp. infections in human
and livestock populations are still lacking in this country.
4.6. Current situation of canine echinococcosis in Southeast Asia
Echinococcus infections seem to be rare in Southeast Asian
countries, which consequently are not considered endemic for
echinococcosis. For instance, 22 human cases of CE and 2 of AE
have been reported in Thailand from 1936 to 2005, although canine
and production animal infections have not been documented for
the same period (Waikagul et al., 2006). Sporadic cases of human
CE, either imported or locally acquired, have also been reported in
Vietnam, Cambodia, Laos, Malaysia, Indonesia, and the Philippines
(Schantz et al., 1995), but the current epidemiological situation of
the parasite in these countries is largely unknown and in need of
update.
5. Canine echinococcosis in Europe
E. granulosus s.l. is present in large areas of Europe, particu-
larly those where the sheep-raising industry still represents an
important contribution to the local economy, such as the Iberian,
Balkan, and Italian peninsulas. Focuses of disease are also known
in Great Britain and the Baltic States (reviewed in Dakkak, 2010
and Romig et al., 2006). E. granulosus s.l. infection has been docu-
mented in wolves from Spain (reviewed in Carmena et al., 2008)
and Italy (Guberti et al., 2004), suggesting an overspill from the
domestic to the sylvatic life cycle of the parasite. In contrast,
the geographical distribution of E. multilocularis comprises a core
endemic area including East-Central France, Switzerland, Southern
Germany, and Western Austria. However the cestode has spread
in recent decades towards adjacent countries including Belgium,
449
Denmark, The Netherlands, and the Baltic States (Davidson et al.,
2012; Enemark et al., 2013; Vuitton et al., 2011, 2003). The typical
transmission cycle of E. multilocularis in Europe is wildlife-based,
involving foxes as definitive host and small rodents as intermedi-
ate hosts. Racoon dogs have also been described as suitable final
hosts in Northwestern Europe (see e.g. Bruzinskaite-Schmidhalter
et al., 2012), though they are thought to play a minor role in the
transmission of the parasite (Davidson et al., 2012).
E. granulosus s.s., E. ortleppi, E. canadensis, and E. equinus are
known to be circulating in Europe (see Cardona and Carmena,
2013). Isolates characterized as E. granulosus s.s. and E. canadensis
are predominantly reported from countries of the Mediterranean
basin. These Echinococcus species are rarely found in Central
Europe, where occurrence of autochthonous CE cases is limited
to sporadic infections due to E. equinus and E. ortleppi (Jenkins
et al., 2005). Regarding E. multilocularis, recent molecular stud-
ies based on microsatellite patterns and mitochondrial sequences
have evidenced a maximal genetic diversity in isolates from Austria,
France, Germany, and Switzerland, and lower genetic diversity in
adjacent countries/regions (Davidson et al., 2012). These findings
provide evidence in support of the ‘mainland-island’ hypothe-
sis, where island populations originated as a consequence of the
spreading of the parasite from long-established mainland popula-
tions exhibit lower genetic variation than their source populations
(Davidson et al., 2012). In addition, European E. multilocularis
isolates constitute a geographical-specific clade that differs signifi-
cantly from Asian and North American isolates (Nakao et al., 2009).
5.1. Current situation of canine echinococcosis in Northern
Europe
Canine echinococcosis is thought to be re-emerging in mid-
Wales (Great Britain), based on increased prevalences of 8.1%
(Buishi et al., 2005a) and 10.6% (Mastin et al., 2011) positive dogs for
Echinococcus copro-antigen in 2002 and 2008, respectively, com-
pared with 3.4% in the same areas during the period 1989–1993
(Table 3). Roaming behaviour, inadequate anthelmintic treatment
and home-slaughter practices were factors strongly associated
with copro-antigen positivity in these studies. Recrudescence of
infection in farm dogs was likely due to the withdrawal of the super-
vised dog-dosing scheme carried out from 1983 to 1989, which
was subsequently replaced by a health promotion and education
campaign (Buishi et al., 2005a). In an attempt to prevent human
infections, a new public awareness campaign and a 10-year de-
worming programme were initiated in 2008. Regarding canine
echinococcosis caused by E. multilocularis, recent field epidemi-
ological studies have failed to demonstrate the presence of this
parasite in wild foxes in Great Britain (Learmount et al., 2012) and
Ireland (Murphy et al., 2012). Based on these data, both countries
are believe to be E. multilocularis-free, providing the epidemiolog-
ical ground to support the maintenance of the current mandatory
regulation (also known as the pet passport scheme) by which any
dog travelling into the UK from an area where E. multilocularis
is endemic must have been treated for tapeworms. The system
is specifically designed to minimize the risk of importation of E.
multilocularis via travelling dogs, and, if abandoned, an accidental
introduction would almost inevitably lead to the establishment and
dispersal of the parasite in these countries (Torgerson and Craig,
2009).
No Echinococcus infection has been reported in dogs from
Denmark, Norway, Sweden, Estonia, and Latvia. In the latter
country, however, the fact that at least 44 human CE and AE cases
have been recorded during the period 1996–2010 (Tulin et al.,
2012) clearly indicates that both E. granulosus s.l. and E. multi-
locularis must be also causing canine infections. In Finland, no
Echinococcus copro-antigen positive results were obtained after
 450
Table 3
Prevalence and molecular epidemiology of Echinococcus granulosus s.l. (font in black) and E. multilocularis (font in red) infections in dogs in Europe (2000 onwards).

