Abstract
Fascioloides magna parasitizes in a broad spectrum of final hosts, mainly free living and domestic ruminants. Final hosts of giant liver fluke are divided into three types (definitive, dead-end and aberrant) according to interrelationships between the parasite and the host, the ability of fluke to reach maturity and produce eggs, pathological changes within the host organism, and the potential to release eggs of F. magna into external environment. Definitive hosts contribute significantly to further spread of propagative stages of F. magna into the environment. Mature flukes localized in thin-walled pseudocysts or fibrous capsules in the liver parenchyma can produce eggs and release them into the host’s small intestine through the bile system. Definitive hosts tolerate fascioloidosis rather well, and infection is very often subclinical. In dead-end hosts, giant liver fluke can reach the liver but parasite matures very rarely. Only few eggs are produced and they are not released into the bile system. In aberrant hosts, giant liver fluke can not successfully complete the migration; parasite may occasionaly move up to the liver but formation of pseudocysts is not successful. Such hosts may often die due to tissue damage, which is associated with migration of immature flukes through peritoneal, thoracic or abdominal cavities.
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Keywords
- Giant liver fluke
- Final host
- Definitive host
- Dead-end host
- Aberrant host
- Host-parasite interrelationship
- Experimental infection
- Natural infection
3.1 Naturally Infected Final Hosts
Natural infections of F. magna occur primarily in representatives of the families Cervidae and Bovidae. According to Pybus (2001), there are three basic categories of final hosts: definitive, dead-end and aberrant. Different terminology has been applied throughout the literature in order to designate various types of final hosts of giant liver fluke. In particular “obligate”, “specific”, “typical” and “normal” have sometimes been used to determine definitive hosts, while terms “non-specific”, “unspecific”, “atypical” and “abnormal” are used to describe dead-end and aberrant hosts. Since the terminology described by Pybus (2001) takes into consideration host-parasite relationships, pathological changes within the final hosts, reproduction and further spread of the parasite, we accept and apply this terminology throughout the publication.
3.1.1 Definitive Hosts
Definitive hosts are characterized by maturation of F. magna flukes in thin-walled pseudocysts (fibrous capsules) in the liver parenchyma. Mature flukes produce eggs which are released into the host’s small intestine through the bile system. Thus, definitive hosts contribute significantly to further spread of propagative stages (eggs) of F. magna into the external environment. All definitive hosts are members of the family Cervidae, and except for the red deer and fallow deer, they are primarily “New World” cervids. From veterinary point of view, infection in this type of hosts is very often subclinical and fascioloidosis is rather well tolerated. The following cervids are considered to be definitive hosts of giant liver fluke:
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white-tailed deer Odocoileus virginianus
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wapiti Cervus elaphus canadensis
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Rocky Mountain elk Cervus elaphus nelsoni
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Roosevelt elk Cervus elaphus roosevelti
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caribou Rangifer tarandus
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black-tailed deer Odocoileus hemionus columbianus
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mule deer Odocoileus hemionus hemionus
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red deer Cervus elaphus elaphus
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fallow deer Dama dama
It is generally known that F. magna is of the North American origin where it co-evolved with ancestral Odocoileus sp. White-tailed deer has significantly contributed to maintenance and spread of fascioloidosis in North America, and till now it represents one of the most frequent definitive hosts of giant liver fluke. In general, white-tailed deer tolerate F. magna infection without significant clinical signs (Pybus 2001).
In North America, F. magna was found in naturally infected white-tailed deer coming from all enzootic regions except for NQL (see Table 3.1 and references therein). The most frequent occurrence of fascioloidosis was determined in SAS enzootic region throughout broad spectrum of southeastern US states, with the highest prevalence (64–84 %) in Texas (Foreyt and Todd 1972; Foreyt et al. 1977). White-tailed deer was also attractive “import article”, which was introduced to European parks, enclosures and reservations in the 19th and 20th centuries. In Europe, fascioloidosis was detected in white-tailed deer in the Czech Republic (Erhardová-Kotrlá 1971). Besides white-tailed deer, wapiti and caribou have significantly contributed to distribution of F. magna within and between enzootic regions in North America. Both cervids acquired giant liver fluke from white-tailed deer in overlapping regions with sympatric occurrence of different cervids (Kennedy et al. 1999; Bazsalovicsová et al. 2015).
