Echinococcus spp are zoonotic cestodes that circulate among different carnivore and herbivore hosts (Table) around the world.1 Echinococcus granulosus is a complex of species and strains, the most important of which—from a public health perspective—circulate among livestock and dogs.1 The G8 and G10 genotypes of E granulosus, which are now known as E canadensis, circulate among cervids (ie, moose, caribou, elk, deer) and canids (ie, wolves, coyotes, dogs). In the northern hemisphere, another important zoonotic species, E multilocularis, primarily circulates among rodents and wild canids, with dogs and cats considered spillover hosts.
Dogs & Cats as Definitive Hosts
In North America, the life cycles of E canadensis and E multilocularis are primarily maintained in wildlife (Figure 1); however, when spillover occurs, dogs can serve as definitive hosts for both species, whereas cats can serve as definitive hosts only for E multilocularis, although prevalence and intensity are low in cats and infections may not be patent.1,2 Definitive hosts are subclinically infected with small adult cestodes 1 to 10 mm in length in the small intestine.3 Even if entire adult cestodes (Figure 2) are passed in feces, they are unlikely to be detected with the naked eye, unlike the segments of long, ribbon-like cestodes such as Dipylidium spp or Taenia spp. Eggs are taeniid type (Figure 3) and cannot be microscopically distinguished from those of nonzoonotic Taenia spp cestodes.
Additional diagnostic challenges of Echinococcus spp infections on fecal flotation from definitive hosts include eggs not being shed during the prepatent period, intermittent shedding throughout patency, and eggs not always floating well in conventional salt and sugar flotation solutions.4 Because of these challenges, definitive diagnosis depends on molecular methods such as PCR5,6 or immunologic methods such as fecal coproantigen ELISA tests.7,8 However, these tests are not routinely available; therefore, there is great need for a sensitive and specific in-clinic test that can detect Echinococcus spp antigens or DNA in the feces of infected animals.
|E granulosus (G1)||E canadensis (G8, G10)||E multilocularis|
|Definitive hosts||Dog||Wolf, coyote, dog||Wolf, coyote, fox, dog, cat|
|Intermediate hosts||Sheep||Cervids||Rodents (eg, lemmings, voles, deer mice)|
|Aberrant intermediate hosts||Humans||Humans||Dogs, humans, nonhuman primates|
|Endemic range||California, Arizona, Utah, Colorado, New Mexico|
In Canada: Alberta, British Columbia, Labrador, Manitoba, Northwest Territories, Nunavut, Ontario, Québec, Saskatchewan, Yukon Territory
In the United States: Alaska, at least 7 contiguous states (ie, California, Washington, Idaho, Montana, Wyoming, Minnesota, Maine)
In Canada: Alberta, British Columbia, Manitoba, Northwest Territories, Nunavut, Ontario, Saskatchewan
In the United States: Alaska, north central United States (ie, Illinois, Indiana, Iowa, Michigan, Minnesota, Missouri, Montana, Nebraska, North Dakota, Ohio, South Dakota, Wisconsin, Wyoming)
|Human disease||Cystic echinococcosis||Cystic echinococcosis||Alveolar echinococcosis|
As definitive host: none
As intermediate host: alveolar echinococcosis
Treatment & Prevention of Adult Echinococcus spp in Dogs & Cats
In regions endemic for Echinococcus spp (see Table for endemic US and Canadian regions), clinicians should treat any dog or cat shedding taeniid-type eggs on fecal flotation with a cestocide labeled for Echinococcus spp such as praziquantel (5 mg/kg PO or 5.7 mg/kg IM),9 bearing in mind that Taenia spp are a more common source of such eggs. Clinicians in endemic regions should also prophylactically prescribe regular cestocidal treatment for any pet at risk for ingestion of infected intermediate hosts (eg, livestock, cervids, rodents).
The frequency of prophylactic treatment depends on the parasite species. The prepatent period for E granulosus and/or E canadensis in dogs is approximately 6 weeks,3 whereas the prepatent period for E multilocularis ranges from 26 to 36 days in dogs.9,10 Therefore, high-risk pets should be treated every 6 weeks in regions endemic for E granulosus and/or E canadensis and every 4 weeks in regions endemic for E multilocularis. Monthly treatment may be preferred to increase compliance, regardless of geographic location.
