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Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

2000

Elaeophorosis in Red Deer from Spain

Mónica Santín-Durán Universidad Complutense de Madrid, [email protected]

J. M. Alunda Universidad Complutense de Madrid

J. M. San Miguel Universidad Complutense de Madrid

Eric P. Hoberg Parasitic Disease Laboratory, Agricultural Research Service, United States Department of Agriculture, [email protected]

C. de la Fuente Universidad Complutense de Madrid

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Santín-Durán, Mónica; Alunda, J. M.; San Miguel, J. M.; Hoberg, Eric P.; and de la Fuente, C., "Elaeophorosis in Red Deer from Spain" (2000). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 822. https://digitalcommons.unl.edu/parasitologyfacpubs/822

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Journal of Wildlife Diseases, 36(4), 2000, pp. 779–782 ᭧ Wildlife Disease Association 2000

Elaeophorosis in Red Deer from Spain

M. SantõÂn-DuraÂn,1,3 J. M. Alunda,1 J. M. San Miguel,1 E. P. Hoberg,2 and C. de la Fuente11Departamento de PatologõÂa Animal I (Sanidad Animal), Facultad de Veterinaria, Universidad Complutense, 28040 Madrid, Spain; 2 U.S. National Parasite Collection, USDA, Building 1180 BARC-East, Beltsville, Maryland 20705, USA; 3 Corresponding author (e-mail: [email protected]).

ABSTRACT: Elaeophorosis, caused by Elaeo- over a 1 yr period and involved monthly phora elaphi, was observed in red deer (Cervus collections from October 1994 to Septem- elaphus) from Toledo Province (Spain) for the ber 1995. One hundred fifty one red deer first time. Adult specimens of Elaeophora ela- Ͻ phi were found in the hepatic vessels of nine in three age groups, 1-yr-old, 1- to 2-yr- of 151 red deer between October 1994 and old and Ͼ2-yr-old and representing two September 1995; intensity of infection was two sex-classes were collected and examined. to 18 per host. Adult nematodes In contrast, collections of fallow deer were were only found during the period from fall through early spring. No differences were pre- limited to 17 and as a conse- sent between sex or age groups. Parasites were quence the focus of the study was on C. not found in a limited sample from fallow deer elaphus. (Dama dama). Blood samples were negative for Immediately following collection, prior the presence of microfilariae. to transport to the necropsy facility at the Key words: Cervus elaphus, , Dama dama, fallow deer, red deer, sur- park, blood samples were drawn from the vey. heart of each animal. At the necropsy, fi- larial worms found in the hepatic vessels Elaeophorosis is caused by nematodes were collected, counted, and fixed in phos- of the genus Elaeophora that localize in phate buffered formalin (5%). Necropsies the heart and arterial vasculature of ru- were generally conducted a short time af- minants and horses. Currently six species ter death in order to avoid potential post- are recognized in the genus, with most be- mortem migration of nematodes as de- ing limited to cervid or bovid hosts from scribed for E. schneideri by Adcock and the Palearctic, Nearctic, and Africa (Table Hibler (1969). Blood samples were filtered 1). Some species have been regarded as through a filter (5 ␮m mesh) and stained serious pathogens in ruminant hosts, but (methylene blue 1/1,000) prior to micro- in many cases data for life history, epide- scopic examination to check the possible miology, and an understanding of the presence of microfilariae. Adult filarial mechanisms for pathogenesis are limited nematodes were studied as temporary (Hibler and Adcock, 1971; Carrasco et al., whole mounts cleared in phenol-alcohol 1995). (80 parts melted phenol crystals and 20 In the present study we report new find- parts absolute ethanol) and examined with ings on the distribution of elaeophorosis in light microscopy using differential inter- red deer (Cervus elaphus) and fallow deer ference contrast optics. In males, the tail (Dama dama) in central Spain. The survey was dissected from some specimens to ex- for the occurrence of Elaeophora sp. in amine the characteristics of the caudal pa- red deer and fallow deer was undertaken pillae. in ‘‘Quintos de Mora’’, a government- Specimens were consistent with those of owned and managed park located near To- E. elaphi, and the caudal structure in ledo (Spain; 39Њ25ЈN, 4Њ04ЈW). The 6,864 males was as described by Herna´ndez- ha park is composed of two different hab- Rodrı´guez et al. (1986) (Fig. 1). Represen- itats including a plateau at 800 m above tative specimens are deposited in the U.S. sea level crossed by the Las Navas River, National Parasite Collection (USDA, Ag- and a mountainous area reaching 1,235 m ricultural Research Service, Beltsville, in elevation. Survey for parasites extended Maryland, USA; USNPC Nos. 88805–

