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Echinocococcus
Cystic and Alveolar Hydatid Disease Caused by Echinocococcus Species in the Contiguous United States Bayer Zoonosis Symposium 2003 Kevin R. Kazacos, DVM, PhD Department of Veterinary Pathobiology Purdue University West Lafayette, Indiana Adult tapeworms in dogs and cats usually cause little pathology and are of minor clinical importance. Eliminating tapeworms in pets is driven primarily by the public's aversion to seeing proglottids crawling on their pets or in the pet's feces or bedding. However, certain tapeworms of pets and wildlife are very important causes of larval infection in humans and animals, in which they may cause serious, life-threatening disease. On a global scale, larval infections with tapeworms of the genus Echinococcus represent some of the most serious and important zoonotic diseases. There are four Echinococcus spp worldwide.
Echinococcus vogeli and Echinococcus oligarthrus occur in South America and primarily maintain sylvatic predator-prey cycles with few reports of human infection. The two main species, Echinococcus granulosus and Echinococcus multilocularis, produce cystic echinococcosis (hydatid disease), and alveolar echinococcosis (alveolar hydatid disease), respectively. Both tapeworms occur in the contiguous United States, with the latter parasite having a larger and expanding range in the north central region.
It is important for veterinarians to be aware of these tapeworms so they may provide sound recommendations and take appropriate steps to protect their clients and the public from infection with these parasites. Echinococcus granulosus E. granulosus is a well-known parasite in Alaska and parts of western Canada, where it exists primarily in a sylvatic cycle. In the contiguous United States, the sylvatic strain of E. granulosus occurs in foci in the north central and western states, where it uses wolves and coyotes as definitive hosts and large wild ungulates (elk, moose, etc.) as inter-mediate hosts. A domestic strain of the parasite, using dogs as definitive hosts and sheep as intermediate hosts, also occurs, primarily within sheep ranching areas of the southwest. The adult tapeworms in dogs and wild canids are about 2 to 7 mm long and usually have three to four segments (Figure 1). When gravid proglottids are shed, they release eggs in the feces that are directly infective to intermediate hosts that may accidentally ingest them.
Although the most common intermediate hosts are sheep and wild ungulates, humans can also become infected from eggs shed by domestic dogs or wild canids. In the intermediate host, the egg hatches and the oncosphere (hexacanth embryo) penetrates the intestine and migrates to the liver or other location, where it transforms into a fluid-filled, cystic metacestode called a hydatid cyst. Hydatid cysts develop slowly and contain daughter cysts and numerous brood capsules and protoscolices, the latter two produced from germinative membranes lining the cyst and daughter cysts. The cystic hydatid of E. granulosus is a unilocular structure with a thick, laminated outer layer that is surrounded by a host-derived fibrous tissue capsule. Hydatid cysts can grow quite large, reaching several centimeters in diameter, and may contain hundreds of thousands of protoscolices (Figure 2).
The definitive host is infected when it consumes the protoscolices either by predation or scavenging of intermediate hosts. Each of the protoscolices has the ability to grow into an adult tapeworm when ingested by the canine host; thus large worm burdens are not uncommon.
Figure 1 Adult E. granulous. (From Zaiman H: A Pictorial Presentation of Parasites, Valley City, North Dakota, with permission.) Figure 2 E. granulosus cyst in the brain of a 7 year old Italian born girl. (From Zaiman H: A Pictorial Presentation of Parasites, Valley City, North Dakota, courtesy of Dr. H. Fink.) Pathologic damage in infected humans is related to cyst size and location, with large cysts impinging on surrounding tissues and organs and interfering with their normal function. Hydatid cysts are more rapidly pathogenic when located in the brain or spinal cord (Figure 2); otherwise, it may take years before they reach sufficient size to cause clinical disease.
Further danger involves rupture or leakage of fluid from a cyst, as may occur during routine surgery or from a traumatic blow to the abdomen. Along with the risk of anaphylaxis, each of the protoscolices in the body cavity has the ability to grow into another hydatid cyst, and extensive secondary hydatidosis may result, with grave consequences. Cystic echinococcosis is diagnosed through radiography and other imaging modalities, and by serology.
