Fascioloides magna

Taxobox
name = Giant liver fluke


regnum = Animalia
phylum = Platyhelminthes
classis = Trematoda
subclassis = Digenea
ordo = Echinostomida
familia = Fasciolidae
genus = "Fascioloides"
binomial = "Fascioloides magna"
binomial_authority = Bassi, 1875

"Fascioloides magna" (Bassi 1875), also known as giant liver fluke, large American liver fluke or deer fluke, is an important parasite of a variety of wild and domestic ruminants in North America and Europe. Adult flukes occur in the liver of the definitive host and feed on blood. Mature flukes measure 4 to 10 cm in length × 2 to 3.5 cm in width, and have an oval dorso-ventrally flattened body with oral and ventral sucker. The flukes are reddish-brown in colour and are covered by tegument. Similarly to that in other digenean trematodes, the life cycle includes intramolluscan phase in snails.Erhardová-Kotrlá, B., 1971. The occurrence of "Fascioloides magna" (Bassi, 1875) in Czechoslovakia. Academia, Prague, 155 pp.] Pybus, M.J., 2001. Liver flukes. In: Samuel, W.M., Pybus, M.J., Kocan, A.A. (eds.), Parasitic diseases in wild mammals, Iowa State Press, Iowa City, pp 121–149.]

History

"Fascioloides magna" is essentially of North American origin but the parasite was introduced into Europe with imported game animals at the second half of the 19th century. In spite of being native to North America the fluke was first described in Italy. Swales, W.E., 1935. The life cycle of "Fascioloides magna" (Bassi, 1875), the large liver fluke of ruminants in Canada with observations on the bionomics of the larval stages and the intermediate hosts, pathology of fascioloidiasis magna, and control measures. Canadian Journal of Research 12, 177–215.] In 1875, Bassi observed massive deaths of red deer in the Royal Park near Torino, Italy. The signs were similar to well known fasciolosis in sheep. He named it "Distomum magnum". The author believed that the parasite was introduced into the park in wapiti imported from USA in 1865.Bassi, R., 1875. Sulla cachessia ittero-verminosa, o marciaia, causata dal Distomum magnum. Medico Veterinaria Torino, S.4, v.4 (11-12), 497–515.] Most workers did not accept Bassi’s species because of his poor description. From 1882 to 1892, the fluke was recorded from different areas of the United States and described separately by many authors. Later, Stiles (1894) pointed out that the American findings are identical with species described previously by Bassi. Stiles made a complete morphological description of the adult fluke and named it "Fasciola magna" (Bassi 1875) Stiles 1894. In 1917, Ward showed that owing to the lack of the distinct anterior cone and the fact that vitellaria are confided to the region ventral to the intestinal branches, he established a new genus "Fascioloides" and rename it to "Fascioloides magna" (Bassi 1875) Ward 1917. [Ward, H.B., 1917. On the structure and classification of North American parasitic worms. Journal of Parasitology 4, 1–12.] In 1895, Stiles suggested that the life cycle of the fluke is very similar to "Fasciola hepatica", i.e. it includes an aquatic snail as an intermediate host. He gave a comparative description of the egg and miracidium of the fluke. [Stiles, C.W., 1895. The anatomy of the large American fluke ("Fasciola magna") and a comparison with other species of the genus "Fasciola", s. str. J Comp Med Vet Arch 16, 139–147, 213–222, 277–282.] However, first reported intermediate hosts of "F. magna" were not published until 1930’s. The complete life cycle of "F. magna", including a description of all the larval stages, was described by Swales (1935) in Canada .

Life cycle

varies 3-7 months and is dependent on host species. Adult "F. magna" can survive in the liver of the host up to 7 years.

Distribution

, respectively) were imported from USA or Canada.Špakulová, M., Rajský, D., Sokol, J., Vodňanský, M., 2003. Giant liver fluke ("Fascioloides magna"), an important liver parasite of ruminants. Parpress, Bratislava, 61 pp.]

