Fascioloides magna
Encyclopedia
Fascioloides magna, also known as giant liver fluke, large American liver fluke or deer fluke, is an important parasite of a variety of wild and domestic ruminant
s 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
. As with other digenea
n trematodes, the life cycle includes intramolluscan phase in snails.
. In 1875, Bassi observed massive deaths of red deer in the Royal Park (now La Mandria Regional 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. 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 confined to the region ventral to the intestinal branches, he established a new genus
Fascioloides and rename it to Fascioloides magna (Bassi 1875) Ward 1917. 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. 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.
and oxygen tension, are known to influence embryonation. During the embryonation of the egg, a larva called a miracidium develops from germinal cells. Fully developed miracidium releases the operculum
of the egg using several proteases. The embryonation period varies from 27 to 44 days in natural conditions. Ciliated miracidia hatch in water and actively seek suitable intermediate hosts that are freshwater snails from family Lymnaeidae
. After attaching to a suitable snail host, the miracidium penetrates into the snail body. After shedding its ciliated cell layer it is called a sporocyst
. The sporocysts are found in the foot, the snail body, digestive glands, reproductive organs, and in the pulmonary sac of the snail. The sporocysts contain germinal cells that give rise to 1-6 mother rediae (a trematode larval form with an oral sucker). Developed mother rediae are released from the sporocyst and migrate into digestive glands, renal organ, reproductive organs, and pulmonary sac of the snail body. Each mother redia can asexually produce up to 10 daughter rediae. However, only 3 to 6 daughter rediae complete their development and leave the mother rediae. In turn, each daughter redia may produce 1-6 Trematode lifecycle stages#Typical lifecyle stagescercariae in experimentally infected snails and 16-22 cercariae under natural conditions. Cercariae emerge from the rediae and mature usually in digestive glands of the snail. Mature cercarie spontaneously emerge from the snail host and swim actively in water for up to two hours before encysting on vegetation. After encystment the flukes are called metacercariae. Development within the snail takes 40 to 69 days depending upon the temperature and the species of snail. The definitive host ingests vegetation containing the metacercariae. In the stomach and the intestine, the metacercariae are stimulated to emerge from the cyst (excystation). Newly excysted juvenile flukes penetrate the wall of the intestine and migrate in the abdominal cavity. Juvenile flukes penetrate the Glisson’s capsule of the liver and continue migrating in the liver tissue. Rarely juvenile flukes penetrate other organs, such as lungs or kidneys. In these organs, however, flukes do not survive and not attain maturity. In the liver, flukes migrate within the parenchyma to search another fluke. If the fluke meet another one, they stop moving, and the fibrous capsule is formed around them. In the capsule, the parasite completes its development and starts egg-laying. Prepatent period 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.
exists and susceptible intermediate hosts are found. However, sporadic works reported unique appearance of the fluke in other continents. F. magna was found in imported animals in South Africa, Australia and Cuba. In all cases, infected animals (brahman heifer, ox, and elk
, respectively) were imported from USA or Canada.
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.
territory, Ullrich reported the first appearance of F. magna in fallow deer as late as 1930. 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. Erhardová-Kotrlá (1971) confirmed red deer, fallow deer and roe deer as main definitive hosts of F. magna in Europe. In 1960’s, F. magna was enzootic in former Czechoslovakia in following four major areas: (1) České Budějovice
and Třeboň
county, including Nové Hrady
Mountains; (2) the area along the Vltava
River on the Vltava-Týn hills near Hluboká
and Bechyně
; (3) Písek
and Milevsko county; (4) the Brdy
mountains and the Hřebeny mountains. In following years, F. magna was only reported from these areas. Recently, geographical distribution of F. magna in cervids was determined in the Czech Republic
. The giant liver fluke was confirmed in the same areas as reported in 1960’s. However, seven new endemic areas of F. magna were discovered suggesting that the parasite is spreading in the Czech Republic. Moreover, the appearance of F. magna in the Šumava Mountains has epizootiological importance due to possibility of spread of the parasite into the German territory (Bavaria
). During the last few years, a new European enzootic area has established in the Danube
watershed in Central Europe. In 1988, F. magna was isolated from a 3-year old red deer female found dead near the Gabčíkovo
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 %. Appearance of American liver fluke was reported in Croatia in January 2000. The prevalence of fascioloidosis among red deer in Hungary was 21,1-60,7 % 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 same period. 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.
