Heidi L. Enemark1, DVM, PhD; Stig M. Thamsborg2, DVM, PhD, DEVPC
The Spread of Echinococcus multilocularis and Its Effects - A European Perspective
Alveolar echinococcosis (AE), a life-threatening zoonotic infection caused by the metacestode stage of the fox tapeworm Echinococcus multilocularis, is expanding in Europe. Globally, E. multilocularis is ranked third among food-borne parasites by FAO/WHO based primarily on public health concerns. However, applying the same multicriteria-based risk ranking analysis, E. multilocularis is ranked first at the European level.1 The adult tapeworm, which is only few millimetres long, resides in the small intestine of wild carnivores (definitive hosts) such as, e.g., red foxes, raccoon dogs and wolves. However, domestic dogs and cats may be involved in the lifecycle as definitive hosts if they prey on infected small mammals, predominantly rodents, serving as intermediate hosts. Dogs that have access to rodents and hunting dogs run the highest risk of infection. Transmission to the intermediate host is faecal-oral via infective eggs excreted in the faeces of definitive hosts. The eggs are highly resistant to cold and capable of surviving for long periods in the environment. Based on a few experimental studies, the role of domestic cats in the transmission of E. multilocularis is thought to be small due to incomplete development and limited egg excretion. However, this has been questioned lately due to the detection of E. multilocularis eggs in a relatively high proportion of cat stools2 including Danish cats. Humans and other mammals may become accidental hosts following ingestion of eggs (e.g., from contaminated fruits and vegetables). Farming, gardening and contact with fox/dog fur are known risk factors for human infection. Although less commonly, dogs may also become accidental hosts and develop AE following ingestion of E. multilocularis eggs (e.g., related to coprophagia) or possibly following autoinfection secondary to intestinal infection.3
Echinococcus multilocularis is widespread in the northern hemisphere with endemic areas in the near Near East, Russia, China, Northern Japan and North America. In Europe, the parasite was considered to be restricted to Central Europe (i.e., Eastern France, southern Germany, parts of Switzerland and Austria) until the 1990s. Yet, expansion in prevalence and geographic range into Northern, Eastern and Western Europe is ongoing and within the past three decades the parasite has been reported in 17 previously non-endemic countries in Europe. Increasing fox populations and colonisation of residential areas are important underlying factors, but climate change, abundance of intermediate hosts, relocation of wildlife, globalization and traffic of pet dogs have also been proposed to play a role together with increased awareness and better diagnostic tools.4-6 So far, continuous surveillance of E. multilocularis in foxes in Finland, Ireland, Malta, Norway (apart from Svalbard) and United Kingdom has documented absence of the infection in these countries,6 but the risk of introduction with wildlife or due to pet travel is estimated to be high. To prevent introduction of E. multilocularis by dogs entering from endemic regions, requirements to show a veterinary deworming certificate at the border have been in place in most Scandinavian countries. Nevertheless, in Sweden the first case of E. multilocularis infection was detected in a fox in 2011; and today the parasite is considered endemic, although at a low prevalence, in Denmark after detection of positive foxes in several locations.7
Currently, AE is considered a rare disease in endemic European countries with incidences of 0.03 to 0.3 per 100 000 inhabitants per year, but numerous studies have documented a general increasing incidence, and in the actual population at risk, incidences from 4.7 to 8.1 cases per 100 000 inhabitants per year are observed. In the Baltic countries, a 10-fold increase of the AE incidence has been reported reaching 0.5–0.77 per 100 000 inhabitants between 2009–12.4 The incidence of AE in dogs is unknown, but several studies have found shedding of eggs in less than 2% of the dogs in endemic regions. The fact that AE is a slowly developing disease means that change in definitive host ecology/transmission patterns will not be reflected in increasing human incidence until 10–15 years later. Thus, the current increasing trend in human incidence may be the tip of the iceberg.
Clinical symptoms are absent in definitive hosts regardless of worm burden. In contrast, the symptoms may be severe in intermediate/accidental hosts. In humans, AE develops over a period of 5–15 years whereas the disease progresses more rapidly in dogs.
The infection is primarily localised to the liver where metacestodes form multiple cysts and transform the organ into an alveolar, sponge-like structure. After a while, protoscoleces are produced and new cysts are formed by exogenous budding. The growth is highly invasive and secondary lesions occurring in e.g., lungs and brain are referred to as metastases. If untreated, the mortality is close to 100%.3,8 In captive primates, AE has been documented to be particularly pathogenic and very difficult to control. A recent Swiss study of 23 dogs with AE found abdominal distension to be the predominant clinical sign followed by lethargy, anorexia, vomiting, diarrhoea and weight loss. The median age of the dogs was 3.1 years and most dogs were regularly walked off leash in rural areas with foxes in the vicinity.3
Excretion of E. multilocularis eggs in the final host can be detected by copro-ELISA or microscopic examination following flotation or sieving. However, PCR verification is needed while the eggs are morphologically indistinguishable from other taeniid type eggs.
