| Issue |
Parasite
Volume 21, 2014
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|
|---|---|---|
| Article Number | 62 | |
| Number of page(s) | 4 | |
| DOI | https://doi.org/10.1051/parasite/2014062 | |
| Published online | 20 November 2014 | |
Research Article
Toxoplasmosis in a bar-shouldered dove (Geopelia humeralis) from the Zoo of Clères, France
Toxoplasmose chez une Géopélie à nuque rousse (Geopelia humeralis) du Zoo de Clères, France
1
Muséum National d’Histoire Naturelle, Département des Jardins Botaniques et Zoologiques, 57 rue Cuvier, 75005
Paris, France
2
Laboratoire Anatomo-Pathologique Vétérinaire, BP 303, 37403
Amboise, France
3
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Beltsville, Maryland
20705-2350, USA
* Corresponding author: rigoulet@mnhn.fr
Received:
1
October
2014
Accepted:
4
November
2014
Toxoplasmosis causes mortality in several avian species, especially passerine birds. Toxoplasmosis was diagnosed in a bar-shouldered dove (Geopelia humeralis) found dead at the zoo of Clères (France). The bird had necrotizing pneumonia and nephritis with intralesional tachyzoites of Toxoplasma gondii. The diagnosis was confirmed by immunostaining with polyclonal rabbit T. gondii antibodies and by transmission electron microscopy. To our knowledge, the bar-shouldered dove is a new host record for T. gondii.
Résumé
La toxoplasmose est une cause de mortalité chez plusieurs espèces d’oiseaux, en particulier les passereaux. La toxoplasmose a été diagnostiquée chez une Géopélie à nuque rousse (Geopelia humeralis) retrouvée morte au zoo de Clères (France). L’oiseau avait une pneumonie nécrosante et une néphrite avec tachyzoïtes de Toxoplasma gondii intralésionnels. Le diagnostic a été confirmé par marquage immunologique avec des anticorps polyclonaux de lapin anti-T. gondii et par microscopie électronique à transmission. À notre connaissance, la Géopélie à nuque rousse est un nouvel hôte pour T. gondii.
Key words: Toxoplasma gondii / toxoplasmosis / bar-shouldered dove / Geopelia humeralis / France
© J. Rigoulet et al., published by EDP Sciences, 2014
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Introduction
Toxoplasma gondii can cause mortality in many species of mammals and birds [1]. Worldwide reports of toxoplasmosis in all avian species have recently been summarized [1, 2]. The passerine birds are especially susceptible to clinical toxoplasmosis [4, 8]. Pigeons can die of natural T. gondii infection, depending on the breed and age of the host [2, 3]. We report fatal toxoplasmosis in a bar-shouldered dove (Geopelia humeralis), which is to our knowledge the first report of T. gondii infection in this host.
History
Since 1919, the zoological park of Clères (France) owns an important collection of captive birds, including Columbidae. Among Columbidae, Geopelia humeralis is an endemic species of East and North Australia, which breeds well in captivity. Geopelia humeralis is monogamic; the female lays two eggs, twice a year. The incubation period is 13–14 days; sexual maturity is reached at about one year; lifespan is 18 years, but reproduction stops at 12 years. The first couple of male and female G. humeralis was brought to Clères from the Taronga Zoo, Sydney, Australia at the end of the 1960s. It began to reproduce in 1970, and in 1996, the zoological park obtained the eighth generation of these doves. All these bar-shouldered doves are exhibited for the public, in large aviaries.
Toxoplasmosis was diagnosed the first time in a 6-year-old male G. humeralis (bird A); the bird was born in August 1989 and died at the end of December 1995. A female (bird B) that lived in the same aviary died one year later. A retrospective search of the zoo records revealed that two other (C and D) 7-year-old G. humeralis died in May–June 1995. Lack of appetite, asthenia, decline in health, and quick death were the recorded clinical signs. The present report is based on findings observed in bird A. Samples were not taken from others birds (B, C, and D).
Materials and methods
A full necropsy was performed. Hemorrhage and pale areas were seen in lung. Portions of lung were fixed in 10% buffered formalin processed routinely in an automatic tissue processor, embedded in paraffin, sectioned at 5 μm, and stained with hematoxylin and eosin (H&E). Paraffin blocks of lung were sent to the Animal Parasitic Diseases Laboratory, US Department of Agriculture, where deparaffinized sections were stained with anti-T. gondii and anti-Neospora caninum antibodies following methods described previously [5]. For electron microscopic examination, 1-mm3 formalin-fixed samples were immersed in 2.5% glutaraldehyde in 0.1 M phosphate buffer, post-fixed in 2% osmium tetroxide, and embedded in epoxy resin. Semithin sections were stained with toluidine blue, and ultrathin sections were stained with uranyl acetate and lead citrate and examined with a Zeiss EM109 electron microscope.