Treatment of hydatid cysts is by careful surgical removal, complicated by the danger of leakage of protoscolices. Chemotherapy with albendazole or mebendazole is a necessary adjunct to surgery. Echinococcus multilocularis E. multilocularisoccurs in the tundra zone of Alaska and northern Canada but is also enzootic throughout much of the north central and midwestern United States and south central Canada. Evidence indicates that its range has been expanding southward and eastward, and its prevalence has been increasing in wild canid populations, with crossover into domestic cats and dogs. The primary definitive hosts of E. multilocularis in the central region are red foxes and coyotes (Figure 3), but domestic dogs are very susceptible to infection and the parasite will also infect cats. The adult tapeworms are quite small, averaging 2 mm (1.2 to 3.7 mm) in length (Figures 4 and 5).
Common intermediate hosts include small rodents such as meadow voles and deer mice. Other intermediate hosts include muskrats, wood rats, and house mice. When intermediate hosts ingest infective eggs in the feces of canids or cats (Figure 6), the oncospheres migrate to the liver and transform into alveolar hydatid cysts. In contrast to the hydatid cyst of E. granulosus, which has a thick, fibrous wall, an alveolar hydatid has a thin outer wall and is composed of numerous small vesicles in a semisolid matrix. The multilocular cyst grows slowly and progressively infiltrates surrounding host tissues by means of tubular processes and thus resembles a highly invasive and proliferative malignant neoplasm (Figure 7).
The many thin-walled vesicles produce protoscolices (Figure 8), which are infective to the definitive host upon ingestion. Figure 3 Indiana coyote heavily infected with E. multilocularis. Figure 4 A Taenia pisiformis adult surrounding numerous adult E. multilocularis, from the coyote in Figure 3. (From Hildreth MB, Johnson MD, Kazacos KR: Echinoccoccus multilocularis: A zoonosis of increasing concern in the United States. Compend Contin Educ Pract Vet 13(5):727-738, 1991, with permission) Figure 5 E. multilocularsis adults recovered from the Indiana coyote in Figure 3. Ruler is in millimeters. (Reprinted from Hildreth MD, Johnson MD, Kazacos KR: Echinococcus multilocularis: A zoonosis of increasing concern in the United States. Compend Contin Educ Pract Vet 13(5):727-738, 1991, with permission.) Figure 6 E. multilocularis egg recovered from a red fox in South Dakota. (Courtesy of Dr. M. Hildreth.) Figure 7 Gerbil infected with E. multilocularis alveolar hydatid cysts, 11 months postinfection with eggs from the coyote in Figure 3. (Reprinted from Hildreth MD, Johnson MD, Kazacos KR: Echinococcus multilocularis: A zoonosis of increasing concern in the United States. Compend Contin Educ Pract Vet 13(5):727-738, 1991, with permission.) Figure 8 E. multilocularis protoscolices recovered from alveolar hydatid cysts in an experimentally infected gerbil. Range of E. multilocularis in Central North America E. multilocularis has traditionally been considered a parasite of the northern tundra, and indeed the majority of human cases reported from the United States are from Alaska. However, since the 1960s, the cestode has been recognized with increasing frequency in a large endemic focus in central North America, encompassing all or part of 13 north central and midwestern states in the United States and three Canadian provinces (Figure 9). In the contiguous United States, E. multilocularis was first identified in the early 1960s in red foxes in North Dakota. It was subsequently identified, in 1965 to 1969, in wild canids or rodents in South Dakota, Iowa, Minnesota, and Montana. By 1982 to 1983, the parasite had been found in Wyoming, Nebraska, northern Illinois, and Wisconsin, and in 1990 to 1991 it was identified in Indiana and Ohio. The parasite is also known to occur in wild canids in southern Michigan (Storandt et al, unpublished) and northeastern Missouri (Bates et al, unpublished). Presently, the southernmost front of the parasite's range extends along the southern border of Wyoming, eastward through central Nebraska, northeastern Missouri, central Illinois and Indiana, and into north central Ohio (Figure 9). Prevalence of infection ranges from a low of 4.8% in red foxes in western Nebraska to a high of 88.9% in red foxes in eastern South Dakota. In northeastern Nebraska, 44.6% of red foxes were infected; in Illinois, 35.3% of coyotes were positive; and in Indiana, 22.5% of red foxes and 18.6% of coyotes were infected. In the latter study, mean intensity of infection for red foxes was 372 worms (range 2 to 3,640) versus 6,579 worms for coyotes (range 1 to 52,000).