North America

During the 20th century, "F. magna" was reported in these American states: Arkansas, California, Colorado, Illinois, Iowa, Kansas, Louisiana, Michigan, Minnesota, Montana, New York, Oklahoma, Oregon, South Carolina, Texas, Washington, and Wisconsin. In Canada, the fluke was reported in Alberta, British Columbia, Ontario, and Quebec. Currently, "F. magna" is enzootic in five major areas: (1) the Great Lakes region; (2) the Gulf coast, lower Mississippi, and southern Atlantic seaboard; (3) northern Pacific coast; (4) the Rocky Mountain trench; and (5) northern Quebec and Labrador. However, within these broad ranges, actual presence of giant liver flukes varies from locally abundant to locally absent.

Europe

"Fascioloides magna" was first reported by Bassi in Torino, Italy. In spite of Bassi’s work, no other data concerning the occurrence of F. magna in Europe were reported until 1930’s . In the Czech territory, Ullrich reported the first appearance of "F. magna "in fallow deer as late as 1930.Ullrich, K., 1930. Über das Vorkommen von seltenen oder wenig bekannten Parasiten der Säugetiere und Vögel in Böhmen und Mähren. Prager Archiv Tiermedicine 10, A (1/2), 19–43.] At the same time, Salomon (1932) diagnosed the fluke in one hunted red deer near Görlitz (Saxony) in Germany. Other isolated findings of the fluke were recorded in Italy and Poland. From 1948 till 1961, sporadic occurrence of the parasite in red deer ("Cervus elaphus"), fallow deer ("Dama dama") and roe deer ("Capreolus capreolus") were reported by several authors in former Czechoslovakia. However, all reports were published on the basis of incident discoveries in hunted deer and no massive infections were documented .In 1960’s, a number of "F. magna" outbreaks in cervids were reported in some areas of former Czechoslovakia. The prevalence of infection varied from 70 to 80 % in red deer and maximum parasite burden was 144 worms. In addition, sudden deaths were documented in free or game ranging deer. The highest mortality was reported in free ranging roe deer in Písek County in the South Bohemia of former Czechoslovakia. In the same region, moreover, the parasite was found in livers of slaughtered cattle.Záhoř, Z., 1965. Výskyt velké motolice ("Fascioloides magna" Bassi, 1875) u srnčí zvěře. Veterinářství 15, 322–324.] [Záhoř, Z., Prokš, C., Vítovec, J., 1968. Morfologie změn způsobených velkou motolicí ("Fascioloides magna", Bassi 1875) u skotu. Veterinary Medicine (Praha) 13, 369–375.] . water plant at the Danube River in Slovakia. The parasite has spread through whole Slovakian Danube watershed.Soon after the Slovakian first report, "F. magna" was found in red deer in Hungarian parts of Danubian floodplain forests. The prevalence reported by the same authors was up to 90 %. "F. magna" infection of cervids is a considerable problem in northern part of Hungary (Szigetköz) and the southern Danubian territory in the Gemenc area. Since the autumn of 2000, "F. magna" has been found in Austrian territory, east of Vienna. In years 2000-2001, the prevalence of the giant liver fluke in red deer in Austrian parts of Danube (east of Vienna) was 66.7 %.Ursprung, J., Joachim, A., Prosl, H., 2006. Epidemiology and control of the giant liver fluke, "Fascioloides magna", in a population of wild ungulates in the Danubian wetlands east of Vienna. Berliner und Müncher Tiermedicine Woch 119, 316–323.] Appearance of American liver fluke was reported in Croatia in January of 2000. [Marinculic, A., N. Dzakula, Z. Janicki, Z. Hardy, S. Lucinger, T.Zivičnjak: Appearance of American liver fluke (Fascioloides magna, Bassi,1875) in Croatia - a case report. Vet. arhiv 72, 319-325, 2002.] The prevalence of fascioloidosis among red deer in Hungary was 21,1-6O,7 % between 1998-2005. During the necropsy of 459 deer livers (using Egri's method) the number of flukes per host ranged from 1 to 138 in the period 1998-2005. [Egri, B.,Sztojkov, V.,1999. Újabb megfigyelések az észak-nyugat-magyarországi gímszarvasok Fascioloides magna fertőzöttségéről. Magy. Állatorv. Lapja 120, 304-305.] Giczi, E., Egri, B., 2006. Quantitative parasitologische Untersuchungsergebnisse zum Vorkommen von Fascioloides magna (Bassi, 1875) bei Rothirschen im Nordwesten von Ungarn (1998-2005). Tierarztl. Umschau 61, 660-666.] Regarding the origin of "F. magna" enzootic area in the Danube River watershed, it is essential to point out that cervids were not introduced into these localities, neither recently nor in the past. Origin of the "F. magna" population in Danubian floodplain forests in Central Europe remains therefore unclear.

