Canine echinococcosis: Global epidemiology and genotypic diversity

Accepted Manuscript Title: Canine echinococcosis: Global epidemiology and genotypic diversity Author: David Carmena Guillermo A. Cardona PII: DOI: Reference:

S0001-706X(13)00207-6 http://dx.doi.org/doi:10.1016/j.actatropica.2013.08.002 ACTROP 3153

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Acta Tropica

Received date: Revised date: Accepted date:

26-5-2013 29-7-2013 2-8-2013

Please cite this article as: Carmena, D., Cardona, G.A., Canine echinococcosis: global epidemiology and genotypic diversity, Acta Tropica (2013), http://dx.doi.org/10.1016/j.actatropica.2013.08.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Canine echinococcosis: global epidemiology and genotypic diversity

Livestock Laboratory, Regional Government of Álava, Ctra. de Azua 4, 01520 Vitoria-Gasteiz,

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David Carmena* and Guillermo A. Cardonaa

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Spain

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Corresponding author: Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de

Salud Carlos III, Ctra. Majadahonda-Pozuelo Km 2, 28220 Majadahonda, Madrid, Spain

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E-mail: [email protected]

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Fax: +34 915097919

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Tel.: +34 918223775

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Abstract Canine echinococcosis is a potential zoonotic infection caused by the adult form of several cestode species belonging to the genus Echinococcus, of which E. granulosus sensu lato

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and E. multilocularis are the most epidemiologically relevant. Dogs infected with E. granulosus and E. multilocularis are widely regarded as the main source of infection for human cystic and

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alveolar echinococcosis, diseases that cause substantial morbidity and socio-economic burden in several regions of the world. Following our previous review on the global situation of cystic

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echinococcosis in livestock species (Cardona and Carmena Vet. Parasitol. 2013; 192, 10–32), we

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summarize here current knowledge on the global epidemiology, geographical distribution and molecular diversity of Echinococcus spp. infection in dogs. We address relevant topics including

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the implications of the increasing urbanization of wildlife species such as foxes, coyotes, and dingoes in the establishment of urban cycles of Echinococcus spp, or the rising concerns

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regarding the role of unsupervised translocation of infected dogs in spreading the infection to

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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

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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.

Key words: Echinococcus; dogs; epidemiology; molecular characterization; zoonoses

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1. Introduction Since their domestication during the Upper Palaeolithic period near 33,000 BP (Ovodov et al., 2011), dogs have developed a unique relationship with man, resulting in the strongest of

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any human-animal bond. In addition to their traditional value as working animals, it is currently well accepted that companion dogs exert also positive effects on the quality of life of their

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owners, not only by promoting physical, psychological, and social health, but also by improving recovery rates from a number of serious health conditions (Beck and Meyers, 1996; Paul et al.,

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2010; Wells, 2007). In spite of these unquestionable benefits, dog ownership may also be

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associated to potential health hazards related to the transmission of zoonoses such as echinococcosis, leishmaniasis, toxocariasis, rabies, Chagas disease, plague, and other bacterial

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infections (Chomel and Sun, 2011; Deplazes et al., 2011).

Canine echinococcosis is chiefly caused by adult stages of taeniid cestodes belonging to

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the species Echinococcus granulosus sensu lato (E. granulosus s.l.) and E. multilocularis. Other

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Echinococcus species including E. vogeli, E. oligarthrus, and E. shiquicus can sporadically induce canine intestinal infections. E. granulosus s.l. has a world-wide distribution and its

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transmission is primarily maintained in a synanthropic cycle through dogs as definitive hosts and livestock species as intermediate hosts (McManus et al., 2003). E. multilocularis is restricted to the Northern hemisphere and its life cycle is predominantly sylvatic, with carnivorous species such as foxes, wolves, and coyotes, (and, to a lesser extent, dogs) acting as definitive hosts, and a variety of small rodent species such as voles, pikas, and lemmings serving as intermediate hosts (Vuitton et al., 2003). Dogs infected by E. granulosus s.l. and E. multilocularis are the main source of infection for human cystic (CE) and alveolar (AE) echinococcosis, respectively. Both CE and AE are important zoonotic diseases that represent major public health problems in several regions of the world, causing a considerable socio-economic burden (Benner et al., 2010; Budke et al., 2006; Torgerson et al., 2010).

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Recent molecular genetic studies based on mitochondrial genome analysis have revealed that E. granulosus s.l. is a cryptic species complex including E. granulosus sensu stricto (E. granulosus s.s., genotypes G1–G3), E. equinus (genotype G4), E. ortleppi (genotype G5), and E.

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canadensis (genotypes G6–G10) (Nakao et al., 2007; Thompson, 2008; Thompson and McManus, 2002). E. granulosus s.s., particularly the genotype G1, is responsible for most cases

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of human infections. E. canadensis and E. ortleppi are also infective to humans, but to a much lesser extent than E. granulosus s.s. Although the genetic diversity of E. multilocularis is more

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limited in comparison with E. granulosus s.l., recent taxonomic studies at global scale have

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demonstrated intra-specific variations within E. multilocularis, allowing the identification of four geographically-restricted genetic groups, European, North American, Asian, and Mongolian

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(Davidson et al., 2012; Ito et al., 2010; Knapp et al., 2009; Nakao et al., 2009). Intestinal infection with Echinococcus spp. adult worms in dogs does not cause

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significant pathology and is typically asymptomatic, even in animals with high parasite burdens.

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Besides, E. multilocularis metacestode infection in domestic dogs has also been sporadically reported in the literature (Heier et al., 2007; Peregrine et al., 2012). However, estimating the

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prevalence, mean abundance, and genotype frequencies of these parasites in definitive host populations is pivotal not only for measuring the progress of CE and AE control programmes already in place, but also for assessing the distribution, host specificity, transmission dynamics, and risk of infection for humans in a specific area (Barnes et al., 2012; Craig and Larrieu, 2006; Craig et al., 2003). With this aim in mind, we have summarized here relevant epidemiological and molecular data published on canine echinococcosis globally. The search was conducted in PubMed covering the period from 2000 to date. Publications with an English abstract were primarily considered, although a number of non-English sources were also included after careful examination to ensure data relevance and consistency. Geographical sub-regions used here followed the classification proposed by the Statistics Division of the United Nations (available at

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http://unstats.un.org/unsd/methods/m49/m49regin.htm). The interested reader is invited to read this paper in conjunction with our previous review on the global prevalence of CE in livestock

2. Estimating the prevalence of Echinococcus infection in dogs

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species (Cardona and Carmena, 2013) for additional complementary information.

