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Domestic cats are involved in the spread of Toxoplasma gondii infection in animals and humans worldwide. All species of felines, including wild ones, are likely to be definitive hosts1 because they are the only animals that can excrete the environmentally resistant oocysts of the parasite.2,3 In Europe or the United States, the domestic cycle of T. gondii involves cats and peridomestic and domestic animals such as pigs and sheep, and most (> 95%) T. gondii strains can be grouped into one of three distinct clonal lineages (types I, II, and III).4,5 In these areas, toxoplasmosis is generally asymptomatic and disseminated cases in patients without any immunodeficiency are rare.6 In French Guiana and Surinam, recent severe toxoplasmoses in immunocompetent patients were described involving genetically atypical strains.7,8 These unusual presentations seem to be linked to a sylvatic cycle involving wild felidae and their prey as intermediate hosts. We report, to our knowledge, the first isolation and molecular characterization of T. gondii from the heart tissue of a free-living jaguar (Panthera onca) in French Guiana.
A free-living male jaguar (Panthera onca) was accidentally killed during game hunting in Belizon, an eastern deep forest area in French Guiana. On the basis of its size and teeth characteristics, it was estimated to be a young adult. Intra-cardiac blood and heart samples were collected within 30 minutes of death. Antibodies to T. gondii were detected with a modified agglutination test (MAT) (Toxoscreen®; bioMérieux, Lyon, France).9 The heart was bioassayed in five Swiss mice after digestion in trypsin solution.10 Microscopic detection of Toxoplasma was performed on various mouse tissues (ascitic fluid, brain, lung). After DNA extraction (Quiagen, Courtaboeuf, France) from hearts, brains and lungs of infected mice, genotyping was performed by sequencing at five microsatellite markers (TUB2, W35, TgM-A, B18, and B17)11,12 and the coding region of the GRA6 gene.13 All sequences were submitted to GenBank (accession numbers DQ009075–DQ009079 and DQ187387). They were aligned with sequences from archetypal type I, II, and III strains (Figure 1
) by using ClustalW software.14
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). In microsatellite markers, the atypical alleles consisted of unique nucleotide polymorphisms in microsatellite flanking regions at W35 and B17 or an unusual number of dinucleotide repeats in the microsatellite region of TgM-A. This atypical allele at TgM-A is allele 4 for this marker and has already been described in other isolates from French Guiana.11 The sequence of GUY-2004-JAG at GRA6 is identical to the type X allele for this marker, an atypical allele consisting of two insertions and many unique polymorphic nucleotide sites that distinguish this allele from the three archetypal alleles.15,16 The primary Amazonian forest of French Guiana is home to wild cats including jaguars (Panthera onca), pumas (Puma concolor), jaguarundis (Herpailurus yaguarondi), margays (Leopardus wiedii), and ocelots (Leopardus pardalis). Since the identification by Hutchison17 of the domestic cat Felis catus as a definitive host for T. gondii, investigators in the Americas, Thailand, and the Czech Republic have experimentally shown that these felids are able to shed oocysts of T. gondii.18–23 In uninhabited forestrian zones in French Guiana, wild felids may serve as definitive hosts. The prevalence of T. gondii in the few wild felids tested in Amazonia suggests high levels of transmission for wild definitive hosts in the Amazonian rain forest: in five of six felids in French Guiana (Demar M, unpublished data) and three of four felids in Brazilian Amazonia.24 Felids in French Guiana may become contaminated by ingestion of raw meat from carcasses or freshly killed animals or by the ingestion of T. gondii oocysts scattered in the environment.
Jaguars are considered opportunistic carnivores, eating whatever is most abundant and easiest to catch. In some border forestrian zones of French Guiana, they occasionally select domestic prey (mostly chickens, but also cattle and even dogs and cats) near remote human habitats. Thus, transmission of Toxoplasma from domestic animals to wild animals is possible.25 In the rainforest uninhabited zones, jaguars usually prey on animals weighing at least 15 kg such as tapirs (Tapirus spp.), peccaries (Tayassu spp.), and cervids, such as white-tailed deer (Odocoileus virginanus) and brocket deer (Mazama spp.).26,27 However, they may also consume smaller prey such as coatis (Nasua narica), raccoons (Procyon spp.), pacas (Agouti paca), armadillos (Dasipus novemcinctus), and even small felids, such as ocelot (Leopardus pardalis).