Country Period Dog No. samplesa Prevalence (%) Worm Diagnostic procedure Molecular characterization Reference
population burden (n)

No. isolatesb Gene markers Genotype frequency

(%)

Albania 2004–09 Domestic 111 2.7 26–11,670 Necropsy/PCR 3 (AW) cox1 G1 (100%) Xhaxhiu et al. (2011)
Cyprus 1997–00 Farm 6551 0.0–3.6c , d – CpAg-ELISA – – – Christofi et al. (2002)

Czech NS NS 118 11.9d – CpAg-ELISA – – – Lenska and Svobodova (2001)

Republic 1998 NS 55 1.8 – Coproscopy/PCR 1 12S rRNA E.m. (100%) Martinek et al. (2001)
2000–01 NS 186 8.1d – CpAg-ELISA – – – Svobodova and Lenska (2002)

France 1999–00 Farm 12 16.7d – CpAg-ELISA – – – Magnaval et al. (2004)

2008–10 Mixed 860 <1.0 – Coproscopy/PCR 0 (E) 12S rRNA No PCR product Umhang et al. (2012)

D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

Germany 2004–05 Domestic 17,894 0.2 – Coproscopy/PCR 43 (E) 12S rRNA E.m. (100%) Dyachenko et al. (2008)

Greece NS Mixed NS 1.0–50.4 NS – – – Sotiraki et al. (2003)

1985–87 NS 110,093 3.3 – Purgation – – – Sotiraki et al. (2003)

Italy NS Mixed 300 3.0–10.0d – CpAg-ELISA – – – Varcasia et al. (2011)

NS Mixed 113 31.8d – CpAg-ELISA – – – Giangaspero et al. (2006)
Kosovo 2003–04 Mixed 305 1.3 – Coproscopy/PCR 4 (E) 12S rRNA G1 (100%) Sherifi et al. (2011)

Lithuania 2005–06 Farm 240 3.8; 0.8 – Coproscopy/PCR 11 (E) cox1; 12S rRNA G6–G7 (81.8%); E.m. Bruzinskaite et al. (2009)
(18.2%)

Romania 2005–06 Farm 40 12.5 – CpAg-ELISA – – – Seres et al. (2006)

2008–09 Farm 48 77.1 – Copro-PCR – 12S rRNA – Seres et al. (2009)
2005–08 Farm 1892 19.2d – CpAg-ELISA – – – Seres et al. (2010)
1956–92 NS 12,009 21.6 – Necropsy – – – Neghina et al. (2010)

Slovakia 2006 Mixed 752 0.1 – Coproscopy/CpAg-ELISA/PCR 1 (E) 12S rRNA E.m. (100%) Szabová et al., 2007
2002–05 Mixed 289 2.8d – Coproscopy/CpAg-ELISA/PCR 12 (E) 12S rRNA E.m. (100%) Antolova et al. (2009)

Spain 2000 Mixed NS 0.2 – Necropsy – – – Jimenez et al. (2002)

NS Shelter 1040 0.5 – Necropsy – – – Benito et al. (2003)
1997–98 Farm 721/754 8.0c , d – CpAg-ELISA/Ab-ELISA – – – Benito et al. (2006)
1994 ND – – – Coproscopy/PCR 12 (E) nad1, 12S rRNA G1 (91.7%); G6–G7 Trachsel et al. (2007)
(8.3%)

Switzerland 1996–97 Feral 86 7.0d – Coproscopy/CpAg-ELISA/PCR 6 (E) U1 snRNA E.m. (100%) Gottstein et al. (2001)
NS Mixed 505 0.4d – Coproscopy/CpAg-ELISA/PCR 1 (E) 12S rRNA E.m. (100%) Sager et al. (2006)
NS Mixed 306 1.0 – Coproscopy/PCR 3 (E) NS E.m. (100%) Nagy et al. (2011)

UK 2002 Farm 1164 8.1 – CpAg-ELISA – – – Buishi et al. (2005a)