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Estimation of canine echinococcosis prevalence may be attempted using ante- and postmortem diagnostic techniques, each one with its own set of advantages and limitations. The gold

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standard method for the detection of Echinococcus spp. infection in definitive hosts comprises

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post-mortem examination of the intestine using the scraping (estimated sensitivity ~78%) or the sedimentation and counting (estimated sensitivity: 96–100%) techniques (Barnes et al., 2012;

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Duscher et al., 2005; Eckert, 2003). While highly specific and sensitive, these procedures present some drawbacks, including intensive labor, requirement of special safety precautions, ethically

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questionable principles, and unsuitability for mass screening surveys or investigations involving

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working or companion dogs. Additionally, studies based on necropsy may be biased if a particular dog class (e.g. unwanted, older or sick) is more likely to be sampled. Thus, a number

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of ante-mortem methods have been developed for diagnostic purposes. Arecoline hydrobromide purging followed by examination of faecal material discharged has been used for mass surveillance in Echinococcus spp. control programs worldwide. This technique is near 100% specific in endemic regions, although discrimination among different Echinococcus species may be problematic in co-endemic areas of Canada, Central Asia, China, and Russia (see below). Necropsy and arecoline treatment allow the estimation of worm burdens and purge worm counts, respectively, which are critical parameters for assessing infection pressure and modeling the transmission of the parasite. Both techniques are also a source of parasitic material for downstream molecular studies. However, arecoline purging has a highly variable sensitivity, is time-consuming, costly, and biohazardous. Some dogs may also suffer serious side-effects, so

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replacing this drug by a less traumatic purgative would be highly desirable (Barnes et al., 2012). Likewise, faecal egg detection is hampered by low sensitivity associated to erratic egg production and the fact that eggs of Echinococcus and Taenia species cannot be differentiated by

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light microscopy. However, conventional microscopy followed by taeniid egg enrichment and further characterization of Echinococcus species by PCR (see below) are widely used in

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genotyping studies. Regarding immunodiagnostic assays, detection of serum antibodies has shown highly variable sensitivities and cross-reactivity with other parasite species, although may

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be useful as a validation test in population studies (Benito et al., 2006). Current diagnosis of

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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

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the detection of the parasite in both necropsied and living definitive hosts and, because of the stability of copro-antigens, also in faecal samples collected in the field. However, obtained

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results in the latter case should be interpreted with caution as feces cannot be traced back to the

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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

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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 CpAgELISA 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 information. Finally, a number of species-specific PCR-based assays have been developed for use directly on faeces or on taeniid eggs isolated from faeces to confirm the presence of Echinococcus infection (Barnes et al., 2012; Deplazes et al., 2011; Dinkel et al., 2004). However, PCR is a laborious and relatively expensive method, features that hamper considerably its use for routine diagnostic or in field surveys. Therefore,

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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).

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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

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human behavioral (e.g. slaughtering practices, dog management, religious belief, migratory patterns) factors determine the dispersal and survival of Echinococcus eggs in a given region,

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influencing the infection pressure to intermediate hosts. Burden rates may also greatly affect the

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diagnostic performance of the method used to detect the infection in a specific definitive host population (Romig et al., 2011). These factors may help explaining, at least partially, the

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aggregated distribution of canine echinococcosis frequently reported in the literature (Al-Qaoud et al., 2003; Dalimi et al., 2002; Himsworth et al., 2010b; Jenkins et al., 2008; Lahmar et al.,

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2001), and should be taken into consideration when designing field epidemiological studies or

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analyzing and evaluating infection prevalence and burden data.

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3. Canine echinococcosis in Africa

E. granulosus s.l. is widespread in all North African states including Algeria, Egypt,

Libya, Morocco, and Tunisia (Dakkak, 2010; Sadjjadi, 2006), and also in most of the subSaharan countries stretching from Sudan to South Africa (Magambo et al., 2006; Romig et al., 2011; Wahlers et al., 2012). Very limited information is currently available from Western, Central, and Southern Africa, where updated, reliable epidemiological data is greatly needed. The infection affects primarily rural pastoralist communities with close contact with dogs, poor hygiene, and limited access to health services. E. granulosus s.l. is mainly transmitted between dogs as definitive host and sheep, goats, cattle, camels, pigs, and equines as intermediate hosts (see Cardona and Carmena, 2013). A

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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

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rare in Africa, with only two autochthonous cases of 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.

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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

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echinococcosis in African dogs include unsupervised home slaughtering, feeding raw offal to

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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

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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

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probably E. equinus are circulating in African livestock species (reviewed in Cardona and

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Carmena, 2013), confirming the existence of sheep-dog, cattle-dog, camel-dog, and pig-dog transmission cycles. Unfortunately, the lack of published data on the molecular characterization

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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 hyenas), 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%), Mauritania (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

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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 Therefore, elevated canine echinococcosis

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considerable environmental contamination.

prevalence rates combined with high parasite burdens will inevitably increase the risk of

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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 livestock

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species from the above mentioned countries (reviewed in Cardona and Carmena, 2013).

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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

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socio-behavioral factors greatly determine the extent of human disease (Wahlers et al., 2012). Epidemiological studies carried out in Kenya (Buishi et al., 2006), Libya (Buishi et al.,

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2005b), and Uganda (Inangolet et al., 2010) based on necropsy and/or CpAg-ELISA have

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evidenced a pattern of age related infection, with young dogs bearing higher prevalence and abundance rates compared to older dogs. High canine echinococcosis prevalence (range: 26–

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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 number 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 echinococcosis 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 prevalence of 14% and a mean intensity of infection of 1277 worms, with older dogs having higher infection and burden rates than

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younger 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 protective immunity in a significant number of dogs re-infected with

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Echinococcus s.l. A seasonal variation in canine echinococcosis occurrence has been reported in Uganda,

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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

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livestock (and consequently facilitating the access of dogs to infected carcasses) were proposed

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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),

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and between stray and domesticated dogs (Inangolet et al., 2010). Sex was not identified as a significant risk factor for canine echinococcosis in some studies (Buishi et al., 2005b; El Shazly

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et al., 2007; Salem et al., 2011), although male dogs have been found carrying higher worm

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burdens than female dogs in an Ugandan study (Inangolet et al., 2010).

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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 Western China (McManus, 2010; Wang et al., 2008), and Northeastern Siberia and Western Arctic (Rausch, 2003). The infection is historically known to be present in many of the East Mediterranean regions (Abdel-Hafez and Kamhawi, 1997), the Arab states bordering 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

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Republics, Mongolia, Northeastern, Central 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

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acting as definitive host and sheep, goats, cattle, buffaloes, camels, yaks or pigs serving as intermediate hosts (Cardona and Carmena, 2013). Wild carnivores including foxes, jackals and

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wolves have been reported to harbor E. granulosus adult worms in China (reviewed in Wang et al., 2008), Iran (Beiromvand et al., 2011; Dalimi et al., 2002) and Kazakhstan (Abdybekova and

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Torgerson, 2012), providing evidence of the co-existence and overlapping of domestic and

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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

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dogs) and a number of small mammal 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

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through dogs preying on infected rodents in close proximity to human settlements in endemic

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areas from China and Japan (Kamiya et al., 2006; Vaniscotte et al., 2011;). Indigenous peoples engaged in livestock herding and/or hunting activities involving dogs are at higher risk of being

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infected with Echinoccocus spp. Major contributing factors to the maintenance of canine echinococcosis in endemic regions include poor awareness of the disease, inadequate sanitation and hygiene practices, 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 mammals (Nonaka et al., 2009; Vaniscotte et al., 2011; Xiao et al., 2006). Regarding the genotypic diversity of Echinococcus in Asia, E. granulosus 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 addition, E. shiquicus,

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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

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isolates from different intermediate and definitive Asian hosts cluster together into a well-

American isolates (Nakao et al., 2009).

