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Occurrence of Sarcocystis falcatula in captive psittacine birds in Brazil.

Abstract: Thirty-eight captive psittacine birds housed in a bird park in Foz do Iguacu, Parana, Brazil, died within a 15-month period as a result of infection with Sarcocystis falcatula. Although fatalities affected 16 species of psittacine birds, mortality was highest in Old World species, which were most susceptible to the pulmonary form of sarcocystosis. Along with the pathologic findings of this disease outbreak, a review of the pathophysiology of sarcosporidiosis is presented.

Key words. Sarcocystis falcatula, pathology, parasitology, avian, psittacine birds

Introduction

The genus Sarcocystis (phylum Apicomplexa) is composed of protozoal organisms that affect mammals, birds, and reptiles. (1-5) Infection has also been reported in amphibians and fish. (6) The life cycle of Sarcocystis involves a predator-prey relationship. Sarcocystis species are generally not pathogenic for the definitive hosts, which include carnivores, domestic and wild omnivores, and humans. Subclinical infection normally occurs in the intermediate host where the parasite forms cysts in the muscles. However, depending on the severity of the infection, as well as the species and susceptibility of the animal, disease may be fatal. (1-5,7)

More than 90 species of Sarcocystis are described, which affect both domestic and wild animals. (8) Sarcocystis falcatula is the most prevalent species that affect birds. Opossums (Didelphis virginiana (9-11) and Didelphis albiventris (12-15)) are the only known definitive hosts. Sarcocystis falcatula is different from other species in this genus, because it has only 1 definitive host and several bird species serving as intermediate hosts. (10,16) Until 1995, S falcatula was the only Sarcocystis species found in the North America opossum, Didelphis virginiana; however, recent studies also revealed the presence of Sarcocystis neurona and Sarcocystis speerei. (17) Both S falcatula and S neurona have been found in the South America opossum, D albiventris, both in the Argentinian and Brazilian territories. (12-15) The dissemination of certain Sarcocystis species may be the result of the ability of its intermediate stages to parasitize migratory birds. (15)

Opossums must ingest birds that contain Sarcocystis cysts in the muscle to perpetuate the parasite's life cycle. Proteolytic enzymes release bradyzoites in the opossum's small intestine, and this stage of the parasite penetrates the lamina propria where sexual reproduction occurs. Microgamonts in various stages of development can be seen dorsal to the nucleus in the intestinal epithelium, and macrogamonts are located in the base of the epithelial cells or lamina propria. (18) As sporogony progresses, the macrogamonts appear to descend from the base of the epithelial cells into the core of the villi. (18) Oocysts and sporocysts are found deep to the basement membrane and more are found at the tips of the villi than toward the crypts. (18) Infective sporocysts are shed in small quantities in the feces of the opossum for a prolonged period. (7,9,18) Prolonged patency in Sarcocystis infections probably occurs because sporocysts trapped in the lamina propria are periodically forced out of the villi, principally at the tips, by intestinal contractions. (18)

Released sporocysts are ingested by birds either via direct contact with contaminated opossum feces or paratenic hosts, such as rats and cockroaches. (7,19,20) Sporocysts release sporozoites in the small intestine of the bird, where they reach the blood stream and go on to invade tissues. Schizonts pass through 2 asexual generations in the endothelium. The first reproductive phase occurs in endothelial cells of the arterioles and the second in endothelial cells of capillaries and venules in most organs of the host. The lungs are the primary organs affected, but pathologic changes may also be observed in the liver, spleen, kidneys, intestines, and skeletal muscles. Merozoites are released and form cysts primarily in the skeletal muscles. (5,7,16,20-22) Cysts can also form in cardiac muscles, which can result in myocarditis. (2,23)

