Elsevier

Veterinary Parasitology

Volume 126, Issue 4, 30 December 2004, Pages 387-395
Veterinary Parasitology

Short communication
The risks of translocating wildlife: Pathogenic infection with Theileria sp. and Elaeophora elaphi in an imported red deer

https://doi.org/10.1016/j.vetpar.2004.07.026Get rights and content

Abstract

It is well known that the translocation of wild animals poses risks of the introduction of pathogens into populations, and regulations and recommendations regarding quarantine and screening protocols for wild animals do exist. Less is known about the infection of imported animals with local endemic pathogens. A red deer stag that had been imported from Germany was found recumbent and died from hemolytic anaemia and a process of exertional myopathy. Infection with Theileria sp. was detected in thin blood smears and confirmed by PCR and sequencing. In addition, massive parasitation by Elaeophora elaphi, a parasite endemic to Iberian red deer, was detected. Sequence comparison between the 18S rRNA gene sequence determined that the Theileria strain involved in this case had a 99.7% identity with a Theileria sp. strain obtained from sika-deer, and 95.3% identity with T. cervi. Using sequence distance analysis, the strain from red deer grouped with isolates from Cervus spp. as opposed to isolates from Odocoileus spp. and bovines. Both detected parasites are of little pathogenicity to local red deer, but were pathogenic for the imported red deer from Northern Europe. This case demonstrates that local endemic pathogens may pose naïve translocated animals at risk, and illustrates the need for thorough examination and planification of translocation protocols.

Introduction

Theileriosis is a tick-borne parasitic disease caused by different species of Theileria. Only some of the members of this genus are pathogenic, while others are considered to be moderately pathogenic or benign (Brown, 1990). Mediterranean theileriosis is recognized to be an endemic disease in domestic cattle in Spain that accounts for important economic losses to the cattle industry. The main species responsible for the disease is Theileria annulata, which is transmitted by ticks of the Hyalomma genus (Viseras et al., 1999, Sayin et al., 2003). Studies on the seroprevalence of T. annulata in dairy and beef cattle as well as fighting bulls have detected a high seroprevalence of the disease (between 50 and 80%) in southern Spain and evidenced continuous spread of the disease to the North of the country. Because of its importance for the cattle industry, a tissue culture attenuated vaccine has been developed and tested in field trials (Viseras et al., 1997, Viseras et al., 1998). Nevertheless, little is known about the epidemiology of the disease in wild ruminants that may act as reservoirs maintaining the disease and ticks, and thus jeopardize efforts to eliminate the disease in domestic livestock populations. Infections with Theileria have been demonstrated in different free-living ungulates such as white-tailed deer (Odocoileus virginianus), elk (Cervus elaphus canadensis) (Chae et al., 1999), sika-deer (C. nippon yesoensis) (Takahashi et al., 1992) and the mule deer (O. hemionus) (Kjemtrup et al., 2000). In the red deer (C. elaphus), subclinical infections with Theileria sp. have been reported in Austria (Hinaidy, 1985) and Slovakia (Cerny, 1958). Also, T. ovis could be transferred experimentally to red deer and caused a subclinical infection (Enigk et al., 1964).

Members of the genus Elaeophora (Family Onchocercidae) are parasitic nematodes that infect the vascular system of artiodactyls and are transmitted by hematophagous arthropods. The genus currently includes six species. Pathological lesions and subsequent clinical manifestation vary with the parasite and host species (Pence, 1991), and have occasionally been related to mortality in wild ungulates (Huchzermeyer et al., 2001). E. elaphi was the latest Elaeophora parasite described (Hernandez et al., 1986) and to date the only known natural definitive host is the Iberian red deer (C. elaphus hispanicus). E. elaphi has only been found in the Southern and Central Iberian Peninsula (Carrasco et al., 1995, Santin-Duran et al., 2000). As E. abramovi, E. elaphi invades the portal vein system. Although it may cause important vascular changes in the liver, clinical symptoms are generally absent, which suggest adaptation between the parasite and its host (Carrasco et al., 1995).

Deer populations in Central and Southern Spain are frequently intensively managed, with measures including fencing of hunting estates, supplemental feeding and translocations of animals between estates, or importation of alocthonous deer from different countries. The latter is done to introduce “new blood” and in order to ameliorate antler trophies (Fierro et al., 2002). A number of publications and incidents have proven and raised concern about the dangers of the movement of wild animals between geographic locations that can act as probable vectors of infectious diseases and of parasites or parasite strains (Brown, 2000, Fernandez-de-Mera et al., 2003). Recently, recommendations about control prior to movement of animals and quarantine measures in the area they are translocated to have been published (Woodford, 2001). Although concern exists, less attention is paid to the fact that translocated animals may acquire local endemic infectious diseases against which they may have no defenses.

Section snippets

Clinical case

A 7-year-old red deer stag was observed with staggering gait and found recumbent the next day in a private fenced hunting estate in central Spain (3°45′E; 500–800 m above sea level) on 26 June 2002. The stag had been imported from Germany in January of the same year by the owners of the estate in order to introduce new genetic material and increase trophy size in the local deer population. The animal was found hyperthermic (43.3 °C), with pale mucosas and showing uncoordinated movements.

Results

The red deer stag imported from Germany was found to be in good nutritional condition (Kidney Fat Index (KFI): 103.1 as opposed to mean KFI: 15.93 in local red deer stags) upon necropsy. Grossly generalized congestion of the internal organs was observed, and multiple focal hemorrhages were present in the serosa and submucosa of the small intestine, in the pericardium and myocardium. Approximately 100 nematode parasites were collected from the large blood vessels of the liver where they were

Discussion

The clinical signs, the macroscopical and histological lesions, and the results from hematology are consistent with hemolytic anemia, presumably caused by infection with a piroplasm identified as Theileria sp. and a process of rhabdomyolysis. In addition, thrombi in hepatic vessels were caused by a heavy infestation with E. elaphi. Infection with both pathogens, together with the extremely high ambient temperatures, may presumably have contributed to the death of the animal. This is the first

Acknowledgements

The authors would like to acknowledge the support by projects AGL2001-3947 of the Ministerio de Ciencia y Tecnología and RTA02-001 of the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA). This is a contribution to the agreement between Yolanda Fierro and Universidad de Castilla – La Mancha. We are grateful to Dr. A.L. García-Pérez for helpful comments and critical discussion.

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