Results and discussion
Necrotizing pneumonia associated with numerous protozoa was observed microscopically (Fig. 1). In H&E sections, the protozoal tachyzoites had a central nucleus and a pale staining cytoplasm; they were 2–3 μm in diameter and most of them showed evidence of degeneration (Fig. 2). The protozoa reacted strongly to T. gondii and not to anti-N. caninum antibodies.
 |
Figure 1. Toxoplasma gondii in a bar-shouldered dove, lung. Note the necrotic process. There are numerous intralesional tachyzoites but non-visible at this magnification. H&E stain. |
 |
Figure 2. Toxoplasma gondii in a bar-shouldered dove, lung. Note a tachyzoite with dividing nucleus (arrow) and individual tachyzoites (arrowheads). H&E stain. |
Ultrastructurally, the protozoa were located in parasitophorous vacuoles in the host cell cytoplasm. Organisms divided in two by endodyogeny (Fig. 3). Organelles typical of T. gondii tachyzoites were seen, including micronemes and rhoptries with labyrinthine contents.
 |
Figure 3. Toxoplasma gondii in a bar-shouldered dove, lung. Two tachyzoites enclosed in a parasitophorous vacuolar membrane (pvm). Note conoid (co), micronemes (mn), rhoptries (ro) with honey-combed contents, and a nucleus (nu) in each tachyzoite. The parasitophorous vacuole has membranous tubules. Transmission electron microscopy. |
The present case was diagnosed as toxoplasmosis based on ultrastructure and immunoreactivity to T. gondii. Diagnosis of avian toxoplasmosis is often difficult. Species of two related protozoans, Atoxoplasma and Sarcocystis, should be considered in the differential diagnosis of avian toxoplasmosis [1, 6, 7]. Atoxoplasma spp. are considered common parasites of passerine birds and have a fecal-oral cycle with extra-intestinal stages in visceral tissues of birds, especially the liver and spleen [1]. Proliferative stages (merozoites) of Atoxoplasma sp. are smaller than T. gondii tachyzoites. Ultrastructurally, Atoxoplasma merozoites divide by schizogony, have small vestigeal rhoptries, and small numbers of micronemes [1]. The parasite in the present case divided by endodyogeny and had long rhoptries.
Sarcocystis spp. (S. falcatula or S. falcatula-like) can cause generalized disease in birds, especially in passerines and psittacines [4, 7]. Pneumonia is the predominant lesion of acute S. falcatula infection and disease is associated with intravascular development of S. falcatula schizonts [7]. Additionally, S. falcatula infections are confined to the geographical distribution (Americas) of the definitive host, opossum (Didelphis spp.). Recently, another species of Sarcocystis, S. calchasi was identified to cause fatality in racing pigeons in Europe and the Americas [6, 9]. However, Sarcocystis schizonts divide by endopolygeny (multiple nuclear lobulation), and merozoites lack rhoptries [1]. Additionally, the polyclonal antibodies used in the present study do not cross react with Sarcocystis and Atoxoplasma (Dubey, own observations).
These four bar-shouldered doves were probably exposed to a strain of Toxoplasma gondii virulent for birds in 1995.
References
- Dubey JP. 2002. A review of toxoplasmosis in wild birds. Veterinary Parasitology, 106, 121–153. [CrossRef] [PubMed] [Google Scholar]
- Dubey JP. 2010. Toxoplasmosis of animals and humans, 2nd edn. CRC Press: Boca Raton, FL. p. 1–313. [Google Scholar]
- Hartley WJ, Dubey JP. 1991. Fatal toxoplasmosis in some native Australian birds. Journal of Veterinary Diagnostic Investigation, 3, 167–169. [CrossRef] [Google Scholar]
- Hillyer EV, Anderson MP, Greiner EC, Atkinson CT, Frenkel JK. 1991. An outbreak of Sarcocystis in a collection of psittacines. Journal of Zoo and Wildlife Medicine, 22, 434–445. [Google Scholar]
- Lindsay DS, Dubey JP. 1989. Immunohistochemical diagnosis of Neospora caninum in tissue sections. American Journal of Veterinary Research, 50, 1981–1983. [PubMed] [Google Scholar]
- Olias P, Gruber AD, Kohls A, Hafez HM, Heydorn AO, Mehlhorn H, Lierz M. 2010. Sarcocystis species lethal for domestic pigeons. Emerging Infectious Diseases, 16, 497–499. [CrossRef] [PubMed] [Google Scholar]
- Smith JH, Neill PG, Box ED. 1989. Pathogenesis of Sarcocystis falcatula (Apicomplexa: Sarcocystidae) in the budgerigar (Melopsittacus undulatus) III. Pathologic and quantitative parasitologic analysis of extrapulmonary disease. Journal of Parasitology, 75, 270–287. [CrossRef] [Google Scholar]
- Vickers MC, Hartley WJ, Mason RW, Dubey JP, Schollam L. 1992. Blindness associated with toxoplasmosis in canaries. Journal of the American Veterinary Medical Association, 200, 1723–1725. [PubMed] [Google Scholar]
- Wünschmann A, Armien AG, Reed L, Gruber AD, Olias P. 2011. Sarcocystis calchasi-associated neurologic disease in a domestic pigeon in North America. Transboundary and Emerging Diseases, 58, 526–530. [CrossRef] [PubMed] [Google Scholar]
Cite this article as: Rigoulet J, Hennache A, Lagourette P, George C, Longeart L, Le Net J-L & Dubey JP: Toxoplasmosis in a bar-shouldered dove (Geopelia humeralis) from the Zoo of Clères, France. Parasite, 2014, 21, 62.
All Figures
|
Figure 1. Toxoplasma gondii in a bar-shouldered dove, lung. Note the necrotic process. There are numerous intralesional tachyzoites but non-visible at this magnification. H&E stain. |
| In the text | |
|
Figure 2. Toxoplasma gondii in a bar-shouldered dove, lung. Note a tachyzoite with dividing nucleus (arrow) and individual tachyzoites (arrowheads). H&E stain. |
| In the text | |
|
Figure 3. Toxoplasma gondii in a bar-shouldered dove, lung. Two tachyzoites enclosed in a parasitophorous vacuolar membrane (pvm). Note conoid (co), micronemes (mn), rhoptries (ro) with honey-combed contents, and a nucleus (nu) in each tachyzoite. The parasitophorous vacuole has membranous tubules. Transmission electron microscopy. |
| In the text | |
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