Chapter Two - Echinococcosis: Control and Prevention

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Abstract

Human cystic echinococcosis (CE) has been eliminated or significantly reduced as a public health problem in several previously highly endemic regions. This has been achieved by the long-term application of prevention and control measures primarily targeted to deworming dogs, health education, meat inspection, and effective surveillance in livestock and human populations. Human CE, however, remains a serious neglected zoonotic disease in many resource-poor pastoral regions. The incidence of human alveolar echinococcosis (AE) has increased in continental Europe and is a major public health problem in parts of Eurasia. Better understanding of wildlife ecology for fox and small mammal hosts has enabled targeted anthelmintic baiting of fox populations and development of spatially explicit models to predict population dynamics for key intermediate host species and human AE risk in endemic landscapes. Challenges that remain for echinococcosis control include effective intervention in resource-poor communities, better availability of surveillance tools, optimal application of livestock vaccination, and management and ecology of dog and wildlife host populations.

Introduction

By the mid 19th century the aetiology of human cystic hydatidosis and colloid ‘carcinoma’ were recognized to be of helminthic parasitic origin caused by a cestode(s) (see Chapter: Immunology of Alveolar and Cystic Echinococcosis (AE and CE) by Gottstein et al., 2017). However, whether both diseases were caused by different forms of Echinococcus granulosus or by two separate species was not fully confirmed until the life cycle biology and pathology of Echinococcus multilocularis in wild mammals was determined in the 1950s (Rausch and Schiller, 1951, Vogel, 1955). In contrast, the life cycle of E. granulosus in domestic mammals was already delineated in 1863 after experimental infection studies by Von Siebold and Naunyn (see Grove, 1990). Furthermore, the public health importance of CE (hydatidosis) in continental Europe and Iceland in the mid 19th century was significant enough for hydatid disease control recommendations to be published in 1854 and 1863 (Grove, 1990). This was followed by an ultimately successful long-term national health education programme against CE in Iceland (1863–90) (Craig and Larrieu, 2006). The earliest control programme for human alveolar echinococcosis (AE) occurred on Reuben Island in northwest Japan from the 1940s when the fox population was deliberately eliminated to eradicate transmission (Ito et al., 2003a). Currently (2016) both Iceland and Reuben Island (Japan) remain free from echinococcosis and still maintain strict controls on dog registrations and/or movement.

Despite several highly successful hydatid control programmes from the 1960s, primarily in regions with relatively well-developed agricultural sectors (e.g., New Zealand, Tasmania, Cyprus, Chile), human CE remains a significant public health problem in the early 21st century over large pastoral areas in South America, North Africa, Eastern Europe, the Middle East, Central Asia, Russia and China (WHO/OIE, 2001, Alvares Rojas et al., 2014). Total numbers of human cases are >>1 million with an associated significant high disease burden (Budke et al., 2006). The highest burden of human CE occurs over a large more or less contiguous transmission zone from North Africa, Near East, Middle East, Central Asia, eastern Russia and western China (Budke et al., 2006, Craig et al., 2007a). Over this endemic zone, however, only a few CE control programmes are currently active (e.g., western China) or planned (e.g., Tunisia) (WHO, 2010a).

At least 18 echinococcosis control programmes to reduce human CE incidence, have been implemented in different world regions since the 1960s, of which 3 were at national level (New Zealand, Cyprus, Uruguay) and the others at provincial level (Table 1). In all of those programmes the key element or control tool initially or eventually applied was the supervised dosing of owned dogs with a praziquantel(PZQ)-based anthelmintic at a frequency of 4–8 times per year (Gemmell et al., 2001, Craig and Larrieu, 2006, Lembo et al., 2013). Five island-based CE control programmes, including Iceland (from 1863), New Zealand, Tasmania, Cyprus and the Falkland Islands (Las Malvinas), were highly successful in eliminating human CE as a public health problem, with all immediately or eventually applying dog-targeted interventions (including culling, purgation and/or anthelmintic treatments) (Gemmell and Roberts, 1998, Economides et al., 1998, Craig and Larrieu, 2006). By contrast several continental-based CE control programmes ranged from highly successful (e.g., Region XII, Chile; Rio Negro, Argentina; La Rioja, Spain), eventually successful (e.g., Uruguay) to more limited impact (e.g., Turkana, Kenya; mid-Wales, UK) (Craig and Larrieu, 2006) (Table 1).

Modern control of E. multilocularis transmission in wildlife cycles is much more difficult to implement compared to E.granulosus in its domestic animal cycles because it requires targeted anthelmintics to the fox population. Distribution of baits containing PZQ in endemic areas can have a significant impact on vulpine prevalence, but logistics, cost and sustainability are difficult to maintain over long periods and over large geographic areas (Hegglin and Deplazes, 2013). Where domestic dogs have an important role in zoonotic risk for human AE, frequent deworming of owned dogs should be implemented for public health reasons (Rausch et al., 1990, Wang et al., 2014).

A critical aspect of echinococcosis control has been the appropriate surveillance of both human CE or AE disease incidence or prevalence, livestock prevalence for CE and canine or vulpine echinococcosis prevalence. Without adequate surveillance data at baseline and at quarterly or annual periods post intervention, the impact of control measures will be difficult or impossible to assess and thus justify ongoing expenditure to maintain costly interventions.