779 780 JOURNAL OF WILDLIFE DISEASES, VOL. 36, NO. 4, OCTOBER 2000 ´guez et al. ´ndez-Rodrı Oshmarin and Belous (1951) Herna (1986) Carrasco et al. (1995) Hibler and Adcock (1968) O. a Ovis aries a ) ), Odocoileus virginianus, Cervus elaphus canadensis, C. Cervus elaphus Alces alces, Cervus elaphus can- a Ovis aries ), adensis, Rangifer tarandus Cervidae ( hemionus, nippon spp. FIGURE 1. Male ventral caudal end of Elaeopho- ra elaphi from red deer showing the pattern of the papillae. Bar ϭ 25 ␮m. Elaeophora 88808) and in the Parasite Collection of the Departamento Patologı´a Animal I (Universidad Complutense de Madrid, Madrid, Spain). Elaeophora elaphi, a filarial worm

branches found in the hepatic vessels, was origi- nally described in red deer from Co´rdoba (Spain) by Herna´ndez-Rodrı´guez et al. (1986). It was reported subsequently from the type host at Ciudad Real (Spain) by Carrasco et al. (1995, 1998), but had not been observed previously in Toledo. In cervids, only this species and E. abramovi (Table 1) occur in the hepatic vessels. Spain Hepatic vessels Cervidae ( Asia and AfricaEuropeUSA Aorta and heart Arteries of limbs Carotid arteries and Bovidae Equidae Sonin (1966) Supperer (1953) Africa Heart Bovidae Bain and Haesevoets (1974) Europe and Asia Hepatic vesselsHerna Cervidae ( ´ndez-Rodrı´guez et al. (1986) pro- vided a distinct differential diagnosis for species of Elaeophora, and the males of E. elaphi and E. abramovi are distin-

spp. Distribution Locationguished by diagnostic Definitive host features of the cau- Reference

1. Geographical distribution, hosts, and location in the host of dal papillae and ‘‘area rugosa’’. The orig- inal description of the male tail is aug- ABLE The usual definitive host. E. elaphi T Elaeophora E. poeli a E. boehmi E. schneideri E. sagittus E. abramovi mented by our Figure 1. SHORT COMMUNICATIONS 781

