Sika Deer (Cervus nippon) are not “Dead-End Hosts” of the Giant Liver Fluke, Fascioloides magna (Bassi, 1875) Ward, 1917

Although of North American origin, with white-tailed deer (Odocoileus virginianus) and wapiti (Cervus canadensis) as primary hosts (Pybus 2001), Fascioloides magna is well established in central Europe. Both white-tailed deer and wapiti were imported into several locations in central Europe in the 19th century, and F. magna was introduced with them. Wapiti either were exterminated or ‘disappeared’ after hybridization with red deer (Cervus elaphus); white-tailed deer still occur in Czech Republic as both free-living and in a few game preserves (Niethammer 1963; Anděra 2006; Anděra and Červený 2009; Apollonio et al. 2010).

Over the past 25 y, F. magna has expanded its range from the historical endemic areas in former Czechoslovakia, downstream following the river Danube, and more recently westwards. Additionally, recent work in Poland confirmed the endemicity of F. magna in Lower Silesia, where the parasite was recorded for the first time in 1930 and demonstrated a northward range expansion (Králová-Hromadová et al. 2016; Rehbein et al. 2021). In Europe, red deer constitute the most important definitive hosts of F. magna, followed by fallow deer (Dama dama). Additional naturally infected final hosts of F. magna among wild ungulates in central Europe include native roe deer (Capreolus capreolus) and wild boar (Sus scrofa) and the naturalized sika deer (Cervus nippon), mouflon (Ovis musimon), and white-tailed deer (Rehbein et al. 2021).

Based on their contribution to the propagation and transmission of F. magna as a result of the host-parasite compatibility and related pathology, Pybus (2001) grouped the final hosts of F. magna into three general types: 1) ‘Definitive hosts’ (suitable definitive hosts), which tolerate the infection relatively well and allow the flukes to reach maturity enclosed in fibrous capsules that communicate with bile ducts, allowing excretion of the eggs produced by the flukes with the feces; 2) ‘Dead-end hosts’ (unsuitable definitive hosts), which mostly tolerate the infection relatively well, but flukes mature only rarely and are enclosed in thick-walled capsules that usually have no connection to the bile ducts so that fecal shedding of eggs is rare; and 3) ‘Aberrant hosts’ (atypical hosts), which exhibit severe pathology caused by excessive migration of immature flukes in the liver and other internal organs, often resulting in death due to massive hemorrhage. Encapsulation and maturation of flukes, and excretion of fluke eggs, is extremely rare in these hosts.

The classification by Pybus (2001) of red deer, fallow deer, and white-tailed deer as definitive hosts, of pigs (wild boar as wild form) as dead-end hosts, and of roe deer as aberrant hosts of F. magna is supported (Kotrlý and Kotrlá 1972; Králová-Hromadová et al. 2016; Konjević et al. 2017; Rehbein et al. 2021). Given that sheep and mouflon successfully interbreed (Piegert and Uloth 2005), and sheep are aberrant hosts for F. magna (Foreyt and Todd 1976; Foreyt and Hunter 1980; Foreyt 1990), the classification of the mouflon by Pybus (2001) as an aberrant host for F. magna may be reasonable, although only three records of F. magna in mouflon have been found (Rehbein et al. 2021). However, the classification of sika deer as natural dead-end hosts has simply been quoted in the literature thereafter (Špakulová et al. 2003; Malcicka 2015; Králová-Hromadová et al. 2016) and lacks robust substantiation.

During investigations of F. magna in sympatric wild ungulates in one area in the Upper Palatinate Forest in northeastern Bavaria, Germany, close to the border to Czech Republic, livers and rectal feces of 24 and 23 sika deer, respectively, were examined for F. magna flukes and fecal Fascioloides eggs (Rehbein et al. 2021).

Fascioloides magna were recovered from the livers of nine of 24 sika deer with infection intensity ranging from 1–7 flukes, ranging in size from about 2–6 cm. Eggs of Fascioloides were detected in the feces of six of the 23 animals (range, 4–44 eggs per gram; median, 16.5 eggs per gram). Analysis of the association of log-transformed F. magna fluke and Fascioloides egg counts demonstrated a linear correlation (Spearman's r_s=0.7785; P<0.0001). Mature flukes in seven of the F. magna-positive deer were isolated from capsules containing two flukes each.