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4.1. Current situation of canine echinococcosis in North Asia

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defined, geographical-specific clade that differs significantly from European and North

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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

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involving wolves as definitive hosts and reindeers and elks as intermediate hosts. A domestic cycle is also known to exist among domestic dogs and domesticated reindeers. Similarly, E.

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multilocularis is maintained in the wild by wolves feeding on small rodents such voles and

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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

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confirmed 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 periodic 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

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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

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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

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per dog could not be demonstrated to develop a significant protection against re-infection (Torgerson et al., 2003). On the other hand, the spatial distribution of E. multilocularis in Central

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Asia seems to be based on small foci of infection determined by local environmental conditions,

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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 similar patchy distribution

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has been reported in other field surveys carried out in different European countries (see Section 5.2.).

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Dog infections caused by E. granulosus s.l. has been estimated to be in the range of 6–

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28% in Kazakhstan, 11–19% in Kyrgyzstan, 15% in Tajikistan, and 8–20% in Uzbekistan. Regarding canine echinococcosis caused by E. multilocularis, epidemiological data are only

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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. multilocularis (genotype frequency: 38–45%), E. canadensis (genotype frequency: 5–22%) and E. equinus (genotype frequency: 1%). Taking together, this information provides evidence of the presence of well-established sheep-dog, pigdog, camel-dog and horse-dog transmission cycles of E. granulosus s.l., though more research is

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necessary to determine the frequency of the parasite genotypes in livestock intermediate host species and humans in Central Asia.

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4.3 .Current situation of canine echinococcosis in Western Asia Echinococcus granulosus s.l. has been mainly reported infecting stray dogs from Irak

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(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

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worms) have been documented in 37% of infected dogs in Irak (Saeed et al., 2000), 4.5% in Iran

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(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

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humans) intermediate hosts are commonplace. Neither dog sex nor dog age seemed to be significantly associated with canine echinococcosis prevalence rates in Iran (Maleky and

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Moradkhan, 2000; Razmi et al., 2006), although this information should be interpreted with

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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,

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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 number, 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. granulosus 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 campaigns, as the G7 genotype has a shorter maturation rate in dogs compared with E. granulosus s.s. (McManus et al.,

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2003). Of particular 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

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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),

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4.4. Current situation of canine echinococcosis in South Asia

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providing evidence of the presence of pig-dog and camel-dog transmission cycles of the parasite.

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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

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epidemiological 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.

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ortleppi, and E. canadensis circulating in India and Pakistan (reviewed in Cardona and Carmena,

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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

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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

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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

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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

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intensities. Overall, prevalence figures based on purgation tended to be lower than those obtained by necropsy or CpAg-ELISA. This is in line with previous investigations (see e.g. Ziadinov et al.,

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2008) highlighting the fact that the intrinsic low diagnostic sensitivity of purging leads to

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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

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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

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finding that pikas can also harbor concurrent infections with both E. multilocularis and E.

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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

Ac ce p

the actual case, as demonstrated in a recent molecular reappraisal survey where canine coproDNA isolates from an earlier canine purgation study (Budke et al., 2005) 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.

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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

ip t

at a prevalence of 13–33% and a mean abundance of 131 worms per dog (Budke et al., 2005b). Seasonality, insufficient infection pressure and differences in the host immunological response to

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E. granulosus s.l. versus E. multilocularis were proposed by the authors as potential explanations for the failure of E. multilocularis in stimulating host protective immunity. Moreover, Budke et

us

al. suggested that the degree of acquired immunity may be linked to the marked differential

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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

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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

d

Eckert, 1983) with E. granulosus s.l. and E. multilocularis. It might be also speculated that this

te

preferential tropism is the result of a co-evolutionary process where E. granulosus s.l. and E. multilocularis avoid direct competition by exploiting nutrient resources in different intestinal

Ac ce p

settings.

Significantly higher canine echinococcosis prevalence rates were found in male dogs in a

study conducted in Western China (Budke et al., 2005a). Territorial behavior 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 efficient, 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

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al., 2006; Li et al., 2008) isolates characterized to date. Interestingly, 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

from the Yushu Tibetan Autonomous Prefecture (Liu et al., 2013).

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human CE cases from the same region (Bart et al., 2006) and more recently in two goat isolates

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E. multilocularis is the only native species of the genus Echinococcus present in Japan. The infection is restricted to Hokkaido, the northernmost island of the country, where wild foxes

us

are the primarily source of infective eggs. However, the increase in urban foxes overlapping with

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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. multilocularis infection rates

M

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 traveling dogs in spreading the infection. It has been

d

estimated that 10,000–12,000 dogs travel annually from Hokkaido to other Japanese prefectures,

te

with up to 30 of them carrying mature worms of the parasite (Doi et al., 2003). Not surprisingly, E. multilocularis infected dogs known (or suspected) to have been originally raised in Hokkaido

Ac ce p

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. multilocularis 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 diagnose 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. compulsory quarantine

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or anthelmintic treatment) to minimize the risk of disease dispersal by dogs traveling to nonendemic areas (Kamiya et al., 2006). Finally, high E. multilocularis and E. granulosus infection rates have been reported in

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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

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on Echinococcus spp. infections in human and livestock populations are still lacking in this

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country.

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4.6. Current situation of canine echinococcosis in Southeast Asia

Echinococcus infections seem to be rare in Southeast Asian countries, which

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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

d

production animal infections have not been documented for the same period (Waikagul et al.,

te

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

Ac ce p

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, particularly 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 documented 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

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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,

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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

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wildlife-based, involving foxes as definitive host and small rodents as intermediate hosts. Racoon dogs have also been described as suitable final hosts in Northwestern Europe (see e.g.

an

transmission of the parasite (Davidson et al., 2012).

us

Bruzinskaite-Schmidhalter et al., 2012), though they are thought to play a minor role in the

E. granulosus s.s., E. ortleppi, E. canadensis, and E. equinus are known to be circulating

M

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

d

Echinococcus species are rarely found in Central Europe, where occurrence of autochthonous CE

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cases is limited to sporadic infections due to E. equinus and E. ortleppi (Jenkins et al., 2005). Regarding E. multilocularis, recent molecular studies based on microsatellite patterns and

Ac ce p

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’ hypothesis, where island populations originated as a consequence of the spreading of the parasite from long-established mainland populations 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 significantly from Asian and North American isolates (Nakao et al., 2009).

5.1. Current situation of canine echinococcosis in Northern Europe

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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, compared with 3.4% in the

ip t

same areas during the period 1989–1993 (Table 3). Roaming behavior, inadequate anthelmintic treatment and home-slaughter practices were factors strongly associated with copro-antigen

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positivity in these studies. Recrudescence of infection in farm dogs was likely due to the withdrawal of the supervised dog-dosing scheme carried out from 1983 to 1989, which was

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subsequently replaced by a health promotion and education campaign (Buishi et al., 2005a). In

an

an attempt to prevent human infections, a new public awareness campaign and a 10-year deworming programme were initiated in 2008. Regarding canine echinococcosis caused by E.