The incidence of mortality resulting from S falcatula varies among different species of birds. The disease in Old World psittacine birds is generally hyperacute and leads to high mortality that results from severe pulmonary lesions. (1,11,24) Species that survive the pulmonary phase of the disease are those that co-evolved environmentally with the opossum. (7) Pulmonary sarcosporidiosis is a superacute disease, and many animals do not show any clinical signs before sudden death. Other birds may demonstrate weakness, dyspnea, neurologic abnormalities, or partial or total anorexia. (1,10,24) Macroscopic lesions can include pulmonary edema, congestion, and hemorrhage; splenomegaly; and hepatomegaly. (1,23) In more chronic cases, weight loss is sometimes evident. (1,23,24) Microscopic findings can include schizonts within the endothelium of pulmonary capillaries and pneumonia. Merogony may result in chronic active hepatitis as well as interstitial myocarditis, myositis, splenitis, nephritis, and encephalitis. (1,20)

Materials and Methods

A total of 47 psittacine birds housed in a bird park in Foz do Iguacu, Parana, Brazil, died within a 15-month period during an outbreak of infection by S falcatula (Table 1). The park is located in a natural area of tropical forest also inhabited by many opossums (D albiventris), reptiles, and small mammals. These animals were able to freely enter the exhibit enclosures. The birds were paired in exhibit enclosures. All psittacine birds that died during this period were submitted for necropsy and tissues were collected, fixed in 10% buffered formaldehyde, and processed according to routine techniques used for paraffin embedding. Sections of 5 mm were stained with hematoxylin and eosin. To investigate the presence of Sarcocystis species in definitive hosts, 6 opossums (D albiventris) living in areas near the park were captured, humanely euthanatized, and submitted for necropsy. Sections of all intestinal regions were collected and processed for histopathologic examination. In addition, 5 budgerigars (Melopsittacus undulatus) that had died after being used as biologic sentinels in enclosures thought to be contaminated were submitted for necropsy to confirm the presence of Sarcocystis species. All tissue samples were sent to the Parasite Biology, Epidemiology and Systematics Laboratory, United States Department of Agriculture, Agricultural Research Service, Animal and Natural Resources Institute where immunohistochemistry and electronic microscopy were used to further evaluate the Sarcocystis species.

Results

Sarcosporidiosis was considered to be the cause of death of 38 of the 47 examined psittacine birds. The distribution of psittacine birds evaluated, the number of individuals suspected of being infected by Sarcocystis species, and those positive for the organism are shown in Table 1. Sixteen species of psittacine birds, including both Old and New World species, were infected with Sarcocystis species. Most of the birds that died exhibited no clinical signs. A small group experienced convulsions before death, and another group exhibited various clinical signs, including dyspnea, tachypnea, dullness, and prostration. Birds in the latter group were subjected to treatment, which was not successful.

At necropsy, the most significant changes observed among the psittacine bird species were moderate-to-severe lung hemorrhage, moderate-to-severe hepatomegaly, marked splenomegaly associated with multifocal pale areas distributed throughout the splenic parenchyma, and air sac opacity (Fig 1). On microscopic examination, the most significant finding was the presence of elongate schizonts, compatible with Sarcocystis species, contained within endothelial cells of the pulmonary vascular plexus (Fig 2) and macrophages and associated with extensive hemorrhage and, in some cases, pneumonia. Other microscopic abnormalities included splenitis marked by histiocytosis and plasmocytosis, as well as acute hepatitis with leukocytosis and hemosiderosis in hepatocytes and Kupffer cells. The 5 budgerigars used as biologic sentinels died within an average of 5 days after being placed in the enclosures. At necropsy, macroscopic examination of the lungs revealed severe hemorrhage and structures compatible with Sarcocystis species within the lung parenchyma and endothelium. Histopathologic examination of the opossum intestine revealed a large number of sporocysts in the submucosa, primarily involving the proximal small intestine. The organisms were compatible with the infective form of Sarcocystis species. Avian tissues that contained structures compatible with Sarcocystis species on histopathologic examination were submitted for immunohistochemistry testing, the results of which were positive for the presence of S falcatula in the lung parenchyma and endothelium. Electron microscopy also revealed structures compatible with S falcatula.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Discussion