Coyotes typically have a more diverse diet than red foxes as well as a larger home range. They can also travel much longer distances than red foxes, a fact that is an important consideration in the spread of this parasite. Figure 9 Current distribution of E. multilocularis in central North America, based on surveys of wild canids. The Role of Dogs and Cats in E. multilocularis Transmission E. multiloculariswill infect both dogs and cats that hunt and consume wild rodents infected with the larvae. Both animals could then serve as sources of infection for humans. Dogs are a much more suitable host for the parasite than cats, and in many parts of the world infected dogs are an important source of human infection. Compared to the infection in dogs, worms recovered from cats are usually smaller, fewer in number, and have poorly developed reproductive organs and fewer eggs. Thus far, there have been only two human cases recorded from central North America but in one of these it is believed that a woman from southwestern Minnesota acquired her infection from an infected farm cat or dog.
To date, E. multilocularis has been recovered from cats in central North America but not from dogs; however, indirect evidence indicates that the parasite also infects dogs in the region. In 1971 to 1976, Kritsky and Leiby (unpublished) found 1% to 5% of farm cats in North Dakota to be infected with E. multilocularis. In another study, Wobeser (1971) found 3 of 131 cats near Saskatoon, Saskatchewan to be infected. From 1988 to 1990, Hildreth examined 20 dogs and 43 cats in South Dakota but none were found to be infected. Our laboratory examined 123 farm dogs from southwestern Minnesota using coproantigen ELISA (performed by Dr. P. Deplazes in Europe) and found 5 of the dogs to be positive for E. multilocularis. We have also isolated and maintained the sylvatic strain of E. multilocularis several times in lab rodents and have repeatedly used it to infect dogs. In every case, the parasite had high infectivity for dogs, which often developed large worm burdens, in one study averaging 43,100 worms (range 6,200 to 75,200). It is clear that in enzootic areas both dogs and cats must be considered as potential sources of human infection and treated accordingly. Diagnosis of E. multilocularis in Dogs and Cats The antemortem diagnosis of E. multilocularis infection in dogs and cats is difficult. The gravid proglottids of the parasite are too small to be easily recognized in fecal samples. The eggs are recoverable by fecal flotation but are indistinguishable from those of Taenia species that may also be present. Mixed infections are also a possibility. It is recommended that all fecal samples be care-fully examined grossly for Taenia proglottids and that their presence or absence be correlated with results of fecal flotation. If taeniid eggs are found in the fecal sample but no proglottids can be found, there should be a high suspicion of Echinococcus infection and the sample and patient treated with great caution. The animal should be quarantined and dewormed with praziquantel and its feces carefully collected and disposed of for at least 2 to 3 days, because worm dissolution results in a large number of eggs being shed in the feces shortly after treatment. The cage should then be decontaminated using boiling water, flaming, strong bleach, or a combination of the three. In areas where E. multilocularis is enzootic, individuals who perform fecal examinations should handle and dispose of feces in a safe manner. Care also should be taken to wash one's hands with soap and wipe down examination tables with bleach or alcohol in between patients. Treatment of Dogs and Cats In addition to removing other cestodes, the anthelmintic praziquantel is highly effective against the intestinal adults and immatures of E. multilocularis and E. granulosus and is considered the drug of choice for treating these parasites in dogs and cats. It is the only product approved in the United States for treating both of these cestodes. Praziquantel is found