Since the 1970s new tools and approaches have become available to assist in planning and implementation of interventions and surveillance strategies. These include an excellent antiworm drug (PZQ) for dogs and foxes (baits); use of portable ultrasound for human screening (CE and/or AE) within endemic communities; a highly effective vaccine (EG95) to prevent ovine echinococcosis; a laboratory-based test [coproantigen enzyme-linked immunosorbent assays (ELISA)] to replace the arecoline purgation test in dogs and to test fox scats; computer-based modelling of cost-benefit for interventions; and transmission dynamics and predictive modelling for intervention combinations (Torgerson and Heath, 2003; Craig et al., 2007b). The reasons for success in some CE control programmes and variable impacts for others are important issues that have been discussed (e.g., Gemmell, 1990, Craig and Larrieu, 2006) but received only little critical analysis (Larrieu and Zanini, 2012, Lightowlers, 2012).

The life cycle biology of all taeniid cestodes, including Echinococcus spp., has evolved through predator–prey transmission between carnivore and herbivore mammalian hosts. Though similar in this respect Echinococcus granulosus senso lato and E. multilocularis differ in utilization of intermediate hosts, i.e., ungulate versus rodent/small mammals respectively. Transmission of E. granulosus s.l. is now primarily represented globally by cycles between dogs and domestic livestock, while E. multilocularis transmission occurs primarily within wildlife cycles between fox definitive and rodent intermediate hosts. From a control perspective the main target for intervention of both Echinococcus species is the definitive host (dogs or foxes) with the aim to reduce or eliminate adult worm burdens. The anticestode drug PZQ provides an excellent cestocidal deworming tool for dogs and foxes but the logistics of regular mass treatment are challenging. Dogs are also an excellent host for E. multilocularis and as such may increase zoonotic risk. Targeting intermediate hosts for CE control may be undertaken through classical meat inspection at slaughter but also using an infection preventive vaccine (EG95). There are currently no usable vaccines for definitive hosts. In contrast control measures directed against small mammals would not usually be considered economic or ecologically sound. Treatment of human CE and AE cases may be a public health priority but will not directly affect transmission because humans are almost always ‘dead-end’ hosts. Health education has the potential to reduce risky behaviour of humans, for example, unhygienic slaughter and dog contact, but education is also probably more important for community acceptance and voluntary participation in long-term hydatid-control programmes.

Section snippets

Targets, Options and Tools for Control of Echinococcus granulosus

At any one time transmission of E. granulosus is dependent on presence of viable parasite stages in dogs or other canids (adult tapeworms), domestic ungulates or wild herbivores (metacestodes) and the environment (eggs). As stated, human infections with the metacestode (CE) do not normally contribute to active transmission (because it requires a dog to ingest hydatid cysts). Removal or reduction in worm biomass in definitive hosts (usually dogs) will have the greatest and quickest effect to

Surveillance of cystic echinococcosis in humans

Surveillance in humans is critical for a decision to embark on a CE control programme and also to inform the public and the control authority about the progress of control. Surgical and medical treatment data have been the key to measuring the public health impact and burden of CE disease in endemic communities (Schantz, 1997, WHO/OIE, 2001, Budke et al., 2006). In addition, community screening using ultrasound scanners for abdominal CE case finding has more recently been adopted to provide

Successful hydatid control programmes

Since the first hydatid control programme was implemented in Iceland in the 1860s at least 18 other intervention programmes have been undertaken in different world regions to reduce the transmission of E. granulosus and to try and reduce or eliminate human CE as a public health problem. Many of these programmes have already been reviewed elsewhere (Gemmell, 1978, Gemmell, 1990, Gemmell and Schantz, 1997, Economides et al., 1998, Gemmell and Roberts, 1998, Gemmell et al., 2001, Craig and

Targets and Tools for Control of Echinococcus multilocularis

The life cycle (and therewith the zoonotic risk) of E. granulosus depends mainly on domestic animals, which are under direct control of the animal keepers. As for E. granulosus, domestic dogs can be an important or even the main source for human infections and should always be regarded as an important target for control measures against E. multilocularis. However, in contrast to E. granulosus, its life cycle is mainly maintained by wild intermediate and final hosts, which are much more

Surveillance of alveolar echinococcosis in humans

In Europe where human AE is a rare disease, hospital records and specific registers are important for epidemiological and surveillance data and are reasonably reliable when based on histo-pathological and/or molecular DNA confirmation (Kern et al., 2003, Vuitton et al., 2003, Vuitton et al., 2015, Said-Ali et al., 2013). In underdeveloped resource-poor endemic regions, for example, in Central Asia and western China, hospital records may be of some value (e.g., Raimkylov et al., 2015), but often

Reuben Island (Japan)

An early example of the successful control of E. multilocularis has been reported from Rebun Island in Japan (Ito et al., 2003a). In 1937 a first case of human AE was diagnosed on this small island, which comprises an area of not more than 83 km2. In the following decades human AE became highly prevalent and until 1964 a total of 111 patients had been diagnosed for this previously unknown disease on the island. This sudden occurrence of human AE was linked with the introduction of 12 pairs of

Conclusions and Future Prospects for Control of Echinococcosis

The global burden of human CE remains significant in the early part of the 21st century. In addition, although human AE is a globally rare disease there remain significant hotspots of transmission in Eurasia. The WHO has added echinococcosis to a list of 17 neglected tropical diseases, and it is prominent in the list of 12 NZDs (WHO, 2010a, WHO, 2010b). Control and prevention of NZDs is difficult especially when treatment of humans has no ability to interrupt transmission as is the case for

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