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Journal of Wildlife Diseases, 44(1), 2008, pp. 172-173
© Wildlife Disease Association  2008
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SHORT COMMUNICATION

Prevalence of Toxoplasma gondii in Raptors from France

 Dominique Aubert1,4, Marie-Eve Terrier2, Aurélien Dumètre3, Jacques Barrat2 and Isabelle Villena1

1 Laboratoire de Parasitologie, EA 3800, IFR53, Université de Reims Champagne-Ardenne, 45 rue Cognacq Jay, 51092 Reims Cedex, France;
2 Agence Française de Sécurité Sanitaire des Aliments (AFSSA), BP40009, 54290 Malzéville, France;
3 Laboratoire de Parasitologie, EA3174, Faculté de Medicine, Université de Limoges, Z Avenue Martin Luther King, 87042, Limoges Cedex, France
4 Corresponding author (email: daubert{at}chu-reims.fr)

ABSTRACT:   Little is known about the prevalence or importance of Toxoplasma gondii infections in raptors. Sera from Eurasian Buzzards (Buteo buteo, n=14), Tawny Owls (Strix aluco, n=12), Barn Owls (Tyto alba, n=18), Eurasian Sparrowhawk (Accipiter nisus, n=1), and Common Kestrels (Falco tinnunculus, n=8) were examined for agglutinating antibodies using the modified agglutination test at 1:25 dilution. Antibodies were not detected in Common Kestrels and the Eurasian Sparrowhawk but were detected in 11 Eurasian Buzzards (79%), six Tawny Owls (50%), and two Barn Owls (11%). Toxoplasma gondii, genotype II, was isolated from the brain of an adult Tawny Owl.
  Key words:  Accipiter nisus, Buteo buteo, Falco tinnunculus, seroprevalence, Strix aluco, Toxoplasma gondii, Tyto alba.

Toxoplasma gondii affects most species of warm-blooded animals, including birds. Little is known about the prevalence of Toxoplasma gondii infections in raptors, but experimental studies indicate that Red-tailed Hawks (Buteo jamaicensis; Lindsay et al., 1991) and owls (Dubey et al., 1992) are susceptible. The purpose of the present study was to determine the prevalence of antibodies of T. gondii in naturally infected wild birds and to attempt to isolate the parasite from raptors.

Birds were sampled in 1989 at the Care and Rehabilitation Center for birds in Chizé, France (46°11'N, 00°34'E). Sera from Eurasian Buzzards (Buteo buteo, n=9), Tawny Owls (Strix aluco, n=8), Barn Owls (Tyto alba, n=14), Eurasian Sparrowhawk (Accipiter nisus, n=1), and Common Kestrels (Falco tinnunculus, n=8) were tested using the modified agglutination test (MAT). Dubey (2002) has shown that the MAT is the most sensitive and specific test for T. gondii antibodies and can be used effectively for testing birds. The test was performed as previously described with mercaptoethanol (Sigma, St. Quentin Fallavier, France) added to the serum sample to remove IgM (Dubey and Desmonts, 1987). Sera were diluted twofold starting at a 1:6 dilution in phosphate-buffered saline (pH 7.2). Sera agglutinating the antigen at a dilution of 1:25 or higher were considered positive for antibodies to T. gondii. In attempts to isolate T. gondii from raptors, one Eurasian Sparrowhawk (Accipiter nisus), five Eurasian Buzzards, four Barn Owls, and four Tawny Owls were obtained during the 2003 nestling season, and in 2004, from a Center for Wildlife Rescue located near Limoges (45°51'N, 01°08'E), Haute-Vienne district, France. Sera obtained from heart fluid were tested for T. gondii antibodies by MAT. The brain and/ or heart of seropositive birds were bioassayed in mice after digestion in pepsin as described previously (Dubey, 1998). Briefly, tissues were ground in five volumes (w/ v) of aqueous 0.9% NaCl (saline), mixed with five volumes of acidic pepsin, and this mixture was incubated in a shaker water bath for 1 hr at 37 C. The digest was centrifuged, neutralized, and mixed with gentamicin (40 mg/l). Tissue imprints of mice that died were examined for T. gondii tachyzoites or tissue cysts. Mice were bled at 4 wk postinoculation, and sera samples were tested with MAT at 1:25 dilution. DNA from brains of infected mice was extracted and tested by a multiplex polymerase chain reaction (PCR) assay as described in Ajzenberg et al. (2005).