in Droncit, Drontal (praziquantel/pyrantel pamoate) for cats, and Drontal Plus (praziquantel/pyrantel pamoate/febantel) for dogs (Bayer HealthCare). In endemic areas, pets that are allowed to roam and hunt wild rodents have a higher likelihood of becoming infected with E. multilocularis. It is recommended that such animals be dewormed with praziquantel on a regular basis to reduce the likelihood of patent infection and egg shedding near humans. Since the prepatent period of E. multilocularis is approximately 28 days following infection with larvae, a deworming interval of 21 to 26 days has been recommended to prevent the development of patent infections and contamination of the environment with eggs. Pet owners should also be advised to take other precautionary steps, including regular fecal cleanup and disposal, hand washing, and, if possible, preventing or modifying their pet's behavior concerning consumption of wild rodents. Summary The hydatid tapeworms E. granulosusand E. multilocularisboth occur in different parts of the contiguous United States. The alveolar hydatid tapeworm, E. multilocularis, is endemic in a larger and expanding area encompassing much of the north central and midwestern United States and south central Canada. Both parasites exist primarily in sylvatic cycles in which wild canids (wolves, coyotes, red foxes) serve as definitive hosts but there is increasing evidence of their crossover to domestic dogs and, in the case of E. multilocularis, to cats. Dogs and cats allowed to roam and hunt wild rodents are at a greater risk of infection with E. multilocularis. Veterinarians should advise the owners of such animals to take appropriate precautions to prevent animal and human infections with this parasite. This would include regular treatment of such animals with the cestocide praziquantel, increased sanitation and hygiene, and, where possible, modification of pet behavior.
Suggested Readings 1. Eckert J: Alveolar echinococcosis (Echinococcus multilocularis) and other forms of echinococcosis (Echinococcus vogeli and Echinococcus oligarthrus), in Palmer SR, Lord Soulsby, Simpson DIH (eds): Zoonoses. New York, Oxford University Press, 1998, pp 689-716. 2. Gemmell MA, Roberts MG: Cystic echinococcosis (Echinococcus granulosus), in Palmer SR, Lord Soulsby, Simpson DIH (eds): Zoonoses. New York, Oxford University Press, 1998, pp 665-688. 3. Hildreth MB, Johnson MD, Kazacos KR: Echinococcus multilocularis: A zoonosis of increasing concern in the United States. Compend Contin Educ Pract Vet 13(5):727-738, 1991. 4. Kazacos KR, Storandt ST: Echinococcus multilocularis in North America. Proc Am Assoc Vet Parasitol 42:92, 1997. 5. Kazacos KR, Storandt ST, Bolka DL, et al: Efficacy of praziquantel (Droncit) against adult Echinococcus multilocularis in dogs. Proc Am Assoc Vet Parasitol 38:53, 1993. 6. Kazacos KR, Storandt ST, Bolka DL, et al: Efficacy of praziquantel (Droncit) against immature and patent Echinococcus multilocularis in dogs. Proc Am Assoc Vet Parasitol 39:65, 1994. 7. Rausch RL: Life cycle patterns and geographic distribution of Echinococcus species, in Thompson RCA, Lymbery AJ (eds): Echinococcus and Hydatid Disease. Wallingford, UK, CAB Publishing, 1995, pp 89-134. 8. 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 Parasito l84:239-250, 1990. 9. Storandt ST, Kazacos KR: Echinococcus multilocularis identified in Indiana, Ohio, and east-central Illinois. J Parasitol 79:301-305, 1993. 10. Storandt ST, Virchow DR, Dryden MW, et al: Distribution and prevalence of Echinococcus multilocularis in wild predators in Nebraska, Kansas, and Wyoming. J Parasitol 88: 420-422,2002. 11. Strategic control of intestinal parasites: Diminishing the risk of zoonotic disease. Compend Cont Educ Pract Vet 19(sup-pl):1-20, 1997. Speaker Information (click the speaker's name to view other papers and abstracts submitted by this speaker) Kevin R. Kazacos, DVM, PhD Department of Veterinary Pathobiology Purdue University West Lafayette, Indiana
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