History
An approximately 5-year-old free-ranging female white-tailed deer (Odocoileus virginianus) was harvested in Louisiana. The hunter reported that the deer was in poor body condition and had multiple nodular lesions present throughout the liver. Fresh samples of the liver, heart, lungs, spleen, and kidneys were obtained by a biologist from the Louisiana Department of Wildlife and Fisheries and submitted to the Southeastern Cooperative Wildlife Disease Study in Athens, Ga, for diagnostic evaluation.
Gross Findings
Throughout the examined section of liver, there were multifocal to coalescing, round (1- to 4-cm-diameter), raised, tan, nodular lesions that contained yellow purulent fluid. In addition, several pairs of 2.0 × 4.5-cm flat, leaf-shaped organisms were enclosed within discrete, firm, white fibrous capsules (Figure 1). Purulent lesions were occasionally in close proximity to, but not directly adjacent to, encapsulated organisms. Numerous fine, branching, linear bands of dark green to black pigment were present through the hepatic parenchyma. There were no notable gross findings in the heart, lungs, spleen, or kidneys.
Photograph of a section of liver from an approximately 5-year-old white-tailed deer that was harvested in Louisiana. Multifocal to coalescing tan, raised, soft nodules are present in the upper left section of the liver (abscesses [asterisk]). In the center of the liver section, there is a well-demarcated fibrous capsule that contains a single leaf-shaped organism (arrow). An additional organism from within the same fibrous capsule is laid flat to the right of the liver. Numerous branching, linear areas of dark green to black pigment course throughout the hepatic parenchyma. Bar = 1 cm.
Citation: Journal of the American Veterinary Medical Association 253, 2; 10.2460/javma.253.2.167
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→
Histopathologic and Microbiological Findings
Sections of the liver, heart, lungs, spleen, kidneys, and intrahepatic organisms were examined histologically. Throughout the liver, there was diffuse, moderate to marked, periportal to bridging fibrosis. Infiltrates of lymphocytes and plasma cells and high numbers of small bile ducts often expanded portal regions in areas with increased fibrous connective tissue. Occasionally, dense bands of fibrous connective tissue admixed with abundant granular brown to black pigment expanded portal tracts (Figure 2). Randomly scattered throughout the liver were several large foci of necrosis characterized by central regions of fibrin and necrotic debris admixed with degenerate and intact neutrophils surrounded by epithelioid macrophages, lymphocytes, and plasma cells, and encapsulated in peripheral rings of dense fibrous connective tissue (abscess; Figure 3). Kupffer cells often contained cytoplasmic aggregates of granular brown to black pigment. The capsule was multifocally thickened by fibrosis and moderate numbers of lymphocytes and plasma cells. Abundant plasma cells were present within splenic sinusoids. There were no notable histopathologic changes in sections of the heart, lungs, or kidneys. Aerobic bacterial culture of a swab specimen from an intrahepatic abscess revealed heavy growth of the bacterium Trueperella pyogenes.
Photomicrograph of a section of the liver from the white-tailed deer in Figure 1. A portal area is expanded by mature fibrous connective tissue admixed with large clusters of granular black pigment. Increased numbers of bile ducts (biliary hyperplasia) and moderate numbers of mononuclear inflammatory cells are also present within this portal tract. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 253, 2; 10.2460/javma.253.2.167
Photomicrograph of a section of the liver from the white-tailed deer in Figure 1. A large nodular lesion with a central core of necrotic debris and neutrophils (asterisk) is surrounded by a band of inflammatory cells (double-ended bar) and encapsulated in peripheral rings of dense fibrous connective tissue (arrows) that expand portal tracts. A small area of relatively normal hepatic parenchyma is visible in the upper left corner of the image. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 253, 2; 10.2460/javma.253.2.167
Additional Findings
In the liver sections, intrahepatic organisms were evident. Examination of cross sections of the intrahepatic organisms revealed a spinous tegument covering a parenchymatous body with paired ceca and a uterus containing developing eggs (Figure 4). Occasional eggs were present within the surrounding hepatic tissue. Whole parasites, preserved in 70% ethanol, were identified as adult Fascioloides magna.