Natural infections of F. magna occur primarily in cervids and bovids. Although many species are susceptible to infection, only a few cervid species contribute significantly to maintaining populations of the fluke. In North America, the common definitive hosts of the giant liver fluke are wapiti (Cervus elaphus canadensis), white-tailed deer
(Odocoileus virginianus) and caribou (Rangifer tarandus). 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. 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.
Pathology 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. Pigment within tissues is a result of migrating of juvenile flukes and it accumulates within hepatic cells without resorption.
F. magna infections in definitive hosts are usually subclinical. However, massive deaths caused by the fluke in red-, fallow- and roe deer were reported. 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. 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.
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.
s of the liver to the diaphragm
, black pigmentation, hematoma
s, necroses, 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. 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 (glutamate dehydrogenase
) was recorded from 14 week after infection in goats experimentally infected with F. magna.
. In North America, a total of 10 lymnaeid snails were reported as intermediate hosts of F. magna. 6 of 10 North American snail species were found naturally infected and the other four were infected only under experimental conditions. In addition, the Australian species Austropeplea (Lymnaea) tomentosa
was exposed to the North American isolate of F. magna and the parasite was able to complete its development. The most common North American natural snail hosts of the fluke are Fossaria (Galba) modicella, Stagnicola (Lymnaea) caperata and Fossaria (Galba) bulimoides techella. In Europe, an intermediate host had not been known until 1960’s. At the beginning, Ślusarski assumed that Lymnaea stagnalis
could act as an intermediate host of F. magna in Europe. His assumption, however, has been neither confirmed by positive findings in the field nor by experimental infection. In 1961, Dr. Erhardová described the life cycle of F. magna based on observations of experimentally and naturally infected snails. She confirmed that Galba truncatula
is an intermediate host of the giant liver fluke in Europe. In later works, the author studied another lymnaeid species in the former Czechoslovakia. However, G. truncatula was repeatedly confirmed as the only snail host of F. magna. In 1979, Chroustová reported successful experimental infection of Stagnicola (Lymnaea) palustris
with F. magna. She considered that this species might serve as an intermediate host of the fluke in the environment. Nevertheless, no naturally infected snails were found. Recent studies indicate that another lymnaeid snail, Radix peregra
, 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 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
, 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.
For control of fascioloidosis in wild ruminants, successful application of anthelminthics in feed is necessary. The drug has to have flavour and smell that do not prevent animals from eating medicated feed. In addition, there should adequate therapeutic scope, i.e. span between therapeutic and minimal toxic dose. Therefore, only some of anthelminthics that are efficient in domestic ruminants have been tested in wild ruminants infected with F. magna. Several drugs, namely oxyclozanide
, rafoxanide
, albendazole
, diamphenetide, closantel, clorsulon, and triclabendazole, have been used in control of F. magna infection in cervids. However, the results have differed between different authors. In the same way as for F. hepatica, triclabendazole seems to be the most effective against F. magna. Fascioloidosis of cervids was successfully controlled with triclabendazole in USA, and triclabendazole with levamizole in Hungary, Canada, Austria, and Croatia. 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. Unfortunately, rafoxanide in a 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.
Ruminant
A ruminant is a mammal of the order Artiodactyla that digests plant-based food by initially softening it within the animal's first compartment of the stomach, principally through bacterial actions, then regurgitating the semi-digested mass, now known as cud, and chewing it again...
s 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
Tegument
Tegument may refer to:* Integumentary system* Tegument * Viral tegument...
. As with other digenea
Digenea
Digenea is a subclass within the Platyhelminthes consisting of parasitic flatworms with a syncytial tegument and, usually, two suckers, one ventral and one oral. Adults are particularly common in the digestive tract, but occur throughout the organ systems of all classes of vertebrates...
n trematodes, the life cycle includes intramolluscan phase in snails.
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 ItalyItaly
Italy , officially the Italian Republic languages]] under the European Charter for Regional or Minority Languages. In each of these, Italy's official name is as follows:;;;;;;;;), is a unitary parliamentary republic in South-Central Europe. To the north it borders France, Switzerland, Austria and...