In human medicine, diagnosis of AE is based on clinical findings (abdominal pain, jaundice, and weight loss), imaging (radiology, ultrasonography, computed axial tomography, magnetic resonance imaging) and detection of specific antibodies against E. multilocularis. The diagnosis can be confirmed histologically by identification of parasitic elements or by PCR. Similar methods are applicable in small animal medicine. AE is a differential diagnosis to liver/abdominal tumours.3,8
In humans, the preferred treatment of AE is radical surgical resection combined with long-term benzimidazole treatment. If complete resection of the lesion is impossible, lifelong anthelmintic treatment is indicated.8 Presently, there is no consensus concerning optimal treatment strategies in dogs, but Corsini et al. suggest "radical surgical resection and medical treatment or, if total resection is not possible, medical treatment alone."3
EU legislation governing preventive health measures for control of E. multilocularis allows member states claiming to be free of the parasite to require dogs to be treated against echinococcosis before being allowed to enter the country. Praziquantel is the drug of choice for treatment of definitive hosts. The drug is active against both immature and mature stages of the worm (but not ovicidal!) and should be given 24–120 hours prior to entry into a "free" area. According to the European Food Safety Authorities, treatment should be given "as close as possible to entry into a free country" while treatment earlier than 24 hours before entering allows a risk of reinfection before moving.9 Definitive hosts diagnosed with E. multilocularis should be treated with praziquantel for two consecutive days and eggs should be removed from the fur by thorough washing. Follow-up examination of faecal samples to secure successful treatment is recommended, and the faeces should be collected and safely destroyed for a period of three days post-treatment. Personnel involved in handling of infected animals are advised to wear mouth protection, gloves and protective clothing. In endemic regions, deworming at monthly intervals to prevent excretion of E. multilocularis eggs and zoonotic infection is recommended.10
Take Home Messages
- Echinococcus multilocularis is an important zoonotic parasite causing AE and high mortality in intermediate/accidental hosts if untreated.
- Veterinarians are considered at risk due to close contact with potential definitive hosts (dogs and cats).
- In Europe, E. multilocularis is mainly transmitted in a wildlife cycle with red foxes as the principal definitive hosts, but dogs may be important for zoonotic transmission due to close contact with humans.
- The role of domestic cats is unresolved - may be more important than previously anticipated.
- Prevalence and geographic range of E. multilocularis is expanding and pet travel is likely to be important for the introduction of the parasite into new areas.
- Dogs are the final hosts of the parasite but may also serve as accidental hosts with symptoms similar to AE in humans.
- Echinococcus multilocularis is particularly pathogenic to captive primates.
- Current AE therapy: surgery and/or lifelong treatment with benzimidazoles.
- Regular deworming of dogs is recommended in endemic areas to prevent zoonotic infection.
1. Bouwknegt M, et al. (under review). Prioritization of foodborne parasites in Europe.
2. Knapp J, et al. Could the domestic cat play a significant role in the transmission of Echinococcus multilocularis? A study based on qPCR analysis of cat feces in a rural area in France. Parasite. 2016;23:42. doi: 10.1051/parasite/2016052.
3. Corsini M, et al. Clinical presentation, diagnosis, therapy and outcome of alveolar echinococcosis in dogs. Vet Rec. 2015;177(22):569.
4. Gottstein B, et al. Threat of alveolar echinococcosis to public health - a challenge for Europe. Trends Parasitol. 2015;31:407–412.
5. Davidson RK, et al. The impact of globalisation on the distribution of Echinococcus multilocularis. Trends Parasitol. 2012;28:239–24 7.
6. Oksanen A, et al. The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis. Parasit Vectors. 2016;9(1):519.
7. Wahlström H, et al. Present status, actions taken and future considerations due to the findings of E. multilocularis in two Scandinavian countries. Vet Parasitol. 2015;213:172–181.
8. World Organisation for Animal Health (Office International des Epizooties) and World Health organization (2001). WHOI OIE Manual on echinococcosis in humans and animals: a public health problem of global concern. pp 1–286.
9. Anonymous. Reconsider timing of E. multilocularis treatment, suggests EFSA. Vet Rec. 2016;178(4):79. doi: 10.1136/vr.i327.
10. European scientific counsel companion animal parasites (ESCCAP) (2015). Worm control in dogs and cats. Guideline 01 2nd edition. http://www.esccap.org/uploads/docs/nkzqxmxn_esccapgl1endoguidelines.pdf (accessed 12 June 2017). (VIN editor: the link could not be accessed as of 1/11/2018; the third edition supersedes the second edition www.esccap.org/uploads/docs/0x0o7jda_ESCCAP_Guideline_01_Third_Edition_July_2017.pdf)