Related to the low fluke burden, overall gross lesions of the livers of the sika deer with F. magna recovered were mild to moderate and mainly characterized by organ enlargement (two livers), fibrinous perihepatitis (two livers; Fig. 1), and streaks of black pigment marking the tracks of fluke migration (four livers; Fig. 2). Cutting of the livers revealed relatively thick-walled, fibrous capsules embedded in the liver parenchyma and not visible from the outer surface (Fig. 3). Livers from three sika had only a few dark pigmented streak lesions, which are considered pathognomonic for F. magna infection (Pybus 2001), but no flukes were detected.

Erhardová-Kotrlá (1971) first reported F. magna in one sika deer from the Lány Game Park in the former Czechoslovakia. Subsequently published cumulative necropsy findings from sika deer in the former Czechoslovakia documented two F. magna cases from Lány Game Park among 136 deer (Kotrlý and Kotrlá 1974), later becoming 2/173 deer (Kotrlý and Kotrlá 1975). Finally, summarizing the results of their examinations of 187 sika deer from the former Czechoslovakia over 25 y, Kotrlý and Kotrlá (1980) reported a total of six F. magna cases, with no information on geographic origin of the animals. No information on liver pathology, fluke counts, or feces examination was provided. Sika deer breeding in the Lány Game Park commenced in the early 1920s with Japanese morphotype animals of unknown origin, supplemented later by two sika deer obtained from the Holešov estate in Moravia (Ambrož 2013). Possibly, F. magna was introduced with the sika deer from Holešov, as both white-tailed deer and wapiti were bred there (Hošek 1983), or with wapiti hybrids, which were kept in the Lány Game Park in the 1960s (Ambrož 2013).

The occurrence of F. magna in sika deer and fallow deer in the Upper Palatinate Forest in Germany is the consequence of natural immigration of cervids from Bohemia (Rehbein et al. 2021), where fascioloidosis is common in both red deer and fallow deer and the parasite is expanding its range (Novobilský et al. 2007; Kasny et al. 2012; no examination of sika deer was reported in these studies). Introduction of sika deer to, and transfer between, estates in Bohemia commenced in the late 19th century (Niethammer 1963; Anděra 2006; Anděra and Červený 2009). Before World War II, sika deer were confined exclusively to game parks in the former Czechoslovakia. After the war, sika deer escaped, or were intentionally released, from these game parks and slowly established in the wild. Since then, sika deer have become abundant and their range overlaps that of both red deer and fallow deer (Anděra and Červený 2009; Dvořák and Palyzová 2016). During 1956 to 1973, examination of sika deer from the Maňetín area (Western Bohemia), which constitute the founders of the free-ranging sika deer population in Bohemia (Wolf and Vavruňek 1975/76; Barančeková et al. 2012; Dvořák and Palyzová 2016), did not reveal F. magna (Kotrlý and Kotrlá 1974, 1975). Thus, the free-ranging sika deer in the Czech Republic, which were recently demonstrated to have Japanese roots only (Barančeková et al. 2012), probably acquired the parasite in habitats of sympatric occurrence with red deer and fallow deer.

The presence of mature flukes encapsulated in the liver, and of ova in the feces of the majority of fluke-positive animals, demonstrated that sika deer play a role in the dissemination of F. magna. The sika deer were judged clinically unsuspicious before culling and at gross inspection by the hunters, which may support their role as definitive hosts. Fluke burden and fecal egg counts were lower in sika deer than in red deer and fallow deer sampled in the same area (Rehbein et al. 2021). This finding could be related to differences among the cervid species in habitat use (and thus exposure to infectious fluke stages) or their general innate susceptibility to the parasite, or it may potentially reflect that the process of adaptation of F. magna to sika deer is still ongoing. Our investigations confirm sika deer as suitable definitive, not dead-end, hosts of F. magna. Sika deer therefore should receive appropriate attention in the context of the monitoring of the dispersal of the parasite and any management interventions to lower the risk of spreading of the infection.