Antibodies to T. gondii were found in 79% of Eurasian Buzzards, 50% of Barn Owls, and 11% of Tawny Owls, while antibodies were not detected in Common Kestrels or the European Sparrowhawk (Table 1Go). Parasite isolation was attempted from four seropositive birds with antibody titers of 50, and Toxoplasma gondii was isolated from the brain of an adult tawny owl. This isolate was a genotype II and was avirulent for mice.


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  		TABLE 1. Prevalence of Toxoplasma gondii in raptors from France.

 
Antibodies to T. gondii have previously been reported from kestrels (Inci et al., 2002). Literak et al. (1992) also reported isolation of T. gondii from tissues of a kestrel in the Czech Republic. Our seropositive results from Barn Owls are consistent with results from Kirkpatrick et al. (1990), who detected antibodies in three of 28 (10.7%) adult and zero of 24 nestling owls, and Niederehe (1964), who detected antibodies in one of 14 Barn Owls. Attempts to isolate T. gondii from six Barn Owls were negative (Lindsay et al., 1993).

Although our observed antibody prevalence (50%) was high, there have been no previous reports of T. gondii infection or antibodies in Tawny Owls. Isolates of T. gondii have been previously reported from 8.1% of 123 Eurasian Buzzards (Literak et al., 1992). Seropositive birds in this study presumably became infected by consuming prey (principally sparrows for Accipiter nisus, common voles for Tyto alba and Falco tinnunculus, and small mammals for Strix aluco), and differences in prevalence may reflect variable infection rates in prey species, especially in small mammals.

This study was supported by the Centre National de Reference on Toxoplasmosis.

LITERATURE CITED

AJZENBERG, D., A. DUMETRE, AND M. L. DARDE. 2005. Multiplex PCR for typing strains of Toxoplasma gondii. Journal of Clinical Microbiology 43: 1940–1943.[Abstract/Free Full Text]

DUBEY, J. P. 1998. Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. Veterinary Parasitology 74: 75–77.[Medline]

———. 2002. A review of toxoplasmosis in wild birds. Veterinary Parasitology 106: 121–153.[Medline]

———, AND G. DESMONTS. 1987. Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19: 337–339.[Medline]

———, S. L. PORTER, F. TSENG, S. K. SHEN, AND P. THULLIEZ. 1992. Induced toxoplasmosis in owls. Journal of Zoo and Wildlife Medicine 23: 98–102.

INCI, A., C. BABUR, Y. CAM, AND A. ICA. 2002. Investigation of seropositivity to Toxoplasma gondii (Nicolle and Manceaux, 1908) in some prey birds using the Sabin-Feldman dye test in Kayseri Region. Firat Üniversitesi Sag lik Bilimleri Dergisi (Veteriner) 16: 177–179.

KIRKPATRICK, C. E., B. A. COLVIN, AND J. P. DUBEY. 1990. Toxoplasma gondii antibodies in common barn-owls (Tyto alba) and pigeons (Columba livia) in New Jersey. Veterinary Parasitology 36: 177–180.[Medline]

LINDSAY, D. S., J. P. DUBEY, AND B. L. BLAGBURN. 1991. Toxoplasma gondii infections in red-tailed hawks inoculated orally with tissue cysts. Journal of Parasitology 77: 322–325.[Medline]

———, P. C. SMITH, F. J. HOERR, AND B. L. BLAGBURN. 1993. Prevalence of encysted Toxoplasma gondii in raptors from Alabama. Journal of Parasitology 79: 870–873.[Medline]

LITERAK, I., K. HEJLICEK, J. NEZVAAL, AND C. FOLK. 1992. Incidence of Toxoplasma gondii in populations of wild birds in the Czech Republic. Avian Pathology 21: 659–665.[Medline]

NIEDEREHE, H. 1964. Toxoplasma-Infektion bei verwilderten Tauben. Tierärztliche Umschau 19: 256–257.

Received for publication 25 October 2006.




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