Definitive hosts

("Rangifer tarandus").Foreyt, W.J., Todd, A.C., 1976. Development of the large American liver fluke, "Fascioloides magna", in white-tailed deer, cattle, and sheep. Journal of Parasitology 62, 26–32.] In Europe, "F. magna" occurs commonly in red deer ("Cervus elaphus"), fallow deer ("Dama dama") and roe deer ("Capreolus capreolus"). Domestic ruminants are also susceptible to natural infection with "F. magna". However, the infection is not patent, and domestic ruminants do not contribute to the propagation of the parasite in the environment.Swales, W.E., 1936. Further studies on "Fascioloides magna" (Bassi, 1875) Ward, 1917, as a parasite of ruminants. Canadian Journal of Research 14, 83–95] In North America, the giant liver fluke is commonly found in cattle, sheep and goats in areas where "F. magna" is enzootic in deer. In contrast, "F. magna" occurs rarely in domestic ruminants in Europe.. The list of all natural definitive hosts of "F. magna" is presented in Table.

The only indigenous primary definitive host of "F. magna" is white-tailed deer. This species has been parasitized by the fluke for the longest time in historical context. Wapiti and caribou are of Eurasian origin and entered North America during the Pleistocene epoch, and overlapped with white-tailed deer in some parts of North America. They might have encountered "F. magna" in these shared biotopes.

Clinical signs, pathology and pathophysiology

According to several American authors, three types of definitive host exist:
* (1) definitive hosts
* (2) dead-end hosts
* (3) aberrant hostsPathology of "F. magna" infection varies according to host type but some features are shared by all three types. Primary lesions usually occur in the liver and are associated with mechanical damage due to migrating juvenile flukes or fibrous encapsulation of sedentary adult flukes. The most common feature of "F. magna" infection is black pigmentation in abdominal or thoracic organs, especially in the liver. The hematin pigment is produced by flukes as a byproduct of feeding on blood.Campbell, W.C., 1960. Nature and possible significance of the pigment in fascioloidiasis. Journal of Parasitology 46, 769–775.] [Blažek, K., Gilka, F., 1970. Contribution to the knowledge of the pigment found in infection with "Fascioloides magna". Folia Parasitologica 17, 165–170.] Pigment within tissues is a result of migrating of juvenile flukes and it accumulates within hepatic cells without resorption.

(1) Definitive hosts

Definitive hosts are primarily New World and some Old World cervids. In definitive hosts, flukes are encapsulated in thin-walled fibrous capsules communicating to the bile system. The eggs are passed through the bile system, enter the small intestine, and leave the host with faeces. Therefore, the infection is patent. The capsules are a result of the defence response of the host to the parasite and are pathognomonic for "F. magna" infection. They contain two to five flukes, greyish-black fluid with eggs and cell detritus.