Psittacine birds are considered accidental hosts that come in contact with feces of opossums carrying Sarcocystis species. The participation of opossums in the epidemiology of sarcocystosis in birds is described in many reports. (9-11,16) Opossums are commonly seen in parks and zoos in Brazil. In this case, opossums from the tropical woods near the park may have freely entered the enclosures by climbing through or over the barriers. Cockroaches can be paratenic hosts, ingesting or coming in contact with contaminated opossum feces. Birds can develop sarcocystosis if they eat a cockroach that has ingested feces that contained S falcatula sporocysts or if they eat food contaminated by cockroach feces. (7,19) Diets of psittacine birds attract both cockroaches and opossums. Once the sporocysts are ingested, they migrate via the blood stream to various organs where they destroy endothelial cells, which results in hemorrhage. The lungs are primarily affected. Old World psittacine birds were highly susceptible to the pulmonary form of sarcosporidiosis described in this report. Enclosures for New World and Old World psittacine birds were adjacent, and the former were rarely clinically affected by Sarcocystis species. Only 5 New World psittacine birds died in the outbreak. It is speculated that avian species that evolved in the same environment as opossums are able to survive pulmonary schizogony with sarcocyst formation and are thus more resistant to fatal pulmonary disease. (7)

Budgerigars are commonly used to investigate the pathogenicity of infection with Sarcocystis species because of their susceptibility to the disease. (3,20) In the scenario described in this report, budgerigars were used as biologic indicators for the presence of Sarcocystis in enclosures. The death of the 5 budgerigars in this report, associated with histopathologic findings, suggested the contamination of the environment by Sarcocystis oocysts or sporocysts.

Sarcocystis falcatula is the main species affecting Old World psittacine birds. (1,24) Although in this study, immunohistochemical examination and electronic microscopy analysis showing the presence of S falcatula were only performed in 5 samples of lung tissue from different birds, we believe the same agent was responsible for deaths of the other birds. Birds lived in the same or in paired enclosures, and the clinical history, as well as macroscopic and microscopic findings, were similar. In addition, studies that involved D albiventris in the Brazilian territory showed the presence of S falcatula. (12,13,15) Important outbreaks of sarcocystosis in breeding facilities of psittacine birds were reported from Florida and San Diego, California, USA. (1,23) In both cases, the species involved, symptoms, and macroscopic and microscopic findings were very similar to the ones observed in the present study.

Because of the rapid development of disease and its high mortality rate, antemortem diagnosis and consequent treatment of infected birds are very hard to perform. Therefore, prevention is the most important tool in the control of avian sarcosporidiosis, particularly involving Old World psittacine birds. Prophylactic measures include preventing opossums from entering enclosures by means of electrical fences or by covering the enclosures at night, disinfecting enclosures when the presence of the agent is confirmed or suspected, and preventing the circulation of paratenic hosts. (7,25) Cockroach control programs may be expanded, although total elimination of cockroaches is not feasible. (1)

Acknowledgments: We thank the Fundacao de Amparo a Pesquisa (FAPESP) for their financial support, J. P. Dubey for laboratory support, and Bruce Rideout and Chris M. Gardiner for assistance with histopathologic analysis.

References

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(7.) McCormick-Rantze ML, Latimer KS, Wilson GH. Sarcocystosis in psittacine birds. Available at: http://www.vet.uga.edu/vpp/clerk/rantze. Accessed January 3, 2009.

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(13.) Dubey JP, Lindsay DS, Rosenthal BM, et al. Isolates of Sarcocystis falcatula-like organisms from South American opossums Didelphis marsupialis and Didelphis albiventris from Sao Paulo, Brazil. J Parasitol. 2001;87(6):1449-1453.

(14.) Dubey JP, Lindsay DS, Venturini L, Venturini C. Characterization of Sarcocystis falcatula isolates from the Argentinian opossum, Didelphis albiventris. J Eukaryot Microbiol. 2000;47(3):260-263.

(15.) Rosenthal BM, Lindsay DS, Dubey JP. Relationships among Sarcocystis species transmitted by New World opossums (Didelphis spp.). Vet Parasitol. 2001;95(2-4):133-142.