Infected animals, and adult nematodes, (1995) for E. elaphi in red deer. Addition- were only found during the period extend- ally, Mtei and Sanga (1990) reported less ing from fall through early spring in than eight nematodes per host in a study months of October to March. The num- involving E. poeli in over 4,000 asymptom- bers of red deer examined and the distri- atic cattle. In the current study histology bution of infected animals during this 6 was not performed, but macroscopic le- mo period were 1/19, 3/18, 2/18, 1/18, 1/ sions were not observed. The absence of 13, and 1/10 in October, November, De- such visible lesions as thrombi in the por- cember, January, February, and March, re- tal system contrasts with observations by spectively. Red deer examined in the re- Carrasco et al. (1995). maining sampling periods, 10 in April and Madden et al. (1991) found that nine each in May, June, July, August and (Alces alces) when parasitized by more September, were uninfected. Among those than 40 adult E. schneideri were ataxic, red deer found to be hosts (five males and wandered in circles, and had poor body four females) parasites were found in all condition. In contrast, all hosts in the cur- age-classes (one in Ͻ1-yr-old; four in 1-to- rent study were in good condition and ap- 2-yr-old; and four in Ͼ2-yr-old). Statistical parently were healthy. This may be attrib- analysis (Chi-square and Fisher’s Test) utable to the infections of low intensity demonstrated no significant differences in demonstrated in red deer from Toledo. infection between males and females (P ϭ Moreover, pathological effects could be re- 0.8706) or among age groups (P ϭ 0.9934). lated to the host-specificity. For example, Microfilariae were not observed in blood E. schneideri does not provoke any clinical samples. signs in its normal definitive The prevalence of infection found in the host. Alternatively, in other cervids (C. current study (6% across the annual sam- nippon and C. elaphus canadensis) and in pling period) was lower than that reported domestic it is the causative agent of by Carrasco et al. (1995) in red deer col- dermatitis, blindness, nervous signs, and lected from an adjacent area (Ciudad Real; occasionally death (Adcock and Hibler, between September and April there were 1969; Hibler and Adcock, 1971). Thus, the 23% with parasites, but the prevalence was host may have an important influence on 41% if we counted those with just lesions the distribution of disease attributable to typical of E. elaphi). In our study, infected infections of Elaeophora spp. This also animals were found only from October to may be of importance in Toledo, where March. Considering prevalence only with- the fallow deer is sympatric with red deer. in this 6 mo period, 8% were infected; no Although only 17 fallow deer have been explanation is available for this apparent examined no filarial worms were found. difference between geographic localities. In the present study there were no mi- This prevalence of infection is relatively crofilariae in blood samples from infected low compared to data for such species as red deer; similar result were reported by E. schneideri in North American cervids. Carrasco et al. (1995). They suggested that It is possible that large variations in prev- the occurrence of microfilaremia was tran- alence may be typical, as indicated by lo- sitory and may be correlated with the sea- calized differences in the distribution of sonal occurrence (summer) of a biting-fly infection for E. schneideri in mule deer acting as the vector for E. elaphi. In E. (Odocoileus hemionus) ranging from 4 to schneideri microfilariae may be present in 90% in western North America (Hibler capillaries of the skin on the forehead and and Adcock, 1971). face, but not in general circulation (Kem- Intensity of infection (x¯ ϭ 9, range ϭ 2– per, 1938; Foreyt and Foreyt, 1979). Kem- 18 nematodes) in our study was compa- per (1938) also obtained microfilariae from rable to that reported by Carrasco et al. cutaneous lesions. Additional studies are 782 JOURNAL OF WILDLIFE DISEASES, VOL. 36, NO. 4, OCTOBER 2000 necessary to elucidate the life cycle for E. phus). Journal of Comparative Pathology 118: elaphi, with particular emphasis on deter- 207–219. FOREYT, W. J., AND K. M. FOREYT. 1979. Elaeophora mination of the arthropod intermediate schneideri in white-tailed deer from Texas. Jour- host(s) and patterns of localization for mi- nal of Wildlife Diseases 15: 55–56. crofilariae in the cervid definitive host. HERNA´ NDEZ-RODRIÂGUEZ, S., MARTIÂNEZ-GO´ MEZ,F., We are grateful for the financial support AND P. G UTIE´ RREZ-PALOMINO. 1986. Elaeophora elaphi n. sp. (Filarioidea: ) para- from ICONA (5280363). Cooperation site of the red deer (Cervus elaphus). Annales de from J. M. Sebastia´n and C. Rodrı´guez Vi- Parasitologie Humaine et Compare´e 64: 457– dal was critical. Official warden services of 463. the ‘‘Quintos de Mora’’ helped with sam- HIBLER,C.P.,AND J. L. ADCOCK. 1968. Redescrip- pling. Laboratory studies and parasite tion of Wehr and Dik- mans, 1935 (Nematoda: Filarioidea). The Journal identification was completed at the Bio- of Parasitology 54: 1095–1098. systematics and National Parasite Collec- HIBLER,C.P.,AND J. L. ADCOCK. 1971. Elaeopho- tion Unit, USDA, Agricultural Research rosis. In Parasite diseases of wild mammals. J. Service, Beltsville, Maryland; we thank J. Davis and R. C. Anderson (eds.). Iowa State Uni- versity Press, Ames, Iowa, pp. 263–278. R. Lichtenfels. KEMPER, H. E. 1938. Filarial dermatosis of sheep. The North American Veterinarian 19: 36–41. LITERATURE CITED MADDEN, D. J., T. R. SPRAKER, AND W. J. ADRIAN. 1991. Elaeophora schneideri in moose (Alces al- ADCOCK, J. L., AND C. P. HIBLER. 1969. Vascular and ces) from Colorado. Journal of Wildlife Diseases neuro-ophthalmic pathology of elaeophorosis in 27: 340–341. . Pathology Veterinary 6: 185–213. MTEI,B.J.,AND H. J. N. SANGA. 1990. Aortic on- BAIN, O., AND E. HAESEVOETS. 1974. Affinite´s entre chocercosis and elaeophorosis in traditional TSZ- deux filaires de l’appareil circulatoire, l’une par- cattle in Tabora (Tanzania): Prevalence and pa- asite de bovide´s, l’autre de cervide´s: Cordophilus thology. Veterinary Parasitology 36: 165–170. sagittus (Linstow, 1907) et C. abramovi (Osh- OSHMARIN,P.G.,AND E. V. BELOUS. 1951. Notes on marin et Belous, 1951) nov. comb. Annales de the filariae of wild animals. Trudy Gel’minto- Parasitologie 49: 119–122. logicheskoi Laboratorii, Akademiya Nauk SSSR 5: 121–127. [In Russian.] CARRASCO, L., Y. FIERRO,J.M.SA´ NCHEZ-CASTIL- SONIN, M. D. 1966. Filariata of animals and man LEJO,M.J.BAUTISTA,J.C.GO´ MEZ-VILLAMAN- and diseases caused by them. Part III. In Es- DOS, AND M. A. SIERRA. 1995. Elaeophorosis in sentials of nematodology. K. I. Skrjabin (ed.). red deer caused by Elaeophora elaphi: Lesions Vol. XXIV. Izdatel’stvo ‘‘Nauka’’, Moskva. Trans- of natural disease. Veterinary Pathology 32: 250– lated by: Israel Program for Scientific Transla- 257. tions. Jerusalem 1974, pp. 353–357. ,J.C.GO´ MEZ-VILLAMANDOS,Y.FIERRO,J.M. SUPPERER, R. 1953. Filariosen der Pferde in O¨ ster- ´ SANCHEZ-CASTILLEJO,M.J.BAUTISTA, AND J. reich. Wiener Tiera¨rztliche Monatsschrift 40: ´ PEREZ. 1998. Immunohistochemical character- 193–220. ization of hepatic lesions associated with Elaeo- phora elaphi parasitism in red deer (Cervus ela- Received for publication 1 July 1999.