2008 Farm 577 10.6 – CpAg-ELISA – – – Mastin et al. (2011)

Cox1: mitochondrial cytochrome c oxidase subunit 1; E.m.: Echinococcus multilocularis; nad1: mitochondrial NADH dehidrogenase subunit 1; NS: not specified; U1 snRNA: U1 small nuclear RNA; 12S rRNA: 12S small subunit
ribosomal RNA.
a
Number of dogs analyzed by necropsy/purgation, or number of faecal supernatants or serum samples analyzed by coproscopy/CpAg-ELISA/Ab-ELISA (ELISAs for the detection of copro-antigens or circulating antibodies,
respectively).
b
An isolate is defined here as parasite DNA extracted from Echinococcus adult worms (AW) or taeniid eggs (E) from an individual, infected dog.
c
Prevalence adjusted for the sensitivity and specificity of the diagnostic technique used.
d
Estimated prevalence for Echinococcus spp.
 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
examining 352 dog faecal samples in reindeer herding areas dur-
ing 1999–2001, despite E. granulosus s.l. was previously known
to circulate in the wild among wolves, reindeers and elks in the
Eastern part of the country (Hirvelä-Koski et al., 2003). In Lithua-
nia, the molecular analysis of taeniid eggs isolated from dog faecal
samples revealed the presence of E. granulosus s.l. and E. multi-
locularis in 3.8% and 0.8% of samples, respectively (Bruzinskaite
et al., 2009). E. multilocularis infections have been frequently doc-
umented in wild foxes and wolves in most of the above mentioned
countries. Of particular relevance is the recent reporting of two
foxes infected with E. multilocularis in Sweden (Osterman Lind
et al., 2011), a country previously thought to be free of this cestode.
Although not completely elucidated, it is believed that the parasite
was introduced by accidental translocation with infected dogs, in
spite of the legal requirement to de-worm dogs before entering the
country. Infected travelling dogs are also the prime suspects for the
introduction of the parasite into Denmark (Davidson et al., 2012),
where E. multilocularis is now known to naturally infect domes-
tic cats and wild foxes (Dyachenko et al., 2008; Enemark et al.,
2013). As in the case of Great Britain, Ireland or Japan, this situa-
tion highlights the importance of implementing effective measures
involving pet travel regulation and tapeworm treatment to prevent
the accidental introduction of the parasite on E. multilocularis-
free areas. Finally, echinococcosis has been eradicated in Iceland,
where no hydatid cysts have been reported in livestock since 1979
(Sigurdarson, 2010).
Very limited information is available regarding the genotypic
variability of E. granulosus in North European dogs (Fig. 1 and
Table 3). E. canadensis G6–G7 genotypes have been identified in
canine isolates in Lithuania, confirming the predominance of this
strain in the Baltic States (Bruzinskaite et al., 2009). Although E.
granulosus s.s. and E. equinus are the only two Echinococcus species
known to be endemic in Great Britain (reviewed in Romig et al.,
2006), molecular evidence on canine echinococcosis infections
from this and other North European countries is currently lacking.
5.2. Current situation of canine echinococcosis in Western Europe
E. multilocularis is highly endemic in Western European
countries. Elevated E. multilocularis prevalence rates are routinely
recorded in wild foxes from Switzerland and several regions of
Belgium, France, and Germany (Davidson et al., 2012; Romig
et al., 2006). The latter three countries also accounted for 77.1%
of confirmed human AE cases reported in the European Union
in 2009 (EFSA, 2011), whereas in Switzerland the mean annual
incidence per 100,000 inhabitants was 0.26 during 2001–2005
(Schweiger et al., 2007). The increase of urban fox populations
observed in recent decades had led to the environmental contami-
nation of city parks and gardens, accentuating the risk of infection
among small rodents and, consequently, the potential infection of
domestic dogs if they prey on infected rodents (Reperant et al.,
2007). Consistent with this epidemiological scenario, E. multilo-
cularis causes the vast majority of canine echinococcosis cases
in these countries (Fig. 1). The infection is generally recorded at
low prevalence rates (see Table 3), suggesting that dogs do not
play a significant role in the maintenance of the parasite’s life
cycle, although they most likely constitute the main source of
human AE infections. In France canine echinococcosis prevalence
rates reported since 2000 varied from <1% to 17%, depending on
the region and method of study. Dog’s owner low compliance
regarding anthelmintic application was considered the main risk
factor associated to the infection in dogs (Umhang et al., 2012).
In an international coprological survey, E. multilocularis was only
identified in 0.2% of dog faecal samples from Germany (Table 3),
but not in dog faecal samples from Austria (n = 812), Denmark
(n = 517), Great Britain (n = 121), France (n = 980), Italy (n = 249),
451
Luxembourg (n = 165), and The Netherlands (n = 734). In this regard,
it is important to bear in mind that a negative result only provides
probability, not proof, of absence of infection. Importantly, in this
study 81% of taeniid egg-positive samples were further confirmed
as E. multilocularis-positive (Dyachenko et al., 2008). Therefore,
from a practical perspective the authors recommended that dogs
shedding taeniid eggs in endemic areas should be assumed to be
infected by E. multilocularis. Finally, occurrence of E. multilocularis
in dogs from Switzerland has been estimated to be in the range of
0.4–7% (Table 3), although neither taeniid eggs nor specific copro-
antigens of this cestode could be detected in the 56 environmental
dog faecal samples in the municipality of Zurich (Stieger et al.,
2002). Access to small rodents, offal, and carrion was identified as
risk factor for canine echinococcosis infection in this country (Sager
et al., 2006).
Canine infections by E. granulosus s.l. seem to be rare in Western
Europe, in line with the very low (or absent) CE prevalence rates in
livestock intermediate hosts reported from countries of this region
(reviewed in Cardona and Carmena, 2013; Umhang et al., 2013).
5.3. Current situation of canine echinococcosis in Eastern Europe
E. granulosus s.l. and E. multilocularis have been recorded from
all Eastern European countries, sometimes occurring sympatrically
(Fig. 1 and Table 3). In Bulgaria, reliable epidemiological data on
canine echinococcosis goes back to the period 1986–1990, when
the reported prevalence was 12%. However, cessation of control
measures as consequence of administrative and economic changes
in the country in the following years has led to an alarming resur-
gence of human CE (Todorov and Boeva, 1999), suggesting that
canine infection rates may have also risen since then. Echinococ-
cus copro-antigen prevalences ranging from 3 to 12% have been
reported in dog populations from areas of the Czech Republic and
Slovakia known to be endemic for E. multilocularis infection in wild
foxes (Table 3). Indeed, PCR-based prevalence data have confirmed
the presence of E. multilocularis in 0.1%–1.8% of dogs analyzed
from these countries. However, the facts that CpAg-ELISA is only a
genus-specific test and that molecular data were obtained using E.
multilocularis-specific primers only do not allow excluding the pos-
sibility of infections caused by E. granulosus in dogs from the Czech
Republic and Slovakia. Canine echinococcosis prevalence rates in
the range of 12–22% have also been recorded in Romania (Table 3),
where E. granulosus s.s. G1 is the only genotype identified infecting
dogs to date (Seres et al., 2009). However, the recent character-
ization of two human isolates as E. multilocularis (see Siko et al.,
2011) and an additional one as E. canadensis (Piccoli et al., 2013)
seems to indicate that these are minority circulating Echinococcus
species in Romanian dogs. Similarly, human CE and AE are both
well documented in Poland and Russia. In Poland, 121 human AE
cases have been recorded during the period 1990–2011, with as
many as 72% of the affected patients declaring to have household
dogs (Nahorski et al., 2013). In this country a total of 36 human CE
and AE cases were reported only in 2010 (Waloch, 2012). On the
other hand, E. granulosus s.s. G1, E. canadensis G6, and E. multilocu-
laris (Asian-type) genotypes have been identified in Russian human
isolates (Konyaev et al., 2012). These data strongly support the idea
that the above mentioned Echinococcus species must be also caus-
ing infections in dogs. This possibility needs further confirmation
in future canine echinococcosis epidemiological studies from these
countries.
Dog age (3–5 years) was found a significant risk factor for a
copro-antigen positive result in a Romanian dog population (Seres
et al., 2010), but not in a Slovakian one (Antolova et al., 2009). In
the latter study, farm dogs were identified as the dog class bearing
the highest risk of Echinococcus infection. Dogs feeding on offal or
small rodents, and incomplete or lacking anthelmintic treatment
452 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