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multilocularis, recent field epidemiological 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.,

d

2012). Based on these data, both countries are believe to be E. multilocularis-free, providing the

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epidemiological 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

Ac ce p

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. multilocularis must be also causing canine infections. In Finland, no Echinococcus copro-antigen positive results were obtained after examining 352 dog faecal samples in reindeer herding areas during 1999–2001, despite E. granulosus s.l. was previously

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known to circulate in the wild among wolves, reindeers and elks in the Eastern part of the country (Hirvelä-Koski et al., 2003). In Lithuania, the molecular analysis of taeniid eggs isolated from dog faecal samples revealed the presence of E. granulosus s.l. and E. multilocularis in 3.8%

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and 0.8% of samples, respectively (Bruzinskaite et al., 2009). E. multilocularis infections have been frequently documented in wild foxes and wolves in most of the above mentioned countries.

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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.

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Although not completely elucidated, it is believed that the parasite was introduced by accidental

an

translocation with infected dogs, in spite of the legal requirement to de-worm dogs before entering the country. Infected traveling dogs are also the prime suspects for the introduction of

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the parasite into Denmark (Davidson et al., 2012), where E. multilocularis is now known to naturally infect domestic cats and wild foxes (Dyachenko et al., 2008; Enemark et al., 2013). As

d

in the case of Great Britain, Ireland or Japan, this situation highlights the importance of

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implementing effective measures involving pet travel regulation and tapeworm treatment to prevent the accidental introduction of the parasite on E. multilocularis-free areas. Finally,

Ac ce p

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.

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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

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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

cr

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

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populations observed in recent decades had led to the environmental contamination of city parks

an

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).

M

Consistent with this epidemiological scenario, E. multilocularis causes the vast majority of canine echinococcosis cases in these countries (Fig. 1). The infection is generally recorded at low

d

prevalence rates (see Table 3), suggesting that dogs do not play a significant role in the

te

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

Ac ce p

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), 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

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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

ip t

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

cr

in this country (Sager et al., 2006).

Canine infections by E. granulosus s.l. seem to be rare in Western Europe, in line with

us

the very low (or absent) CE prevalence rates in livestock intermediate hosts reported from

an

countries of this region (reviewed in Cardona and Carmena, 2013; Umhang et al., 2013).

M

5.3. Current situation of canine echinococcosis in Eastern Europe

E. granulosus s.l. and E. multilocularis have been recorded from all Eastern European

d

countries, sometimes occurring sympatrically (Fig. 1 and Table 3). In Bulgaria, reliable

te

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

Ac ce p

administrative and economic changes in the country in the following years has led to an alarming resurgence of human CE (Todorov and Boeva , 1999), suggesting that canine infection rates may have also risen since then. Echinococcus copro-antigen prevalences ranging from 3–12% 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 possibility 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

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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 characterization of two human isolates as E. multilocularis (see Siko et al., 2011) and an additional one as E. canadensis (Piccoli et al., 2013)

ip t

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

cr

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

us

of 36 human CE and AE cases were reported only in 2010 (Waloch, 2012). On the other hand, E.

an

granulosus s.s. G1, E. canadensis G6, and E. multilocularis (Asian-type) genotypes have been identified in Russian human isolates (Konyaev et al., 2012). These data strongly support the idea

M

that the above mentioned Echinococcus species must be also causing infections in dogs. This possibility needs further confirmation in future canine echinococcosis epidemiological studies

d

from these countries.

te

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.,

Ac ce p

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 were allegedly reported in these studies as the most likely causes of contracting and maintaining Echinococcus infections in dogs.

5.4. Current situation of canine echinococcosis in Southern Europe Available canine echinococcosis epidemiological data from Southern European countries indicate that E. granulosus s.s. accounts for the vast majority of Echinococus infections in dogs, with E. multilocularis playing a marginal role (Table 3). The infection is endemic in Spain, where earlier necropsy-based studies revealed infection rates between 0% and 1.4% of the

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investigated dog populations, depending on the region of origin and dog class (reviewed in Carmena et al., 2008). More recent surveys have reported prevalence rates ranging from 0.2% to 0.5% at necropsy (Table 3), although some others failed to detect the presence of the parasite

ip t

using the same technique (Martinez-Carrasco et al., 2007; Martinez-Moreno et al., 2007). A high infection rate of 8% was observed in sheep dogs by antibody and CpAg-ELISA tests, confirming

cr

this dog class as the one mainly involved in the domestic transmission of Echinococcus in this region (Benito et al., 2006). In this survey no correlation between copro-antigen positive values

us

and dog age could be demonstrated. A similar result was previously obtained in domestic dogs

an

from Kazakhstan at a prevalence of 5.8%, suggesting an insufficient parasite infection pressure to trigger the dog protective immune response (Torgerson et al., 2003). Canine echinococcosis is

M

also assumed to be present in adjacent Portugal, although a recent copro-epidemiological survey failed to amplify Echinococcus-specific DNA from taeniid eggs isolated from farm dogs

d

(Cardoso et al., in press).

te

CE represents also a serious human and animal health problem in Italy, being the island of Sardinia one of the most affected regions. Canine echinococcosis prevalences in the range of

Ac ce p

4–25% have been previously recorded in Northern Italy and Sicily (Garippa, 2006), while more recent studies reported infection rates of 3–32% in the Central part of the country and Sardinia (Table 3). For a detailed review of the canine echinococcosis epidemiological situation in Italy before 2000, the interested reader is referred to earlier reviews (e.g. Garippa et al., 2004). No autochthonous cases of human AE or canine infections by E. multilocularis have been documented to date, although this Echinococcus species is known to naturally infect wild fox populations in Northern Italy (Manfredi et al., 2006). In Slovenia, confirmed cases of human CE (n = 34) and AE (n = 9) have been documented during 2001–2005 (Logar et al., 2007). E. granulosus s.l. is also the only Echinococcus species known to cause human infections in Serbia, where official figures have

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reported 409 cases during 1998–2010 (Bobic et al., 2012). Although the current epidemiological situation of canine echinococcosis is unknown, these results indicate that infected dogs are the most likely source of human CE and AE infections in these countries. In line with these findings,

ip t

E. granulosus s.s. G1 genotype has been recently identified infecting 1.3% and 2.7% of dogs in adjacent Kosovo and Albania, respectively (Figure 1 and Table 3). However, because only PCR

cr

primers for detecting this specific strain were used in Kosovo’s study, this result does not exclude the possibility of the presence of other Echinococcus genotypes in dogs from that

an

us

country (Sharifi et al., 2011).