"F. magna" infections in definitive hosts are usually subclinical. However, massive deaths caused by the fluke in red-, fallow- and roe deer were reported. [Novobilský, A., Horáčková, E., Koudela, B., 2005. Current distribution of the giant liver fluke "Fascioloides magna" in the Czech Republic. Proceedings of the 13th Helminthological Days Held at Ředkovec, Czech Republic, May 9-13th 2005. Helminthologia 42, 181–182.] Lethargy, depression, weight loss and decreased quality of antlers can occur sporadically. In addition, nervous symptoms were observed very rarely. In the first case, urging motion followed by apathy was reported in one experimentally infected fallow deer.Erhardová-Kotrlá, B., Blažek, K., 1970. Artificial infestation caused by the fluke "Fascioloides magna". Acta Veterinaria Brno 39, 287–295.] Authors suggested that these symptoms were associated with hepatocerebral syndrome. Other author has observed partial paralysis in naturally infected wapiti caused by migrating juvenile flukes in the spinal cord. [Sharma, A., 2002. Final diagnosis: "Fascioloides magna" in spinal cord. [http://www.addl.purdue.edu/newsletters/2002/fall/fall2002.pdf] ] Biochemical and haematological profiles are little investigated in definitive hosts. A decrease of haemoglobin, elevation of γ-globulins, and increase of eosinophils in serum was observed in experimentally infected white-tailed deer. [Presidente, P.J., McCraw, B.M., Lumsden, J.H., 1980. Pathogenicity of immature "Fascioloides magna" in white-tailed deer. Canadian Journal of Comparative Medicine 44, 423–32.] [ Foreyt, W.J., Todd, A.C., 1979. Selected clinicopathologic changes associated with experimentally induced "Fascioloides magna" infection in white-tailed deer. Journal of Wildlife Diseases 15, 83–89.]

(2) Dead-end hosts

Dead-end hosts are represented by large bovids, suids, llamas, horses and some Old World cervids. Infections in dead-end hosts are characterized by excessive fibrosis, thick-walled encapsulation of flukes within hepatic parenchyma, and black pigmentation of various tissues. Both afferent and efferent bile ducts are totally occluded and are marked by tracts of fibrous tissue. The eggs can not be passed into the bile system, and, therefore, the infection is not patent. In addition, flukes rarely mature in dead-end hosts probably due to strong immune response. Nevertheless, appearance of "F. magna" eggs in the faeces of single experimentally infected calf has been documented. Pathophysiology or clinical symptoms in dead-end hosts have been rarely studied. In cattle, significant elevations of eosinophil counts in periphery blood but only slight increases of AST and GGT have been observed.Conboy, G.A., Stromberg, B.E., 1991. Hematology and clinical pathology of experimental "Fascioloides magna" infection in cattle and guinea pigs. Veterinary Parasitology 40, 241–255.] While American authors have not observed any clinical symptoms in cattle, anorexia and weight loss were recorded in naturally infected bulls in the former Czechoslovakia. [Chroustová, E., Hůlka, J., Jaroš, J., 1980. Prevence a terapie fascioloidózy skotu bithionolsulfoxidem. Veterinary Medicine (Praha) 25, 557–563.]

(3) Aberrant hosts

s, and haemorrhagic tracts in which juvenile flukes are located . While a lack of fibrous capsules within hepatic parenchyma has been reported by several authors , flukes in fibrous capsules have also been documented in sheep.Stromberg, B.E., Conboy, G.A., Hayden, D.W., Schlotthauer, J.C., 1985. Pathophysiologic effects of experimentally induced "Fascioloides magna" infection in sheep. American Journal of Veterinary Research 46, 1637–1641.] However, the wall of the capsule is different from those found in cervids and large bovids. The dominant feature is a diffuse fibrosis throughout the liver and haemorrhagic migratory tracts containing erythrocytes, black pigment, and cell detritus. The liver lesions are infiltrated by eosinophils, plasma cells, and pigment-laden macrophages. Sheep and goats die acutely without any previous clinical signs.. Only elevation of eosinophils and slight increase of γ-globulins were observed in experimentally infected sheep. Recently, several changes in biochemical and haematological profile have been documented in experimentally infected goats. The significant increase of GLDH (glutalaldehyde dehydrogenase) was recorded from 14 week after infection in goats experimentally infected with "F. magna". [Novobilský, A., Pavlata, L., Mišurová, Ľ., Antoš, D., Koudela, B., 2006. Porovnání průběhu infekce "Fascioloides magna" a "Fasciola hepatica" u experimentálně infikovaných koz. Proceedings of the 7th Slovakian and Czech Parasitological Days, Modra-Harmónia, Slovakia, May 23-27th 2006, p 27.]