were allegedly reported in these studies as the most likely causes epidemiological information is currently available from Bolivia
of contracting and maintaining Echinococcus infections in dogs. and Paraguay, whereas the disease seems to be rare or absent in
Colombia, Ecuador, Guyana, French Guiana, Surinam, Venezuela,
and the Central American and Caribbean countries. Localized
5.4. Current situation of canine echinococcosis in Southern
foci of infection have also been identified in Western USA (Moro
Europe
and Schantz, 2006, 2009). In all these regions the infection is
transmitted through the classical domestic cycle involving dogs
Available canine echinococcosis epidemiological data from
as definitive hosts and sheep, goats, cattle, equines, pigs, and
Southern European countries indicate that E. granulosus s.s.
alpacas as livestock intermediate hosts (reviewed in Cardona and
accounts for the vast majority of Echinococus infections in dogs,
Carmena, 2013). A wildlife transmission cycle is also known to be
with E. multilocularis playing a marginal role (Table 3). The infec-
maintained among wolves and moose, caribou, and other cervids in
tion is endemic in Spain, where earlier necropsy-based studies
Northern America including Canada and Alaska (Moro and Schantz,
revealed infection rates between 0% and 1.4% of the investigated
2006). The geographical distribution of E. multilocularis comprises
dog populations, depending on the region of origin and dog class
Northern North America and Central areas of USA, where foxes and
(reviewed in Carmena et al., 2008). More recent surveys have
coyotes have been reported as the sole definitive host species of this
reported prevalence rates ranging from 0.2% to 0.5% at necropsy
Echinococcus strain (Catalano et al., 2012; Davidson et al., 2012).
(Table 3), although some others failed to detect the presence of
Human populations at risk of CE/AE in the Americas are predom-
the parasite using the same technique (Martinez-Carrasco et al.,
inantly those engaged in sheep farming, transhumant pastoralism,
2007; Martinez-Moreno et al., 2007). A high infection rate of 8%
and hunting/trapping activities. Typical contributing factors to the
was observed in sheep dogs by antibody and CpAg-ELISA tests, con-
transmission of Echinococcus spp. infection in these regions include
firming this dog class as the one mainly involved in the domestic
extensive ovine husbandry, home slaughter of adult sheep, lack
transmission of Echinococcus in this region (Benito et al., 2006). In
of veterinary supervision, and low socio-economic and cultural
this survey no correlation between copro-antigen positive values
status of the population (Larrieu et al., 2000; Moro and Schantz,
and dog age could be demonstrated. A similar result was previ-
2006).
ously obtained in domestic dogs from Kazakhstan at a prevalence of
Available molecular data from American isolates reveal a com-
5.8%, suggesting an insufficient parasite infection pressure to trig-
plex epidemiological situation where several Echinococcus species
ger the dog protective immune response (Torgerson et al., 2003).
may co-exist in a given region. Only in South America at least 6 par-
Canine echinococcosis is also assumed to be present in adjacent
asite variants have been documented infecting livestock species
Portugal, although a recent copro-epidemiological survey failed to
to date, including E. granulosus s.s. G1, G2, and G3 genotypes,
amplify Echinococcus-specific DNA from taeniid eggs isolated from
E. ortleppi, and E. canadensis G6 and G7 genotypes (reviewed in
farm dogs (Cardoso et al., in press).
Cardona and Carmena, 2013). E. granulosus G1 is, with difference,
CE represents also a serious human and animal health problem
the most ubiquitous genotype identified, highlighting the predom-
in Italy, being the island of Sardinia one of the most affected regions.
inance of the sheep-dog cycle in the transmission of the parasite.
Canine echinococcosis prevalences in the range of 4–25% have been
In addition, E. vogeli and E. oligarthrus are also known to circulate
previously recorded in Northern Italy and Sicily (Garippa, 2006),
among wild animal species in the tropical forest of South and Cen-
while more recent studies reported infection rates of 3–32% in the
tral America (D’Alessandro and Rausch, 2008). Genotypic variability
Central part of the country and Sardinia (Table 3). For a detailed
of Echinococcus seems more limited in North America, where only E.
review of the canine echinococcosis epidemiological situation in
granulosus s.s. G1, E. canadensis G7, and the North American-specific
Italy before 2000, the interested reader is referred to earlier reviews
clade of E. multilocularis have been identified so far (Davidson et al.,
(e.g. Garippa et al., 2004). No autochthonous cases of human AE or
2012; Jenkins et al., 2005; Nakao et al., 2009).
canine infections by E. multilocularis have been documented to date,
although this Echinococcus species is known to naturally infect wild
6.1. Current situation of canine echinococcosis in Northern
fox populations in Northern Italy (Manfredi et al., 2006).
America
In Slovenia, confirmed cases of human CE (n = 34) and AE (n = 9)
have been documented during 2001–2005 (Logar et al., 2007). E.
Echinococcus s.s. infection almost certainly caused by the G1
granulosus s.l. is also the only Echinococcus species known to cause