Dogs and cats are clinically unaffected when serving as definitive hosts for Echinococcus spp; however, treatment is important because of public health considerations. Eggs of E granulosus, E canadensis, and E multilocularis shed in pet feces are immediately infective and are environmentally resistant, with the ability to survive for months to years, and impervious to most chemicals (eg, formalin, ethanol, most commercial disinfectants). Eggs are inactivated by freezing at negative temperatures between -94°F and -112°F (-70°C to -80°C) for 3 to 7 days, by heating at temperatures greater than 140°F (60°C; ie, boiling, autoclaving, incineration), or by treating with 3.75% sodium hypochlorite for 5 minutes in the absence of organic material.11
Dogs as Intermediate Hosts for E multilocularis
For E multilocularis, rarely, dogs can serve as aberrant intermediate hosts, in which the larval stages do not fully develop, or as true intermediate hosts, in which the larval stage fully develops and protoscolices are present (Table). The larval stage of E multilocularis takes the form of alveolar hydatid cysts that generally begin in the liver (Figure 4) and may spread throughout the abdominal cavity and, in progressive cases, throughout the body.12 This is known as alveolar echinococcosis, and canine alveolar echinococcosis, which is often fatal, has been increasingly diagnosed pre- or postmortem in endemic regions of Europe and North America and in regions of North America beyond the previously established western and eastern distributional limit of the parasite.12-15 In North America, this recent emergence may be because of the introduction of European strains of E multilocularis (likely via importation of infected dogs from Europe) that have been subsequently established in wild canids.13,16,17
Dogs are presumably infected via consumption of eggs in the feces of wild canids in rural and remote areas; in urban areas, peri-urban green areas and off-leash parks may be contaminated.15,17 Rarely, cases of dogs with both adult cestodes in their intestines and alveolar echinococcosis have been described, which indicates that dogs could theoretically self-infect internally—as the eggs produced by adult cestodes are immediately infective—or externally via ingestion of eggs in their own feces.9
Breed and/or age predilections for canine alveolar echinococcosis cannot be inferred because few cases have been described. In 2 European studies of 23 and 11 cases, affected breeds included the shih tzu, dachshund, boxer, and Labrador retriever; in these studies, median age at time of diagnosis was 3.1 and 4.1 years, respectively.15,18 The most common clinical signs were abdominal distension, lethargy, and nonspecific GI signs.
Diagnosis of Alveolar Echinococcosis in Dogs
Radiography and ultrasonography may show suggestive space-occupying lesions, especially in the liver, that are similar in appearance to other cystic, neoplastic, or granulomatous lesions.18 Further imaging (ie, CT, MRI) may be more discriminatory and offer the option of clinical staging, as is similarly done in patients with neoplastic diseases.19 A serologic test is available in Europe but is only suggestive of alveolar echinococcosis, and false positives are possible.15,20
Definitive diagnosis of alveolar echinococcosis in dogs relies on microscopic or molecular confirmation using fluid from abdominocentesis or material obtained by fine-needle aspiration, biopsy, or surgical excision. In humans, fine-needle aspiration of hydatid cysts poses risks for anaphylactic reactions and/or seeding of protoscolices (ie, larval cestodes) throughout the abdominal cavity.19 Cytology may yield a definitive diagnosis with detection of characteristic cestode calcareous corpuscles or, rarely, protoscolices.9,15,21 Alternatively, or in questionable cases, there are a variety of PCR assays that can be performed in any diagnostic or research laboratory to detect E multilocularis DNA.13,22-24 Molecular techniques—which require fresh, frozen, or ethanol-fixed material—also allow for further genetic characterization,25,26 which is needed to better understand the source of exposure for dogs and to determine whether there are parasite genetic differences in zoonotic potential and pathogenicity.27
Prognosis & Treatment for Alveolar Echinococcosis in Dogs
Prognosis for canine alveolar echinococcosis is poor if the infection is detected after it is well established, if abdominal effusion is present, and if treatment is delayed.15 Whereas complete surgical resection is ideal, long-term administration of benzimidazoles (eg, albendazole [10 mg/kg PO q24h]) has been reported to be as effective as a combination of debulking surgery (ie, incomplete resection) and long-term albendazole treatment.15 On initial diagnosis, dogs should also receive a cestocide labeled for adult Echinococcus spp infection (eg, praziquantel) for 2 consecutive days in case adult cestodes are concurrently present in the intestine.9 It is not known whether praziquantel will prevent alveolar echinococcosis in dogs; in humans, it has little demonstrable effect against established alveolar echinococcosis. Owners should be advised to consult their healthcare provider, as they may have been exposed to the same source of infection as the dog.9
Disease in Humans
Diseases caused by Echinococcus spp in humans, although uncommon, are potentially serious. In humans, eggs may develop into larval cestodes (ie, hydatid cysts) that initially serve as space-occupying lesions in the liver and lungs and can cause problems when they grow too large, rupture, and/or spread in the abdominal cavity or to distant organs.19 In North America, endemically acquired cases of human echinococcosis are rare and are generally caused by E canadensis, which has decreased pathogenicity as compared with E granulosus and E multilocularis.28
Domestically acquired human alveolar echinococcosis is exceedingly rare in North America but is potentially fatal; before modern early detection and aggressive treatment protocols, human alveolar echinococcosis was associated with case fatality rates of approximately 90%.29 Human echinococcosis has been linked to close association with dogs.30,31 For these reasons, owners of pets with definitively diagnosed intestinal Echinococcus spp infections should be advised to consult their healthcare provider.9
Echinococcus spp cestodes are globally distributed and contribute significantly to human morbidity and mortality, as well as economic losses in livestock, especially in developing nations.34 Human echinococcosis is considered a neglected tropical disease by the World Health Organization (see Suggested Reading). Despite the term tropical, these parasites are well represented in the northern hemisphere, and some species (eg, E multilocularis) appear to be increasing in geographic range and prevalence in wildlife, pets, and humans.1,15,32,33 Veterinarians play a key role in the surveillance and control of these important tapeworms, which have both public and animal health significance.
