FASCIOLOIDES MACNA (CIANT AMERICAN LIVER FLUKE)

CAUSATIVE AGENT (CLASSIFICATION, morphology) Fascioloides magna (Order Echi- nostomatiformes, Family Fasciolidae) (App. 1: Table 3) is the only species of this genus. Also called the giant liver fluke, this trematode has been described as ranging up to 10 cm (Davis and Libke 1971) in length.

host range and distribution Fascioloi- des magna lives in the liver parenchyma of cer- vids in North America; deer (Odocoileus spp.) are considered its natural hosts (Davis and Libke 1971). In addition to white-tailed deer (Odocoi- leus virginianus), it also has been reported in natural infections from other cervids including mule and black-tailed deer (Odocoileus hemio- nus), elk (Cervus elaphus), moose (Alces alces), and caribou (Rangifer tarandus), as well as bison (Bison bison), cattle, sheep, goats, pigs, horses, yaks (Bos grunniens; now Poephagus grunniens), llamas (Lama glama), and collared peccaries (Pecari tajacu) in North America (Davis and Libke 1971, Pybus 2001). Although considered a North American species, it first was identified from an American elk in an Italian zoo (Bassi 1875). Since then it has become firmly estab­lished among many native ungulates in Euro­pean game reserves, including red deer (Cervus elaphus), roe deer (Capreolus capreolus), fallow deer (Dama dama), and chamois (Rupicapra rupicapra) (Pybus 2001); it continues to spread geographically (Janicki et al. 2005).

Three types of final hosts are defined (Pybus 2001). Definitive hosts are those in which F. magna mature in thin-walled fibrous cap­sules within the host liver, eggs are voided into the small intestine via the bile system, and patent infections are established; these are pri­marily North American cervids. Aberrant hosts are those in which the parasite cannot success­fully complete migration and which often die from tissue damage associated with migrat­ing immature flukes; ovine species occur in this group.

life cycles and variations In normal definitive hosts, adult F. magna commonly live in pairs in liver parenchyma. Adult F. magna produce up to 4,000 eggs per day, which leave the liver through the bile system, enter the small intestine, and are shed with feces (Swales 1935). Miracidia hatch through the operculum in aer­ated water (Swales 1935) and have 1 to 2 days to find a suitable snail intermediate host before dying; they have a strong positive phototaxis and strong chemotaxis for mucus produced by suitable intermediate hosts (Campbell 1961, Erhardova-Kotrla 1971). After penetrating the snail pulmonary sac, each miracidium pro­duces a sporocyst which, in turn, produces 14 rediae (Swales 1935, Erhardova-Kotrla 1971). After migrating to the snail liver, these rediae each produce 9 daughter rediae; in turn, each redia produces 9 or 10 cercariae (Swales 1935, Erhardova-Kotrla 1971); thus one miracidium can produce 1,000 cercariae in a snail. After escaping from their aquatic snail hosts, cercar- iae encyst on vegetation to form metacercariae.

Once ingested and activated in the gut of the definitive host, the metacercariae excyst, penetrate the intestinal wall, and migrate to the liver, where they develop into adult trema­todes (Pybus 2001). Within the liver, flukes pair up before becoming encapsulated and matur­ing (Foreyt et al. 1977). The prepatent period of the flukes in deer is about 7 months (Foreyt 1981), and adult flukes may live in the defini­tive host at least 5 years (Erhardova-Kotrla 1971); however, ova of older flukes tend to lose their viability (Erhardova-Kotrla 1968).

reservoirs and transmission The res­ervoirs for this parasite are white-tailed deer and other cervid species (Pybus 2001). Almost all known intermediate hosts of F.

Environmental factors can affect comple­tion of the life cycle (Pybus 2001). For example, prolonged snow cover in spring may delay emergence of snails and slow the development of miracidia within eggs (Pybus 2001). Freez­ing temperatures can kill developing eggs (Swales 1935), although these impacts can be mitigated by protective snow cover (Erhardova- Kotrla 1971). Land use patterns that improve habitats for snails or ungulates may increase the overlap of suitable intermediate and defini­tive hosts (Erhardova-Kotrla 1971). Snails in shallow warm water are more readily infected by miracidia than snails in cold-water streams (Erhardova-Kotrla 1971).

clinical effects and identification There is little evidence of pathology in most normal definitive hosts such as white-tailed deer. The cysts tend to be thin-walled and cause minimal impacts on the liver or bile functions (Davis and Libke 1971). Some tran­sitory anemia and eosinophilia have been attributed to F. magna during early prepatent periods (Foreyt 1981).

In dead-end hosts such as moose, cattle, and bison, the parasite becomes encapsulated in the liver before it reaches maturity. This reduces its pathogenicity; further, fibrous cysts prevent the eggs from reaching the bile ducts and completing the life cycle (Davis and Libke 1971, Pybus 2001).

In aberrant hosts such as wild and domes­tic sheep, roe deer, and chamois, infections are characterized by wandering of immature flukes, a lack of encapsulation, and often death of the host (Pybus 2001). Most damage occurs in the liver, with acute hemorrhagic tracks and associated trauma and necrosis throughout (Erhardova-Kotrla and Blazek 1970, Foreyt and Todd 1976a, Pybus 2001).