Photomicrograph of a cross section through an intrahepatic organism from the liver of the white-tailed deer in Figure 1. Notice the spinous tegument (arrow) covering a parenchymatous body. Female (F) reproductive organs and a section of the intestinal tract (double-ended bar) are present in this section. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 253, 2; 10.2460/javma.253.2.167
Morphologic Diagnosis and Case Summary
Morphologic diagnosis: moderate, chronic, periportal to bridging, lymphoplasmacytic and sclerosing hepatitis with biliary hyperplasia, multifocal hepatic abscesses, and intrahepatic adult trematodes.
Case summary: hepatic fascioloidosis with concurrent hepatic abscesses in a white-tailed deer.
Comments
Fascioloides magna is a trematode parasite (fluke) of cervids. The parasite is native to North America and although once widespread, it now has a fragmented distribution with populations in eastern North America being genetically distinct from those in western areas.1 As a result of the translocation of elk, this parasite has also been introduced to numerous European countries.2 Because the parasite uses freshwater snails of the genus Lymnaea as required intermediate hosts, the parasite is most often found in hosts that live near water or wetlands.3 In aquatic environments, trematode eggs develop into free-swimming miracidia that directly penetrate the soft tissues of the snail intermediate host and mature into cercariae. After exiting the snail, cercariae encyst on vegetation and develop into infectious metacercariae. These metacercariae are then ingested by hosts that consume the vegetation.4 Immature flukes migrate throughout the liver and in some hosts, such as sheep and goats, through other organs. Once mature, flukes become encapsulated in pairs within dense fibrous connective tissue capsules that communicate with bile ducts.5 Eggs from mature flukes are passed through bile ducts into the intestinal tract and later excreted in the feces.4 The prepatent period of this parasite varies between 3 and 7 months.6 The absence of trematode eggs in the liver tissue of the deer of the present report suggested that the flukes may not have been fully mature.
White-tailed deer and several other cervid species, including elk, are considered the definitive hosts of F magna.6–8 In the definitive host, clinical signs and lesions associated with F magna infection are most severe in young animals and consist of mild transitory anemia with eosinophilia, subcapsular fibrous tracks in the liver, and granulomas in multiple tissues.9 Periportal fibrosis with biliary hyperplasia associated with mononuclear inflammation and aggregates of fluke pigment (hematin) are the most commonly reported lesions in chronically affected adult animals.6,9 These lesions are generally not associated with hepatic dysfunction; however, rare infections with large numbers of adult flukes have been reported as the cause of death in definitive host species.8,10
In dead-end hosts, such as cattle, moose, pigs, llamas, and rarely horses, ingested metacercariae develop into larval flukes that migrate to the liver where they mature into adults, become encapsulated, and cause severe hepatic fibrosis and occasionally biliary obstruction. Infections in dead-end hosts are usually not patent (ie, eggs are not shed in the feces) and generally do not cause clinically important disease or death.6,8,11 There is a single report12 of fatal intrapulmonary hemorrhage as a result of vascular disruption from migrating flukes in a steer. In aberrant hosts, such as domestic goats and sheep, immature flukes are unable to mature, and excessive migration of the immature flukes can cause severe hepatic damage (necrosis and fibrosis), which is often fatal.6,8 Experimental treatment of white-tailed deer with albendazole has been reported to reduce the number of eggs per gram of feces; however, this application is likely to only be of use in captive populations.13
The apparent association between F magna infection and hepatic abscess formation in the deer of the present report is of interest. Microscopic abscesses in the liver of cattle have been associated with Fasciola hepatica infections14; however, an abattoir study of bovine livers found no significant association between the presence of grossly visible abscesses and F hepatica infections.15 Although it seems reasonable to hypothesize that hepatic damage induced by migrating trematodes could predispose animals to local infection and abscess formation induced by bacteria present in the portal blood supply, there is little published evidence to support this conclusion. Because F magna infections are generally considered incidental findings in white-tailed deer, it is possible that the presence of hepatic abscesses in the case described in the present report may have been unrelated to trematode infection.