Taxonomy of the genus Cervus is not univocal and different authors accept different scientific names and terminology. In general, Cervus elaphus is supposed to include many subspecies, including the most frequent “Old World” cervid, red deer Cervus elaphus elaphus, and common North American species, wapiti Cervus elaphus canadensis. In North America, there are numerous subspecies of C. elaphus, including Rocky Mountain elk Cervus elaphus nelsoni and Roosevelt elk Cervus elaphus roosevelti (Bryant and Maser 1982). Some authors consider red deer and wapiti to be separate species, Cervus elaphus and Cervus canadensis, respectively (e.g. Groves 2006). In order to avoid any misunderstanding in terminology of deer, we use the original scientific names of all cervids as provided in the reference literature.
Wapiti (Fig. 3.1), one of the largest species of family Cervidae, was found to be infected with F. magna mainly in foothills and mountain endemic areas of the Rocky Mountain trench (RMT) enzootic region, in Canadian provinces Montana and Alberta (Banff National Park) (see Table 3.1 and references therein). In NPC enzootic region, fascioloidosis was detected in wapiti from British Columbia and Oregon (Table 3.1). The prevalence detected in RMT and NPC enzootic regions reached up to 80–100 % (Whiting and Tessaro 1994; Hood et al. 1997; Pybus et al. 2015). Sporadic occurrence of F. magna in wapiti was detected in Cuba, where it was imported from North America (Lorenzo et al. 1989).
Others “New World” cervids susceptible to F. magna infection are Rocky Mountain elk, Roosevelt elk, caribou, black-tailed deer and mule deer (see Table 3.1 and references therein). While Rocky Mountain elk and mule deer were found mainly in RMT region, Roosevelt elk and black-tailed deer infected with F. magna were detected in coastal states and provinces of NPC region.
Along with wapiti and white-tailed deer, third dominant definitive host of F. magna is reindeer or caribou, terrestrial herbivore of many northern ecosystems (Pollock et al. 2009). The George River herd is the largest caribou population in eastern Canada (mainly Labrador), and represents the only endemic caribou herd in North America infected with F. magna (Wobeser et al. 1985; Pollock et al. 2009). Caribou infected with F. magna was found only in NQL region, where the dynamics of fascioloidosis is similar to dynamics in populations of wapiti and white-tailed deer (Lankester and Luttich 1988). Excessive number of flukes may lead to mortality even in this type of definitive host (Pybus 2001).
In Europe, the most frequent and dominat definitive host of F. magna is red deer. Similarly to white-tailed deer and wapiti in North America, red deer plays an important role in maintaining and spread of fascioloidosis in Europe. Red deer infected with F. magna was found in all European natural foci (IT, CZ-PL and DFF) in all countries (see Table 3.1 and references therein). A very high prevalence, reaching up to 100 % was determined in Italy (Balbo et al. 1987), Czech Republic (Erhardová-Kotrlá 1971) and Danube floodplain forests (Rajský et al. 2002; Ursprung and Prosl 2011). Fallow deer is second ruminant species known as definitive host of F. magna in Europe; fascioloidosis in fallow deer was detected in all natural foci (Table 3.1); the highest prevalence was reported from Czech Republic reaching up to 95 % (Novobilský et al. 2007).
The prevalence of fascioloidosis in definitive hosts is age-dependent. While young hosts are rarely infected, infection is increasing in older age classes (Flook and Stenton 1969; Foreyt et al. 1977; Lankester and Luttich 1988; Mulvey and Aho 1993). Prevalence of adult flukes is comparable in both sexes in wapiti (Pybus 2001), white-tailed deer (Foreyt et al. 1977), and caribou (Lankester and Luttich 1988).
3.1.2 Dead-End Hosts
In dead-end hosts, giant liver fluke can reach the liver but the parasite matures very rarely and few produced eggs are usually not released into the bile system, intestine and further to the external environment. Contrary to definitive hosts, dead-end hosts do not contribute to maintenance of the infection and spread of propagative stages of F. magna. Fascioloidosis in this type of hosts may have a lethal effect. Dead-end hosts represent taxonomically diverse category, in particular:
Family Cervidae
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moose Alces alces
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sika deer Cervus nippon
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sambar deer Cervus unicolor
Family Bovidae
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cattle Bos taurus
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bison Bison bison
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yak Bos grunniens
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blue bull Boselaphus tragocamelus
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muscox Ovibus moschatus
Family Equidae
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horse Equus sp.