genotype is known to have significantly affected sheep rearing
human infections in Serbia, where official figures have reported 409
areas in Western USA, including Arizona, California, New Mexico,
cases during 1998–2010 (Bobic et al., 2012). Although the current
and Utah in past decades. Implementation of CE control pro-
epidemiological situation of canine echinococcosis is unknown,
grammes in these regions successfully reduced, or even ceased, the
these results indicate that infected dogs are the most likely source
transmission of the parasite (Jenkins et al., 2005). Consequently,
of human CE and AE infections in these countries. In line with
the disease is currently maintained at low prevalence levels, and
these findings, E. granulosus s.s. G1 genotype has been recently
autochthonous human CE cases occur only sporadically (Moro and
identified infecting 1.3% and 2.7% of dogs in adjacent Kosovo and
Schantz, 2009). E. canadensis G8 genotype has been identified circu-
Albania, respectively (Fig. 1 and Table 3). However, because only
lating among wolves and dogs (definitive hosts) and large cervids
PCR primers for detecting this specific strain were used in Kosovo’s
such as moose and caribou (intermediate hosts) in Canada and
study, this result does not exclude the possibility of the presence
Alaska (Moro and Schantz, 2006; Rausch, 2003). Recent copro-
of other Echinococcus genotypes in dogs from that country (Sherifi
epidemiological and molecular studies have reported the presence
et al., 2011).
of E. canadensis G10 in Canadian stray dogs at a prevalence of 4–6%
and a mean intensity of infection of 22 worms per dog (Himsworth
6. Canine echinococcosis in the Americas et al., 2010a,b and Table 4). The authors noted an aggregated pattern
of infection, with few dogs harbouring most of the parasite biomass
Echinococcosis caused by E. granulosus s.l. is a major public and the remainder of the population having lower infection inten-
health problem in sheep rearing areas of South America. Major sities. These data suggest that infected dogs are a very probable
endemic areas include Patagonian Argentina, Southern parts source for human disease in Canada, where at least 19 human CE
of Brazil and Chile, Central and Southern Peruvian Andes, and cases have been confirmed between 1991 and 2001 (Somily et al.,
Uruguay (Jenkins et al., 2005; Moro and Schantz, 2006). Little 2005). In addition, eight human CE cases (but no human AE cases)
 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
have been reported since 1990 in Alaska (DHSS, 2003). The zoonotic
potential of the E. canadensis G10 genotype and the fully character-
ization of its natural intermediate host reservoir (very likely cervid
species) remain to be completely elucidated.
The distribution of E. multilocularis, historically accepted to be
confined to the Northern tundra region of Canada and USA, is now
believed to have expanded to South Canada and North Central USA,
as the geographical range of suitable definitive and intermediate
host species is increasing in these regions (Jenkins et al., 2005; Moro
and Schantz, 2009). Interestingly, high infection levels in wild ani-
mal hosts do not seem to directly translate in increased numbers of
human infection, as only two human AE cases have been reported
in this area to date (Jenkins et al., 2005). It might be speculated that
this situation is caused, at least partially, by the lack of overlapping
between sylvatic and domestic transmission cycles of the parasite.
However, this hypothesis may be disproved by recent epidemiolog-
ical evidence demonstrating that fox and coyote populations have
been increasingly found in urban areas (Catalano et al., 2012). As
previously reported in other parts of the world (see Sections 4.5 and
5.2), environmental faecal contamination by foxes and/or coyotes
may infect small rodent populations in urban settlements. Conse-
quently, domestic dogs occasionally preying on infected rodents
will also acquire the disease, leading to the establishment of a peri-
domestic cycle of E. multilocularis and becoming a potential source
of human disease. Given this situation, more research is advisable
in order to complete our current knowledge on the geographical
distribution of the cestode in North America. Genetic characteriza-
tion of wild animal isolates would also provide useful information
to assess its zoonotic potential.
6.2. Current situation of canine echinococcosis in Central America
Echinococcus granulosus s.l. is thought to be rare or non-existent
in most countries of Central America (Moro and Schantz, 2006).
Nevertheless, E. vogeli and E. oligarthrus occur in the humid tropical
forests of this geographical area (D’Alessandro and Rausch, 2008).
The natural cycle of E. vogeli is primarily sylvatic and includes the
bush dog as a definitive host, and the paca as an intermediate host.
Because pacas are extensively hunted for human consumption and
domestic dogs are often fed their infected raw viscera, this ces-
tode probably circulates also within a partially synanthropic cycle.
Indeed, domestic dogs are the most likely source of infection of the
human infections allegedly caused by E. vogeli in Ecuador (n = 11),
Costa Rica (n = 1), Nicaragua (n = 1), and Panama (n = 2) until 2007
(D’Alessandro and Rausch, 2008). On the other hand, E. oligarthrus
has wild cats (e.g. cougar, ocelot, and jaguar) as definitive hosts,