Conclusion & Future Considerations
Surveillance in pets, wildlife, and humans is needed to detect and prevent geographic range expansion and global spread of Echinococcus species and strains. Clinicians play a key role in the detection and diagnosis of these parasites (see Global Relevance). Ideally, surveillance in animals can serve as early warnings of changes in parasite epidemiology and the risks posed to humans. The first detection of canine alveolar echinococcosis in Europe in the late 1980s9 was concurrent with an increase in the geographic range of the parasite in Europe32 and was followed by an increase in the human incidence of alveolar echinococcosis with a 20-year lag, as the incubation period in humans is 5 to 15 years.19,33
Increasing reports of canine alveolar echinococcosis in North America since 2009, in combination with detection of European strains of the parasite in both dogs and wildlife,13,16 may be an early warning of an emergence of human cases in North America in the next decade. Control of echinococcosis is possible, largely through veterinary interventions such as routine cestocide use in high-risk dogs in high-risk areas; risk assessment, screening, and treatment of translocated animals (both pets and wildlife); and client and public education.
- Deplazes P, Rinaldi L, Alvarez Rojas CA, et al. Global distribution of alveolar and cystic echinococcosis. Adv Parasitol. 2017;95:315-493.
- Kapel CM, Torgerson PR, Thompson RC, Deplazes P. Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats. Int J Parasitol. 2006;36(1):79-86.
- Jones A, Pybus MJ. Taeniasis and echinococcosis. In: Samuel WM, Pybus MJ, Kocan AA, eds. Parasitic Diseases of Wild Mammals. 2nd ed. Ames, IA: Iowa State University Press; 2001:150-192.
- Liccioli S, Kutz SJ, Ruckstuhl KE, Massolo A. Spatial heterogeneity and temporal variations in Echinococcus multilocularis infections in wild hosts in a North American urban setting. Int J Parasitol. 2014;44(7):457-465.
- Trachsel D, Deplazes P, Mathis A. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology. 2007;134(6):911-920.
- Wahlström H, Comin A, Isaksson M, Deplazes P. Detection of Echinococcus multilocularis by MC-PCR: evaluation of diagnostic sensitivity and specificity without gold standard. Infect Ecol Epidemiol. 2016;6. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4788769. Accessed May 31, 2017.
- Deplazes P, Alther P, Tanner I, Thompson RA, Eckert J. Echinococcus multilocularis coproantigen detection by enzyme-linked immunosorbent assay in fox, dog, and cat populations. J Parasitol. 1999;85(1):115-121.
- Morel N, Lassabe G, Elola S, et al. A monoclonal antibody-based copro-ELISA kit for canine echinococcosis to support the PAHO effort for hydatid disease control in South America. PLoS Negl Trop Dis. 2013;7(1):e1967.
- Deplazes P, Eckert J. Veterinary aspects of alveolar echinococcosis—a zoonosis of public health significance. Vet Parasitol. 2001;98(1):65-87.
- Rausch RL, Wilson JF, Schantz PM. A programme to reduce the risk of infection by Echinococcus multilocularis: the use of praziquantel to control the cestode in a village in the hyperendemic region of Alaska. Ann Trop Med Parasitol. 1990;84(3):239-250.
- Eckert J, Gottstein B, Heath D, Liu FJ. Prevention of echinococcosis in humans and safety precautions. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, eds. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. World Organization for Animal Health; 2001:238-246.