. In 1875, Bassi observed massive deaths of red deer in the Royal Park (now La Mandria Regional Park
La Mandria Regional Park
La Mandria Regional Park is a park in the communes of Venaria Reale and Druento, near Turin, northern Italy. Founded in 1978 by the regional council of Piedmont, it occupies a wide area between the Stura di Lanzo torrent and the north-western part of Turin and Venaria.It is the largest enclosed...
) 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. 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 confined to the region ventral to the intestinal branches, he established a new genus
Genus
In biology, a genus is a low-level taxonomic rank used in the biological classification of living and fossil organisms, which is an example of definition by genus and differentia...
Fascioloides and rename it to Fascioloides magna (Bassi 1875) Ward 1917. In 1895, Stiles suggested that the life cycle of the fluke is very similar to Fasciola hepatica
Fasciola hepatica
Fasciola hepatica, also known as the common liver fluke or sheep liver fluke, is a parasitic flatworm of the class Trematoda, phylum Platyhelminthes that infects the livers of various mammals, including humans. The disease caused by the fluke is called fascioliasis . F...
, i.e. it includes an aquatic snail as an intermediate host. He gave a comparative description of the egg and miracidium
Miracidium
Trematodes are small parasitic flatworms that use vertebrates as their definitive host, and molluscs as their intermediate host. In order to accomplish this, they have several varied lifecyle stages....
of the fluke. 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
The life cycle of F. magna is relatively complex and is similar to the development of the related fluke, F. hepatica. A detailed account of the F. magna life cycle was given by Swales (1935), Erhardová-Kotrlá (1971), and reviewed by Pybus (2001).Adult flukes occur in pairs or groups within a fibrous capsule in the liver parenchyma of the definitive host. Mature flukes release eggs which are collected in the cavity of the capsule. The capsule contains a great mass of eggs and has duct connections to bile ducts. The eggs are passed together with bile into the bile collecting system, enter the small intestine, and leave the definitive host along with the faeces. The eggs which are passed out in the faeces into the environment are undeveloped and undergo embryonation outside the host. Several physical-chemical factors, especially temperature, humidityHumidity
Humidity is a term for the amount of water vapor in the air, and can refer to any one of several measurements of humidity. Formally, humid air is not "moist air" but a mixture of water vapor and other constituents of air, and humidity is defined in terms of the water content of this mixture,...
and oxygen tension, are known to influence embryonation. During the embryonation of the egg, a larva called a miracidium develops from germinal cells. Fully developed miracidium releases the operculum
Operculum
Operculum may refer to:*Operculum , a stiff structure resembling a lid or a small door that opens and closes**Operculum , a lid on the shell of some gastropods**Operculum , a lid on the orifice of some bryozoans...
of the egg using several proteases. The embryonation period varies from 27 to 44 days in natural conditions. Ciliated miracidia hatch in water and actively seek suitable intermediate hosts that are freshwater snails from family Lymnaeidae
Lymnaeidae
Lymnaeidae is a taxonomic family of small to large air-breathing freshwater snails, aquatic pulmonate gastropod mollusks, that belong to the clade Hygrophila....
. After attaching to a suitable snail host, the miracidium penetrates into the snail body. After shedding its ciliated cell layer it is called a sporocyst
Sporocyst
Sporocyst is a common name of a lifecycle stage in two unrelated groups of species:*Apicomplexa parasites: see Apicomplexa lifecycle stages*Trematode flatworms: see Trematode lifecycle stages...
. The sporocysts are found in the foot, the snail body, digestive glands, reproductive organs, and in the pulmonary sac of the snail. The sporocysts contain germinal cells that give rise to 1-6 mother rediae (a trematode larval form with an oral sucker). Developed mother rediae are released from the sporocyst and migrate into digestive glands, renal organ, reproductive organs, and pulmonary sac of the snail body. Each mother redia can asexually produce up to 10 daughter rediae. However, only 3 to 6 daughter rediae complete their development and leave the mother rediae. In turn, each daughter redia may produce 1-6 Trematode lifecycle stages#Typical lifecyle stagescercariae in experimentally infected snails and 16-22 cercariae under natural conditions. Cercariae emerge from the rediae and mature usually in digestive glands of the snail. Mature cercarie spontaneously emerge from the snail host and swim actively in water for up to two hours before encysting on vegetation. After encystment the flukes are called metacercariae. Development within the snail takes 40 to 69 days depending upon the temperature and the species of snail. The definitive host ingests vegetation containing the metacercariae. In the stomach and the intestine, the metacercariae are stimulated to emerge from the cyst (excystation). Newly excysted juvenile flukes penetrate the wall of the intestine and migrate in the abdominal cavity. Juvenile flukes penetrate the Glisson’s capsule of the liver and continue migrating in the liver tissue. Rarely juvenile flukes penetrate other organs, such as lungs or kidneys. In these organs, however, flukes do not survive and not attain maturity. In the liver, flukes migrate within the parenchyma to search another fluke. If the fluke meet another one, they stop moving, and the fibrous capsule is formed around them. In the capsule, the parasite completes its development and starts egg-laying. Prepatent period 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
Currently, F. magna occurs only in North America and Europe where suitable habitatHabitat
* Habitat , a place where a species lives and grows*Human habitat, a place where humans live, work or play** Space habitat, a space station intended as a permanent settlement...