but no infections in humans or dogs have been reported in these
countries to date.
6.3. Current situation of canine echinococcosis in South America
CE control programmes implemented in Argentina from 1970
to 1990 have achieved a substantial decline in the prevalence of
infection among definitive and intermediate animal hosts (Larrieu
and Zanini, 2012; Moro and Schantz, 2006). For instance, canine
echinococcosis prevalence decreased from 41.5% in 1980 to 2.3%
in 1997 in the province of Rio Negro (Larrieu et al., 2000), and
from 28.2% in 1970 to 2.9% in 1990 in the province of Neuquén
(Pierangeli et al., 2010). A disturbing finding is the confirmation of
the infection in stray and domestic dogs from urban settlements,
providing evidence of the presence of an urban cycle of the para-
site, and highlighting the associated risk to human infection in these
areas (Lavallén et al., 2011). Despite the unquestionable progress
attained canine echinococcosis is still present in Argentina at
prevalence rates ranging from 3% to 19%, depending on the method
of analysis (Table 4). Consistent with the long-term control effort
453
maintained, most infected dogs harboured relatively low numbers
(5–100) of Echinococcus adult worms, with few canine infections
accounting for most of the parasite biomass (Pierangeli et al., 2010).
Taking together, these facts suggest that canine echinococcosis in
Argentina has reached a steady state in recent years, sufficient to
sustain the parasite at low prevalence but not to eradicate the
infection. Therefore, it would be highly advisable to maintain, or
even intensify, the control programmes currently in place in order
to avoid the spread of the disease. Regarding genotype variabil-
ity, canine isolates characterized to date have been allocated to
the E. granulosus s.s. G1 and E. canadensis G6 genotypes (Soriano
et al., 2010). Although not formally confirmed yet, E. granulosus
G2–G3, E. ortleppi, and E. canadensis G7 are also expected to be
circulating in dogs, as all these genotypes have been previously
reported in livestock species (reviewed in Cardona and Carmena,
2013).
Available epidemiological and molecular data on canine
echinococcosis in Brazil are restricted to the Rio Grande do Sul state,
contiguous to the Uruguayan and Argentinean borders. A CE control
programme was launched in this area in 1983, but after an initial
success it was shortly discontinued and, consequently, Echinococ-
cus prevalence rates reverted to pre-programme levels (Larrieu and
Zanini, 2012). Present canine echinococcosis prevalence rates have
been reported in the range of 11–39% (Table 4). Recent molecular
analyses have confirmed the presence of E. granulosus s.s. G1/G3
and E. ortleppi in canine isolates, mirroring the cestode genotypic
variation previously reported in humans and livestock species in
this state (de la Rue et al., 2011).
In Chile, a CE control programme at national scale was success-
fully implemented in 1982. Unfortunately, the decentralization of
the programme in 1997, together with the reduction of the pro-
phylactic anthelmintic intervention in dogs has inevitably leaded
to the recrudescence of the disease in the country (Larrieu and
Zanini, 2012). Canine echinococcosis prevalence rates in the range
of 2–11% have been documented from 2000 to date (Table 4). As
in other South American countries, an increasing urbanization of
the parasite’s life cycle has been also demonstrated in Chile, most
likely associated to customary home slaughter practices (Acosta-
Jamett et al., 2010). Therefore, younger dogs living in urban areas
and with no de-worming treatment have been demonstrated more
likely to be copro-antigen positive than older dogs in the Coquimbo
region (Acosta-Jamett et al., 2010). However, opposite results were
obtained in a canine purgation study carried out in the XII region,
where older dogs were significantly more infected by Echinococcus
s.l. than younger dogs (Alvarez et al., 2005). The absence of worm
burden data in these studies does not allow elucidating the poten-
tial role of acquired host immunity responses in explaining the age
pattern observed.
Canine echinococcosis is highly endemic in Peru, particularly
affecting indigenous pastoralist communities in the highlands of
the country. The infection is also present in urban settlements,
where stray dogs seem to easily gain access to hydatid-infected
offal improperly discarded at abattoirs (Moro et al., 2004; Reyes
et al., 2012). Recent infection rates reported in the literature range
from 6% to 79%, depending on the dog population and region of
study and the diagnostic test used (Table 4). Mean intensity of
infection has been estimated at 95 adult worms (Lopera et al.,
2003). A CpAg-ELISA-based study performed in the district of
Pacaraos (province of Huaral) found that younger dogs, dogs fed
with infected offal, and female dogs were significantly more likely
to have a CpAgELISA positive result, although the authors did not
believe that the age distribution of infection observed was due to
acquired immunity to Echinococcus re-infection (Moro et al., 2005).
In contrast, neither dog sex nor age was associated with likelihood
of infection in domestic dogs from the capital Lima (Reyes et al.,
2012).
 454
Table 4
Prevalence and molecular epidemiology of Echinococcus granulosus s.l. infection in dogs in the Americas (2000 onwards).