6. Canine echinococcosis in the Americas

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Echinococcosis caused by E. granulosus s.l. is a major public health problem in sheep rearing areas of South America. Major endemic areas include Patagonian Argentina, Southern

d

parts of Brazil and Chile, Central and Southern Peruvian Andes, and Uruguay (Jenkins et al.,

te

2005; Moro and Schantz, 2006;). Little epidemiological information is currently available from Bolivia and Paraguay, whereas the disease seems to be rare or absent in Colombia, Ecuador,

Ac ce p

Guyana, French Guiana, Surinam, Venezuela, and the Central American and Caribbean countries. Localized foci of infection have also been identified in Western USA (Moro and Schantz, 2009; 2006). In all these regions the infection is transmitted through the classical domestic cycle involving dogs as definitive hosts and sheep, goats, cattle, equines, pigs, and alpacas as livestock intermediate hosts (reviewed in Cardona and Carmena 2013). A wildlife transmission cycle is also known to be maintained among wolves and moose, caribou, and other cervids in Northern America including Canada and Alaska (Moro and Schantz, 2006). The geographical distribution of E. multilocularis comprises Northern North America and Central areas of USA, where foxes and coyotes have been reported as the sole definitive host species of this Echinococcus strain (Catalano et al., 2012; Davidson et al., 2012).

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Human populations at risk of CE/AE in the Americas are predominantly those engaged in sheep farming, transhumant pastoralism, and hunting/trapping activities. Typical contributing factors to the transmission of Echinococcus spp. infection in these regions include extensive

ip t

ovine husbandry, home slaughter of adult sheep, lack of veterinary supervision, and low socioeconomic and cultural status of the population (Larrieu et al., 2000; Moro and Schantz, 2006).

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Available molecular data from American isolates reveal a complex epidemiological situation where several Echinococcus species may co-exist in a given region. Only in South

us

America at least 6 parasite variants have been documented infecting livestock species to date,

an

including E. granulosus s.s. G1, G2, and G3 genotypes, E. ortleppi, and E. canadensis G6 and G7 genotypes (reviewed in Cardona and Carmena 2013). E. granulosus G1 is, with difference,

M

the most ubiquitous genotype identified, highlighting the predominance of the sheep-dog cycle in the transmission of the parasite. In addition, E. vogeli and E. oligarthrus are also known to

d

circulate among wild animal species in the tropical forest of South and Central America

te

(D'Alessandro and Rausch, 2008). Genotypic variability of Echinococcus seems more limited in North America, where only E. granulosus s.s. G1, E. canadensis G7, and the North American-

Ac ce p

specific clade of E. multilocularis have been identified so far (Davidson et al., 2012; Jenkins et al., 2005; Nakao et al., 2009).

6.1. Current situation of canine echinococcosis in Northern America Echinococcus s.s. infection almost certainly caused by the G1 genotype is known to have

significantly affected sheep rearing areas in Western USA, including Arizona, California, New Mexico, and Utah in past decades. Implementation of CE control programs in these regions successfully reduced, or even ceased, the transmission of the parasite (Jenkins et al., 2005). Consequently, the disease is currently maintained at low prevalence levels, and autochthonous human CE cases occur only sporadically (Moro and Schantz, 2009). E. canadensis G8 genotype

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has been identified circulating among wolves and dogs (definitive hosts) and large cervids such as moose and caribou (intermediate hosts) in Canada and Alaska (Moro and Schantz, 2006; Rausch, 2003). Recent copro-epidemiological and molecular studies have reported the presence

ip t

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 et al., 2010a,b and Table 4). The authors noted an

cr

aggregated pattern of infection, with few dogs harbouring most of the parasite biomass and the remainder of the population having lower infection intensities. These data suggest that infected

us

dogs are a very probable source for human disease in Canada, where at least 19 human CE cases

an

have been confirmed between 1991 and 2001 (Somily et al., 2005). In addition, eight human CE cases (but no human AE cases) have been reported since 1990 in Alaska (DHSS, 2003). The

M

zoonotic potential of the E. canadensis G10 genotype and the fully characterization of its natural intermediate host reservoir (very likely cervid species) remain to be completely elucidated.

d

The distribution of E. multilocularis, historically accepted to be confined to the Northern

te

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

Ac ce p

increasing in these regions (Jenkins et al., 2005; Moro and Schantz, 2009;). Interestingly, high infection levels in wild animal 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 epidemiological 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. Consequently, domestic dogs occasionally preying on infected rodents will also acquire the

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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

to assess its zoonotic potential.

6.2. Current situation of canine echinococcosis in Central America

cr

ip t

America. Genetic characterization of wild animal isolates would also provide useful information

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Echinococcus granulosus s.l. is thought to be rare or non-existent in most countries of

an

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

M

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

d

and domestic dogs are often fed their infected raw viscera, this cestode probably circulates also

te

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

Ac ce p

(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 programs 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

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al., 2006). 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 parasite, and highlighting the associated risk to human infection in these areas (Lavallén et al., 2011). Despite

ip t

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).

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Consistent with the long-term control effort maintained, most infected dogs harbored relatively low numbers (5–100) of Echinococcus adult worms, with few canine infections accounting for

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most of the parasite biomass (Pierangeli et al., 2006). Taking together, these facts suggest that

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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

M

highly advisable to maintain, or even intensify, the control programmes currently in place in order to avoid the spread of the disease. Regarding genotype variability, canine isolates

d

characterized to date have been allocated to the E. granulosus s.s. G1 and E. canadensis G6

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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

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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 program was launched in this area in 1983, but after an initial success it was shortly discontinued and, consequently, Echinococcus prevalence rates reverted to pre-program 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).

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In Chile, a CE control program at national scale was successfully implemented in 1982. Unfortunately, the decentralization of the program in 1997, together with the reduction of the prophylactic anthelmintic intervention in dogs has inevitably leaded to the recrudescence of the

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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

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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).

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Therefore, younger dogs living in urban areas and with no de-worming treatment have been

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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

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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

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the age pattern observed.

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does not allow elucidating the potential role of acquired host immunity responses in explaining

Canine echinococcosis is highly endemic in Peru, particularly affecting indigenous

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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 (provice 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

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associated with likelihood of infection in domestic dogs from the capital Lima (Reyes et al., 2012). Historically, Uruguay has been regarded as one of the most endemic regions for

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echinococcosis worldwide (Cohen et al., 1998; Craig et al., 1995). A successful long-term CE control program has been in place in this country since 1992 to date. As a consequence, canine

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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

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canine echinococcosis/CE prevalence has been published since then, so the current status of the

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infection in this country remains unknown.

Finally, there is an important lack of information regarding the Echinococcus species

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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

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assess the risk to human infection.

7. Canine echinococcosis in Oceania

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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 fastgrowing livestock and dog populations and becoming a serious public health concern in sheepfarming areas shortly after (Jenkins, 2005; Pharo, 2002). In Australia, the most affected regions encompass New South Wales, the Australian Capital Territory, Victoria, Southwest Western 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

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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 considered the main source of echinococcal infection to domestic animals in Australia (Jenkins and

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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

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authors highlighted that areas frequented by these animals may become contaminated with worm eggs and be a potential source of human infection. It has been speculated that wild dogs may be

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directly responsible for a proportion of the human CE cases occurring in Australia (Jenkins and

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Morris, 2003).