exists and susceptible intermediate hosts are found. However, sporadic works reported unique appearance of the fluke in other continents. F. magna was found in imported animals in South Africa, Australia and Cuba. In all cases, infected animals (brahman heifer, ox, and elk
Elk
The Elk is the large deer, also called Cervus canadensis or wapiti, of North America and eastern Asia.Elk may also refer to:Other antlered mammals:...
, respectively) were imported from USA or Canada.
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 LakesGreat Lakes
The Great Lakes are a collection of freshwater lakes located in northeastern North America, on the Canada – United States border. Consisting of Lakes Superior, Michigan, Huron, Erie, and Ontario, they form the largest group of freshwater lakes on Earth by total surface, coming in second by volume...
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 CzechCzechoslovakia
Czechoslovakia or Czecho-Slovakia was a sovereign state in Central Europe which existed from October 1918, when it declared its independence from the Austro-Hungarian Empire, until 1992...
territory, Ullrich reported the first appearance of F. magna in fallow deer as late as 1930. At the same time, Salomon (1932) diagnosed the fluke in one hunted red deer
Red Deer
The red deer is one of the largest deer species. Depending on taxonomy, the red deer inhabits most of Europe, the Caucasus Mountains region, Asia Minor, parts of western Asia, and central Asia. It also inhabits the Atlas Mountains region between Morocco and Tunisia in northwestern Africa, being...
near Görlitz
Görlitz
Görlitz is a town in Germany. It is the easternmost town in the country, located on the Lusatian Neisse River in the Bundesland of Saxony. It is opposite the Polish town of Zgorzelec, which was a part of Görlitz until 1945. Historically, Görlitz was in the region of Upper Lusatia...
(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
Fallow Deer
The Fallow Deer is a ruminant mammal belonging to the family Cervidae. This common species is native to western Eurasia, but has been introduced widely elsewhere. It often includes the rarer Persian Fallow Deer as a subspecies , while others treat it as an entirely different species The Fallow...
(Dama dama) and roe deer
Roe Deer
The European Roe Deer , also known as the Western Roe Deer, chevreuil or just Roe Deer, is a Eurasian species of deer. It is relatively small, reddish and grey-brown, and well-adapted to cold environments. Roe Deer are widespread in Western Europe, from the Mediterranean to Scandinavia, and from...
(Capreolus capreolus) were reported by several authors in former Czechoslovakia
Czechoslovakia
Czechoslovakia or Czecho-Slovakia was a sovereign state in Central Europe which existed from October 1918, when it declared its independence from the Austro-Hungarian Empire, until 1992...
. 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
Czechoslovakia
Czechoslovakia or Czecho-Slovakia was a sovereign state in Central Europe which existed from October 1918, when it declared its independence from the Austro-Hungarian Empire, until 1992...
. In the same region, moreover, the parasite was found in livers of slaughtered cattle. Erhardová-Kotrlá (1971) confirmed red deer, fallow deer and roe deer as main definitive hosts of F. magna in Europe. In 1960’s, F. magna was enzootic in former Czechoslovakia in following four major areas: (1) České Budějovice
Ceské Budejovice
České Budějovice is a city in the Czech Republic. It is the largest city in the South Bohemian Region and is the political and commercial capital of the region and centre of the Roman Catholic Diocese of České Budějovice and of the University of South Bohemia and the Academy of Sciences...
and Třeboň
Trebon
Třeboň is a historical town in South Bohemian Region of Czech Republic. The population stands at 8,862 .-History:Třeboň was established around the middle of the 12th century. In 1366 the House of Rožmberk become owner of the estate...
county, including Nové Hrady
Nové Hrady
Nové Hrady is name of several places in the Czech Republic:* Nové Hrady , a town in South Bohemian Region* Nové Hrady , a village in Pardubice Region...