Family Suidae
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wild boar Sus scrofa
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domestic swine Sus scrofa f. domestica
Family Tayassuidae
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collared peccary Pecari tajacu
Family Camelidae
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llama Lama glama
Moose represents one of the most frequent dead-end hosts of the family Cervidae. Fascioloidosis in this type of host was detected in NPC, RMT and GLR enzootic regions (see Table 3.2 and references therein), with the highest prevalence determined in British Columbia (63 %; Pybus et al. 2015) and Minnesota (89 %; Murray et al. 2006). In Europe, sika deer was found to be infected with F. magna in Czech Republic and Germany (Erhardová-Kotrlá 1971; Rehbein et al. 2012; Plötz et al. 2015).
Regarding domestic ruminants, a cattle represents the most common dead-end host of F. magna in North America and Europe. Giant liver fluke mature in the liver, eggs are produced, but stay trapped within hepatic parenchyma and do not enter bile ducts (Foreyt and Todd 1976). Fascioloidosis in cattle causes chronic liver lesions (Price 1953), but the infection is usually not lethal (Lankester 1974; Foreyt and Todd 1976; Foreyt and Parish 1990). Cattle infected with F. magna was reported in all North American enzootic regions except for NQL, and in two European countries, Italy and Czech Republic (see Table 3.2 and references therein). A sporadic occurrence was detected in South Africa (Boomker and Dale-Kuys 1977) and Australia (Arundel and Hamir 1982). Within the family Bovidae, F. magna infections were also found in bison and yak from Alberta (RMT) (Cameron 1923 c.i. Pybus 2001; Swales 1935), in muskox from Quebec (NQL) (Bazsalovicsová et al. 2015), and in blue bull from Italy (Bassi 1875 c.i. Pybus 2001).
A rather rare dead-end host of F. magna is wild boar; infections were documented in Italy (Balbo et al. 1987, 1989) and Texas, with high prevalence ranging from 51.7 % (Foreyt and Todd 1972) to 69 % (Foreyt et al. 1975). Dangerous for pigs may be feeding on pastures contaminated by eggs of infected white-tailed deer, or other definitive hosts (Schwartz et al. 1993). Wild boar does not shed F. magna eggs to environment and, therefore, does not contribute to further spread of fascioloidosis (Foreyt et al. 1975). Rare F. magna infections were detected in horse (McClanahan et al. 2005) and llama (Conboy et al. 1988) from Minnesota (GLR), in horse from Italy (Balbo et al. 1987), and in collared peccary from Texas (SAS) (Samuel and Low 1970).
3.1.3 Aberrant Hosts
In aberrant hosts, giant liver fluke can not successfully complete migration within the ruminant host; parasite may move up to the liver but formation of pseudocysts is not successful. These hosts may often die due to tissue damage, which is associated with migration of immature flukes through peritoneal, thoracic or abdominal cavities. According to Pybus (2001), aberrant hosts are mainly domestic, but also free living ruminants:
Family Bovidae
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domestic sheep Ovis aries
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domestic goat Capra hircus
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chamois Rupicapra rupicapra
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bighorn sheep Ovis canadensis
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mouflon Ovis orientalis
Family Cervidae
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roe deer Capreolus capreolus
In aberrant hosts, such as sheep and goat, unrestricted migration of fluke through the liver, lungs and peritoneal cavities is typical. It results to massive tissue damage, usually with fatal effects caused even by relatively low intensity of infection (Conboy and Stromberg 1991). Fascioloidosis in domestic sheep and goat was documented both in North America and Europe (see Table 3.3 and references therein). Roe deer, the only cervid species recognized as an aberrant host, was found to be infected with F. magna only in Europe, in particular CZ-PL and DFF (see Table 3.3 and references therein). The highest prevalence of fascioloidosis in roe deer was detected in Czech Republic (70–80 %; Erhardová-Kotrlá 1971) and Slovakia (60 %; Rajský et al. 2002).
3.2 Experimentally Infected Final Hosts
The experimental infections of different types of final hosts with F. magna were aimed to determine the clinical signs, pathological changes and immunological responses of final hosts under controlled experimental conditions. The major contribution in this field has to be addressed to William J. Foreyt from Washington State University in Pullman, Washington, USA.
Experimental infections were studied in all types of final hosts of F. magna, in particular in definitive hosts (white-tailed deer, wapiti, mule deer and fallow deer), dead-end hosts (moose, cattle, bison and llama), and aberrant hosts (sheep, bighorn sheep, chamois and guinea pig) (see Table 3.4 and references therein). The animals were infected with dose of 8–2,000 infective stages (metacercariae) per animal, most frequently in the number of 200–500. The main monitored parameters were localization of parasite, ability of parasite to reach the maturity, detection of F. magna eggs in host’s faeces and determination of overall clinical signs of infected hosts (including lethal effect). In some cases, haematological and blood chemistry values were determined, as well. The results on experimental infections can be correlated with data known from natural infections; the classification of final hosts can thus be determined in more details.