Country Period Dog population No. samplesa Prevalence (%) Worm burden (n) Diagnostic procedure Molecular characterization Reference

No. isolatesb Gene markers Genotype frequency

(%)

Argentina 1996 Domestic 598 2.8 NS Purgation – – – Larrieu et al. (2000)

2003 Farm 1042 2.9 – CpAg-ELISA/WB – – – Cavagion et al. (2005)

D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460

2001–03 Farm 365 5.2 NS Purgation – – – Perez et al. (2006)
2003 Farm 687 5.4 – CpAg-ELISA/WB – – – Perez et al. (2006)
2005–08 Farm 403 3.7 5 to >1000 Purgation – – – Pierangeli et al. (2010)
2005–08 Farm 403 12.4 – CpAg-ELISA – – – Pierangeli et al. (2010)
2005–09 Farm 10 – NS Purgation/PCR 10 (AW) cox1 G1 (90.0%); G6 (10.0%) Soriano et al. (2010)
2004 Mixed 46 8.7 – CpAg-ELISA/WB – – – Lavallén et al. (2011)
NS Farm 42 19.1 – CpAg-ELISA/WB – – – Dopchiz et al. (in press)

Brasil 2001–02 Domestic 44 11.4 NS Purgation – – – Farias et al. (2004)

2001–02 Domestic 44 38.6 – CpAg-ELISA – – – Farias et al. (2004)
2004–07 Farm 12 – NS Purgation/PCR 12 (AW) cox1, 12S rRNA G1 (83.4%); G3 (8.3%); de la Rue et al. (2011)
G5 (8.3%)

Canada NS Semi-stray 155 5.8 – Coproscopy/PCR 7 (E) nad1 G10 (100%) Himsworth et al. (2010a)
NS Semi-stray 155 4.5 – Coproscopy/PCR NS nad1 Putative G10 (100%) Himsworth et al. (2010b)

Chile 1992–97 Domestic 1932 11.0 NS Purgation – – – Apt et al. (2000)

2002 Farm 228 1.8 NS Purgation – – – Alvarez et al. (2005)
2005–06 Domestic 334 7.2 – CpAg-ELISA – – – Acosta-Jamett et al. (2010)

Peru 1998 Farm 74 33.8 95c Purgation – – – Lopera et al. (2003)

1998 Farm 106 79.2 – CpAg-ELISA – – – Lopera et al. (2003)
NS Stray 48 6.3 NS Necropsy – – – Moro et al. (2004)
NS Mixed 61 50.8 – CpAg-ELISA – – – Moro et al. (2005)
NS Domestic 22 36.4 – CpAg-ELISA – – – Reyes et al. (2012)