Canine echinococcosis prevalence in Australian wild dog populations based on necropsy

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and CpAg-ELISA results are in the range of 22% to 100%. Wild dogs frequently have also large parasite burdens, ranging from 1 to >300,000 adult worms (Table 5). Heavy worm burdens

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(>1000 worms) have been found in 66% of the infected wild dogs in the Maroochy Shire,

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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),

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suggesting that domestic dogs may 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 definitive 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 programs 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;).

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8. Concluding remarks Echinococcosis/hydatidosis remains a serious public veterinary health concern in many

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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

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consideration is the influence, either directly or indirectly, of human intervention in the prevalence, epidemiology, and geographical distribution of canine echinococcosis. For instance,

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discontinuation or cessation of control campaigns in endemic areas normally translates into an

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immediate recrudescence of the disease in definitive and livestock hosts species. Translocation of infected dogs from prevalent regions to Echinococcus-free areas is the primarily suspected

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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

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entry Echinococcus-free countries. In addition, the fox vaccination campaigns against rabies

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launched in Western Europe during the late 70s and early 80s led to the recovery of fox populations, which since then have expanded and colonized new habitats, including urban

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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 echinococcosis 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

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humans. This includes not only defining the range of wild host species susceptible to be infected by Echinococcus spp., but also the prevalence and intensity of the infection. These data would be valuable to model the transmission of the parasite and estimate infection pressures to

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intermediate host species in a given region. The task is particularly pressing in the case of the recently identified E. felidis and E shiquicus, given the very limited epidemiological information

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currently available on these Echinococcus species, including their zoonotic potential. Canine echinococcosis prevalence and molecular data are also lacking from Northern European dogs,

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where Echinococcus spp. infection may be much higher than initially suspected. An issue that

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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 importantly, there

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is a real need to develop rapid and accurate diagnostic molecular tools able to discriminate different Echinococcus species occurring sympatrically in a given region.

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Although control does not fall within the scope of this review, it is worth mentioning that

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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

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implementing measures for disease control and prevention. 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 Echinococcusfree 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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Table 1 Prevalence and molecular epidemiology of Echinococcus granulosus s.l. infection in dogs in Africa (2000 onwards). Diagnostic procedure Necropsy Necropsy Necropsy Necropsy Necropsy CpAg-ELISA Necropsy CpAg-ELISA Necropsy Necropsy Necropsy Purgation Necropsy Necropsy Coproscopy/CpAg-ELISA

ip t

Worm burden (n) 421b NS NS NS 540b – 1064b – 1227b/172c 75–547 2534b NS 848b 845b –

cr

Prevalence (%) 5.0 16.0 16.7 61.5 33.3 26.1e 25.8 20.1d,e5 14.0 55.0–58.0 21.0 3.5 18.4 66.3 8.0e

us

No. samplesa 540 50 18 13 42 161 58 334 121 151 NS 375 60 327 540

Dog Population Stray Stray Stray Stray Stray Farm Stray Farm Stray Stray Stray Semi-stray Stray Mixed Farm

an

Period NS NS Ethiopia NS NS Kenya NS NS Libya 2001–02 2001–02 Mauritania NS Morocco NS Tunisia NS NS 2007 Uganda 2007–08 Zambia 2005–06

M

Country Egypt

a

Ac ce p

te

d

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.

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Table 2 Prevalence and/or molecular epidemiology of Echinococcus granulosus s.l. (font in black), E.

Diagnosti c procedure

Molecular characterization Gene Genotype No. isolates marker frequency b s (%)

NS

Necropsy

–

80e; 131e

Purgation

–

No. samp lesa

China

NS

NS

53

2003 –03

Farm

371

NS

Dome stic

139

36.0f

–

2004 –05

Stray

–

–

NS

NS

Farm

–

–

10,00 0

NS

Dome stic

–

–

2004 –05

Stray

30

2000

Stray

23

NS

Stray

–

NS

–

2007

Stray

12

f

–

–

–

–

He et al. (2000) Budke et al. (2005a)

NS

Purgation/ PCR

1 (65 AW)

rrnL

NS

Necropsy/ PCR

17 (NS AW)

12S rRNA

Necropsy

–

–

–

Necropsy

4 (AW)

atp6, coxI, nadI

G1 (100%)

Ma et al. (2008)

NS

Necropsy

–

–

–

Yu et al. (2008)

–

Coprosco py/CpAgELISA/P CR

14 (E)

12S rRNA

E.g. (100%)

Yu et al. (2008)

–

13 (45 AW) 1 (NS AW)

M

d

NS

–

66.7; 8.3

–

G1 (93.3%); G6 (6.7%) G1 (NS); E.m. (NS) E.g (27.7%); E.m. (72.3%) G1 (NS); E.m. (NS)

te

56.7; 3.3 27.0; 32.0

–

Reference

CpAgELISA Necropsy/ PCR Necropsy/ PCR

Ac ce p

NS

13.2; 17.0 8.0– 19.0c; 13.0– 33.0c

us

Dog Popul ation

an

Perio d

cr

Wor m burde n (n)

Countr y

Preval ence (%)

ip t

multilocularis (font in red), and E. shiquicus (font in green) infections in dogs in Asia (2000 onwards).

cox1

12S rRNA

Wang et al. (2005) Bart et al. (2006) Wen et al. (2006) Xiao et al. (2006) Zhang et al. (2006) Huang et al. (2007)

Stray

149

38.9

Stray

9

55.5

NS

Necropsy

–

–

–

Han et al. (2009)

Necropsy

–

–

–

Yang et al. (2009)

2000

Stray

22

27.0; 36.0

10– 50; 500– 100,0 00

2000

Mixe d

580

50.0f

–

CpAgELISA

–

–

–

Yang et al. (2009)

17.0

<100 – 35,00 0

Purgation

–

–

–

Zhang et al. (2009)

NS

Purgation

–

–

–

39.6e

Purgation/ Copro-

–

12S rRNA

–

1987 –90 2004 –07 2002

Farm Mixe d Dome stic

291 74 228

23.0; 5.4 14.8

Zhao et al. (2009) Wang et al. (2010)

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2006 –07

Japan

Jordan

22.5 –

2003 –03

Farm

371

–

NS

Stray

35

NS

Stray

35

1991 –98

Stray

97

1997 –99

Stray

NS

12S rRNA

E.g. (50.0%); E.m. (50.0%) E.m. (75.0%); E.s. (62.5%)

NS

Necropsy/ PCR

1 (2 AW)

cox1

–

Purgation/ PCR

8 (AW, E)

nad1

NS/1

Necropsy

–

–

–

–

CpAgELISA

–

–

–

49.5

200– 1000

Necropsy

–

–

–

120

16.7

1026d

Necropsy

–

–

–

Stray

60

48.3

NS

Necropsy

1997 –00

Stray

115

19.1

421d

Necropsy

NS

Stray

83

13.2

NS

Necropsy

2002 –03

Stray

100

22.0

636d

NS

Dome stic

59

27.1f

–

2009 –10

Mixe d

77

16.9; 6.5

2011

Stray

71

28.2

1966 –99

Mixe d

9849

2003 –04

Dome stic

1999 –05 2004 –05 2004 –05

Shelte r Dome stic Dome stic

11.4; 2.8 8.6– 11.4f

Vaniscotte et al. (2011)