Fascioloides magna is the only fluke living in liver parenchyma of North American wild ungulates; other liver flukes such as Fasciola hepatica or Dicrocoelium dendriticum live in the bile ducts. Adult F. magna can be relatively easy to distinguish from Fasciola hepatica; however, larval stages and eggs of both flukes are morpho­logically almost indistinguishable. Some PCR- based techniques can distinguish larval and egg stages of these parasites (Kralova-Hromadova et al. 2008). Use of DNA sequences can dis­tinguish adult F. magna from F. hepatica when individual parasites cannot be distinguished due to improper preparation (Bildfell et al. 2007). Hemosiderin, a black iron pigment in livers, is associated with F. magna infections and is con­sidered to be a pathognomonic feature of this liver fluke infection (Foreyt and Todd 1976a).

population effects Generally, liver flukes do not cause significant population impacts among wildlife in North America (Pybus 2001). However, F. magna infections were cited as the single greatest source of mortality in a declin­ing Minnesota moose population, causing considerable pathology in the infected animals (Murray et al. 2006). Prevalence of F. magna commonly increases with age of the definitive hosts (Pybus 2001)

In addition to its role as a mortality fac­tor, F. magna also may serve as a welfare fac­tor. For example, a higher frequency of flukes was observed in winter kills than in hunter kills among white-tailed deer in New York (Cheatum 1951). Also, the presence of F. magna was associated with reduced body size and low­ered number of antler points in white-tailed deer; thus the parasite may reduce male fitness and competitive ability for females (Mulvey and Aho 1993). Fascioloides magna infection also may predispose infected moose to increased predation and reduced productivity (Lankester 1974^, B^erg 1975).

special problems Domestic species cannot maintain populations of F. magna in the absence of infected wild definitive hosts; however, pasturing on areas containing infected wildlife leads to infections of domestic livestock in North America and Europe (Pybus 2001). Condemna­tion of livers, loss of weight, loss of milk produc­tion, and unthrifty offspring may accompany F. magna infections in cattle (Schillhorn van Veen 1987). Also, infections among local wild defini­tive hosts may preclude husbandry of domestic sheep (Stromberg et al. 1983) or goats (Foreyt and Leathers 1980) in some regions.

Human-caused translocation of liver flukes to new areas has been of ongoing concern (Pybus 2001). For example, F. magna was introduced with white-tailed deer and American elk into Europe, where it has become firmly established and caused losses among red deer, roe deer, and fallow deer of Europe (Erhardova-Kotrla and Kotrly 1968, Kotrla and Kotrly 1977). The para­site continues to spread (Majoros and Sztojkov 1994, Janicki et al. 2005) and cause manage­ment problems, especially among cervids of European reserves and parks (Bojovic and Halls 1984, Pybus 2001). The parasite was imported with an elk into Cuba (Lorenzo et al. 1989).

Translocation of game-ranched cervids also is considered a risk with F. magna in North America (Corn and Nettles 2001). The occur­rence of the parasite in the southeastern United States may stem from translocation of infected deer (Holland 1959, Pursglove et al. 1977). Translocation of infected elk has led to cases of F. magna in bison ofWood Buffalo National Park (Pybus 2001), in elk on a game farm in Alberta, Canada (Pybus 1990), and perhaps in central Saskatchewan (Wobeser et al. 1985, Pybus 2001). The parasite also has spread to captive elk in Montana (Hood et al. 1997).

A cultural anecdote associated with this parasite is that residents in some regions of the United States refer to F. magna as “swamp butterflies” and deep-fry them for consump­tion (Bush et al.

control and host immunity There is lit­tle evidence for an effective immune response against F. magna in most hosts (Pybus 2001).

Because the flukes are encapsulated in the liver parenchyma rather than living in bile ducts, many anthelminthics administered to ani­mals cannot effectively penetrate the capsules to affect the flukes (Foreyt and Todd 1976b). However, triclabendazole can control F. magna in white-tailed deer (Qureshi et al. 1989, 1994) and is reported to reduce both the prevalence and numbers of eggs in feces of free-ranging red deer in Croatia (Slavica et al. 2006). Alben­dazole also has been used to control F. magna in white-tailed deer (Qureshi et al. 1990).

In the United States, a complicating factor is that most drugs of potential value for controlling parasites are not licensed for use in treating free- ranging wildlife. However, the Animal Medicinal Drug Use Clarification Act of 1994 does allow the use of otherwise licensed drugs for judicious use off-label for non-food wildlife (Waldrup 1998).

Because domestic stock require exposure to infected wildlife to acquire F. magna infections, a number of management recommendations have been proposed to reduce the risk of trans­mission to susceptible domestic hosts. These include treating captive cervids in enzootic areas regularly with anthelminthics, as well as when anticipating translocation to other sites; further, pasture management to exclude access by normal definitive hosts, limiting access by domestic species to contaminated wetlands, and regular treatment with fasciolicides are recommended (Pybus 2001).

Another liver fluke, Fasciola hepatica, in the same Family (Fasciolidae) as F. magna, is an important parasite of domestic animals (Spithill and Dalton 1998). It also can affect wildlife, but infected wild species do not appear capable of maintaining populations of F. hepatica in a region in the absence of domestic stock (Pybus 2001). The life cycles of the two flukes are very similar, but differ in the species of snails serving as intermediate hosts (Pybus 2001).