Intermediate hosts

", may be also involved in the transmission of "F. magna" in Europe. This opinion is supported by successful experimental infection of "R. peregra" in the lab as well as by findings of naturally infected "R. peregra" in the environment Faltýnková, A., Horáčková, E., Hirtová, L., Novobilský, A., Modrý, D., Scholz, T., 2006. Is "Radix peregra" a new intermediate host of "Fascioloides magna" (Trematoda) in Europe? Field and experimental evidence. Acta Parasitologica 51, 87–90.] These findings suggested that the intermediate host spectrum of "F. magna" should be, similarly to North America, diverse in Europe. The list of intermediate hosts of "F. magna" is presented in following table.

(*) Snails originated from Australia infected with United States isolate of "F. magna"
(**) Snails originated from France infected with Czech isolate of "F. magna"

Diagnosis

While the eggs of "F. magna" resemble those of "F. hepatica", this similarity is of limited use; eggs usually are not passed in cattle and sheep. Recovery of the parasites at necropsy, as well as proper identification of "F. hepatica" or "F. gigantica" is necessary for definite diagnosis. When domestic ruminants and deer share the same grazing areas, the presence of disease due to "F. magna" should be kept in mind. Mixed infections with "F. hepatica" occur in cattle.

Control of "F. magna" and prevention

, have been used in control of "F. magna" infection in cervids. However, the results have differed between different authors. Same in the case of "F. hepatica", triclabendazole seems to be most effective against "F. magna". [Novobilský, A., Koudela, B., 2005. Treatment and control of "Fascioloides magna" infection in cervids – review. Veterinářství 55, 98–102.] Fascioloidosis of cervids was successfully controlled with triclabendazole in USA [Qureshi, T., Drawe, D.L., Davis, D.S., Craig, T.M., 1994.] , and triclabendazole with levamizole in Hungary [,Giczi, Egri.,2006. Use of bait containing triclabendazole to treat "Fascioloides magna" infections in free ranging white-tailed deer. Journal of Wildlife Diseases 30, 346–350.] , Canada [Pybus, M.J., Onderka, D.K., Cool, N., 1991. Efficacy of triclabendazole against natural infections of "Fascioloides magna" in wapiti. Journal of Wildlife Diseases 27, 599–605.] , Austria , and Croatia. [Janicki, Z., Konjevic, D., Severin, K., 2005. Monitoring and treatment of "Fascioloides magna" in semi-farm red deer husbandry in Croatia. Veterinary Research Communications 29, 83–88.] In contrast, rafoxanide is commonly used in treatment in Czech Republic Slovakia and Hungary . Nevertheless, recent studies suggested that use of rafoxanide in control of "F. magna" infection should be considered . Unfortunetally, rafoxanide in commercial drug called Rafendazol Premix is the only registered drug for wild ruminants. Triclabendazole and others are produced as drugs for domestic animals and it can be used in free-living animals only with special permit.

See also

* Fascioliasis
* "Fasciola hepatica"

References

External links

* [http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1680019 "F. magna" in Canada]
* [http://www.vef.hr/vetarhiv/papers/2006-76-7-1.pdf Control of fascioloidosis in Croatia (PDF format)]
* [http://www.usask.ca/wcvm/herdmed/specialstock/elk/diseases/liverfluke.html "F. magna" and wapiti]
* [http://www.unbc.ca/nlui/wildlife_diseases_bc/liver_flukes.htm Liver flukes]
* [http://www.addl.purdue.edu/newsletters/2002/fall/fall2002.pdf Final diagnosis: "Fascioloides magna" in spinal cord (PDF format)]
* [http://www.oie.int/eng/publicat/rt/2102/HAIGH.pdf Viral, parasitic and prion diseases of farmed deer and bison (PDF format)]


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