–

Ma et al. (2012) Boufana et al. (in press)

Huang et al. (in press) Huang et al. (in press) Saeed et al. (2000) Abdullah and Jarjees (2005) Maleky and Moradkhan (2000) Dalimi et al. (2002) Dalimi et al. (2006) Razmi et al. (2006) Zare-Bidaki et al. (2009)

cr

–

–

(2010)

us

NS

rRNA

an

2006 –10

–

–

–

–

–

–

–

–

–

Necropsy

–

–

–

CpAgELISA

–

–

–

–

CoproPCR

–

nad1, 12S rRNA

–

Beiromvand et al. (2011)

NS

Necropsy/ PCR

20 (20 AW)

cox1, nad1

G1 (75.0%); G2 (10.0%); G3 (15.0%)

Parsa et al. (2012)

1.0

NS

Necropsy

–

–

–

Takahashi and Mori (2001)

183

1.1

–

1 (E)

12S rRNA

E.m. (100%)

Morishima et al. (2006)

550

0.2

–

1460

0.3

–

1460

0.4

–

d

M

–

te

Iran

142

Ac ce p

Irak

Dome stic

CoproPCR CoproPCR

ip t

stic

CpAgELISA/P CR Coprosco py/PCR CoproPCR CpAgELISA

1997 –07

Dome stic

4768

0.9

–

Coprosco py/CpAgELISA/P CR

1994 –95

Stray

94

13.8

3– >10,0

Necropsy

1 (E) –

12S rRNA 12S rRNA

E.m. (100%) –

Yamamoto et al. (2006) Kamiya et al. (2007) Kamiya et al. (2007)

–

–

–

18 (E)

cox1, 12S rRNA, U1 snRN A

E.m. (100%)

Nonaka et al. (2009)

–

–

–

el-Shehabi et al. (2000)

65

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00 –

CpAgELISA

–

–

–

el-Shehabi et al. (2000)

29.5

1306d

Necropsy/ PCR

23 (115 AW)

ITS2

G1 (92.8%); G4-like (7.2%)

Al-Qaoud et al. (2003)

268

4.1f

–

CpAgELISA

–

–

–

Farm

606

23.0

631e

Purgation

–

–

–

NS

Dome stic

1463

5.8

27e

Purgation

–

–

–

2002

Farm

131

13.7f

NS

31 (E)

12S rRNA

G1 (57.1%); E.m. (42.9%)

Stefanic et al. (2004)

2002

Farm

131

28.2f

–

–

–

–

Stefanic et al. (2004)

nad1, 12S rRNA

G1 (33.3%); G6–G7 (22.2%); E.m. (44.5%)

Trachsel et al. (2007)

–

–

–

–

–

–

139 (E, AW)

nad1, 12S rRNA

G1–G3 (56.2%); G4 (0.7%); G6– 7 (5.0%); E.m. (38.1%)

1998 –99

Stray

112

India

NS

Stray

Kazak hstan

NS

Tajikis tan Turke y Uzbek istan

2001

–

Coprosco py/PCR

632

13.4 ; 4.6

812d; 72d

Purgation

1214

11.2

496d

Necropsy

2005

Dome stic

466

19.0c; 18.0c

NS

NS

67

25.4f

NS

Stray

14

35.7

Stray

120

NS

NS

Purgation/ Coprosco py/PCR

–

CpAgELISA

–

–

–

330

Necropsy

–

–

–

15.2

NS

Necropsy

–

–

–

1

–

–

Purgation/ PCR

1 (AW)

cox1

G1 (100%)

Farm

279

20.1

NS

Purgation

–

–

–

Dome stic

240

7.9

NS

Purgation

–

–

–

2005 –06 NS

50e; 65e

9 (E)

M

Dome stic Mixe d

–

d

2003 –05

–

te

Mong olia

Farm

Ac ce p

Kyrgy zstan

2002

Purgation/ Coprosco py/PCR CpAgELISA

Prathiush et al. (2008) Torgerson et al. (2003) Torgerson et al. (2003)

ip t

17.0

cr

94

us

Stray

f

an

1994 –95

Torgerson et al. (2009) Torgerson et al. (2006) Ziadinov et al. (2008) Zoljargal et al. (2001) Wang et al. (2005) Torgerson et al. (2006) Utuk et al. (2008) Torgerson et al. (2006) 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 CpAgELISA (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).

66

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d

M

an

us

cr

ip t

Mean abundance of infection (mean number of parasites per dog examined). Estimated prevalence for Echinococcus spp.

te

f

Ac ce p

e

67

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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).

Germ any Greec e

NS 198 5– 87

Italy

NS

Koso vo

NS 200 3– 04

Lithu ania Roma nia

200 5– 06 200 5– 06 200 8– 09 200

Dom estic

111

2.7

26– 11,670

Necropsy/ PCR

3 (AW)

cox1

G1 (100%)

Farm

6551

0.0– 3.6c,d

–

CpAgELISA

–

–

–

NS

118

11.9d

–

–

NS

55

1.8

– E.m. (100%)

Christofi et al. (2002) Lenska and Svobodova (2001) Martinek et al. (2001)

NS

186

Farm Mixe d

ip t

Diagnostic procedure

Molecular characterization No. Genotype isolat Gene frequency markers (%) esb

Reference

us

cr

Xhaxhiu et al. (2011)

1

– 12S rRNA

8.1d

–

CpAgELISA

–

–

–

Svobodova and Lenska (2002)

12

16.7d

–

CpAgELISA

–

–

–

Magnaval et al. (2004)

860

<1.0

–

Coproscop y/PCR

0 (E)

12S rRNA

No PCR product

(Umhang et al. (2012)

0.2 1.0– 50.4

–

Coproscop y/PCR

43 (E)

12S rRNA

E.m. (100%)

NS

–

–

–

Dyachenko et al. (2008) Sotiraki et al. (2003)

–

–

–

–

–

–

113

31.8d

–

Purgation CpAgELISA CpAgELISA

–

300

3.3 3.0– 10.0d

–

–

–

305

1.3

–

Coproscop y/PCR

4 (E)

12S rRNA

Farm

240

3.8; 0.8

–

Coproscop y/PCR

11 (E)

cox1; 12S rRNA

G1 (100%) G6–G7 (81.8%); E.m. (18.2%)

Farm

40

12.5

–

CpAgELISA

–

–

–

Seres et al. (2006)

Farm Farm

48 1892

77.1 19.2d

– –

CoproPCR CpAg-

– –

12S rRNA –

– –

Seres et al. (2009) Seres et al.