Mountains; (2) the area along the Vltava
Vltava
The Vltava is the longest river in the Czech Republic, running north from its source in Šumava through Český Krumlov, České Budějovice, and Prague, merging with the Elbe at Mělník...
River on the Vltava-Týn hills near Hluboká
Hluboká
Hluboká is a name of several locations in the Czech Republic:* Hluboká nad Vltavou, town in South Bohemian Region * Hluboká , a village in Pardubice Region...
and Bechyně
Bechyne
Bechyně , is a town in the South Bohemian Region of the Czech Republic. It is located on the Lužnice River 20 km southwest of Tábor and has a population of 5,695 ....
; (3) Písek
Písek
Písek is a town in the South Bohemian Region of the Czech Republic. It has a population of 29 909 .-About:Písek is usually called "The Athens of the South", although Athens is much more southerly, because it has many high schools and schools of higher education, e.g. the Film School in Písek...
and Milevsko county; (4) the Brdy
Brdy
Brdy are hills in the Czech Republic, forming a long massif stretching for cca.60 km from Prague in the direction of southwest. The northern section of the Brdy is called "Hřebeny" and features one narrow ridge . The Brdy proper starts south of the Litavka river gorge and consists of several...
mountains and the Hřebeny mountains. In following years, F. magna was only reported from these areas. Recently, geographical distribution of F. magna in cervids was determined in the Czech Republic
Czech Republic
The Czech Republic is a landlocked country in Central Europe. The country is bordered by Poland to the northeast, Slovakia to the east, Austria to the south, and Germany to the west and northwest....
. The giant liver fluke was confirmed in the same areas as reported in 1960’s. However, seven new endemic areas of F. magna were discovered suggesting that the parasite is spreading in the Czech Republic. Moreover, the appearance of F. magna in the Šumava Mountains has epizootiological importance due to possibility of spread of the parasite into the German territory (Bavaria
Bavaria
Bavaria, formally the Free State of Bavaria is a state of Germany, located in the southeast of Germany. With an area of , it is the largest state by area, forming almost 20% of the total land area of Germany...
). During the last few years, a new European enzootic area has established in the Danube
Danube
The Danube is a river in the Central Europe and the Europe's second longest river after the Volga. It is classified as an international waterway....
watershed in Central Europe. In 1988, F. magna was isolated from a 3-year old red deer female found dead near the Gabčíkovo
Gabcíkovo
Gabčíkovo is a municipality in Slovakia. It has around 5,100 inhabitants of whom 90% are Hungarians.The Hungarian name of the village was first recorded in 1102 as Beys and preserves the name of its erstwhile pecheneg inhabitants, pecheneg being besenyő in Hungarian...
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
Szigetköz
The Szigetköz is an island plain in Western Hungary, part of the Little Hungarian Plain. The name literally means island alley, because the territory is located on an island. Its borders are the Danube and its branches; with a length of 52.5 km, with an average width of 6–8 km, and with...
) and the southern Danubian territory in the Gemenc
Gemenc
Gemenc is a unique forest that is found between Szekszárd and Baja, in Hungary. This is the only remaining tidal area of the Danube in Hungary. The wood's fauna include stags, boars, storks, grey herons, gyrfalcons, meadow eagles, and kites. Various amphibians and reptiles can also be found...
area. Since the autumn of 2000, F. magna has been found in Austrian territory, east of Vienna
Vienna
Vienna is the capital and largest city of the Republic of Austria and one of the nine states of Austria. Vienna is Austria's primary city, with a population of about 1.723 million , and is by far the largest city in Austria, as well as its cultural, economic, and political centre...
. 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 %. Appearance of American liver fluke was reported in Croatia in January 2000. The prevalence of fascioloidosis among red deer in Hungary was 21,1-60,7 % 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 same period. 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
White-tailed Deer
The white-tailed deer , also known as the Virginia deer or simply as the whitetail, is a medium-sized deer native to the United States , Canada, Mexico, Central America, and South America as far south as Peru...