The bacterium T pyogenes (formerly Actinomyces pyogenes) was isolated from the liver abscesses in the deer of the present report. This bacterium has been previously identified in cases of disseminated abscesses in a white-tailed deer,16 and is the organism most frequently isolated from white-tailed deer with intracranial abscess syndrome.17 Trueperella pyogenes is a commensal organism of the skin and mucous membranes of domestic and exotic bovids and cervids18 and is an opportunistic pathogen secondary to trauma or mucosal compromise. Although the entire carcass of the deer of the present report was not available for examination, it was likely that previous cutaneous or mucosal trauma predisposed this animal to T pyogenes bacteremia and subsequent hepatic abscess formation. Animals with evidence of systemic disease are typically considered unfit for human consumption.
References
1 Bazsalovicsová E, Králová-Hromadová I, Sntefka J. Genetic interrelationships of North American populations of giant liver fluke Fascioloides magna. Parasit Vectors 2015;8:288–303.
2 Králová-Hromadová I, Bazsalovicsoá E, Sntefka J, et al. Multiple origins of European populations of the giant liver fluke Fascioloides magna (Trematode: Fasciolidae), a liver parasite of ruminants. Int J Parasitol 2011;41:373–383.
3 Swales WE. The life cycle of Fascioloides magna (Bassi. 1875), the large liver fluke of ruminants, in Canada. Can J Res 1935;12:177–215.
4 Malcicka M. Life history and biology of Fascioloides magna (Trematoda) and its native and exotic hosts. Ecol Evol 2015;5:1381–1397.
5 Foreyt WJ, Samuel WM, Todd AC. Fascioloides magna in white-tailed deer (Odocoileus virginianus): observations on the pairing tendency. J Parasitol 1977;63:1050–1052.
6 Foreyt WJ, Todd AC. Development of the large American liver fluke, Fascioloides magna, in white-tailed deer, cattle, and sheep. J Parasitol 1976;62:26–32.
7 Olsen OW. White-tailed deer as a reservoir host of the large American liver fluke. Vet Med 1949;44:26–30.
8 Pybus MJ. Liver Flukes. In: Samuel WM, Pybus MJ, Kocan AA, eds. Parasitic diseases of wild mammals. 2nd ed. Ames, Iowa: Iowa State University Press; 2001:121–149.
9 Presidente PJ, McCraw BM, Lumsden JH. Pathogenicity of immature Fascioloides magna in white-tailed deer. Can J Comp Med 1980;44:423–432.
10 Pybus MJ, Butterworth EW, Woods JG. An expanding population of the giant liver fluke (Fascioloides magna) in elk (Cervus canadensis) and other ungulates in Canada. J Wildl Dis 2015;51:431–445.
11 McClanahan SL, Stromberg BE, Hayden DW, et al. Natural infection of a horse with Fascioloides magna. J Vet Diagn Invest 2005;17:382–385.
12 Wobeser BK, Schumann F. Fascioloides magna infection causing fatal pulmonary hemorrhage in a steer. Can Vet J 2014;55:1093–1095.
13 Qureshi T, Davis DS, Drawe DL. Use of albendazole in feed to control Fascioloides magna infections in captive white-tailed deer (Odocoileus virginianus). J Wildl Dis 1990;26:231–235.
14 Marcos LA, Yi P, Machicado A, et al. Hepatic fibrosis and Fasciola hepatica infection in cattle. J Helminthol 2007;81:381–386.
15 O'Sullivan EN. Two-year study of bovine hepatic abscessation in 10 abattoirs in County Cork, Ireland. Vet Rec 1999;145:389–393.
16 Turnquist SE, Fales WH. Disseminated Actinomyces pyogenes infection in a free-ranging white-tailed deer. J Vet Diagn Invest 1998;10:86–89.
17 Baumann CD, Davidson WR, Roscoe DE, et al. Intracranial abscessation in white-tailed deer of North America. J Wildl Dis 2001;37:661–670.
18 Zulty JC, Montali RJ. Actinomyces pyogenes infection in exotic bovidae and cervidae: 17 cases (1978–1986). J Zoo Wildl Med 1998;19:30–32.