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(17.) Dubey JP, Garner MM, Stetter MD, et al. Acute Sarcocystis falcatula-like infection in a carmine bee eater (Merops nubicus) and immunohistochemical cross reactivity between Sarcocystis falcatula and Sarcocystis neurona. J Parasitol. 2001;87(4):824-832.

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(19.) Clubb SL, Frenkel JK. Sarcocystis falcatula of opossums: transmission by cockroaches with fatal pulmonary disease in psittacine birds. J Parasitol. 1992;78(1):116-124.

(20.) Neill PJG, Smith JH, Box ED. Pathogenesis of Sarcocystis falcatula (Apicomplexa: Sarcocystidae) in the budgerigar (Melopsittacus undulatus). IV. Ultrastructure of developing, mature and degenerating sarcocysts. J Protozool. 1989;36(4): 430-437.

(21.) Smith JH, Craig TM, Dillard EA, et al. Naturally occurring apicomplexan acute interstitial pneumonitis in thick-billed parrots (Rhynchopsitta pachyrhyncha). J Parasitol. 1990;76(2):285-288.

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Silvia Neri Godoy, DVM, PhD, Catia Dejuste De Paula, DVM, MSc, Zalmir Silvino Cubas, DVM, MSc, Eliana Reiko Matushima, DVM, PhD, and Jose Luiz Catao-Dias, DVM

From the Faculdade de Medicina Veterinaria e Zootecnia da Universidade de Sao Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, Cidade Universitaria Sao Paulo, SP, Brazil, 05508 270 (Godoy, De Paula, Matushima, Catao-Dias); and Itaipu Binacional, Refugio da Vida Silvestres, Av. Tancredo Neves, 6.731, Foz do Iguacu, Parana, Brazil, 85866-900 (Cubas). Present address (Godoy): Instituto Chico Mendes de Conservacao da Biodiversidade, SQN 216 Bloco B, apto 518, Brasilia, DF, Brazil, 70.875-020.
Table 1. Summary of the psittacine birds examined for sarcosporidiosis
in Foz do Iguacu, Parana, Brazil, 2006.

Scientific names           Common names               No. animals

Amazona vinacea            Vinaceous Amazon                3
Aratinga jandaya           Jandaya conure                  2
Cacatua alba               White cockatoo                  3
Chalcopsitta duivembodei   Duivenbode's lory               1
Chalcopsitta sintilata     Yellow-streaked lory            2
Chalcopsitta cardinalis    Cardinal lory                   3
Eos bornea bornea          Red lory                        3
Eos squanutta              Violet necked lory              2
Lorius chlorocercus        Yellow-bibbed lory              4
Lorius garrulus            Chattering lory                 2
Lorius lory                Black-capped lory               4
Melopsittacus undulatus    Budgerigar                      5
Psittacula derbiana        Derbyan parakeet                1
Psittacus erithacus        African grey parrot             2
Trichoglossus haematodus   Rainbow lorikeet                8
  haematodus
Trichoglossus haematodus   Swainson's Blue Mountain        2
  moluccanus                 rainbow lorikeet
Total                                                     47

Scientific names           Suspected   Positives

Amazona vinacea                0           3
Aratinga jandaya               0           2
Cacatua alba                   0           3
Chalcopsitta duivembodei       0           1
Chalcopsitta sintilata         1           1
Chalcopsitta cardinalis        2           1
Eos bornea bornea              1           2
Eos squanutta                  0           2
Lorius chlorocercus            1           3
Lorius garrulus                0           2
Lorius lory                    0           4
Melopsittacus undulatus        0           5
Psittacula derbiana            0           1
Psittacus erithacus            0           2
Trichoglossus haematodus       4           4
  haematodus
Trichoglossus haematodus       0           2
  moluccanus
Total                          9          38
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Title Annotation:Retrospective Study
Author:Godoy, Silvia Neri; De Paula, Catia Dejuste; Cubas, Zalmir Silvino; Matushima, Eliana Reiko; Catao-D
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Geographic Code:3BRAZ
Date:Mar 1, 2009
Words:2862
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