(Odocoileus virginianus) and caribou (Rangifer tarandus). 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. 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
Pleistocene
The Pleistocene is the epoch from 2,588,000 to 11,700 years BP that spans the world's recent period of repeated glaciations. The name pleistocene is derived from the Greek and ....
epoch, and overlapped with white-tailed deer in some parts of North America. They might have encountered F. magna in these shared biotopes.
| Common name of species | Latin name of species | References |
|---|---|---|
| NORTH AMERICA | ||
| Bison Bison Members of the genus Bison are large, even-toed ungulates within the subfamily Bovinae. Two extant and four extinct species are recognized... |
Bison bison | |
| Black-tailed deer Black-tailed Deer Two forms of black-tailed deer or blacktail deer occupying coastal temperate rainforest on North America's Pacific coast are subspecies of the mule deer. They have sometimes been treated as a species, but virtually all recent authorities maintain they are subspecies... |
Odocoileus hemionus columbianus | |
| Caribou | Rangifer tarandus | |
| Cattalo | Bos taurus × Bison bison | |
| Cattle Cattle Cattle are the most common type of large domesticated ungulates. They are a prominent modern member of the subfamily Bovinae, are the most widespread species of the genus Bos, and are most commonly classified collectively as Bos primigenius... |
Bos taurus | |
| Collared peccary Collared Peccary The collared peccary is a species of mammal in the family Tayassuidae that is found in North, Central, and South America. They are commonly referred to as javelina, saíno or báquiro, although these terms are also used to describe other species in the family... |
Dicotyles tajacu | |
| Goat Goat The domestic goat is a subspecies of goat domesticated from the wild goat of southwest Asia and Eastern Europe. The goat is a member of the Bovidae family and is closely related to the sheep as both are in the goat-antelope subfamily Caprinae. There are over three hundred distinct breeds of... |
Capra hircus | |
| Horse Horse The horse is one of two extant subspecies of Equus ferus, or the wild horse. It is a single-hooved mammal belonging to the taxonomic family Equidae. The horse has evolved over the past 45 to 55 million years from a small multi-toed creature into the large, single-toed animal of today... |
Equus caballus | |
| Llama Llama The llama is a South American camelid, widely used as a meat and pack animal by Andean cultures since pre-Hispanic times.... |
Lama glama | |
| Moose Moose The moose or Eurasian elk is the largest extant species in the deer family. Moose are distinguished by the palmate antlers of the males; other members of the family have antlers with a dendritic configuration... |
Alces alces | |
| Mule deer Mule Deer The mule deer is a deer indigenous to western North America. The Mule Deer gets its name from its large mule-like ears. There are believed to be several subspecies, including the black-tailed deer... |
Odocoileus hemionus hemionus | |
| Pig Pig A pig is any of the animals in the genus Sus, within the Suidae family of even-toed ungulates. Pigs include the domestic pig, its ancestor the wild boar, and several other wild relatives... |
Sus scrofa var. domesticus | |
| Sheep | Ovis aries | |
| Wapiti Wapiti - Animals :* Elk , from the Cree language waapiti, a large deer species native to western North America and eastern Asia- Places :* Wapiti Pass, a mountain pass in British Columbia, Canada... |
Cervus elaphus canadensis | |
| White-tailed deer White-tailed Deer The white-tailed deer , also known as the Virginia deer or simply as the whitetail, is a medium-sized deer native to the United States , Canada, Mexico, Central America, and South America as far south as Peru... |
Odocoileus virginianus | |
| Wild boar | Sus scrofa | |
| Yak Yak The yak, Bos grunniens or Bos mutus, is a long-haired bovine found throughout the Himalayan region of south Central Asia, the Tibetan Plateau and as far north as Mongolia and Russia. In addition to a large domestic population, there is a small, vulnerable wild yak population... |
Bos grunniensis | |
| EUROPE | ||
| Blue bull | Bosephalus tragocamelus | |
| Cattle | Bos taurus | |
| Fallow deer Fallow Deer The Fallow Deer is a ruminant mammal belonging to the family Cervidae. This common species is native to western Eurasia, but has been introduced widely elsewhere. It often includes the rarer Persian Fallow Deer as a subspecies , while others treat it as an entirely different species The Fallow... |
Dama dama | |
| Goat | Capra hircus | |
| Horse | Equus caballus | |
| Red deer Red Deer The red deer is one of the largest deer species. Depending on taxonomy, the red deer inhabits most of Europe, the Caucasus Mountains region, Asia Minor, parts of western Asia, and central Asia. It also inhabits the Atlas Mountains region between Morocco and Tunisia in northwestern Africa, being... |
Cervus elaphus | |
| Roe deer Roe Deer The European Roe Deer , also known as the Western Roe Deer, chevreuil or just Roe Deer, is a Eurasian species of deer. It is relatively small, reddish and grey-brown, and well-adapted to cold environments. Roe Deer are widespread in Western Europe, from the Mediterranean to Scandinavia, and from... |
Capreolus capreolus | |
| Sambar | Cervus unicolor | |
| Sheep | Ovis aries | |
| Sika deer Sika Deer The Sika Deer, Cervus nippon, also known as the Spotted Deer or the Japanese Deer, is a species of deer native to much of East Asia and introduced to various other parts of the world... |
Sika nippon | |
| White-tailed deer | Odocoileus virginianus | |
| Wild boar | Sus scrofa | |
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 hosts
Pathology 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. 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. 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. 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.
