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A Review of Sarcocystis Spp. Shed by Opossums (Didelphis Spp.) in Brazil

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A Review of Sarcocystis Spp. Shed by Opossums (Didelphis Spp.) in Brazil REVIEW ARTICLE A review of Sarcocystis spp. shed by opossums (Didelphis spp.) in Brazil Revisão sobre Sarcocystis spp. excretados por gambás (Didelphis spp.) no Brasil Samantha Yuri Oshiro Branco VALADAS-; Rodrigo Martins SOARES-; David Scott LINDSAY4 - Universidade de São Paulo, Faculdade de Medicina Veterinária e Zootecnia, Departamento de Medicina Preventiva e Saúde Animal, São Paulo – Brazil 4 Virginia Polytechnic Institute and State University, Virginia-Maryland Regional College of Veterinary Medicine, Department of Biomedical Sciences and Pathobiology, Center for Molecular Medicine and Infectious Disease, Blacksburg – VA, United States of America Abstract South American opossums are the definitive hosts of Sarcocystis neurona, Sarcocystis falcatula, Sarcocystis speeri and Sarcocystis lindsayi. The sporocysts of these species of Sarcocystis are morphologically similar and methods like infectivity and pathogenicity for intermediate hosts (immunodeficient mice and psittacine birds) and molecular tools are used for identification. Opossums are synanthropic wild animals, and widely distributed in Brazilian territory. Previous studies have shown high environmental contamination with S. neurona sporocysts in several Brazilian regions. This paper reviews information on Sarcocystis spp. shed by various opossum species and its occurrence in Brazil. Keywords : Sarcocystis spp.. Brazil. Didelphis spp.. Sarcocystis neurona . Sarcocystis falcatula . Resumo Os gambás Sul-americanos são os hospedeiros definitivos de Sarcocystis falcatula , Sarcocystis neurona , Sarcocystis speeri e Sarcocystis lindsayi . Estas espécies de Sarcocystis são morfologicamente similares, mas podem ser distinguidas por sua patogenicidade e infectividade em hospedeiros intermediários (aves e camundongos imunodeficientes) e técnicas moleculares. Os gambás são animais silvestres e sinantrópicos e amplamente distribuídos no território nacional. Estudos anteriores demonstraram uma alta contaminação ambiental com esporocistos de S. neurona em diversas regiões brasileiras. Este artigo revisa informações sobre Sarcocystis spp. excretados por gambás e sua ocorrência no Brasil. Palavras-chave: Sarcocystis spp.. Brasil. Didelphis spp.. Sarcocystis neurona . Sarcocystis falcatula . Correspondence to: cycle consisting of a definitive host that is a predator or Rodrigo Martins Soares omnivore and an intermediate host that is an omnivore Universidade de São Paulo, Faculdade de Medicina Veterinária e Zootecnia, VPS or herbivore. Miescher first reported Sarcocystis in Av. Prof. Dr. Orlando Marques de Paiva, 87 1843 as “milky white threads” in the skeletal muscle of CEP 05508-270, São Paulo, SP, Brazil E-mail: [email protected] a mouse in Switzerland. In 1882, Lankester introduced the genus name Sarcocystis (in Greek, Sarkos = flesh, Received: 03/12/2015 kystis = bladder) (DUBEY et al., 2015a) based on the Approved: 01/06/2016 appearance and location of the characteristic muscle cyst stage now known as a sarcocyst. It was not until INTRODUCTION AND HISTORY 1972 that the mandatory two-host life cycle was The genus Sarcocystis belongs to the protozoan described in experimentally infected animals and the phylum Apicomplexa. Members of this phylum cause identity of the Sarcocystis oocyst was determined. It significant human and animal disease including now became apparent that coccidia named “Isospora malaria, coccidiosis, and toxoplasmosis. Members of bigemina ” observed in dog and cat feces were actually the genus Sarcocystis are closely related to Toxoplasma Sarcocystis species (LINDSAY et al., 1997). gondii and other tissue cyst-forming-parasites. They The definitive host becomes infected after ingesting have evolved to have an obligatory heteroxenous life raw muscle (occasionally neural tissue) that has mature Braz. J. Vet. Res. Anim. Sci., São Paulo, v. 53, n. 3, p. 214-226, 2016 DOI: 10.11606/issn.1678-4456.v53i3p214-226 | 215 sarcocysts containing asexual stages known as There are about 180 valid named Sarcocystis bradyzoites. Bradyzoites are released from the species; however, the complete life cycles are known sarcocyst by digestion in the stomach and intestine. only for 26 of them (DUBEY et al., 2015a). Molecular Bradyzoites penetrate the mucosa of the small intestine methods are gaining importance in naming new and transform into male (micro) and female (macro) species but morphological descriptions of sarcocysts gamonts in the lamina propria. After fertilization, a and animal feeding studies are also important in thin oocyst wall develops around the zygote and the validating a new species. unsporulated oocyst is formed. Sporulation of the oocysts occurs in the lamina propria, resulting in two SARCOCYSTIS SPP . sporocysts each containing four sporozoites. Because South American opossums are the definitive hosts the oocyst wall is thin, it often ruptures while exiting of Sarcocystis neurona , Sarcocystis falcatula , the lamina propria releasing sporocysts into the Sarcocystis speeri (DUBEY; LINDSAY, 1998; DUBEY; intestinal lumen that are passed in feces. The prepatent LINDSAY, 1999) and Sarcocystis lindsayi (DUBEY et period for most Sarcocystis species is between seven to al., 2001d). 