The majority of experiments were performed in white-tailed deer, the primary definitive host of F. magna. The fluke was localized in liver, with occasional occurence in lungs, abdominal and thoracic cavities (see Table 3.4 and references therein). The important finding was detection of F. magna eggs in feaces of white-tailed deer, what clearly demonstrates its ability to provide suitable conditions for parasite’s maturity, production of eggs, their release into the external environment and consequent spread of the infection.
White-tailed deers were without significant clinical signs and were confirmed to be definitive host for F. magna. Presidente et al. (1980) studied haematological values of white-tails infected experimentally with F. magna. A reduction of erythrocytes and an elevation of reticulocytes, macrocytic cells and eosinophils were detected in the mentioned study. On the other hand, serum proteins, albumins and globulins remained under the physiological values. Another study confirmed decrease of haemoglobin, increase of total serum proteins, β- and γ-globulin fractions (Foreyt and Todd 1979).
In wapiti, localization of parasite in liver and peritoneal cavity was detected (Foreyt 1996a). Using 250 metacercariae as an infectious dose, no significant clinical signs were recorded and eggs of F. magna were detected in faeces. However, a massive infection of wapiti (2,000 metacercariae as infectious dose) was proved to have a lethal effect (Foreyt 1996a). Lethal effect was determined also after experimental infection of mule deer (Foreyt 1992, 1996b), in which giant liver fluke was primarily localized in liver, but even in lungs, pleural and peritoneal cavities; eggs of F. magna were found in faecal samples of mule deer. At the end of experimental infection of fallow deer, poor appetite, apathy and paroxysm appeared, and increased γ-globulins and hypoalbuminaemia were detected. Infection had a lethal effect; flukes were found in the liver, peritoneal and abdominal cavities (Erhardová-Kotrlá and Blažek 1970).
In dead-end hosts (moose, cattle and llama) experimentally infected with F. magna, dominant localization of the parasite was liver (Erhardová-Kotrlá and Blažek 1970; Foreyt and Todd 1976; Foreyt and Parish 1990; Conboy and Stromberg 1991; Lankester and Foreyt 2011), although presence of F. magna was confirmed also in lungs and abdominal cavity of cattle (Foreyt and Todd 1976; Conboy and Stromberg 1991). The important finding in all studied dead-end hosts was that eggs were not released into faeces, but were found to be retained in liver (Foreyt and Todd 1976). These results correspond to definition of dead-end hosts, which do not contribute to spread of propagative stages of the parasite into external environment. No clinical signs were detected in moose (Lankester and Foreyt 2011) and cattle (Conboy and Stromberg 1991). Fascioloidosis did not develop in experimentally infected bison (Foreyt and Drew 2010).
Experimental infections in aberrant hosts (sheep and bighorn sheep) revealed presence of parasite in liver, but also in lungs, peritoneal and abdominal cavities; fascioloidosis in this type of hosts had a lethal effect (Erhardová-Kotrlá and Blažek 1970; Foreyt and Todd 1976; Foreyt 1996a). In chamois experimentally infected with F. magna, no clinical signs were observed during the whole period of experiment. However, on the 138th day after infestation the chamois suddenly died and flukes were found in liver and lungs (Erhardová-Kotrlá and Blažek 1970). As generally known for aberrant hosts, eggs were not detected in faeces.
Already small dose of infective metacercariae (10 and 20) resulted in lethal effect of fascioloidosis in guinea pig, in which natural infections were not determined. As expected, the infection was quite extensive; except for liver, flukes were determined in lungs, peritoneal, abdominal and thoracic cavities, and even in skeletal muscles and subcutaneous tissues (Foreyt and Todd 1979; Conboy and Stromberg 1991). The response observed in guinea pigs was similar to that reported in sheep, suggesting the suitability of the guinea pig as a model for F. magna infection in sheep (Conboy and Stromberg 1991).
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Králová-Hromadová, I., Juhásová, L., Bazsalovicsová, E. (2016). Final Hosts of Fascioloides magna . In: The Giant Liver Fluke, Fascioloides magna: Past, Present and Future Research. SpringerBriefs in Animal Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-29508-4_3
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