- Eckert J, Deplazes P. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev. 2004;17(1):107-135.
- Jenkins EJ, Peregrine AS, Hill JE, et al. Detection of a European strain of Echinococcus multilocularis in North America. Emerg Infect Dis. 2012;18(6):1010-1012.
- Skelding A, Brooks A, Stalker M, et al. Hepatic alveolar hydatid disease (Echinococcus multilocularis) in a boxer dog from southern Ontario. Can Vet J. 2014;55(6):551-553.
- Corsini M, Geissbühler U, Howard J, Gottstein B, Spreng D, Frey CF. Clinical presentation, diagnosis, therapy and outcome of alveolar echinococcosis in dogs. Vet Rec. 2015;177(22):569-569.
- Gesy K, Hill JE, Schwantje H, Liccioli S, Jenkins EJ. Establishment of a European-type strain of Echinococcus multilocularis in Canadian wildlife. Parasitology. 2013;140(09):1133-1137.
- Massolo A, Liccioli S, Budke C, Klein C. Echinococcus multilocularis in North America: the great unknown. Parasite. 2014;21:73.
- Scharf G, Deplazes P, Kaser-Hotz B, et al. Radiographic, ultrasonographic, and computed tomographic appearance of alveolar echinococcosis in dogs. Vet Radiol Ultrasound. 2004;45(5):411-418.
- Brunetti E, Kern P, Vuitton DA, Writing Panel for the WHO-IWGE. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114(1):1-16.
- Staebler S, Grimm F, Glaus T, et al. Serological diagnosis of canine alveolar echinococcosis. Vet Parasitol. 2006;141(3-4):243-250.
- Oscos-Snowball A, Tan E, Peregrine AS, et al. What is your diagnosis? Fluid aspirated from an abdominal mass in a dog. Vet Clin Pathol. 2015;44(1):167-168.
- Bowles J, McManus DP. NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. Int J Parasitol. 1993;23(7):969-972.
- Dinkel A, von Nickisch-Rosenegk M, Bilger B, Merli M, Lucius R, Romig T. Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. J Clin Microbiol. 1998;36(7):1871-1876.
- Davidson RK, Oines O, Madslien K, Mathis A. Echinococcus multilocularis—adaptation of a worm egg isolation procedure coupled with a multiplex PCR assay to carry out large-scale screening of red foxes (Vulpes vulpes) in Norway. Parasitol Res. 2009;104(3):509-514.
- Knapp J, Bart JM, Maillard S, Gottstein B, Piarroux R. The genomic Echinococcus microsatellite EmsB sequences: from a molecular marker to the epidemiological tool. Parasitology. 2009;137(3):439-449.
- Nakao M, Xiao N, Okamoto M, Yanagida T, Sako Y, Ito A. Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitol Int. 2009;58(4):384-389.
- Davidson RK, Lavikainen A, Konyaev S, et al. Echinococcus across the north: current knowledge, future challenges. Food Waterborne Parasitol. 2016;4:39-53.
- Schurer JM, Rafferty E, Farag M, Zeng W, Jenkins EJ. Echinococcosis: an economic evaluation of a veterinary public health intervention in rural Canada. PLOS Negl Trop Dis. 2015;9(7):e0003883.
- Kern P, Bardonnet K, Renner E, et al. European echinococcosis registry: human alveolar echinococcosis, Europe, 1982-2000. Emerg Infect Dis. 2003;9(3):343-349.
- Stehr-Green JK, Stehr-Green PA, Schantz PM, Wilson JF, Lanier A. Risk factors for infection with Echinococcus multilocularis in Alaska. Am J Trop Med Hyg. 1988;38(2):380-385.
- Yang YR, Sun T, Li Z, et al. Community surveys and risk factor analysis of human alveolar and cystic echinococcosis in Ningxia Hui autonomous region, China. Bull World Health Organ. 2006;84(9):714-721.
- Davidson RK, Romig T, Jenkins EJ, Tryland M, Robertson LJ. The impact of globalization on the distribution of Echinococcus multilocularis. Trends Parasitol. 2012;28(6):239-247.
- Schweiger A, Ammann RW, Candinas D, et al. Human alveolar echinococcosis after fox population increase, Switzerland. Emerg Infect Dis. 2007;13(6):878-882.
- Torgerson P. Economic effects of echinococcosis. Acta Trop. 2003;85(2):113-118.
World Health Organization. Neglected tropical diseases. http://www.who.int/neglected_diseases/diseases/en. Accessed May 31, 2017.
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