cox1: mitochondrial cytochrome c oxidase subunit 1; nad1: mitochondrial NADH dehidrogenase subunit 1; 12S rRNA: 12S small subunit ribosomal RNA; NS: not specified.
a
Number of dogs analyzed by necropsy/purgation or number of faecal supernatants analyzed by coproscopy/CpAg-ELISA (ELISA for the detection of copro-antigens) or CpAg-WB (Western blot for the detection of copro-antigens).
b
An isolate is defined here as parasite DNA extracted from Echinococcus adult worms (AW), cysts (C) or taeniid eggs (E) from an individual, infected dog.
c
Mean intensity of infection (mean number of parasites per infected dog).
 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
Table 5
Prevalence and molecular epidemiology of Echinococcus granulosus s.l. infection in dogs in Australia (2000 onwards).
Period Dog population No. samplesa Prevalence (%)
NS Wild 23 100
2002 Wild 27 22.2
NS Wild 221 64.7
NS Wild 21 76.2
NS Domestic 22 0.0
NS Farm 561 24.4
2003–06 Wild 126 39.7
a
Number of dogs analyzed by necropsy/purgation or number of faecal supernatants analyzed byCpAg-ELISA (ELISA for the detection of copro-antigens).
Historically, Uruguay has been regarded as one of the most
endemic regions for echinococcosis worldwide (Cohen et al., 1998;
Craig et al., 1995). A successful long-term CE control programme
has been in place in this country since 1992 to date. As a conse-
quence, canine echinococcosis infection rates decreased to 0.7% by
1997, with the goal of eradicating the infection by the year 2002
(Larrieu and Zanini, 2012). However, no new epidemiological data
on canine echinococcosis/CE prevalence has been published since
then, so the current status of the infection in this country remains
unknown.
Finally, there is an important lack of information regarding the
Echinococcus species causing infection in dogs from Chile, Peru, and
Uruguay. Molecular analyses of canine isolates from these regions
are required to understand the genotypic variability of the parasite
and to assess the risk to human infection.
7. Canine echinococcosis in Oceania
Echinococcus infection was probably introduced to Australia and
New Zealand with infected sheep imported in late 18th and early
19th centuries, spreading quickly in the fast-growing livestock and
dog populations and becoming a serious public health concern
in sheep-farming areas shortly after (Jenkins et al., 2005; Pharo,
2002). In Australia, the most affected regions encompass New South
Wales, the Australian Capital Territory, Victoria, Southwest West-
ern Australia, and Eastern Queensland (Jenkins and Macpherson,
2003). In all these areas Echinococcus s.s. is perpetuated through
the classical dog-sheep cycle. Of great epidemiological relevance is
the spillover of the parasite into wildlife, greatly enhanced by the
transhumant grazing practices in place until mid-1970s (Jenkins
and Morris, 2003). The sylvatic transmission of the parasite occurs
among dingoes, feral dogs, and foxes acting as definitive hosts
and macropodid marsupials (kangaroos, wallabies, and wombats)
and feral pigs as intermediate hosts (Banks et al., 2006; Jenkins,
2006; Jenkins et al., 2000). Indeed, wildlife is currently consid-
ered the main source of echinococcal infection to domestic animals
in Australia (Jenkins and Macpherson, 2003). In addition, infected
wild dogs wandering in the vicinity of outer suburbs have been
reported in the literature (Brown and Copeman, 2003; Jenkins et al.,
2008). The authors highlighted that areas frequented by these ani-
mals may become contaminated with worm eggs and be a potential
source of human infection. It has been speculated that wild dogs
may be directly responsible for a proportion of the human CE cases
occurring in Australia (Jenkins and Morris, 2003).
Canine echinococcosis prevalence in Australian wild dog popu-
lations based on necropsy and CpAg-ELISA results are in the range
of 22–100%. Wild dogs frequently have also large parasite burdens,
ranging from 1 to >300,000 adult worms (Table 5). Heavy worm
burdens (>1000 worms) have been found in 66% of the infected
wild dogs in the Maroochy Shire, Queensland, with 12% of the
infected animals carrying 85% of the parasite biomass (Jenkins
et al., 2008). Lower infection rates (up to 24%) have been reported
in working dogs (Table 5), suggesting that domestic dogs may
455
Worm burden (n) Diagnostic procedure Reference
2–42,600 Necropsy Jenkins et al. (2000)
NS Necropsy Brown and Copeman (2003)
10–309,750 Necropsy Jenkins and Morris (2003)
NS Necropsy Banks et al. (2006)
NS Purgation Banks et al. (2006)
NS CpAg-ELISA Jenkins et al. (2006)
30–104,000 Necropsy Jenkins et al. (2008)
have lesser significance than wild dogs as definitive hosts for the
transmission of E. granulosus s.s. in Australia (Banks et al., 2006).
Echinococcus granulosus s.s. G1 is the only member of the genus
Echinococcus known to occur in Australia (Jenkins et al., 2005),
although recent molecular studies of isolates obtained from defini-
tive host species are lacking. The remarkable ability of this strain to
infect a wide range of host populations may explain its successful
spread among the Australian wildlife.
Finally, CE has been declared provisionally eradicated in both
Tasmania and New Zealand, where well-funded and organized
control programmes have been in place for more than 30 years.
No autochthonous CE cases have been reported in Tasmania and
New Zealand since 1996 and 2000, respectively (Elliot, 1996; Pharo,
2002).
8. Concluding remarks
Echinococcosis/hydatidosis remains a serious public veterinary
health concern in many areas of the world. In most instances dogs
are regarded as the main definitive host species implicated in the
transmission of Echinococcus infection to humans. A concept that
needs special consideration is the influence, either directly or indi-
rectly, of human intervention in the prevalence, epidemiology, and
geographical distribution of canine echinococcosis. For instance,
discontinuation or cessation of control campaigns in endemic areas
normally translates into an immediate recrudescence of the dis-
ease in definitive and livestock hosts species. Translocation of
infected dogs from prevalent regions to Echinococcus-free areas is
the primarily suspected cause of the introduction of the infection
in countries like Denmark and Sweden, a fact that highlights the
relevance of national schemes enforcing anthelmintic treatment of
dogs prior to entry Echinococcus-free countries. In addition, the fox
vaccination campaigns against rabies launched in Western Europe
during the late 70s and early 80s led to the recovery of fox popula-
tions, which since then have expanded and colonized new habitats,
including urban environments. The increasing number of foxes in
European and Asian cities has been linked to the establishment
of an urban transmission cycle of E. multilocularis and higher risk
for human AE cases. Likewise, migration of infected coyotes and
wild dogs into urban settlements has been recently documented in
North America and Australia, respectively.
A number of unresolved questions regarding the transmission
dynamics of Echinococcus spp. in dogs need addressing in the near
future. The current epidemiological situation of canine echinococ-
cosis is unknown or outdated in many regions of the world. This
is particularly true for African countries, where prevalence data
are scarce and molecular studies aiming to estimate the genetic
diversity of canine isolates are completely lacking. More research
is also required to assess the relevance of sylvatic populations as
reservoir of disease to domestic species and humans. This includes
not only defining the range of wild host species susceptible to be
infected by Echinococcus spp., but also the prevalence and inten-
sity of the infection. These data would be valuable to model the
transmission of the parasite and estimate infection pressures to
456 D. Carmena, G.A. Cardona / Acta Tropica 128 (2013) 441–460
intermediate host species in a given region. The task is particu-
larly pressing in the case of the recently identified E. felidis and
E. shiquicus, given the very limited epidemiological information
currently available on these Echinococcus species, including their
zoonotic potential. Canine echinococcosis prevalence and molec-
ular data are also lacking from Northern European dogs, where
Echinococcus spp. infection may be much higher than initially sus-
pected. An issue that also deserves attention is the estimation of
the zoonotic potential of E. canadensis G10, a genotype recently
found infecting domestic dogs in Northern America. No less impor-
tantly, there is a real need to develop rapid and accurate diagnostic
molecular tools able to discriminate different Echinococcus species
occurring sympatrically in a given region.
Although control does not fall within the scope of this review,
it is worth mentioning that canine echinococcosis is a preventable
infection. Policy makers, educational and health authorities should
take into consideration many of the issues discussed here when
designing and implementing measures for disease control and pre-
vention. These must include the necessity of (i) educating the public
in order to improve hygiene habits, to minimize the parasite’s
chance of transmission, and to prevent initial contamination of
the environment; (ii) implementing and harmonizing international
laws to reduce the risk of introducing the infection in Echinococcus-
free areas/countries by dog/livestock movement; (iii) controlling
the size of stray dog populations, and (iv) routinely treating dogs
with appropriate anthelmintic drugs.
Conflict of interest
The authors declare that there is no conflict of interest.
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