Recent studies have provided support for a wildlife toxoplasmosis cycle, with demonstration of a significant toxoplasmosis seroprevalence in non-carnivorous wild mammals (i.e., folivores, frugivores, and granivores) living in an uninhabited forest zone (Petit Saut, French Guiana) that are major game species.28,29 Terrestrial mammals such as deer, armadillos, pacas, and peccaries were significantly more exposed to T. gondii than other mammals, which is consistent with levels of oral exposure related to ground-dwelling behavior. However, to date, no Toxoplasma isolate was collected from wild fauna in the Amazonian rain forest. This first report of Toxoplasma isolation in a free-living jaguar is a further argument for the existence of a T. gondii wildlife cycle. Less than 20% of the population of French Guiana has contact with the wild environment in inland areas and the inhabitants of the coastal region may occasionally have contact with the forest during their work or leisure activities.
We have reported severe cases of acquired toxoplasmoses in immunocompetent human patients in French Guiana and in a Surinamese border village.7,8 These patients had a severe and non-specific infectious syndrome with no response to traditional antibiotics and antimalarial drugs, visceral involvement of the pulmonary and hepatic systems, toxoplasmic seroconversion with high levels of toxoplasma-specific IgG and IgM, and a favorable response after treatment.7,8 All patients reported forest-related activities such injestion of surface water, consumption of undercooked game meat, and hunting.
Toxoplasma isolates collected from peripheral blood of these patients had an atypical genotype that was different from type I, II, or III isolates described in Europe or North America.11 The atypical allele in TgM-A found in the jaguar isolate and in most of human isolates in French Guiana has been described to date, only in isolates from South America (French Guiana, Brazil, and Surinam) typed with the five microsatellite markers used in this study (French Biologic Resource Center for Toxoplasma, unpublished data). Moreover, a type X allele at GRA6 was unexpected in genotype analysis of the jaguar because it was originally described in California sea otters.15,16 This indicates that the T. gondii wild gene pool circulates in a large area from South to North America. This emerging parasitic zoonosis suggests that human contact with wild strains of T. gondii may extend beyond French Guiana or the Amazonian area. Demographic characteristics and human encroachment on wildlife habitats in the Amazonian forest can increase contacts between humans and the wild reservoir of Toxoplasma, thus increasing the risk for severe toxoplasmosis. With the increase in international travel, health care providers in Europe or North America should be aware of such a risk.
Further molecular analysis should be performed with tissues of wild mammals and environmental samples (soil, water) from different geographic sites to obtain a better understanding of the wildlife cycle and clearly proves its existence. Moreover, broad sampling of isolates from human toxoplasmoses (congenital cases or reactivation in immunocompromised patients) and domestic asymptomatic animals living in urban or peri-urban areas should provide more information about the genetic diversity of T. gondii in French Guiana.
Received February 25, 2007. Accepted for publication June 6, 2007.
Acknowledgments: We thank the hunters and the National Office of Hunting for cooperation, and the Pasteur Institute of French Guiana for use of their animal facility.
* Address correspondence to M. Demar, Unité de Maladies Infectieuses et Tropicales, Centre Hospitalier Andrée Rosemon, Avenue des Flamboyants, BP 6006 Cayenne 97306, French Guiana. E-mail: mdemar{at}yahoo.com 
Authors’ addresses: M. Demar, B. Serrurier, and B. Carme, Unité de Maladies Infectieuses et Tropicales, Centre Hospitalier Andrée Rosemon, Avenue des Flamboyants, BP 6006 Cayenne 97306, French Guiana, Telephone: 594-395-040, Fax: 594-395-041, E-mails: mdemar{at}yahoo.com, bserrurier{at}free.fr, and b.carme{at}wanadoo.fr. D. Ajzenberg and M. L. Dardé, Laboratoire de Parasitologie et Mycologie, Centre Hospitalier Universitaire Dupuytren, 2 Avenue Martin-Luther-King, 87042 Limoges 87042 Cedex, France, E-mails: ajz{at}unilim.fr and darde{at}unilim.fr.
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  S. Sousa, D. Ajzenberg, M. Marle, D. Aubert, I. Villena, J. C. da Costa, and M.-L. Darde Selection of Polymorphic Peptides from GRA6 and GRA7 Sequences of Toxoplasma gondii Strains To Be Used in Serotyping Clin. Vaccine Immunol., August 1, 2009; 16(8): 1158 - 1169. [Abstract] [Full Text] [PDF]
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