14 days, while the patent period is a month or longer Bioassay is used to aid in species identification of (DUBEY et al., 2015a). opossum transmitted Sarcocystis because it is not The intermediate host becomes infected by possible to identify the species using morphology of ingesting sporocysts from the environment while sporocysts. Bioassay separates the sample into avian grassing or in contaminated food or water. Sporozoites infective (S. falcatula , S. lindsayi , S. falcatula Arg) and excyst from sporocysts in the small intestine and mammalian infective (S. neurona , S. speeri ). All avian migrate to endothelial cells in vessels or other cells, infective species form sarcocysts in budgerigars while where they undergo asexual reproduction by S. speeri will form sarcocysts in immunodeficient mice schizogony and produce merozoites. The number of and S. neurona will cause encephalitis but not make generations of schizogony and the type of host cell sarcocysts (MARSH et al., 1997; DUBEY; LINDSAY, infected can vary with each species of Sarcocystis. 1998). Merozoites liberated from the terminal generation of schizogony penetrate striated muscle (occasionally Sarcocystis neurona neural) cells and initiate sarcocyst formation. Sarcocystis neurona is the main cause of equine Merozoites transform into metrocytes that divide by protozoal myeloencephalitis (EPM). The clinical endodyogeny and form bradyzoites. As the sarcocyst syndrome associated with EPM was first described in matures, it is filled with bradyzoites, which are the 70s. In 1991, the parasite was first isolated from infectious for the definitive host (DUBEY et al., 2001c, neural tissue of infected horses, described as a 2015a). Sarcocystis species, and named by Dubey et al. (1991). The number and distribution of sarcocysts may S. neurona was first isolated in Brazil in 2001 from the vary. This is influenced by several factors, such as the intestines of two opossums (D. albiventris ) from the number of sporocysts ingested, the species of state of São Paulo (DUBEY et al., 2001a). Sarcocystis , the species of the intermediate host, and its The North American opossum (D. virginiana ) was immune status. The majority of sarcocysts develop in proposed as the definitive host of the parasite in 1995, skeletal muscle; however they can occasionally be based on comparisons between cultivated merozoites found in smooth muscle (S. mucosa ) and the central and sporocysts from the intestine of opossums through nervous system (DUBEY et al., 1989). the analysis of their SSURNA (FENGER et al., 1995). Braz. J. Vet. Res. Anim. Sci., São Paulo, v. 53, n. 3, p. 214-226, 2016 | 216 In 1997, Fenger et al. (1997) induced clinical EPM in S. the random location of the parasite in the white and neurona negative horses fed with sporocysts from gray matter (DUBEY et al., 2001c). opossums. The life cycle was concluded when Overall, infected horses remain alert and responsive laboratory-raised opossums fed with muscle tissue of with vital signs within normality; some may present experimentally infected cats (Felis catus ) shed depression and weight loss. Neurological examination sporocysts of S. neurona (DUBEY et al., 2000b). normally reveals asymmetrical ataxia, weakness and The North American opossum (Didelphis spasticity of the four limbs. Areas of hyporeflexia, virginiana ) and the South American opossum (D. hypoalgesia or complete sensory loss are frequently albiventris ) are S. neurona known definitive hosts. present (MACKAY et al., 2000; DUBEY et al., 2001c). Several other animal species are its intermediate or The frequency of horses with S. neurona antibodies aberrant hosts. Laboratory-raised opossums excreted in the United States has ranged from 6.5% to 89.2% by sporocysts after feeding naturally infected skunk, Western Blot and from 26% to 27.6% by indirect armadillo, raccoon and sea otter muscles (CHEADLE fluorescent antibody test (IFAT). In Argentina, the et al., 2001, 2002; DUBEY et al., 2001e; 2001f; frequency of horses presenting S. neurona antibodies TANHAUSER et al., 2001). has ranged from 26.1% to 35.5% by Western Blot. In Horses are considered aberrant hosts for S. neurona Brazil, it has ranged from 33.7% to 69.6% by Enzyme since mature sarcocysts are not found in tissue of Linked Immuno Sorbent Assay (ELISA). The horses. In 2005, a case of
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