Biochemical and haematological profiles are little investigated in definitive hosts. A decrease of haemoglobin, elevation of γ-globulins
Gamma globulin
Gamma globulins are a class of globulins, identified by their position after serum protein electrophoresis. The most significant gamma globulins are immunoglobulins , more commonly known as antibodies, although some Igs are not gamma globulins, and some gamma globulins are not Igs.-Use as medical...
, and increase of eosinophils in serum was observed in experimentally infected white-tailed deer.
(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. 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.(3) Aberrant hosts
Aberrant hosts of F. magna are sheep and goats. However, the course of infection is similar in guinea pigs, rabbits, bighorn sheep (Ovis canadensis) and chamois (Rupicapra rupicapra) that were infected experimentally. Infections in aberrant hosts are characterized by excessive wandering of juvenile flukes and death of the host. Aberrant hosts die usually within 6 months post-infection and the death is associated with acute peritonitis or extensive haemorrhage caused by migrating flukes. In aberrant hosts, flukes do not mature and migrate until the host dies. Occasionally, a few flukes mature and eggs can be found in the faeces. Hepatic lesions in aberrant hosts generally include firm adhesionAdhesion
Adhesion is any attraction process between dissimilar molecular species that can potentially bring them in close contact. By contrast, cohesion takes place between similar molecules....
s of the liver to the diaphragm
Thoracic diaphragm
In the anatomy of mammals, the thoracic diaphragm, or simply the diaphragm , is a sheet of internal skeletal muscle that extends across the bottom of the rib cage. The diaphragm separates the thoracic cavity from the abdominal cavity and performs an important function in respiration...
, black pigmentation, hematoma
Hematoma
A hematoma, or haematoma, is a localized collection of blood outside the blood vessels, usually in liquid form within the tissue. This distinguishes it from an ecchymosis, which is the spread of blood under the skin in a thin layer, commonly called a bruise...
s, necroses, 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. 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 (glutamate dehydrogenase
Glutamate dehydrogenase
Glutamate dehydrogenase is an enzyme, present in most microbes and the mitochondria of eukaryotes, as are some of the other enzymes required for urea synthesis, that converts glutamate to α-Ketoglutarate, and vice versa. In animals, the produced ammonia is, however, usually bled off to the urea...
) was recorded from 14 week after infection in goats experimentally infected with F. magna.
Intermediate hosts
Since the presence of an intermediate host is essential to the completion of the life cycle, snails occupy the important role in the epidemiology of F. magna. The intermediate hosts of the giant liver fluke belong to the family LymnaeidaeLymnaeidae
Lymnaeidae is a taxonomic family of small to large air-breathing freshwater snails, aquatic pulmonate gastropod mollusks, that belong to the clade Hygrophila....