Dom estic Mixe d

17,89 4 NS

NS Mixe d Mixe d Mixe d

110,0 93

–

an

–

CpAgELISA Coproscop y/PCR

M

Franc e

NS 199 8 200 0– 01 199 9– 00 200 8– 10 200 4– 05

Worm burden (n)

d

Cypru s Czech Repu blic

Preva lence (%)

te

Alban ia

Per iod 200 4– 09 199 7– 00

No. sampl esa

Ac ce p

Count ry

Dog Popu latio n

Sotiraki et al. (2003) Varcasia et al. (2011) Giangaspero et al. (2006) Sherifi et al. (2011) Bruzinskaite et al. (2009)

68

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5– 08 195 6– 92

NS

12,00 9

21.6

–

Slova kia

200 6

Mixe d

752

0.1

–

289

2.8d

Spain

200 2– 05 200 0

NS

NS

UK

NS 200 2 200 8

–

Neghina et al. (2010)

1 (E)

12S rRNA

E.m. (100%)

Szabova et al. (2007)

–

12 (E)

12S rRNA

E.m. (100%)

0.2

–

Necropsy

–

–

–

1040

0.5

–

–

–

–

721/7 54 –

8.0c,d –

– –

Necropsy CpAgELISA/Ab -ELISA

–

–

Coproscop y/PCR

12 (E)

86

7.0d

–

505

0.4d

–

306

1.0

–

Farm

1164

8.1

–

Farm

577

10.6

–

Feral Mixe d Mixe d

nad1, 12S rRNA

Antolova et al. (2009) Jimenez et al. (2002) Benito et al. (2003)

cr

us

an

Coproscop y/CpAgELISA/PC R Coproscop y/CpAgELISA/PC R Coproscop y/PCR CpAgELISA CpAgELISA

M

ND

ip t

–

d

Switz erland

199 6– 97

Farm

–

te

199 4

Mixe d Mixe d Shelt er

(2010)

Necropsy Coproscop y/CpAgELISA/PC R Coproscop y/CpAgELISA/PC R

Ac ce p

NS 199 7– 98

ELISA

– G1 (91.7%); G6–G7 (8.3%)

Benito et al. (2006) Trachsel et al. (2007)

6 (E)

U1 snRNA

E.m. (100%)

Gottstein et al. (2001)

1 (E)

12S rRNA

3 (E)

NS

E.m. (100%) E.m. (100%)

–

–

–

–

–

–

Sager et al. (2006) Nagy et al. (2011) Buishi et al. (2005a) 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 coproantigens 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.

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Table 4 Prevalence and molecular epidemiology of Echinococcus granulosus s.l. infection in dogs in the Americas (2000 onwards). Preval ence (%)

Wor m burde n (n)

Diagnosti c procedur e

Molecular characterization Genotype No. frequency isolates Gene b markers (%)

598

2.8

NS

–

–

–

2003 2001 –03

Farm

1042

2.9

–

Purgation CpAgELISA/ WB

–

–

–

Farm

365

5.2

NS

–

–

2003

Farm

687

5.4

–

–

Farm

403

3.7

– 5– >100 0

Purgation CpAgELISA/ WB

–

–

–

Farm

403

12.4

–

–

Farm

10

–

NS

Pierangeli et al. (2010) Pierangeli et al. (2010) Soriano et al. (2010)

2004

Mixed

46

8.7

–

Lavallén et al. (2011)

NS 2001 –02 2001 –02

Farm Domes tic Domes tic

42

19.1

44

11.4

44

38.6

–

12

–

NS

155

5.8

–

155

4.5

1932

Brasi l

2004 –07 Cana da

NS

Chile

NS 1992 –97

Peru

Farm Semistray Semistray Domes tic

cr

–

–

Perez et al. (2006)

– 10 (AW)

cox1

– G1 (90.0%); G6 (10.0%)

–

–

–

–

–

–

Purgation CpAgELISA

–

–

–

– 12 (AW)

– G1 (83.4%); G3 (8.3%); G5 (8.3%)

7 (E)

nad1

–

Purgation /PCR Coprosco py/PCR Coprosco py/PCR

– cox1, 12S rRNA

NS

nad1

G10 (100%) Putative G10 (100%)

11.0

NS

Purgation

–

–

–

Purgation CpAgELISA

–

–

–

–

–

–

–

–

–

–

–

–

–

–

–

–

NS

2002 2005 –06

Farm Domes tic

228

1.8

NS

334

7.2

–

1998

Farm

74

33.8

95c

1998

Farm

106

79.2

–

Purgation CpAgELISA

NS

Stray

48

6.3

NS

Necropsy

Reference Larrieu et al. (2000)

Cavagion et al. (2005) Perez et al. (2006)

us

an

Purgation CpAgELISA Purgation /PCR CpAgELISA/ WB CpAgELISA/ WB

M

2005 –08 2005 –08 2005 –09

d

1996

te

Perio d

ip t

No. sampl esa

Ac ce p

Coun try Arge ntina

Dog Popula tion Domes tic

Dopchiz et al. (in press) Farias et al. (2004) Farias et al. (2004) de la Rue et al. (2011) Himsworth et al. (2010a) Himsworth et al. (2010b) Apt et al. (2000) Alvarez et al. (2005) Acosta-Jamett et al. (2010) Lopera et al. (2003) Lopera et al. (2003) Moro et al. (2004)

70

Page 70 of 74

NS NS

Mixed Domes tic

61

50.8

–

22

36.4

–

CpAgELISA CpAgELISA

–

–

–

–

–

–

Moro et al. (2005) Reyes et al. (2012)

Ac ce p

te

d

M

an

us

cr

ip t

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).

71

Page 71 of 74

Table 5 Prevalence and molecular epidemiology of Echinococcus granulosus s.l. infection in dogs in Australia (2000 onwards).

a

Prevalence (%) 100 22.2 64.7 76.2 0.0 24.4 39.7

Worm burden (n) 2–42,600 NS 10–309,750 NS NS NS 30–104,000

Diagnostic procedure Necropsy Necropsy Necropsy Necropsy Purgation CpAg-ELISA Necropsy

ip t

No. samples1 23 27 221 21 22 561 126

cr

Dog Population Wild Wild Wild Wild Domestic Farm Wild

us

Period NS 2002 NS NS NS NS 2003–06

Referenc Jenkins e Brown a Jenkins a Banks et Banks et Jenkins e Jenkins e

Number of dogs analyzed by necropsy/purgation or number of faecal supernatants analyzed

Ac ce p

te

d

M

an

byCpAg-ELISA (ELISA for the detection of copro-antigens).

72

Page 72 of 74

Figure 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 intestinal dog

ip t

echinococcosis has been reported during the same period, but no molecular data are currently

Ac ce p

te

d

M

an

us

cr

available.

73

Page 73 of 74

ip t

us

cr

Graphical Abstract Intestinal dog echinococcosis: global epidemiology and genotypic diversity David Carmena. Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Ctra. MajadahondaPozuelo Km 2, 28220 Majadahonda, Madrid, Spain Guillermo A. Cardona. Livestock Laboratory, Regional Government of Álava, Ctra. de Azua 4, 01520 Vitoria-Gasteiz, Spain

Ac

ce pt

ed

M an

Global distribution and molecular epidemiology of Echinococcus spp. intestinal infections in dogs based on published literature from 2000 to date.

Page 74 of 74