. In North America, a total of 10 lymnaeid snails were reported as intermediate hosts of F. magna. 6 of 10 North American snail species were found naturally infected and the other four were infected only under experimental conditions. In addition, the Australian species Austropeplea (Lymnaea) tomentosa
Lymnaea tomentosa tomentosa
Lymnaea tomentosa is a species of freshwater snail, an aquatic gastropod mollusc in the family Lymnaeidae.This species lives in New Zealand. These snails are found in both the North and South Islands, on aquatic plants in swamps, ponds and quiet waters generally, but not in fast-running streams...
was exposed to the North American isolate of F. magna and the parasite was able to complete its development. The most common North American natural snail hosts of the fluke are Fossaria (Galba) modicella, Stagnicola (Lymnaea) caperata and Fossaria (Galba) bulimoides techella. In Europe, an intermediate host had not been known until 1960’s. At the beginning, Ślusarski assumed that Lymnaea stagnalis
Lymnaea stagnalis
Lymnaea stagnalis, better known as the great pond snail, is a species of large air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Lymnaeidae.-Distribution:The distribution of this species is Holarctic...
could act as an intermediate host of F. magna in Europe. His assumption, however, has been neither confirmed by positive findings in the field nor by experimental infection. In 1961, Dr. Erhardová described the life cycle of F. magna based on observations of experimentally and naturally infected snails. She confirmed that Galba truncatula
Galba truncatula
Galba truncatula is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Lymnaeidae, the pond snails.Until recently, this species was commonly known as Lymnaea truncatula.-Description:...
is an intermediate host of the giant liver fluke in Europe. In later works, the author studied another lymnaeid species in the former Czechoslovakia. However, G. truncatula was repeatedly confirmed as the only snail host of F. magna. In 1979, Chroustová reported successful experimental infection of Stagnicola (Lymnaea) palustris
Stagnicola palustris
Stagnicola palustris is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Lymnaeidae, the pond snails.-Description:...
with F. magna. She considered that this species might serve as an intermediate host of the fluke in the environment. Nevertheless, no naturally infected snails were found. Recent studies indicate that another lymnaeid snail, Radix peregra
Radix peregra
Radix peregra, previously known as Lymnaea peregra or Lymnaea pereger, is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod in the family Lymnaeidae, the pond snails....
, 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 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.
| Snail species | Naturally infected | Experimentally infected | Country | Reference |
|---|---|---|---|---|
| NORTH AMERICA | ||||
| Fossaria (Galba) bulimoides techella | yes | yes | United States | |
| Fossaria (Galba) modicella | yes | yes | United States, Canada | |
| Pseudosuccinea columella | yes | yes | United States | |
| Fossaria (Galba) parva | yes | yes | Canada | |
| Stagnicola palustris nuttalliana | yes | yes | Canada | |
| Lymnaea stagnalis | no | yes | United States | |
| Stagnicola palustris | no | yes | United States | |
| Stagnicola (Lymnaea) caperata | yes | yes | United States | |
| Lymnaea ferruginea | no | yes | United States | |
| Austropeplea (Lymnaea) tomentosa | no | yes | Australia* | |
| Lymnaea umbrosa | no | yes | United States | |
| EUROPE | ||||
| Galba truncatula | yes | yes | Czech Republic | |
| Stagnicola (Lymnaea) palustris | no | yes | Czech Republic | |
| Omphiscola glabra | no | yes | France** | |
| Radix peregra | yes | yes | Czech Republic | |
(*) 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. hepaticaFasciola hepatica
Fasciola hepatica, also known as the common liver fluke or sheep liver fluke, is a parasitic flatworm of the class Trematoda, phylum Platyhelminthes that infects the livers of various mammals, including humans. The disease caused by the fluke is called fascioliasis . F...
, 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
Oxyclozanide
Oxyclozanide is a salicylanilide anthelmintic. It is used in the treatment and control of Fascioliasis in ruminants mainly domestic animals like Cattle, Sheep and Goats. It mainly acts by uncoupling of Oxidative phosphorylation in flukes....
, rafoxanide
Rafoxanide
Rafoxanide is a salicylanilide used as an antiparasitic agent....
, albendazole
Albendazole
Albendazole, marketed as Albenza, Eskazole, Zentel and Andazol, is a member of the benzimidazole compounds used as a drug indicated for the treatment of a variety of worm infestations. Although this use is widespread in the United States, the U.S. Food and Drug Administration has not approved...
, diamphenetide, closantel, clorsulon, and triclabendazole, have been used in control of F. magna infection in cervids. However, the results have differed between different authors. In the same way as for F. hepatica, triclabendazole seems to be the most effective against F. magna. Fascioloidosis of cervids was successfully controlled with triclabendazole in USA, and triclabendazole with levamizole in Hungary, Canada, Austria, and Croatia. 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. Unfortunately, rafoxanide in a 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.